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v.23(4); Oct 2012 >
PMC3469864

J Gynecol Oncol. 2012 October; 23(4): 282287.
Published online 2012 September 19. doi: 10.3802/jgo.2012.23.4.282
PMCID: PMC3469864
New insights into cervical cancer screening
Jonathan D. Boone,
1
Britt K. Erickson,
2
and Warner K. Huh
2

Author information Article notes Copyright and License information
Go to:
Abstract
Worldwide, cervical cancer is a leading cause of cancer related morbidity and mortality. For over
50 years, cervical cytology has been the gold standard for cervical cancer screening. Because of
its profound effect on cervical cancer mortality in nations that have adopted screening programs,
the Pap smear is widely accepted as the model screening test. Since its introduction, many
studies have analyzed the Pap smear and found that it is not without its shortcomings including
low sensitivity for detection of cervical intraepithelial neoplasia 2/3. Additionally, the discovery
of infection with the human papillomavirus (HPV) as a necessary step in the development of
cervical cancer has led to the development of HPV testing as an adjunct to cytology screening.
More recently, researchers have compared HPV testing and cytology in the primary screening of
cervical cancer. In this review, we will discuss cytologic testing limitations, the role of HPV
DNA testing as an alternative screening tool, the impact of the HPV vaccine on screening, and
future directions in cervical cancer screening.
Keywords: Co-testing, Cytology, HPV vaccine, Pap smear limitations, Screening
Go to:
INTRODUCTION
Cervical cancer screening is hailed as one of the major public health advances in the 20th
century. In the process of evaluating vaginal smears as an indicator of hormone status, Dr.
George Papanicolaou [
1
] incidentally noticed that malignancy could be detected during cytologic
evaluation. He and his colleague, Dr. Herbert Traut, eventually published "The diagnostic value
of vaginal smears in carcinoma of the uterus" which was the beginning of an era of the
Papanicolaou, or "Pap smear," screening [
1
].
Despite a drastic decrease in cervical cancer morbidity and mortality in communities that have
adopted cytology screening programs, cervical cancer is still the third most commonly diagnosed
cancer in women with 529,800 new cases estimated worldwide annually [
2
]. More recent data
have suggested limitations of the Pap smear including low sensitivity, high false negative rates,
and interobserver variability. These limitations have forced many to revisit the utility of cytology
as a primary screening test particularly when compared to human papillomavirus (HPV) testing.
Go to:
THE LIMITATION OF PAP SMEARS
As the first cancer screening test of the modern era, the Pap smear was never initially scrutinized
through a standard evidence based approach as many of our modern screening tests are today.
However, the epidemiologic data are convincing. In nations that have adopted cytologic
screening programs, the incidence and mortality from cervical cancer has declined dramatically
[
3-5
]. Because of its success in cervical cancer prevention, the Pap smear has come to be known
as the archetype of screening tests [
6
]. Although it had a profound effect on cervical cancer
morbidity and mortality in an era of highly prevalent cervical disease, cytologic screening has
inherent limitations, particularly as the patterns of incidence have changed and the morbidity
from overtreatment is now fully appreciated.
Despite the acceptance of cytologic testing as the primary screening method for cervical cancer,
it has shown a high false negative rate (i.e., missed cervical intraepithelial neoplasia [CIN] 2+).
Studies have shown that 20% to 40% of new cervical cancer cases are diagnosed in women who
have had "proper" screening [
7-9
]. As data from population based trials have emerged, the Pap
smear has shown low sensitivity for the detection of CIN 2+ and even more variable sensitivity
depending on a woman's age, highest in the 50 and older age group [
10
]. A systematic review
performed by Nanda et al. [
11
] to evaluate the diagnostic accuracy of the Pap smear found its
sensitivity to be 51% (range, 30% to 87%), and specificity to be 98%, (range, 86% to 100%). In
a meta-analysis by Spence et al. [
12
], the false negative rate of cytologic testing was as high as
35.5% on average. Cytologic testing has also been shown to have a lower specificity for high-
grade CIN than low-grade lesions, which can lead to overtreatment [
11,13
]. Additionally, the
sensitivity of cervical smears for adenocarcinoma is lower than for squamous cell carcinoma [
14
].
In conjunction with this and the rising incidence of adenocarcinoma which accounts for nearly a
quarter of all newly diagnosed cervical cancers, cytologic tests will continue to become less
useful [
15,16
].
In addition to its limitations regarding low sensitivity, the Pap smear limitations also include
failure to acquire adequate specimens, interobserver bias, and misinterpretations. Inflammation,
scant cellularity, and blood contaminating samples have all been cited as reasons for inadequate
or unsatisfactory samples. Approximately 1% to 8% of Pap smears have been reported as
unsatisfactory [
17,18
]. In one trial, when inadequate samples were reevaluated, cytologic atypia
including high grade lesions and carcinoma was seen in 7% of the samples [
18
]. Even with
satisfactory samples, cytologic interpretation is subject to interobserver variability despite
international standards. Woodhouse et al. [
19
] showed the discrepancy between low and high
grade lesions to range from 9% to 15% among different laboratories and their personnel.
Furthermore, the diagnosis of atypical squamous cells of undetermined significance (ASC-US) is
well-documented as a poorly reproducible category. Even with experienced cytologists and
adequate samples, varied interpretations continue to reduce cytologic testing's diagnostic
accuracy [
20
].
The most effective screening tests must achieve a balance between high sensitivity and
acceptable specificity. Equally important is identifying a screening interval that is frequent
enough to detect lesions before they become invasive while still minimizing cost and morbidity
associated with overtreatment. This ensures the low likelihood that an abnormal result, in this
case invasive cervical cancer, will be present before the next screening event. Because of its low
sensitivity, cytologic testing alone requires regular exams with diligent follow-up. In a meta-
analysis by Spence et al. [
12
], even when optional screening is available, 65% of women had
deficient screening histories and 14% of women had poor follow-up after an abnormal Pap
smear. Therefore, a screening test with a high negative predictive value, which safely allows for
extension of screening intervals, is of greatest benefit.
Go to:
THE INFLUENCE OF THE HUMAN PAPILLOMAVIRUS
Infection with the oncogenic HPV is necessary for the development of cervical cancer [
21,22
]. Dr.
Harald zur Hausen [
23
], a German virologist and physician, first proposed the role of HPV in the
development of cervical cancer in the 1970s. By 1984, he had specifically isolated HPV 16 and
HPV 18, the two HPV types that today are known to cause approximately 70% of cervical cancer
[
24
]. HPV is now the most commonly diagnosed sexually transmitted infection with prevalence
estimated at 43% for females aged 14-59 in the US [
25
]. Currently, 14 high-risk HPV DNA types
have been associated with the development of cervical cancer [
26,27
].
Young women clear the HPV at a high rate of 40% to 70% in the first year of infection and as
high as 70% to 100% two to five years after infection [
28-32
]. The prevalence of HPV infection
along with its subsequent clearance in adolescents is extremely high but the incidence of cervical
cancer is negligible at 0.1 per 100,000 [
31,33-37
]. Additionally, CIN 2 in this same age group will
regress 60% of the time within the first three years [
38
]. Screening adolescents may cause more
harm because it increases unnecessary evaluation and treatment [
38
]. Therefore, regardless of risk
factors, screening should begin at age 21.
Low risk HPV clears more quickly than high risk HPV with HPV types 16, 31, 54, and 53
resulting in the longest course of infectivity [
29,39
]. HPV 16 has been proven to be responsible for
most of the persistent infections [
13
]. These persistent infections have shifted the focus towards
high risk HPV DNA testing as the new paradigm for cervical cancer screening.
Go to:
HPV SCREENING: A NEW HORIZON
In theory, invasive cervical cancer is a preventable disease. Due to the limitations of the Pap
smear and an improved understanding of the role of HPV in cervical carcinogenesis, primary
prevention has shifted to high-risk HPV (HR-HPV) testing and HPV vaccination.
The American Society for Colposcopy and Cervical Pathology (ASCCP) has recommended the
use of HR-HPV testing in a variety of situations. These include triage for ASC-US Pap smears,
initial workup of atypical glandular cell (AGC) Pap smears, "co-testing" with cytology in women
over thirty years old, follow-up CIN 1 testing when the preceding Pap was ASC-US, ASC-H, or
LSIL, follow-up testing after an excision or ablative procedure is performed for CIN 2/3, and
"reflex" testing in postmenopausal women with LSIL cytology. Testing specifically for HPV 16
and 18 is also emerging as an important test for further triage of women greater than 30 years of
age who are HR-HPV positive but cytology negative.
Reflex testing (that is, HPV testing when cytology is abnormal) was first studied and found to be
a viable option for screening in the ASC-US/LSIL Triage Study (ALTS) trial. The ALTS trial
found that testing for HPV after an ASC-US Pap smear was a sensitive and cost effective
strategy. HPV testing detected CIN 3 with a sensitivity of 96% and it decreased the number of
colposcopies by 50% [
40
].
In women over thirty, HPV DNA testing combined with cytology, known as "co-testing", was
approved for screening in the US in 2006. Combining these tests results improved detection of
pre-invasive and invasive lesions. The natural history of HPV infection has shown decreased
incidence in women over the age of 30. Therefore, combining cytology with HR-HPV testing in
this age group also allows for extended screening intervals if both tests are negative, given its
high negative predictive value [
41-43
].
Numerous studies have shown a benefit of using HPV testing for the primary detection of
cervical dysplasia. Much of the benefit of HPV DNA testing is drawn from increased sensitivity
with acceptable specificity and high negative predictive values for detecting CIN 2/3 relative to
cervical cytology [
41,44-48
]. Several large international trials have shown that primary HPV testing
has better sensitivity alone than cytology, and when combined with cytology triage, the
specificity is similar to cytology alone [
20,44-46,48,49
]. Ronco et al. [
41
] suggested that HPV DNA
testing might be better than cytology in preventing invasive cancer because it detects high-grade
lesions earlier. The Population-Based Screening Study Amsterdam (POBASCAM) trial also
confirmed this by showing CIN 2+ was detected earlier with HR-HPV testing than with cytology
[
46
].
In addition to its improved sensitivity, HPV testing has other advantages. HPV testing is more
objective and reproducible than the other cervical cancer screening tests while also being less
demanding in terms of training and quality assurance [
45
]. It can be automated, centralized, and
be quality-checked for large specimen input while avoiding the subjective interpretation
associated with cytology [
20
]. It may also be more cost-effective than cytology if deployed for
high volume testing such as in primary screening.
An additional advantage to primary HPV testing is seen in developing countries where the
burden of cervical cancer is highest. Large prospective trials have compared once per lifetimes
screening methods of HPV testing, cytology and visual inspection with acetic acid. Compared
with a control group, only HPV testing reduced the rate of cervical cancer. Therefore, in low
resource settings, HPV testing in women over 30 may be an effective large scale method of
cervical cancer screening [
45
].
Despite the positive results seen with HPV testing, the ASCCP has not yet adopted primary
screening with HPV testing because of concerns for an evidence based approach to subsequent
follow-up. A new approach which is currently utilized many European nations and is being
evaluated in the US is primary HPV testing with cytology triage. In this screening method, a
positive HR-HPV test is then followed by cytology. Patients with abnormal cytology then
proceed with colposcopic evaluation. With this method, the test with the higher sensitivity (HPV
testing) is followed by the test with the higher specificity (cytology), thus improving detection
rates while eliminating false positive results. In support of this method, a prospective Finnish
trial demonstrated that primary HPV DNA screening with cytology triage had improved
sensitivity and equivalent specificity for detection of CIN 2/3. Moreover, in women 35 years or
older, HPV testing with cytology triage was more specific than cytology alone and decreased
colposcopy referrals and follow-up tests [
49
].
Go to:
HPV VACCINATIONS AND ITS EFFECT OF THE
VACCINE ON SCREENING
With a better understanding of the biology of HPV infections, vaccinations have been developed
to help prevent primary infection. There are currently two commercially available vaccines in the
US that protect against cervical cancer and pre-invasive disease by targeting specific HPV types:
GARDASIL (Merck & Co. Inc., Whitehouse Station, NJ, USA), which is a quadrivalent vaccine
and protects against HPV type 6, 11, 16, and 18, and Cervarix (GlaxoSmithKline, Rixensart,
Belgium) which is a bivalent vaccine and protects against HPV types 16 and 18.
As more women are successfully vaccinated there will be a reduction in prevalence of
cytological abnormalities and this may further limit the effectiveness of cytology as a primary
screening tool. It is estimated that there will be a reduction from the current 50% to 70% positive
predictive value of cytology to 10% to 20% if there is a decrease in prevalence of pre-invasive
cervical lesions. HPV testing may therefore be more effective in regions and countries with a
lower HPV prevalence due to effective vaccination programs [
20
].
The second major impact of the vaccine on Pap testing is a change in cytologic interpretation.
With fewer abnormal lesions, there may be greater interobserver variability in cytologic
interpretation. This could raise false-negative diagnoses and further reduce the sensitivity of
cytology [
20
].
Go to:
FUTURE DIRECTIONS
Improved screening algorithms, which may in the future include primary HPV testing, followed
by cytology triage will likely continue to change as data from large prospective trials emerge.
This method has shown some promise by maintaining high sensitivity, prolonged screening
intervals, and may ultimately prove to be more efficacious in the post-vaccinations era. Other
areas of current research include identification of other novel molecular markers associated with
protein expression and cell cycle regulators that are present in high-grade lesions. E6 and E7
viral oncogenes are necessary for HPV carcinogenesis and tests for E6/E7 mRNA, already
commercially available, could help identify women at higher risk for developing cancer [
50
].
Staining for p16 overexpression has already shown promise in the triage of abnormal cytology,
specifically in those with ASC-US, ASC-H, and LSIL cytology [
50,51
]. Additionally, high-grade
lesions have genetic expression profiles that resemble invasive disease [
50
]. Therefore, DNA
micro-array analysis may be able to better stratify a woman's risk in the setting of a positive HR-
HPV test [
50
].
The utilization of the Pap smear in preventive care and cervical cancer screening has been a
cornerstone in women's health for over 70 years. Decline of cervical cancer rates after
implementation of cytology programs is considered one of the greatest successes in cancer
prevention of all time. Through a better understanding of the role of HPV in cervical cancer
carcinogenesis and the development of HR-HPV tests, cervical cancer screening strategies have
already shown a drastic shift from conventional annual cytology to a more complex interplay of
HPV triage, extended screening intervals, and varying methods of follow-up. These changes
likely represent just the beginning of a paradigm shift in cervical cancer prevention. As we move
forward with cervical cancer screening programs, HPV testing will likely emerge as a primary
screening method followed by triage with either cytology, HPV genotyping, or other genetic
profiling, which will more efficiently guide clinicians in the prevention of invasive disease.
Go to:
Footnotes
The author, Warner K. Huh has worked as a consultant for Roche Diagnostics and Merck & Co.
Inc.
Go to:
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Global cancer statistics. [CA Cancer J Clin. 2011]
Effect of screening on incidence of and mortality from cancer of cervix in England:
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Mass screening programmes and trends in cervical cancer in Finland and the Netherlands.
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Invasive cervical cancer and screening: what are the rates of unscreened and
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Overview of the European and North American studies on HPV testing in primary
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Review Accuracy of the Papanicolaou test in screening for and follow-up of cervical
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Review Process of care failures in invasive cervical cancer: systematic review and meta-
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Colposcopic and histopathologic evaluation of women participating in population-based
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Atypical glandular cells in conventional cervical smears: incidence and follow-up. [BMC
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Reprocessing unsatisfactory ThinPrep Papanicolaou test specimens increases sample
adequacy and detection of significant cervicovaginal lesions. [Cancer. 2004]
Interobserver variability in subclassification of squamous intraepithelial lesions: Results
of the College of American Pathologists Interlaboratory Comparison Program in
Cervicovaginal Cytology. [Arch Pathol Lab Med. 1999]
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Epidemiologic evidence and human papillomavirus infection as a necessary cause of
cervical cancer. [J Natl Cancer Inst. 1999]
Condylomata acuminata and human genital cancer. [Cancer Res. 1976]
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Natural history of cervicovaginal papillomavirus infection in young women. [N Engl J
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High-risk HPV infection after five years in a population-based cohort of Chilean women.
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Risks for incident human papillomavirus infection and low-grade squamous
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The natural history of type-specific human papillomavirus infections in female university
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Comparison of three management strategies for patients with atypical squamous cells of
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and cervical intraepithelial neoplasia: a randomised controlled trial. [Lancet Oncol. 2010]
Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia
grade 3 and cancer: 5-year follow-up of a randomised controlled implementation trial.
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and cervical intraepithelial neoplasia: a randomised controlled trial. [Lancet Oncol. 2010]
Randomized controlled trial of human papillomavirus testing versus Pap cytology in the
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2006]
Routine cervical screening with primary HPV testing and cytology triage protocol in a
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Human papillomavirus testing for the detection of high-grade cervical intraepithelial
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Public Health Rep >
v.124(5); Sep-Oct 2009 >
PMC2728666

Public Health Rep. 2009 Sep-Oct; 124(5): 733744.
PMCID: PMC2728666
Family Planning Provider Referral,
Facilitation Behavior, and Patient Follow-up
for Abnormal Pap Smears
Holly C. Felix, PhD, MPA,
a
Janet Bronstein, PhD,
b
Zoran Bursac, PhD, MPH,
c
M. Kathryn Stewart, MD,
MPH,
a
H. Russell Foushee, PhD,
d
and Joshua Klapow, PhD
b

Author information Copyright and License information
Go to:
SYNOPSIS
Objectives
Family planning (FP) clinics are important access points for cervical cancer screening and
referrals for follow-up care for abnormal Papanicolaou (Pap) smears for a substantial number of
U.S. women. Because little is known about referral and facilitation practices in these clinics or
client action based on referrals, we sought to determine FP provider referral and facilitation
practices when seeing FP clients with abnormal Pap smear results, and FP client follow-up for
abnormal Pap smears due to FP provider referrals.
Methods
We conducted a mail survey of Medicaid-enrolled FP providers in Arkansas and Alabama, and
conducted a telephone survey with a sample of FP clients of those providers responding to the
provider survey.
Results
Major provider factors associated with referral included rural location, health department and
clinic institutional setting, large Title X practice/clinic size, and high FP clinic focus. Major
factors associated with facilitation included rural location, non-physician specialty, health
department and clinic institutional setting, and small Title X clinic size. Of women reporting
abnormal results, 62.4% reported follow-up care. Of those who received follow-up care, 40.0%
received some care and a referral from their FP provider. A major factor associated with clients
seeking follow-up care was being told by their FP provider where to go for follow-up care. Age
was a major factor associated with clients actually obtaining follow-up care.
Conclusions
Where follow-up care is not available at the FP site, referrals are critical and are a major factor
associated with whether women seek care for the condition. Interventions to increase follow-up
rates should focus on provider and system features, rather than clients.
A substantial number of U.S. women of childbearing age (1544 years) receive family planning
(FP) services through two federally supported programs: Title X and Medicaid FP demonstration
programs.
1,2
These programs provide contraceptive services and FP-related counseling to low-
income and uninsured women, as well as access to screenings for many sexual and reproductive
health conditions, including Papanicolaou (Pap) smears to detect preinvasive lesions and
invasive cervical cancer. Results from normal Pap smears are reported as negative for lesions or
malignancy, epithelial cell abnormality, or other (when there are no cell abnormalities but
findings indicate increased risk).
3
Women receiving abnormal results are given follow-up
diagnostic recommendations that range from repeat Pap smears at six and 12 months, to
colposcopic examination (with or without endocervical sampling), to human papillomavirus
DNA testing, to loop electrosurgical excision.
4

Early detection from Pap smears leading to treatment has been credited with dramatically
reducing deaths from cervical cancer during the last half century.
5
Title X and FP waivers do not
cover treatment for cervical cancer; however, un/underinsured and low-income women
diagnosed with precancerous lesions or cervical cancer may be able to access treatment coverage
through state Medicaid plans as a result of a 2000 federal law that permits states to expand
Medicaid programs for such treatment.
6

In 2004, 84% of U.S. women (18 years of age) reported having a Pap smear within the
preceding three years.
7
Despite high rates of screening and reduced mortality, many women do
not follow up after receiving abnormal Pap smear results. A review of follow-up adherence
studies conducted between 1985 and 1999 found that an estimated 15% to 42% of women did
not seek follow-up care for abnormal Pap smears.
8

A number of studies have been conducted to identify factors associated with women following
up on abnormal Pap smears. In 2007, Eggleston and colleagues published a comprehensive
review of 26 published studies conducted between 1990 and 2005, which identified factors
associated with following up on abnormal Pap smear results. Although the 26 studies defined the
term adherence differently, they all represented a patient following through with additional
diagnostic or treatment recommendations made in response to abnormal Pap smear results.
Individual factors moderately to strongly associated with follow-up adherence to abnormal Pap
smears included minority race/ethnicity (African American and Asian),
knowledge/understanding of the Pap smear and results, and severity of the results. The studies
found cost of care to the patient as one reported barrier to follow-up adherence, and some, but
not all of the studies suggested an association between private health insurance coverage and
follow-up. Psychosocial factors moderately to strongly associated with follow-up adherence
included social support and marital status. Health-care system factors having a moderate to
strong association with adherence included enhanced provider-patient communication, on-site
colposcopy, and referral facilitation activities (e.g., follow-up appointment reminders). The
studies found no significant difference in adherence based on clinician specialty or the type of
facility to which the referral was being made. No studies identified through this review
investigated adherence rates based on the type of health-care site providing the referral (e.g.,
public health clinic vs. private physician office).
9

The Eggleston et al. review indicated that most studies investigating factors associated with
adherence focused primarily on patient characteristics, with few studies conducted to identify
clinicians and health-care facility characteristics associated with adherence.
9
Furthermore, very
little research has investigated the specific referral practices and facilitation activities of FP
providers and the characteristics of adherent women receiving referrals through FP clinics. One
known study set in an FP clinic found that unmarried, less educated, younger women with fewer
health problems were less likely to adhere to follow-up recommendations.
10

Our study focused on a population of women with public funding for FP services only, and the
array of providers, including FP-focused clinics (many based in public health departments
11
) and
private physicians participating in Medicaid, who provide FP services to this population.
Publicly funded FP clinics are highly focused on providing preventive care
12
and are less likely
than other providers to offer other sexual and reproductive health services (such as colposcopy)
or primary care services.
1315
Other settings may offer these services but require payment out of
pocket or with insurance before they can be provided. They may refer patients with abnormal
Pap smears to other providers who can offer follow-up services to patients without financial
resources.
This article explores the various policies regarding follow-up for abnormal Pap smear maintained
by this array of providers, and the impact that the reported actions of FP providers has on
patients' decisions to seek follow-up care when they report having received an abnormal Pap
smear.
Go to:
METHODS
To collect information about referral practices and facilitation activities of FP providers and
follow-up adherence to referrals for care for an abnormal Pap smear, we fielded two surveys: (1)
a mailed survey sent to all Medicaid-enrolled providers in Arkansas and Alabama (as identified
through provider lists obtained from the respective state Medicaid agencies), and (2) a telephone
survey with women receiving FP services from providers who returned the provider survey. We
sent the mail survey to all FP providers in Arkansas and Alabama. We stratified the client sample
based on whether the responding provider had scored above or below the median on the
weighted summary score regarding extent of facilitating referrals.
Provider survey
The provider survey asked providers about their referral practices, facilitation activities, and
referral resources for follow-up care for abnormal Pap smears, as well as for nine other non-FP
health conditions (data not shown in this article). Facilitation activities included identification of
clients' usual primary care provider, providing contact information on referral provider, writing a
referral, calling referral provider, making the referral appointment, reminding client of
appointment, arranging transportation, following up with referral provider, and following up with
the client. Using a scale of 1 to 5, with 1 indicating always engages in activity and 5 indicating
never engages in activity, we asked providers to indicate the extent to which they engaged in
each of these facilitation activities should they decide to refer a patient with abnormal Pap smear
results.
To ease interpretation, during the analysis phase, we inverted the facilitation score so that a
higher score represented more engagement in facilitation activities and a lower score represented
less engagement in facilitation activities. We created a facilitation score based on the sum of
facilitation activities used with women receiving abnormal Pap smears (ranging from 9 to 45,
with a high facilitation score indicating the maximum of almost always engages in all
facilitation activities). The survey asked providers if there were any local providers who would
accept referrals for abnormal Pap smears for patients who have difficulty paying for care, and, if
such local providers existed, whether they had a professional relationship with those providers.
Additionally, we asked providers about their concern regarding patient competence to adhere to
referrals and systemic barriers to adherence, as well as demographic and practice characteristics.
We pretested and revised the survey before mailing it in May 2006 to all Medicaid-enrolled FP
providers in Alabama and Arkansas, whose names and addresses were provided by the respective
state Medicaid offices. Following the Tailored Design Method for mail surveys,
16
we made up to
five attempts to encourage participation of nonresponding providers. Data collection ended in
September 2006. Prior to mailing the survey, we distributed a press release to media outlets and
provider organizations to inform providers of the survey and its purpose.
Twenty-six percent (n=459) of all Medicaid-enrolled FP providers (n=1,743) in Arkansas and
Alabama returned completed surveys. The response rate for public clinic-based providers was
higher (59%) than for office-based physicians (22%).
Client survey
The client survey asked clients of survey-responding FP providers about their use of and
satisfaction with Medicaid FP waiver services, the presence of non-FP health conditions
(presented as a list from which the respondent selected as many conditions as applied), whether
they discussed these non-FP conditions with their FP provider, and whether their FP provider
made a referral for the health condition and facilitated the referral. Additionally, we asked clients
how they evaluated the urgency of the condition, whether they sought and received care for the
condition, and what difficulties they faced in seeking and receiving care. The client survey
included a measure of trust of physicians
17
and of self-efficacy,
18
along with demographic
measures.
We pretested and revised the survey before fielding it from April to September 2007. We used
computer-assisted telephone interviewing procedures to minimize data entry errors and to control
survey administration. Calls were placed at various days and times with up to eight attempts or
until final disposition. We attempted to reach respondents at least two times to participate in the
survey, with those refusing to participate on two occasions being coded as a final refusal and not
contacted again. The upper-bound response rate for the client surveycalculated as the number
of completions (n=1,976) divided by the number of completions plus number of refusals and
surveys terminated (n=2,517)was 79%. Of those who completed the survey, 12% (n=234)
reporting having an abnormal Pap smear. Of those with an abnormal Pap smear, 94% discussed
with or learned about their abnormal Pap smear from their FP provider.
The University of Alabama at Birmingham (UAB) Survey Research Unit administered the
surveys in both states to maintain consistency in mailing and telephone interviewing, data
collection, and data entry. Both surveys are available upon request to the authors.
Other data
The study team collected data on available safety net resources that provided services to low-
income clients in each state. For abnormal Pap smears, we viewed sites that participated in the
Breast and Cervical Cancer Early Detection Program (BCCEDP), operated by the Divisions of
Health in each state, as available resources. We counted the number of resources available within
30 minutes driving time from each responding provider as the number of referral resources
available. We used geographic information software
19
to identify the number of sites falling
within the drive-time parameter for each respondent. We obtained rural/urban commuting area
codes for providers and clients from U.S. Census files and used them to indicate the rural,
suburban, or urban nature of their location.
Data analysis
We performed all analyses using SAS software.
20
We generated descriptive statistics including
proportions, means, and standard deviations for all variables. Univariate comparisons for
continuous variables included two-sample t-tests and one-way analysis of variance, and for
categorical variables Chi-square and Fisher's exact tests. We used multivariate logistic regression
to identify characteristics associated with provider referral and characteristics associated with
client seeking and receiving treatment for an abnormal Pap smear. We adjusted all odds ratios
(ORs) produced by these models for covariates.
We restricted the multivariate analysis for the client behavior to those clients who either reported
no treatment for the condition from the FP provider or reported receiving treatment from their FP
provider as well as a referral for further care, to avoid confounding the analysis by including
clients who received sufficient care at their FP provider site. We used multivariable linear
regression to identify characteristics associated with provider facilitation. We considered
associations to be significant at the alpha <0.05 level; however, we discussed associations with
significance levels of 0.050.10 as indicative of possible trends.
In the final multivariate analyses of provider behavior, we included the measure of perceived
resources but excluded the measure of actual resources because the two were highly correlated.
The pattern of the correlation was generally that those who perceived having local resources
were accurate relative to the measure of actual resources, although some of those who perceived
that they did not have local resources were inaccurate, when local was defined as within a 30-
minute drive time. To help address these perception issues, our project summarized the findings
on referral resource availability as a handbook and distributed this handbook to all provider
survey recipients.
The Institutional Review Boards at the UAB and the University of Arkansas for Medical
Sciences approved the study design.
Go to:
RESULTS
Provider survey
Slightly more than half (55%) of FP providers reported that they would refer a woman who had
an abnormal Pap smear outside their clinic or practice for follow-up care. However, referral
behavior varied significantly by the provider's institutional setting (Table 1). Private office-based
providers were much more likely to report providing follow-up care personally or within their
practice. Conversely, public providers (e.g., those from health departments and from other types
of clinics) were more likely to report referring women for follow-up care to providers outside
their clinic. Among providers from all institutional settings who reported that they would refer a
woman who had an abnormal Pap smear (n=274), 70% reported the availability of local
resources to which they could refer women for follow-up care for abnormal Pap smears. We
found no significant difference in perception of available referral resources based on institutional
setting. Overall, referring providers were equal in reporting having (50%) and not having (50%)
professional relationships with providers to whom they could make referrals for abnormal Pap
smears. We found no significant difference in provider relationships based on institutional
setting.

Table 1
Referral behavior of family planning provider by institutional setting and characteristics of providers
who refer for abnormal Pap smears
Referring providers from each of the three institutional settings had relatively high overall
referral facilitation scores (indicating that they often engaged in the facilitation activities);
however, referring providers from health departments had significantly higher overall facilitation
scores compared with referring providers from private offices and referring providers from other
types of clinics.
We found significant differences in the use of six of the nine individual facilitation activities by
referring providers from the three different institutional settings: provider referral contact
information, write a referral, remind clients, arrange transportation, follow up with providers,
and follow up with clients (all p<0.05). Specifically, referring providers from health departments
reported engaging in seven of the nine facilitation activities (all activities except calling the
referral provider and making a referral appointment) more than referring providers from other
institutional settings. Referring private office-based providers reported calling referral providers
more frequently than referring providers from other settings. Referring providers from other
clinics reported making referral appointments more than referring providers from other settings.
Referring private office-based providers reporting identifying primary care physicians and
providing referral contact information more than other facilitation activities. Referring health
department providers and referring providers from other clinics reported providing referral
contact information more often than the other facilitation activities. Providers from all three
institutional settings reported identifying a transportation source as the least used facilitation
activity.
Provider referral.
Characteristics associated with provider referral are presented in Table 2. Characteristics related
to the urban/rural nature of the community, institutional setting, and Title X status were
associated with greater odds of referring outside of the practice for follow-up of abnormal Pap
smears as opposed to providing initial treatment within the FP practice/clinic. Specifically,
providers from rural areas, health departments, other clinics, and large patient-volume Title X
practices/clinics had adjusted ORs (AORs) that were statistically significant at the 90% level
(AOR=1.81, 95% confidence interval [CI] 1.08, 3.04; AOR=3.75, 95% CI 1.23, 11.43;
AOR=1.78, 95% CI 1.00, 3.17; and AOR=2.82, 95% CI 0.98, 8.10, respectively) for referring
out abnormal Pap smears compared with their provider counterparts. The wide CIs indicate high
variability in the practice policies on referrals out for follow-up of Pap smears.

Table 2
Characteristics associated with family planning provider referral for and with facilitation of referrals for
abnormal Pap smears
We found a significant difference in the odds of making referrals based on the level of provider
participation in the Medicaid FP program. Providers from practices/clinics with a high Medicaid
FP focus (i.e., practices/clinics with many FP patients with Medicaid coverage) had significantly
lower odds (AOR=0.45, CI 0.25, 0.81) of referring out abnormal Pap smears compared with
providers from practices/clinics with a low Medicaid FP focus (practices/clinics with few FP
patients with Medicaid coverage), controlling for institutional setting.
Provider and practice characteristics not significantly associated with higher or lower odds of
referring out for abnormal Pap smears included perception of patient competence, provider
profession (physician/non-physician), perception of referral resources, relationships with referral
providers, availability of additional direct care staff, availability of patient support staff, and
availability of information support staff.
Provider facilitation.
We asked all providers to indicate the extent to which they would engage in facilitation activities
should they decide to refer a client for an abnormal Pap smear. Provider and practice
characteristics significantly associated with an increased likelihood of facilitating referrals for
abnormal Pap smears included provider profession (physician/non-physician), urban/rural nature
of the community, and institutional setting (Table 2). Specifically, non-physician providers were
significantly more likely to facilitate referrals than physicians. Providers from rural communities
were significantly more likely to facilitate referrals than providers from urban communities.
Providers from both health departments and from other types of clinics were significantly more
likely to facilitate referrals than providers from private practices. In addition, providers from
small patient volume Title X practices/clinics were significantly less likely to facilitate referrals
than providers from small patient volume non-Title X practices/clinics.
Providers' perception of patient competence, available resources, relationships with referral
providers, volume of Medicaid FP clients, and availability of additional direct care staff, patient
support staff, and information support staff were not significantly associated with facilitation
levels for referrals. Again, the wide CI indicated the high variability of responses to this question
across the respondents.
Client survey
Nearly all respondents who reported having an abnormal Pap smear (94%) reported that they
discussed with or learned about the abnormal Pap smear result from their FP provider. Table 3
shows the portion of clients who reported receiving a referral from their FP provider (asked as
Did your FP provider tell you a place that you could go to get care for the condition?), and
who reported seeking and receiving care from other providers for their abnormal Pap smear,
broken out by those who reported being treated or not being treated by their FP provider for the
abnormal test.

Table 3
Client action taken for abnormal Pap smear
Overall, of the 234 respondents who reported having an abnormal Pap smear, 146 received
follow-up care, including 86 who received this care from their FP provider and 60 who received
care elsewhere. This constitutes a 62% follow-up completion rate. However, this rate may be an
overestimate of the follow-up completion rate, because 31 of the 86 clients who were treated by
their FP provider were also referred to another provider for care, but either did not seek or sought
but did not receive that follow-up care. If we consider that their follow-up treatment was not
really complete, then the actual number of completions was 115, constituting a 49% completion
rate. Table 3 also shows that clients who received referrals were more likely to seek care, but
were not necessarily more likely to receive care. Overall, 74% of those who sought care reported
receiving care for the abnormal Pap smear.
Table 4 shows that when other factors are controlled with multivariate analysis, clients receiving
referrals were more likely to seek care from other sources, although those with referrals who had
also received treatment from the FP provider were less likely to seek other care than those who
had not received treatment. We also found trends toward seeking care among clients reporting
high trust in physicians (p=0.05) and those who reported having a usual source of care (p<0.10).
Among those who sought care from a source other than the FP provider, clients were more likely
to report having received care if they had also been treated by their FP provider, if they were
younger than age 30, and if they had some college education. They were less likely to report
receiving care if they perceived themselves to be in poorer health and if they believed that they
could solve new health problems. We noted a trend toward a greater likelihood of receiving care
among those reporting a usual source of care (p=0.06).

Table 4
Client characteristics associated with seeking and receiving treatment for abnormal Pap smear
Go to:
DISCUSSION
To date, little has been known about the referral practices and referral facilitation behaviors of
FP providers for FP clients with abnormal Pap smears or the follow-up action taken by FP clients
who receive referrals from their FP providers. Our study fills this gap by providing several new
findings to the existing literature on this subject.
Among our most important results, we found that private office-based FP providers were
significantly more likely to provide treatment for clients with abnormal Pap smears personally or
within their practice. And, should they make referrals for follow-up care for these abnormal Pap
smears, they were significantly less likely to engage in referral facilitation activities compared
with referring FP providers based in health departments and other types of clinics. Conversely,
we found that health department-based FP providers were significantly more likely to refer
clients with abnormal Pap smear results and less likely to provide treatment.
Referring providers from health departments were significantly more likely to engage in referral
facilitation activities than referring providers from other institutional settings. We also found that
clients who received a referral from their FP provider were more likely to seek care for the
abnormal Pap smear. In addition, clients who actually received some treatment from their FP
provider for abnormal Pap smears along with a referral were more likely to actually receive
additional follow-up care than those who did not receive treatment. This may be because they
were better able to use the resources of the BCCEDP after having received additional diagnostic
procedures from their FP provider. We also found an association between having a usual source
of general medical care and an increased likelihood of seeking and receiving care for an
abnormal Pap smear, suggesting that general access to care issues play a role in Pap smear
follow-up completion rates.
As other studies have suggested, there are several mediating factors that affect clients' receipt of
follow-up care for abnormal Pap smears, no matter what actions are taken by the FP provider.
Women younger than age 30 and women with more college education were most likely to
receive follow-up care. These factors are important, but difficult to alter with an intervention at
the FP provider level. However, we found an association between higher trust in physicians and
a greater likelihood of seeking care, as well as between measures of self-efficacy and being less
likely to seek and receive treatment. The latter finding suggests that clients were not aware of or
convinced of the negative implications of having an abnormal Pap smear. However, given the
positive association found with physician trust, this may indicate an important intervention point
for FP providers to educate patients on these implications.
Health departments are among the largest providers of Title X and Medicaid FP demonstration
waiver services
21,22
and are thus in a position to provide initial cervical cancer screenings for a
substantial number of women. However, health departments are less likely than other providers
to offer additional diagnostic services on-site (e.g., colposcopy)
1315
and do not provide on-site
treatment for precancerous lesions and cervical cancer. Where follow-up treatment is not
available at the FP site, referrals are critical and a driving factor in whether women seek care for
the condition. We found that referring FP providers based in health departments were
significantly more likely to engage in referral facilitation activities compared with referring
providers from other settings. This may be due in part to health department providers' access to
resources available through BCCEDP, which is funded by the Centers for Disease Control and
Prevention but operated by state health departments. Although these programs differ by state,
23

they provide funds for diagnostic services and case management.
6

Other studies have shown that provider facilitation activities, such as those reported by health
department providers in our study, are effective in improving follow-up adherence.
24
Given the
importance of these activities, interventions to increase client follow-up rates should focus on
provider and system features, rather than clients. Such interventions may include educational
programs aimed at improving providers' knowledge of referral resources, or programs aimed at
expanding diagnostic and treatment services within health departments.
Limitations
Our study had several limitations. This study relied on the FP providers' self-report of their
referral and facilitation behavior and on FP clients' report of FP providers' referral and
facilitation behavior. Given the discordance between providers' self-reported behavior (nearly all
reported they treated or referred clients with abnormal Pap smears) and clients' reports of
providers' referral behavior (one-third reported their provider neither treated nor referred them),
these reports may not reflect actual referral and facilitation practices. However, the results may
also reflect a problem in communication between providers and patients.
While our provider survey had a low overall response rate (26%), the response rate among public
providers was much higher (59%). This is important because these providers serve the majority
of the low-income women of interest to this study in Arkansas (79%)
21
and Alabama (71%).
22
In
addition, low response rates from health-care providers compared with the general population are
not uncommon in survey research.
25
Also, because some of the providers to which the instrument
was mailed are no longer practicing, our denominator may be inflated, meaning our true response
rate is higher.
We had a relatively low sample size of those reporting an abnormal Pap smear on the client
survey, thereby limiting the robustness of the multivariate analysis. Also, because the questions
were generic to multiple health conditions, we do not know the content of the treatment that
clients reported receiving for abnormal Pap smears from their FP providers. Thus, it is possible
that clients who reported being treated and also referred elsewhere for care were being referred
based on the results of a colposcopy or other biopsy procedure.
Go to:
CONCLUSIONS
Our study findings indicate that the settings at which most low-income women receive FP
services are precisely those settings that are less likely to provide follow-up care for abnormal
Pap smears on-site. Expanding the availability of additional diagnostic services and treatment for
abnormal Pap smears within health departments may facilitate improvements in follow-up
adherence rates, as well as improve outcomes for many womenin particular, women of
racial/ethnic minority groups who have poorer follow-up adherence rates
9
and higher mortality
from cervical cancer.
26,27
Inclusion of treatment of abnormal Pap smears as a reimbursable
service under Medicaid FP coverage would greatly facilitate provision of this care. However,
given the wide CIs for some variables included in the different multivariate models, further
research in this area is also warranted.
Go to:
Footnotes
This research was supported by the Department of Health and Human Services Office of
Population Affairs, Family Planning Service Delivery Improvement Award 4FPRPA 006018-02.
Go to:
REFERENCES
1. RTI International. Family planning annual report: 2005 national summary. Research Triangle Park (NC):
RTI International; 2006. Nov, [cited 2007 Jan 25]. Also available from: URL:
http://opa.osophs.dhhs.gov/titlex/Final_FPAR_2005_NationalReport_WebPDF.pdf.
2. Gold RB. The Guttmacher Report on Public Policy October. 2003. Medicaid family planning expansions
hit stride; pp. 114.
3. Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M, et al. The 2001 Bethesda System:
terminology for reporting results of cervical cytology. JAMA. 2002;287:21149. [PubMed]
4. Wright TC, Jr, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D. 2006 consensus guidelines
for the management of women with abnormal cervical screening tests [published erratum appears in J
Low Genit Tract Dis 2008;12:255] J Low Genit Tract Dis. 2007;11:20122. [PubMed]
5. Saslow D, Runowicz CD, Solomon D, Moscicki A, Smith RA, Eyre HJ, et al. American Cancer Society
guidelines for the early detection of cervical neoplasia and cancer. CA Cancer J Clin. 2002;52:34262.
[PubMed]
6. Lantz PM, Keeton K, Ramano L, Degroff A. Case management in public health screening programs: the
experience of the National Breast and Cervical Cancer Early Detection Program. J Public Health Manag
Pract. 2004;10:54555. [PubMed]
7. Centers for Disease Control and Prevention (US) 2004 Behavioral Risk Factor Surveillance System
survey data. Atlanta: Department of Health and Human Services (US); 2006.
8. Abercrombie PD. Improving adherence to abnormal Pap smear follow-up. J Obstet Gynecol Neonatal
Nurs. 2001;30:808.
9. Eggleston KS, Coker AL, Das IP, Cordray ST, Luchok KJ. Understanding barriers for adherence to follow-
up care for abnormal Pap tests. J Womens Health (Larchmt) 2007;16:31130. [PubMed]
10. Michielutte R, Diseker RA, Young LD, May WJ. Noncompliance in screening follow-up among family
planning clinic patients with cervical dysplasia. Prev Med. 1985;14:24858. [PubMed]
11. Frost JJ, Frohwirth L, Purcell A. The availability and use of publicly funded family planning clinics: U.S
trends, 19942001. Perspect Sex Reprod Health. 2005;36:20615. [PubMed]
12. Corso LC, Wiesner PJ, Halverson PK, Brown CK. Using the essential services as a foundation for
performance measurement and assessment of local public health systems. J Public Health Manag Pract.
2000;6:118. [PubMed]
13. Finer LB, Darroch JE, Frost JJ. U.S. agencies providing publicly funded contraceptive services in 1999.
Perspect Sex Reprod Health. 2002;34:1524. [PubMed]
14. National Association of County and City Health Officials. 2005 national profile of local health
departments. Washington: NACCHO; 2006. Jul,
15. Lindberg LD, Frost JJ, Sten C, Dailard C. Provision of contraceptive and related services by publicly
funded FP clinics, 2003. Perspect Sex Reprod Health. 2006;38:13947. [PubMed]
16. Dillman DA. Mail and Internet surveys: the Tailored Design Method. 2nd ed. New York: John Wiley &
Sons; 1999.
17. Hall M, Dugan E, Zheng B, Mishra AK. Trust in physicians and medical institutions: what is it, can it be
measured, and does it matter? Milbank Q. 2001;79:61339. [PMC free article] [PubMed]
18. Hibbard JH, Stockard J, Mahoney ER, Tusler M. Development of the Patient Activation Measure
(PAM): conceptualizing and measuring activation in patients and consumers. Health Serv Res. 2004;39(4
Pt I):100526. [PMC free article] [PubMed]
19. ERSI, Inc. ArcView Geographic Information Systems: Version 9.2. Redlands (CA): ERSI, Inc; 2006.
20. SAS Institute, Inc. SAS: Version 9.0. Cary (NC): SAS Institute, Inc; 2003.
21. Felix HC, Stewart MK, Bronstein J, Rickard DL, Bennett JL. Arkansas Medicaid FP waiver services:
what physicians should know. J Arkansas Medical Society. 2007;102:3014.
22. Bronstein JB. Birmingham (AL): School of Public Health, University of Alabama at Birmingham; 2007.
Alabama's Plan First Medicaid demonstration program summary evaluation, demonstration year 6,
October 2005September 2006.
23. Tangka F, Gardner JG, O'Hara B, Turner J, Bauder M. National Breast and Cervical Cancer Early
Detection Program: methods to determine participation of eligible populations. Presented at the UICC
World Cancer Congress; 2006 Jul 812; Washington. [cited 2008 Apr 10]. Also available from: URL:
http://2006.confex.com/uicc/uicc/techprogram/P10154.HTM.
24. Yabroff KR, Kerner JF, Mandelblatt JS. Effectiveness of interventions to improve follow-up after
abnormal cervical cancer screening. Prev Med. 2000;31:42939. [PubMed]
25. Kellerman SE, Herold J. Physician response to surveys: a review of the literature. Am J Prev Med.
2001;20:617. [PubMed]
26. Howell EA, Chen YT, Concato J. Differences in cervical cancer mortality among black and white
women. Obstet Gynecol. 1999;94:50915. [PubMed]
27. Garner EI. Cervical cancer: disparities in screening, treatment, and survival. Cancer Epidemiol
Biomarkers Prev. 2003;12:S2427.

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2006 consensus guidelines for the management of women with abnormal cervical screening
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cancer. [CA Cancer J Clin. 2002]
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and cervical cancer early detection program. [J Public Health Manag Pract. 2004]
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Womens Health (Larchmt). 2007]
Noncompliance in screening follow-up among family planning clinic patients with cervical
dysplasia. [Prev Med. 1985]
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[Perspect Sex Reprod Health. 2004]
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assessment of local public health systems. [J Public Health Manag Pract. 2000]
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Health. 2002]
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[Perspect Sex Reprod Health. 2006]
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matter? [Milbank Q. 2001]
Development of the Patient Activation Measure (PAM): conceptualizing and measuring
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U.S. agencies providing publicly funded contraceptive services in 1999. [Perspect Sex Reprod
Health. 2002]
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[Perspect Sex Reprod Health. 2006]
Case management in public health screening programs: the experience of the national breast
and cervical cancer early detection program. [J Public Health Manag Pract. 2004]
Effectiveness of interventions to improve follow-up after abnormal cervical cancer screening.
[Prev Med. 2000]
Review Physician response to surveys. A review of the literature. [Am J Prev Med. 2001]
Review Understanding barriers for adherence to follow-up care for abnormal pap tests. [J
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Differences in cervical cancer mortality among black and white women. [Obstet Gynecol. 1999]
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BMC Infect Dis >
v.11; 2011 >
PMC3025856

BMC Infect Dis. 2011; 11: 8.
Published online 2011 January 7. doi: 10.1186/1471-2334-11-8
PMCID: PMC3025856
Prevalence and cumulative incidence of
abnormal cervical cytology among HIV-
infected Thai women: a 5.5-year retrospective
cohort study
Amphan Chalermchockcharoenkit,
1
Chenchit Chayachinda,
1
Manopchai Thamkhantho,
1
and
Chulaluk Komoltri
2

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background
Cervical cancer is one of the most common AIDS-related malignancies in Thailand. To prevent
cervical cancer, The US Public Health Service and The Infectious Disease Society of America
have recommended that all HIV-infected women should obtain 2 Pap smears 6 months apart
after the initial HIV diagnosis and, if results of both are normal, should undergo annual
cytological screening. However, there has been no evidence in supporting whether this guideline
is appropriate in all settings - especially in areas where HIV-infected women are living in
resource-constrained condition.
Methods
To determine the appropriate interval of Pap smear screenings for HIV-infected Thai women and
risk factors for subsequent abnormal cervical cytology, we assessed the prevalence, cumulative
incidence and associated factors of cervical cell abnormalities (atypical squamous cell of
undetermined significance or higher grades, ASCUS+) among this group of patients.
Results
The prevalence of ASCUS+ was 15.4% at the first visit, and the cumulative incidence of
ASCUS+ gradually increased to 37% in the first 3.5 years of follow-up appointments (first 7
times), and tended to plateau in the last 2 years. For multivariate correlation analysis, women
with a CD4 count <350 cells/L had a significant correlation with ASCUS+ (P = 0.043). There
were no associations of subsequent ASCUS+ with age, pregnancy, contraceptive method, highly
active anti-retroviral treatment, assumed duration of infection, or the CD4 count nadir level.
Conclusion
There are high prevalence and cumulative incidence of ASCUS+ in HIV-infected Thai women.
With a high lost-to-follow-up rate, an appropriate interval of Pap smear screening cannot be
concluded from the present study. Nevertheless, the HIV-infected Thai women may require more
than two normal semi-annual Pap smears before shifting to routinely annual cytologic screening.
Go to:
Background
Thailand is one of the world's endemic areas for HIV infection. In 2007, approximately 250,000
women were living with HIV infection[1]. Women living with HIV-AIDS clearly have an
increased risk of cervical cancer. A recent study in HIV-infected women in Thailand found that
cervical cancer was the most common AIDS-related malignancy[2]. Sufficient Papanicolaou
(Pap) smear screening would render a high yield in early detection because of its affordability,
availability and accessibility. Cervical squamous cell abnormalities in HIV-infected women,
compared with women who are not infected, progress more rapidly to more significant cervical
intraepithelial neoplasia (CIN) or even invasive cervical cancer[3].
Our previous study indicated that 13.3% of HIV-infected pregnant women had cervical
squamous cell abnormalities[4], while the prevalence of abnormal Pap smears from many studies
seemed to be higher (20%-40%)[5-8]. However, there are different backgrounds. Many studies
reported that cytology was primarily subject to false negative results[3,7,9-12]. Even with a
negative for intraepithelial lesion (NIL) with an initial Pap smear, 20% of HIV-infected women
will be later found with biopsy-confirmed cervical squamous cell intraepithelial lesions (SILs) in
3 years[3]. This may either reflect an incident lesion or reflect a prevalent lesion missed on Pap
smear. Moreover, a study aimed at evaluating the sensitivity and specificity of Pap smears
showed that 38% of all CIN would have been missed if routine colposcopy and biopsy had not
been performed[7].
HIV treatment guidelines issued by The US Public Health Service and The Infectious Disease
Society of America have recommended that all HIV-infected women should obtain two Pap
smears 6 months apart after an initial HIV diagnosis and, if the results of both are normal, these
women should then undergo annual cytologic screening[13]. However, the guideline has not
been revised since 1995 and there has been no evidence to support that this guideline is
appropriate in all settings, especially for HIV-infected women living in resource-constrained
conditions where long-term studies are difficult to conduct. Moreover, currently no national
cervical screening guidelines are in use in Thailand.
For these reasons, semi-annual Pap smear screenings for all HIV-infected Thai women, (not only
women with CD+ 4 counts <200 cells/L), development of health education and improved
efforts to increase the trust between health care providers and women, have been implemented in
our clinic since 2004. The present study aimed to determine an appropriate strategy for Pap
smear screening and risk factors related to subsequent abnormal cervical cytology. Prevalence,
cumulative incidence and associated factors of cervical cell abnormalities (atypical squamous
cell of undetermined significance; ASCUS or higher grades, i.e. atypical squamous cells cannot
exclude high grade squamous intraepithelial lesion; ASC-H, low grade squamous intraepithelial
lesion; LSIL, High grade squamous intraepithelial lesion; HSIL, squamous cell carcinoma)
designated as ASCUS+ among this group of patients were assessed.
Go to:
Methods
With the program implementation of semi-annual Pap smear screening for all HIV-infected
women at the Female Sexually Transmitted Disease Clinic (STD Clinic), Faculty of Medicine
Siriraj Hospital, Mahidol University from January 2004 to December 2009, the STD-medical
records of 901 HIV-infected women were available for review to search for the results from first
Pap smears. In our clinical protocol, all HIV-infected women were counselled to receive baseline
Pap smear screening, and were required to come back for the next screening every 6 months.
Sociodemographic data were collected using a structured medical record form. Blood sample for
CD4+ count was obtained every 6 months. The result was determined in a local laboratory
conducted by the Department of Microbiology in our hospital.
After a clinical and pelvic examination, women with signs of STDs were counselled and treated,
and asked to return to the clinic 2 weeks later for baseline Pap smear screening. All Pap smear
specimens were obtained by gynaecologists from the endocervix, cervical transformation zone
and discharge at posterior fornix of vagina using a cotton tip stick and Ayre spatula, as described
in the VCE technique. Cytological analyses were undertaken at the Division of Cytology of
Department of Obstetrics and Gynaecology, Faculty of Medicine Siriraj Hospital. All Pap smear
tests were processed and read by our certified senior cytotechnologists based on the 2001
Bethesda system guideline[14]. According to our policy, colposcopy must be offered in all cases
of ASCUS+, but due to the occurrence of lost to follow-up, some of them were not able to have
colposcopy. If indicated by colposcopy or cytology results, lesions were further evaluated by
biopsy, endocervical curettage, or loop electrical excision. Definite surgical treatment
(hysterectomy) was provided as indicated[15].
Participants who initially had NIL and came for their second Pap smear screening were included
in the subgroup analysis to assess the cumulative incidence and factors associated with
ASCUS+: namely age, parity, abortion, contraceptive methods, antiretroviral treatment, assumed
duration HIV infection, CD4 count nadir and baseline CD4 count. All women with subsequent
ASCUS/LSIL were not repeatedly enrolled among the rest of the study population. The assumed
duration HIV infection was the duration that was estimated by the patient after counseling and
the CD4 count nadir was the lowest CD4 count recorded. Data entry and analysis was performed
by SPSS version 13 (SPSS, Chicago, IL, USA). Data were presented as frequency, percentage,
mean standard deviation (SD), or median with ranges as appropriate. The cumulative incidence
of ASCUS+ was estimated over the course of this study using standard life table methods. The
student's t-test was used to compare means and Pearson X
2
-test or Fisher's exact test was used to
compare proportions between HIV-infected women with ASCUS+ and NIL at first Pap smear,
and between HIV-infected women with subsequent ASCUS+ and NIL who had a NIL at first
Pap smear. Statistically significant differences were defined as p < 0.05. The Mann Whitney U
test was used for variables that were not normally distributed. Multivariate correlation analysis
was used to adjust for potential confounding factors. The study was conducted in accordant with
the ethics principle of declaration of Helsinki, and the study protocol was approved by the Siriraj
Institutional Review Board.
Go to:
Results
Of 901 HIV-infected women, 80 women were excluded as 18 women did not received Pap smear
screening, 12 women did not have an intact cervix at baseline, 31 women had a previous
diagnosis or treatment of cervical intraepithelial neoplasia, and 19 women had no documentation
of CD4+ count. As a result, 821 women were included in the analysis. The study population had
a mean age of 30.1 years (range 14 - 65), a median baseline CD4 count of 324 cells/L (range 2 -
999) and a median CD4 count nadir of 206 cells/L (range 2 - 930).
Of the 821 women, 237 women (28.9%) had CD4 counts less than 200 cells/L and 395 women
(48.1%) were receiving highly active antiretroviral therapy (HAART). There were 443 women
who initially came to the clinic for antenatal care (ANC), 43 women for postpartum Pap smear
screening, 37 women with STD related problems or positive pre-operative gynaecologic anti-
HIV screening, and 298 women referred from the HIV clinic, Department of Preventive
Medicine, for Pap smear screenings. The Pap smear screening data were from the women's first
12 semi-annual visits (over a period of 5.5 years) and consisted of 2,852 Pap smear tests.
Prevalence of ASCUS+
The prevalence of cervical squamous cell abnormalities from 821 initial Pap smear screenings
was 15.4%, consisting of ASCUS 2.8%, atypical squamous cells cannot exclude high grade
squamous intraepithelial lesion (ASC-H) 0.6%, LSIL 8.5%, and HSIL 3.5% (Table (Table1).1).
The most common coincident genital infection was fungal infection at 19.4% of the women.
Compared with women with NIL, those with ASCUS+ had significantly higher proportions of
receiving HAART and the baseline CD4 count <200 cells/L (58.3% vs. 46.3%, 37.8% vs.
28.2%, respectively). A higher proportion of baseline CD4 count <350 cells/L was also found
in women with ASCUS+ (66.9% vs. 52.4%). In addition they had a significantly longer mean of
assumed duration of HIV infection but a lower mean of CD4 count nadir (7.1 4.1 years vs. 5.9
3.4 years and 188.9 142.7 cells/L vs. 239.9 182.8 cells/L, respectively) as shown in
Table Table22.

Table 1
Frequency of cervical cytological findings at the first visit

Table 2
Comparison of the baseline characteristics of women with ASCUS+ and NIL at first Pap smear
Cumulative incidence of ASCUS+
Of the 444 women who had NIL at initial Pap smear screening and came for the second test, the
cumulative incidence of ASCUS+ was 15%. The cumulative incidence was gradually increased
in the first 7 visits to 37% and tended to plateau in the last 4 visits (Figure (Figure1).1). There
was a median follow-up time of 12 months when the first ASCUS+ was detected. The mean and
median number of Pap smears per patient was 2.7 and 2.0, respectively. None of the patients got
pregnant during the follow-up visits in this study. There was no statistical difference between
development of ASCUS+ from NIL in terms of age, number of abortions, contraceptive methods,
receiving HAART, assumed duration of HIV infection, or CD4 count nadir level. However, the
proportion of multipara women and women with CD4 count < 200 cells/L showed statistically
significant differences between the two groups (84.2% vs. 72.8%, p 0.022; 37.9% vs.20.9%, p =
0.016, respectively). In addition the proportion of women with CD4 count < 350 cells/L was
still significantly higher (62.1% vs.48.4%, p = 0.018)(Table 0.018)(Table3).3). By multivariate
correlation analysis, adjusted for multiparity women and CD4 count < 350 demonstrated that the
CD4 count <350 cells/L was the only significant risk factor for developing subsequent
ASCUS+ (p = 0.043).

Figure 1
Cumulative incidence of ASCUS+.

Table 3
Comparison of the baseline characteristics of women with subsequent ASCUS+ and NIL who
had a NIL at first Pap smear
Colposcopic and histologic diagnosis of ASCUS+
Of the 95 women with subsequent ASCUS+, 16 (16.8%) had ASCUS, 1 (1.1%) had ASC-H, 60
(63.2%) had LSIL and 18 (18.9%) had HSIL (data not shown). Seventy six women were able to
undergo colposcopic investigation and 19 of them (25.0%) were subsequently colposcopically-
diagnosed CIN II-III (Table (Table4).4). Nineteen of twenty-four women who were
colposcopically diagnosed CINII-III and/or cytologically diagnosed HSIL were able to undergo
loop electrical excision procedure of cervix (LEEP) or cold knife conization at this hospital.
There were histological assessments which confirmed CIN II-III in 12/19 (63%) and invasive
squamous carcinoma in 1/19 (5.3%).

Table 4
Colposcopic results in women with abnormal Pap smears
Go to:
Discussion
This is the first long-term retrospective cohort study of cervical squamous cell abnormalities in
HIV-infected Thai women. It is well recognized that women with HIV infections have a higher
prevalence, incidence, persistence, and progression of squamous intraepithelial lesions as
compared with those without the infection. The prevalence of cervical squamous cell
abnormalities and SILs in the present study was similar to that in our previous study[4].
Compared with several previous studies[5-8], the result of Pap smear screenings from the present
study showed a slightly lower prevalence (15.4% vs.20%-40%). In addition to the different
backgrounds, this may be due to the fact that the majority of participants in this study were either
ante-partum, or immediate postpartum.
Interestingly, the cumulative incidence of ASCUS+ in the present study gradually increased to
37% in the first 3.5 years of follow-up appointments (first 7 times) and tended to plateau in the
last 2 years. In addition, one woman with cytological diagnosis of HSIL and with a histologic
diagnosis of CINIII was diagnosed from the Pap smear at her seventh follow-up appointment.
Comparable with this study, a previous study found that among HIV- infected women whose
initial Pap smear was negative for intraepithelial lesion (NIL), about 20%-35% of them would
develop cytologic abnormalities over 3.0-5.5 years[3]. This supports the fact that there is a high
rate of false negative Pap smear results among HIV-infected patients, as mentioned in a previous
study[16]. The findings prompted us to reconsider the appropriate interval of Pap smear
screenings for HIV-infected women as recommended by The US Public Health Service and The
Infectious Disease Society of America in our setting. Our population might require more than
two normal semi-annual Pap smear before shifting to annual cytologic screening. As the present
study had high drop-out rate in the first 2 years, we believe that the real incidence of ASCUS+
might be higher. Previous studies have base analysis on less frequent Pap smears than ours; some
of them did not pay sufficient attention to the lag period which is supposed to play an important
part in cervical carcinogenesis.
Many studies demonstrated that women with a CD4 count < 200 cells/L were at particular risk
of cervical cell abnormalities[4,16-19]. This means that immunological status also plays a crucial
part in cervical carcinogenesis. We found that the women with ASCUS+ had significantly higher
proportions of receiving HAART than those with NIL. This is the most likely reflection that
these women had an underlying poor immune status by their own merit without any correlation
of HAART. The CD4 count cut-off point that we used to predict cumulative incidence of
ASCUS+ was 350 cells/L, which is compatible with a study from Brazil[19]. Recently, the Thai
Ministry of Public Health initiates HAART for all HIV-infected patients who have CD4 counts
at this level or lower. The CD4 counts < 200 cells/L seem to be far too low to detect new
ASCUS+ cases and may be too low for basing a decision to initiate HAART regimen. However,
we did not look at the change of CD4 count and its impact on cumulative incidence of ASCUS+.
A well-designed study demonstrated that the incidence of SILs increased with time, especially
the ones with lower CD4 count and oncogenic HPV infection[17]. In addition, a study from Italy
with 132 HIV-infected women who had invasive cervical cancer (ICC) showed that the interval
between the first HIV-positive test and invasive cancer diagnosis was longer than 10 years in
almost half of the women[20]. We also found that the assumed duration of HIV infection and the
CD4 count nadir level were associated with a high prevalence of ASCUS+ from the initial Pap
smear. However, they were not associated with the cumulative incidence of ASCUS+.
In the present study only 0.1% (1/821) of HIV-infected women had invasive squamous cell
carcinoma. This woman had a baseline CD4 count of 148 cells/L and had a 14-year duration
assumed HIV infection. She had a cytologic HSIL at the third Pap smear and colposcopic
diagnosis of HSIL. With a lower incidence of invasive squamous cell carcinoma, our study may
not represent the whole picture of HIV-infected women in Thailand - since the incidence in this
study was lower than the figure reported from a previous study conducted in Thailand[21]. A
high number of women were already on HAART at commencement of the study. HAART might
have beneficially protective on preventing cervical carcinogenesis[22,23]. More important
reasons were the early detection by a regular semi-annual check-up, the development of health
education, and the growth of trust between health care providers and patients. Smoking was not
included in the baseline characteristics because almost all Thai women were not current or ex-
smokers.
Several studies are currently investigating the benefits of adding HPV DNA tests to improve
screening for cervical lesions and cancer - as screening for oncogenic HPV types is a more
sensitive predictor of high grade squamous intra-epithelial lesions. Overall, the HPV test had a
higher sensitivity among HIV-infected women as compared with HIV-uninfected women. One
study in Thailand reported that the prevalence of high risk HPV infection in Thai HIV-
seropositive women was 38.6%[21], which was lower than that found in American (83.2%) and
Brazilian women (44.5%)[24,25]. However, HPV DNA testing is not a routine screening test in
this clinic due to its high cost. In addition, the specificity for cervical lesions of the test was low
in HIV-infected women, resulting largely from a very high prevalence of HPV infection in
women without cervical lesions. Thus, a HPV test may not provide benefits for cervical
surveillance in the setting of HIV, because of its low specificity and poor predictive
value[26,27].
In 1999, Holcomp, et al. demonstrated the significance of ASCUS in HIV-infected women by
comparing cytological and histological results[28]. They found that 32% of ASCUS had
histological cervical intraepithelial neoplasia (CIN). As a result, they suggested that early
colposcopy should be considered in HIV infected women with ASCUS. There were a total of 16
women with ASCUS in our study, 14 were able to undergo colposcopy and 10 had colposcopic
diagnosis of SILs (9 women with HPV/CIN I and 1 woman with CIN II-III) (Table (Table4).4).
Although our study demonstrated that there was a high incidence of colposcopic diagnosis of
SILs in women with ASCUS, only one woman in this group had colposcopic diagnosis of CIN
II-III which had to be confirmed by tissue diagnosis. Since most of them had colposcopic
diagnosis of HPV/CIN I and had a low socio-economic background, it was unlikely that biopsies
with pathological reports in these cases could be met.
There were a number of limitations in the present study that warranted mentioning. (1) The
primary outcome was mainly the surrogate outcome of cervical cancer. Even though the
incidence of abnormal lesions was high, these were mainly low grade lesions which could be
regression, especially in younger women[29]. (2) False negative Pap smear was not included in
the scope of the present study and this might have impact the findings as a previous study found
a high false negative Pap smear rate in HIV-infected women with CD4 count < 500 cells/L[16].
(3) The lack of viral load, colposcopy with tissue biopsy could not be performed in all cases;
instead, a 'see and treat' technique was applied in order to decrease costs. (4) Due to the
government universal coverage program and limited seats at Siriraj Hospital, many participants,
especially a number in our study who were either ante-partum, or immediate post partum, were
required to follow-up at their registered hospitals causing 250 women to be lost to follow up by
the 6 month visit (36%) and a further 133 (20%) lost at 12 months. This is a loss of over 50% of
study participants in the first year of follow-up. In addition, an effort to try to establish some
relationship between health care providers and HIV- infected women was very difficult because
of stigmatization of HIV. As a consequence, the rate of follow-up was quite low leading to the
potential biases, such as survivorship bias/retention in care. In addition, other AIDS-indicated
conditions and established risk factors of cervical cancer were not accounted for and there was
one patient who died from an opportunistic infection during the follow-up period.
Go to:
Conclusions
There are high prevalence and cumulative incidence of ASCUS+ in HIV-infected Thai women.
With a high lost-to-follow-up rate, an appropriate interval of Pap smear screening cannot be
concluded from the present study. Nevertheless, the HIV-infected Thai women may require more
than two normal semi-annual Pap smears before shifting to routinely annual cytologic screening.
Go to:
Competing interests
The authors declare that they have no competing interests.
Go to:
Authors' contributions
AC and CC took initiative in developing the research project, and drafted the manuscript. AC
participated in the design of the study. AC and CK participated in the data analysis. AC, CC and
MT participated in the writing of the manuscript. All authors read and approved the final
manuscript.
Go to:
Pre-publication history
The pre-publication history for this paper can be accessed here:
http://www.biomedcentral.com/1471-2334/11/8/prepub
Go to:
Acknowledgements
This study was financially supported by a Grant from Faculty of Medicine Siriraj Hospital,
Mahidol University. The authors deeply appreciate the contribution of all the staff nurses at the
Female STD Clinic, Department of Obstetrics and Gynaecology, Siriraj Hospital, Mahidol
University for their dedicated work.
Go to:
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PMC3139476

J Cancer Educ. Author manuscript; available in PMC 2011 July 19.
Published in final edited form as:
J Cancer Educ. 2009; 24(2): 114119.
doi: 10.1080/08858190902854590
PMCID: PMC3139476
NIHMSID: NIHMS153568
Cervical Cancer Attitudes and BeliefsA
Cape Town Community Responds on World
Cancer Day
MAGHBOEBA MOSAVEL, PHD, CHRISTIAN SIMON, PHD, CATHERINE OAKAR, BA, and SALOME MEYER,
MW, UCT
Author information Copyright and License information
See other articles in PMC that cite the published article.
Go to:
Abstract
Background
Attitudes and beliefs affect womens cervical cancer screening behavior.
Methods
We surveyed 228 women in Cape Town, South Africa about their screening history, knowledge,
beliefs, and access barriers regarding Papanicolaou (Pap) smears and cervical cancer.
Results
More than half of the participants had never had a Pap smear or had 1 more than 10 years ago.
One third did not know what a Pap smear was. Lengthy wait times and fatalistic beliefs also
affected screening behavior. Ethnicity was associated with differences in beliefs.
Conclusions
Opportunistic cancer screening events are an effective way that women can obtain Pap smears
and cancer education.
Cervical cancer is the second most common cancer in women worldwide
1
and the most common
cancer among women in developing countries.
2
In South Africa, where this study was conducted,
cervical cancer is the most common cancer in Black women.
3,4
Significant disparities exist
between Black and White women. Peltzer (2001) found that 60.5% of Black women had never
received a Papanicolaou (Pap) smear, whereas only 8.4% of White women never had (P <
.0001).
5
A study in South Africa found that women having a Pap smear were associated with
70% lower odds of cervical cancer when compared to women who have never been tested.
6

Research has demonstrated that South African women who are less likely to know about and
obtain Pap smears tend to be poorer, less educated, and unemployed.
7
Recognizing the disparities
in incidence and mortality rates, the South African National Department of Health has introduced
a screening policy that provides a free Pap smear every 10 years to women 30 and older.
8
It has
been suggested that the new South African policy of 3 Pap smears per woman at the age of 30,
40, and 50 may reduce the incidence of cancer by as much as 87%.
9

A variety of factors influence womens screening practices for cervical cancer. Accessibility,
costs, wait time, and quality of services serve as major barriers to routine screening.
10-12
The
discomfort associated with the procedure and an overall distrust of the medical system can also
affect screening behavior.
13-15
Furthermore, characteristics of health providers, such as negative
attitudes
16
or a lack of suggesting that a woman obtain a Pap smear,
17
also play an important role.
Additionally, research has demonstrated that womens knowledge about cervical cancer and Pap
screening is extremely low in developing countries,
18
and knowledge among immigrant women
in the Western world is equally poor.
19
In Africa, although knowledge about cervical cancer has
generally been linked to education and socioeconomic status,
16,20-22
a survey of well-educated
women
10
revealed a lack of adequate knowledge of the disease or a lack of perceived personal
risk of getting cervical cancer.
23
Nonetheless, cultural beliefs about cervical cancer also
contribute to low screening rates. Many of the rural South African women surveyed by Lartey et
al.
17
and others
24
felt that screening is unnecessary when a woman does not feel ill. Certain
ethnic groups, including Latina,
25
Korean American,
26
and African American women,
27-29
may
be more likely to entertain fatalistic beliefs about cancer, preventing them from seeking
appropriate preventative care. Similar to women in South Africa,
24
women in Botswana
reportedly viewed cervical cancer as a disease that eats the inside of a womb, and associated
hysterectomy with loss of sexual pleasure, divorce, and failure to get a husband.
16
To therefore
eliminate access barriers and educate women about the fundamental need to get screened, it is
crucial to identify how the combination of these factors influences womens screening behavior.
In this article, we report on a survey that investigated access to and knowledge about Pap smears
and cervical cancer in a peri-urban community in Cape Town, South Africa. Along with other
local agencies, we were approached by the Cancer Association of South Africa to participate in
outreach activities on World Cancer Day celebrated on February 5, 2005. Events included free
cancer screening tests for women and men at the local clinic, cancer support groups, a press
conference, and an open community event featuring various speakers at the local sports ground.
The community in which we administered the survey is 1 of the few in South Africa where
Blacks and Coloreds are integrated. (Although the Population Registration Act of 1950, which
authorized registration by race, was repealed in 1991, our use of these racial categories reflects
the historical background of participants, their continued attempts at self-identification, and the
remaining legacy of apartheid. Black refers to indigenous people of South Africa who speak 1
of the Bantu languages as their native language. Colored refers to people considered to be of
mixed race, classified as such by the former apartheid government of South Africa.) We used
this health promotion event as an opportunity to administer a survey designed to obtain local data
on knowledge, attitudes, and access issues related to Pap smears and cervical cancer. This
information is critical in enhancing the development of effective screening programs for
urbanized, resource-poor communities.
Go to:
MATERIALS AND METHODS
Instrument Selection and Design
The development of this survey was partly informed by previous work on attitudes and beliefs
about cervical cancer,
24,30
which included items that measure feelings of embarrassment,
fatalistic beliefs, and attitudes toward general prevention behavior. There were 12 close-ended
and 4 open-ended questions (16 total). The close-ended questions assessed prior history of
having a Pap smear, reasons for not having a Pap smear, and attitudes toward Pap smears. The
open-ended questions asked participants to specify (1) what a Pap smear was, (2) the reasons that
may have prevented them from obtaining a Pap smear in the past, (3) why they decided to have a
Pap smear, and (4) how they heard about the free screenings. Prior to survey administration, we
tested the questions with 6 community residents to ensure comprehension and cultural
sensitivity. Staff at the Cancer Association of South Africa also reviewed the questions and
provided feedback.
We hired an ethnically and linguistically diverse team of 5 community members to administer
the survey. We received formal approval from our local institutional review board to conduct the
survey. The surveys were professionally translated into, and administered in, the native language
of the participant (English, Afrikaans, or Xhosa).
Sample
We administered the survey to separate samples drawn from 2 events on World Cancer Day. We
interviewed 228 women, 156 at the local clinic and 72 at the community event. No incentive was
offered to participants. The first cluster was approached by interviewers at the clinic while they
were waiting in line to be registered for the free cancer screening. Eligible women had to wait in
line to receive their screening test. We administered our surveys during a 3 hour waiting period.
Of those women asked to participate in the survey, 90% agreed. Most respondents surveyed at
the clinic were Colored (63%) and 34% were Black.
1
The second sample was drawn from those
who attended the open community event on cancer prevention. Of those who attended the
community events, 56% were Black and 44% were Colored.
Data Analysis
Descriptive statistics were performed on the survey data to identify the distribution of answers to
each question. We used SPSS version 12.0 for the quantitative analyses. We examined (1) Pap
smear knowledge and history; (2) attitudes and beliefs about Pap smears, cervical cancer, and
prevention; and (3) barriers to obtaining a Pap smear. When differences are statistically
significant, we report the data for the clinic and community sample and for Blacks and Coloreds
separately.
For the open-ended questions, we developed coding categories that captured the key themes.
Responses were first discussed and grouped into similar clusters. Next, we defined these
categories into more specific groupings and pretested this coding pattern. Based on these results,
changes were made to the categories. A final test of the codes was performed, and there was 98%
agreement between the coders.
Go to:
RESULTS
A total of 228 women participated in this study. Most of the women (57%) answered the
questions in Afrikaans (n = 129), 39% in Xhosa (n = 89), and 4% in English (n = 10). Most of
the women interviewed identified as Colored (59%) or Black (41%). The average age reported
for the sample was 42 (median = 41; SD = 11.5). The age of the clinic women averaged 42 years
(SD = 10.9; range, 20-71), and the women interviewed at the community event averaged 43
years (SD = 12.7; range, 21-84).
Pap Smear History and Knowledge
Table 1 presents the Pap smear history, knowledge, access barriers, and attitudes and beliefs in
the total sample and in clinic and community participants separately. Table 2 summarizes those
questions that had significant differences in Colored and Black womens responses.

Table 1
Clinic and Community Responses

Table 2
Responses by Ethnicity
Pap Smear History
More than one third of women (34%) reported that they had never had a Pap smear, although
22% of the sample said their last Pap smear was more than 10 years ago. Of the 77 (34%)
women in the combined sample who never had a Pap smear, the average age was 39.5 years
(median = 37; SD = 13.4). Moreover, most (68%) of those who never had a Pap smear were
Black (
2
1
= 32.8, P < .001).
Pap Smear Knowledge
We asked all women in the study (N = 228) through a close-ended question if they knew what a
Pap smear was. Most of the clinic (63%) and community participants (71%) were knowledgeable
about a Pap smear (see Table 1).
Of those who knew what a Pap smear was, 22% explained in an open-ended question that it was
to check if something was wrong with the womb. However, others said that a Pap smear was to
test for cancer (22%), that it was preventive and important for the maintenance of womens
health (15%), or that they associated a Pap smear with pregnancy (4%).
A Pearson
2
test indicated that having had a Pap smear in the past was strongly correlated with
knowledge about Pap smears (
2
X
= 112.9, P < .001). Furthermore, more Colored women than
Black women knew what a Pap smear was (
2
1
= 15.9, P < .001; see Table 2).
Access
We asked close-ended questions about barriers to obtaining a Pap smear related to wait time,
child care, and clinic access. Among all of the participants, more than half (54%) agreed with the
statement, One has to wait too long to get an appointment before you can get a Pap smear, and
over one third (34%) indicated that they not know where to go to have a Pap smear (see Table 1).
Through an open-ended question, we asked participants to explain what may have prevented
them from obtaining a Pap smear prior to the opportunistic screening event held in their
community. Most women (59%) said that there was no particular reason that prevented them
from having a Pap smear in the past. Others (16%) cited personal reasons, such as fear or being
very busy. Some (12%) said that the South African policy of waiting for 10 years
7
between Pap
smears prevented them from obtaining one earlier, whereas others (9%) said that access issues,
such as wait time or inability to pay, and family reasons, such as taking care of children, made it
too difficult.
A Pearson
2
test (categorical by categorical) determined that clinic (63%) and community (36%)
participants differed significantly in their answers to the question regarding wait time (
2
X
=
14.3, P < .001), as did Colored (69%) and Black (33%) women (
2
X
= 28.3, P < .001). However,
more Black (52%) than Colored women (22%) agreed with the statement, I did not know where
to go to get a Pap smear (
2
1
= 21.0, P < .001; see Table 2).
Attitudes and Beliefs
Both groups were asked 6 close-ended questions regarding their attitudes and beliefs about Pap
smears and cervical cancer. Slightly more than half (52%) agreed with the statement, If I am
meant to get cervical cancer, I will get itthat is fate. Yet, only 17% reported, I am afraid of
hospitals/clinics, and Its embarrassing to get a Pap smear (see Table 1).
We used the Pearson
2
statistic to determine differences between Coloreds and Blacks on
attitudes and beliefs about cervical cancer. Significantly, more Colored than Black women
reported that Its embarrassing to get a Pap smear, and Id rather not know if I have cervical
cancer (
2
X
= 24.3, P < .001;
2
X
= 11.5, P < .001, respectively). However, almost half of the
Black women (49%) said I dont like to be examined by the doctor, whereas only 36% of
Colored women agreed with that statement (
2
1
= 4.0, P = .045; see Table 2).
Sources of Event Information
Finally, participants indicated that they had heard about the World Cancer Day events from a
variety of sources. Most (46%) heard from staff at the clinic. Others (13%) learned about it by
written materials, such as flyers, posters, or local newspapers (13%); word of mouth from
neighbors, family, and friends (13%); community activities (12%); radio (6%); bullhorn
announcements (5%); and schools (4%).
Go to:
DISCUSSION
In this study, we examined the knowledge, access barriers, and beliefs related to Pap smears and
cervical cancer of women attending cancer awareness events in a peri-urban community in Cape
Town, South Africa. As part of the days activities, 175 women were able to receive a free Pap
smear at the local health clinic, and many attended an open community event on cancer
education. At both the clinic and community events, we surveyed a total of 228 women. The
strong attendance at both these events could be an indication of the openness of women in this
community to health outreach efforts as well as their compelling need for cancer education and
accessible preventive services.
Particularly relevant given the high cervical cancer incidence in South Africa is that at least half
of study participants have never had a Pap smear or had one more than 10 years ago. In addition,
knowledge about Pap smears and cervical cancer prevention in this community appears far from
optimal. One third of the total sample did not know what a Pap smear was, whereas others
interpreted a Pap smear as a method for cleaning of the womb. This finding is consistent with
other studies that many South African women construct cervical cancer in nonmedical terms and
rarely use the term cervix in reference to cervical cancer.
24
However, several women in our study
reported knowing that the Pap smear was a test for cancer or that it was preventative and
important for the maintenance of womens health. Certainly, this finding has important
implications for cancer education efforts in that it suggests that some women in this community
are thinking of preventing illness as a first step instead of waiting for illness to occur and then
treating it.
In addition, the fatalistic attitudes and beliefs regarding cervical cancer screening resonate with
previous findings on fatalism and cervical cancer in the South African
24,31
as well as US
32-34

contexts. Our data add to this scenario the possibility that fatalism is only part of the picture:
Despite some suggestions from surveyed participants that nothing could be done if they
developed cancer, many women in our study were still proactively seeking a Pap smear and
waiting in line for several hours to obtain it. Although fatalism is often associated with
passiveness and lack of interest in health care,
26,35
our data suggest that the issue could be more
complex. This is especially encouraging to cancer education efforts in resource-poor settings. It
suggests that the apparent incongruence in belief and subsequent behavior might suggest that
fatalistic attitudes may be more of an expression of access issues and other obstacles rather than
an unwavering belief about cancer prevention or a lack of desire or capacity for proactive health
care.
Our study findings also point to the legacy of apartheid in shaping the differential knowledge
levels and access to resources between Blacks and Coloreds. Fewer Black women knew what a
Pap smear was, had a Pap smear previously, knew that it was necessary to have a Pap smear, or
knew where to obtain a Pap smear. These differences most likely reflect that Blacks are more
recently urbanized than Coloreds, tend to frame female and other disorders in more traditional
and not biomedical vocabulary,
24
and may have fewer resources and less time available to access
health care. Interestingly, though, more Colored women said it is embarrassing to have a Pap
smear and that they would rather not know if they had cervical cancer. Consequently, there is a
great need for cancer education and prevention in South Africa to account for, and respond
appropriately to, these differences and overall access barriers, attitudes, and beliefs about Pap
smears and cervical cancer.
Nevertheless, that so many women were present to obtain free Pap smears and learn about cancer
has positive implications for opportunistic cancer interventions. For example, whereas 63% of
clinic participants reported that One has to wait too long to get an appointment before you can
get a Pap smear, only 36% of community participants did. This most likely suggests that those
women who previously had trouble obtaining a Pap smear appointment took advantage of the
free screenings that day and were thus more represented in the clinic group. Second, the strong
attendance suggests that these women may be receptive to cancer education and willing to act on
it. Third, it may suggest that even women with alternative constructions of cancer may hold
positive attitudes toward cancer prevention. Fourth, and perhaps most important of all, our study
findings suggest that cancer screenings for low-income women may need to be promoted within
the broader context of womens health. It is likely that if outreach efforts are focused on only
cancer screening, they will appeal to a different audience than efforts aimed at addressing
womens general health. More women are likely to respond and benefit from integrated health
outreach efforts and in this way, allay their cancer-related fears and uncertainties in a broader
health context.
Ideally, women from low-income and resource-poor communities can obtain Pap smears through
opportunistic events such as World Cancer Day. Certainly, this screening is the first step to
preventing cervical cancer. However, it is essential to question what happens after these women
obtain a Pap smear. What if their results are abnormal? What if they need treatment? Future
research and future screening programs must focus not only on reaching underserved women but
also on processing Pap smears, returning results as rapidly as possible, having an efficient means
of follow-up and referral for patients, creating and designating treatment centers that can provide
treatment for early lesions, and creating a system that deals with women with advanced disease.
36

Additionally, cervical cancer prevention programs and future research need to address the
complexities of what women may mean by responses such as, No reason prevented me from
obtaining a Pap smear. One possible explanation is that the survey administration setting (the
waiting lines) did not lend itself to obtaining more detailed and nuanced information from
participants on this issue. The data could also simply mean that the main reason why these
women did not get a Pap smear before is that they were not aware that it was in their best interest
to do so or that they could not think of anything else to say. Future studies also need to include
women who do not participate in cancer education events such as World Cancer Day, as they
perhaps represent a cluster most in need of cancer education and screening.
Finally, the direction for future cancer outreach efforts in this community is indicated by the fact
that most clinic women in our study learned of the screening event from clinic staff. This may
suggest that many of these women or their family members had received other services at the
clinic. At the very least, it suggests that the clinic staff have community influence and credibility.
The importance of social networks
37
and the influence of significant others to increase a
womans likelihood to obtain screening has been noted elsewhere.
13
Furthermore, other sources
such as family, media, and direct marketing efforts indicate the potential and impact of using
multiple informants in outreach and cancer education efforts.
Go to:
ACKNOWLEDGEMENTS
The authors acknowledge and appreciate the dedicated commitment of their research team in
South Africa. We also sincerely thank the women who participated in this study.
Supported by an NIH NCI R25 Prevention Research Educational Postdoctoral Training Grant,
and supplementary funding was provided by the Case Comprehensive Cancer Center in
Cleveland, Ohio.
Go to:
References
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Obstet. 1997;58:137. [PubMed]
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108. [PubMed]
3. CANSA [Accessed March 3, 2005];Cervical Cancer: Numbers and Incidence. Available at:
http://www.cansa.co.za/registry_cervix.asp.
4. Bradshaw D, Nannan N, Laubscher R, et al. South African National Burden of Disease Study 2000,
Estimates of Provincial Mortality. South African Medical Research Council; Cape Town, South Africa:
2004.
5. Peltzer K. Breast Self-examination and Cervical (Pap) smear test: attitudes and practices among South
African Women. Psychological Reports. 2001;89:2732. [PubMed]
6. Hoffman A, Cooper D, Carrara H, et al. Limited Pap screening associated with reduced risk of cervical
cancer in South Africa. Int J Epidemiol. 2003;32:573577. [PubMed]
7. Bradley J, Risi L, Denny L. Widening the cervical cancer screening net in a South African township: who
are the underserved? Health Care Women Int. 2004;25:227241. [PubMed]
8. Department of Health National Guideline on Cervical Cancer Screening Program. The Department of
Health; South Africa: Dec, 2002.
9. Hatch KD, Berek JS. Intraepithelial disease of the cervix, vagina, and vulva. In: Berek JS, editor. Novaks
Gynecology. 13th ed Lippincott Williams & Wilkins; Philadelphia, PA: 2002. pp. 478479.
10. Adanu RM. Cervical cancer knowledge and screening in Accra, Ghana. J Womens Health (Larchmt)
2002;11:487488.
11. Agurto I, Bishop A, Sanchez G, Betancourt Z, Robles S. Perceived barriers and benefits to cervical
cancer screening in Latin America. Prev Med. 2004;39:9198. [PubMed]
12. Coronado GD, Thompson B, Koepsell TD, Schwartz SM, McLerran D. Use of Pap test among Hispanics
and non-Hispanic whites in a rural setting. Prev Med. 2004;38:713722. [PubMed]
13. Jernigan JC, Trauth JM, Neal-Fergus D, Cartier-Ulrich C. Factors that influence cancer screening in
older African American men and women: focus group findings. Fam Community Health. 2001;24(3):27
33. [PubMed]
14. Buki LP, Borrayo EA, Feigal BM, Carrillo IY. Are all Latinas the same? Perceived breast cancer
screening barriers and facilitative conditions. Psychol Women Q. 2004;28:400411.
15. Byrd TL, Peterson SK, Chavez LR, Heckert A. Cervical cancer screening beliefs among young Hispanic
women. Prev Med. 2004;38:192197. [PubMed]
16. McFarland DM. Cervical cancer and Pap smear screening in Botswana: knowledge and perceptions.
Int Nurs Rev. 2003;50:167175. [PubMed]
17. Lartey M, Joubert G, Cronje HS. Knowledge, attitudes and practices of rural women in South Africa
regardding the Pap smear. Int J Gynaecol Obstet. 2003;83:315316. [PubMed]
18. Adanu R. Cervical cancer knowledge and screening in Accra, Ghana. J Womens Health (Larchmt)
2002;11:487488.
19. McMullin JM, De Alba I, Chavez LR, Hubbell FA. Influence of beliefs about cervical cancer etiology on
Pap smear use among Latina immigrants. Ethn Health. 2005;10:318. [PubMed]
20. Abrahams N, Wood K, Jewkes R. Research report. Medical Research Council and Centre for
Epidemiological Research of South AfricaWomens Health; Cape Town, South Africa: 1996. Cervical
Screening in Montagu District: Womens Experiences, Coverage, and Barriers to Uptake.
21. Pillay AL. Rural and urban South African womens awareness of cancers of the breast and cervix.
Ethn Health. 2002;7:103114. [PubMed]
22. Wellensiek N, Moodley M, Moodley J, Nkwanyana N. Knowledge of cervical cancer screening and use
of cervical screening facilities among women from various socioeconomic backgrounds in Durban,
Kwazulu Natal, South Africa. Int J Gynecol Cancer. 2002;12:376382. [PubMed]
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Med J. 1998;75:411416. [PubMed]
24. Wood K, Jewkes R, Abrahams N. Cleaning the womb: constructions of cervical screening and womb
cancer among rural black women in South Africa. Soc Sci Med. 1997 July;45:283294. [PubMed]
25. Chavez LR, Hubbell FA, Mishra SI, Valdez RB. The influence of fatalism on self-reported use of
Papanicolaou smears. Am J Prev Med. 1997;13:418424. [PubMed]
26. Lee M. Knowledge, barriers, and motivators related to cervical cancer screening among Korean-
American women. Cancer Nurs. 2000;23:168175. [PubMed]
27. Mayo RM, Ureda JR, Parker VG. Importance of fatalism in understanding mammography screening in
rural elderly women. J Women Aging. 2001;13:5772. [PubMed]
28. Phillips J, Cohen M, Moses G. Breast cancer screening and African American women: fear, fatalism,
and silence. Oncol Nurs Forum. 1999;26:561571. [PubMed]
29. Scroggins TG, Bartley TK. Enhancing cancer control: assessing cancer knowledge, attitudes, and
beliefs in disadvantaged communities. J La State Med Soc. 1999;151:202208. [PubMed]
30. Schulmeister L, Lifsey DS. Cervical cancer screening knowledge, behaviors, and beliefs of Vietnamese
women. Oncol Nurs Forum. 1999;26:879887. [PubMed]
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urban settlement. S Afr Med J. 1996;86:11851188. [PubMed]
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papanicolaou smears. Am J Prev Med. 1997;13:418424. [PubMed]
33. Baileff A. Cervical screening: patients negative attitudes and experiences. Nurs Stand.
2000;14(44):3537. [PubMed]
34. Matin M, LeBaron S. Attitudes toward cervical cancer screening among Muslim women: a pilot
study. Womens Health. 2004;39:6377.
35. Reynolds D. Cervical cancer in Hispanic/Latino women. Clin J Oncol Nurs. 2004;8:146150. [PubMed]
36. Miller A. Report on consensus conference on cervical cancer screening and management. Int J
Cancer. 2000;86:440447. [PubMed]
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Screening for cervical cancer: a review of women's attitudes, knowledge, and behaviour. [Br J
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v.7; 2010 >
PMC2848216

Virol J. 2010; 7: 65.
Published online 2010 March 22. doi: 10.1186/1743-422X-7-65
PMCID: PMC2848216
Prevalence of various Human Papillomavirus
(HPV) genotypes among women who
subjected to routine Pap smear test in
Bushehr city (South west of Iran)2008-2009
Keivan Zandi,
1
Seyed Sajjad Eghbali,
1
Rasool Hamkar,
2
Shahnaz Ahmadi,
1
Elissa ramedani,
1

Iman Deilami,
1
Heidar Aziz Nejad,
1
Fatemeh Farshadpour,
1
and Zahra Rastian
1

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background
Some genotypes of human papillomaviruses can infect the genital tract and they are important
infectious agents which their oncogenicity is regardable. Thus the aim of this study was to
determine the prevalence of various genital human papillomaviruses (HPV) among women being
subjected to routine pap smear test in Bushehr city of Iran.
Results
Based on the collected data, 11(5.5%) samples were detected positive for HPV DNA and
189(94.5%) samples out of 200 samples were detected negative for HPV DNA. Meanwhile
4(2%) samples detected positive for HPV DNA by PCR were detected positive for HPV by pap
smear test as well. On the other hand 5 samples which were detected positive for HPV by pap
smear test didn't have HPV DNA after being tested by PCR method. Among the 11 positive
samples 7 samples were identified as HPV-16, 3 samples were HPV-18 and one was HPV-53.
Conclusion
Regarding the prevalence of highly carcinogen genotypes of HPV in our study determination of
genital HPV prevalence among the normal population of women of Bushehr city is
recommended.
Go to:
Background
Worldwide, cervical cancer is the second most common cancer affecting women. Nowadays
screening programs have reduced the mortality and morbidity of this disease, but 500,000 new
cases of invasive cancer of the cervix are still diagnosed annually. Epidemiological and
molecular studies have demonstrated that certain types of human Papillomaviruses (Highly
carcinogen genotypes) are the major cause of most cases of cervical cancer [1].
Human papillomaviruses (HPVs) belong to Papillomaviridaefamily[2]. So far, 118 types have
been identified according to their biological niche, oncogenic potential and Phylogenetic
position. There are about 40 HPV viral types that are commonly found in the genital tract which
are classified in the Alphapapillomavirus genus[3,4]. On the basis of molecular epidemiologic
evidence, genital HPV types have been subdivided in to low-risk types and high-risk ones [5,6].
Several HPV types, such as HPVs 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59 and 66 have been
implicated in cervical carcinogenesis (high risk types), whereas other types, such as HPVs 6 and
11, are frequently detected in benign lesions such as condylomata acuminate [1]. Women
infected with high risk HPV types are considered to be at a higher risk for the development of
cervical cancer than those who are not infected with HPV or are infected with low risk HPV
types [6].
HPV-16 is the most prevalent type worldwide [7-9]. HPV18, 45, 31 and 33 are the next most
prevalent types. In Asia, HPV58 and HPV52 are the next most common after HPV16 and 18[9].
HPV infection by multiple genotypes has been reported to occur in 10% to 20% of HPV-positive
cases [10]. These epidemiologic findings in combination with follow-up studies often
demonstrate the role of certain HPV types in cervical cancer development [1,11-13].
HPV DNA testing has been used as an adjunct to Pap smear cytology test in the diagnosis of
cervical cancers to improve screening sensitivity and negative predictive value [11-13]. In fact,
HPV DNA PCR is now recommended for patients with cytological abnormalities based on the
new American College of Obstetricians and Gynecologists guidelines [14]. In addition, the
importance of HPV genotyping in diagnostic practices is increasingly recognized in
distinguishing high-risk from low-risk infections as well as in the development of cancer
intervention strategies such as vaccine preparation[9,10]. Therefore, genotyping of HPV in
clinical settings is regarded as an important diagnostic tool for cervical cancer, and also as means
for providing valuable information necessary for its prevention and treatment.
In this study, we determined the prevalence of various HPV genotypes among the women
subjected to routine Pap smear test in Abolfazl outpatient clinic of Bushehr University of
Medical Sciences, Iran, by PCR and subsequent sequencing. Cytological diagnoses were also
done on all samples based on the new Bethesda system.
Go to:
Methods
This study has been approved by the Ethical Committee of Bushehr University of Medical
Sciences.
Two hundred samples were collected from women admitted at Abolfazl outpatient clinic in
Bushehr and voluntarily subjected to gynecological examination by gynecologist from 2008 to
2009. Two Samples were collected from each patient by cytobrush: one for Pap-smear test for
detection of cytopahic effects of HPV and another one for HPV DNA PCR assay which was
stored at -20C until PCR test time.
DNA Extraction
All samples were subjected to centrifugation 2000 rpm for 5 minutes and precipitated cells were
digested using digestion buffer containing proteinase K, followed by extensive extraction with
phenol/chloroform [15]. The extracted DNA was stored at 4C until tasted. DNA quality was
evaluated by PCR using forward primer PCO3: 5'-ACACAACTGTGTTCACTAGC-3' and
reverse primer PCO4: 5'-CAACTTCATCCACGTTCACC-3' that amplify a 110 bp product from
the human -Globin gene[12].
HPV PCR
-Globin positive samples were subjected to HPV PCR by forward primer GP5+: 5'-
TTTGTTACTGTGGTAGATACTAC-3' and reverse primer GP6+:5'-
AAAAATAAACTGTAAATCATATTC-3' for L1 open reading frame (ORF) that amplifies a
150 bp product from the HPV L1 ORF [12]. PCR was performed according to the procedure
described previously[12]. Extracted DNA from HeLa cell line was used as HPV positive control
and no DNA was added for negative control. Samples were subsequently subjected to agarose
gel electrophoresis.
DNA Sequencing Assay
HPV positive PCR products were subjected for automated sequencing (Kawsar Biotech Co.,
Tehran, Iran). Nucleotide sequences were aligned with CLUSTALW program using BioEdit
software (BioEdit Sequence Alignment Editor Software, Department of Microbiology, North
California State University) and confirmed by visual inspection. Genetic distance was estimated
using the Kimura two-parameter matrix[16]. A phylogenetic tree was constructed by the
neighbor-joining (NJ) method[17]. Bootstrap resampling and reconstruction were carried out
1000 times to confirm the reliability of the phylogenetic tree[18]. The analysis and calculated
nucleotide differences within and between the isolate sequences were carried out by MEGA
program, version 4[19]. The nucleotide sequences of HPV isolates reported in this article can be
found in the GenBank database under accession numbers GU076513 through GU076523.
Statistical Analysis
Data was processed by SPSS 16 Package program for statistical analysis (Chicago, IL, USA).
Go to:
Results
The result of HPV DNA PCR for collected samples revealed that there were 11(5.5%) samples
with HPV DNA by using general primers for all genotypes of HPV. The result of genotyping
based on MEGA software using which is based on genetic distances and phylogenetic tree
informations (Table (Table1)1) showed that 7 samples out of 11 HPV DNA positive samples
were detected as HPV-16, three samples were identified as HPV-18 and one sample was detected
as HPV-53.

Table 1
Results of Sequencing for amplified L1 ORF of HPV Positive Samples
Results of pap smear showed that 9(4%) samples were detected as HPV positive meanwhile 4 of
them were detected as HPV DNA positive by PCR method. On the other hand 7 samples which
identified as HPV DNA positive by PCR method were negative for HPV infection when they
investigated by pap smear test.
Mean of age for HPV infected women were 31.9 years old and it is concordant with the sexual
active age which is very important for incidence of any kind of genital infections. The youngest
one was 24 years old and the oldest one was 44 years old.
Based on clinical findings of HPV positive women we have found that five HPV infected women
didn't have any clinical manifestations and there was no evidence for cervisitis and/or genital
warts. Six women out of 11 HPV infected individuals have shown acute cervisitis but there was
no sign related to genital warts and just one women showed the cervisitis and gentital warts
together.
Besides, among five women who were detected positive for HPV infection by pap smear
meanwhile they were detected negative for HPV infection by PCR method we have found that
just two of them showed acute cervisitis without any genital warts manifestation.
By using SPSS software and regarding to the collected data, the sensitivity of pap smear test
comparing to PCR method in our study was calculated 36.36%(95% Confidence Interval = 6.91-
65.43). Besides the specificity value of our pap smear test was 97.35(95% Confidence Interval =
94.57-99.43).
Go to:
Discussion and Conclusion
Cervical cancer is an invasive cancer affecting approximately 500000 women each year of whom
80% live in developing countries. The vast majority of cervical cancer cases are caused by
infection with certain genotypes of human papillomaviruses[1].
Pap smears for the detection of cytomorphologically abnormal cells have decreased the number
of deaths from cervical cancer but have not eradicate the disease in any screened population to
date[13,20]. cervical cytology is considered to be a very specific test for high grade pre
cancerous leisions or cancer but even if the quality of collection and spreading of cells, fixation,
and staining of smears, and reporting by well trained technicians and cytophatologists are good
it's sensitivity is only moderate[21]. The result of meta analysis suggest that cytological
screening has a very wide range of sensitivity to detect lesions[12]; for example, cytology is
estimated to have mean sensitivity of 58% and a mean specificity of 69% in one study[12].
There is international consensus that "high risk" genotypes, including genotypes
16,18,31,33,35,39,45,51,52,56,58,59 and 66 can lead to cervical cancer. Infections with low risk
genotypes, including 6, 11, ... can cause benign or low grade cervical tissue changes and genital
warts[1,15,22]. HPV can not be cultured in vitro, thus analysis of DNA sequences can be used to
identify HPV genotypes. PCR and in situ hybridization are two of the most sensitive
methods[15]. The detection of HPV in cervical biopsies using these methods in conjunction with
cytology could potentially improve screening for cervical cancer[15]. In this study we used the
PCR method for initial detection of HPV and regarding to our facilities sequencing of the PCR
products were performed by automated sequencing instead of in situ hybridization in order to
genotyping of HPVs.
By using PCR, it was revealed that out of 200 samples, there were 11 (5.5%) positive samples
for HPV DNA but there were only 4 (2%) positive samples with HPV related cytopathologic
evaluation.
Based on results, seven samples (3.5%) were detected as negative for HPV by cytopathology
method meanwhile they were positive for HPV DNA by PCR method. Such results express the
false negativity of cytophatologic method. On the other hand five samples (2.5%) were
recognized positive by cytopathology method for HPV, meanwhile they were negative for HPV
DNA by using PCR method. This result confirmed the false positivity of cytopathologic
methods. The sensitivity and specificity of cytopathology method in our study were 36.36% and
97.35% respectivly. Meanwhile in one study these criteria were reported as 58% and 64%,
respectively [23]. In our study the prevalence of HPV was 11(5.5%) in 200 samples but in other
study the HPV prevalence was 34.6 in Zagreb region and also the presence of HPV DNA was
99.7% in women with histologically confirmed SCC [24]. In one study in Mazandaran province
(Iran) 33 (78%) cases were HPV positive based on PCR screening in cancerous group [15]. The
difference in result of these studies could be due to type of patients and the sample size. As it is
mentioned in results section five HPV infected women didn't show any clinical manifestations
such as cervisitis or genital warts. Also, just in one HPV infected women genital warts was
detected beside the acute cervisitis so we can conclude that HPV infections can occur without
any significant symptoms and we couldn't rely on clinical manifestations and/or cytopathological
examinations such as Pap smear test. Also, using colposcopy technique is recommended for
further clinical investigations.
Out of 11 positive samples for HPV DNA 7 samples were HPV-16, determined by genotyping
method, meanwhile 3 samples were HPV-18 and one sample was recognized as HPV-53. This
showed that HPV-16 is the most prevalent type among high risk HPV in Bushehr city. Also the
prevalent type of HPV in most studies was reported HPV-16 [7-9,21]. So as high-risk HPV types
has correlation with cervical cancer, there is daily increase in need of screening test for women at
risk of HPV infection [11-13,21]. Also, based on our and other studies results, using the PCR
method for the detection of HPV infection is recommended.
Go to:
Competing interests
The authors declare that they have no competing interests.
Go to:
Authors' contributions
KZ and RH designed and conceived the PCR test. SSE performed the pap smear test ER, ID and
SA have collected the samples. HA, ZR and FF co operated as lab staff for PCR performing. We
confirm that all authors read and approved the final manuscript.
Go to:
Acknowledgements
We thank Dr. Iraj Nabipour for providing us laboratory facilities during our projects and his
invaluable comments.
Go to:
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PMC3032635

Health Care Women Int. Author manuscript; available in PMC 2011 December 1.
Published in final edited form as:
Health Care Women Int. 2010 December; 31(12): 10681081.
doi: 10.1080/07399332.2010.499183
PMCID: PMC3032635
NIHMSID: NIHMS265670
Socioeconomic factors, immigration status,
and cancer screening among Mexican
American women aged 75 and older
Carlos A. Reyes-Ortiz, MD, PhD
a
and Kyriakos S. Markides, PhD
b

Author information Copyright and License information
The publisher's final edited version of this article is available at Health Care Women Int
Go to:
Abstract
To explore the association between socioeconomic factors and acculturation with cancer
screening methods, we analyzed data from the Hispanic Established Population for the
Epidemiologic Study of the Elderly, on 1,272 women aged 75 and older residing in the United
States in 2004-2005. We found that lower Pap smear or mammography uses were associated
with older age, lower education, and having public health insurance compared to private. Other
factors associated with mammography use were depressive symptoms, cognition and functional
limitations. In sum, socioeconomic factors and health insurance coverage determine cancer
screening utilization in very old Mexican American women but not acculturation.
Keywords: Mammography, Pap Smear, Hispanic EPESE, Older Women, Cancer Screening
Hispanic American women have the highest invasive cervical cancer incidence rates of any
group other than Vietnamese American women (American Cancer Society, 2009; Parker, Davis,
Wingo, Ries, & Heath, 1998). Underutilization of Pap smear screening in this population is the
main factor related to higher mortality from cervical cancer among Hispanic women residing in
the United States (US) (Parker, et al, 1998) or Latin America as well as women residing in
developing countries (Arrossi, Sankaranarayanan & Parkin, 2003; Sankaranarayanan, Budukh &
Rajkumar, 2001). On the other hand, even though Hispanic women have lower rates of breast
cancer compared to non-Hispanic white women or black women, breast cancer is the leading
cause of cancer death among Hispanic women (American Cancer Society, 2009; Parker et al.,
1998). Similarly, underutilization of a mammography for screening is also a crucial factor for
late detection of breast cancer among Hispanic women residing in the US (Parker, et al, 1998) or
Latin America as well as women residing in developing countries (Robles & Galanis, 2002;
Bosetti, Malvezzi, Chatenoud, Negri, Levi & La Vecchia, 2005).
Overall, older Hispanic women have higher incidence rates of cervical cancer but lower
incidence rates of breast cancer than older non-Hispanic white women in the US. Indeed,
Hispanic women aged 65+ have higher incidence rates of cervical cancer than women of the
same age from any other ethnic group (SEER, 2006). By contrast, Hispanic women aged 65+
have lower incidence rates of breast cancer than older white and black women but higher rates
than American Indian and Pacific Islander origin women. Finally, older Hispanic women have
lower screening rates than other ethnic groups in the US (Wu, Black, Freeman, & Markides,
2001). Factors related to the lower rates of screening services utilization among older Hispanic
women include poverty, lack of insurance, low education, limited access to health care,
acculturation levels and barriers related to language, culture, and negative provider attitudes (Wu
et al., 2001; Suarez, Ramirez, Villarreal, Marti, McAlister, Talavera, Trapido & Perez-Stable,
2000; Coughlin & Uhler, 2002; Randolph, Freeman, & Freeman, 2002; Peek, 2003; Rodriguez,
Ward, & Perez-Stable, 2005; Palmer, Fernandez, Tortolero-Luna, Gonzales, & Dolan Mullen,
2005; Valdez, Banerjee, Ackerson, Fernandez, Otero-Sabogal & Somkin, 2001; Zambrana,
Breen, Fox, & Gutierrez-Mohamed, 1999; Kagay, Quale, & Smith-Bindman, 2006; Reyes-Ortiz,
Freeman, Pelez, Markides, & Goodwin, 2006; Reyes-Ortiz, Camacho, Amador, Velez,
Ottenbacher & Markides, 2007); however, most studies are focused on adult Hispanic women
and there are not studies related to cancer screening utilization in the very old Hispanic women
(75+). In 2000, people of Mexican origin were the largest Hispanic group United States,
representing 59% (21 million) of the countrys total Hispanic population (United States Census
Bureau, 2004).
The objective of the authors was to explore the association between socioeconomic factors, and
acculturation levels with Pap smear and mammography use among older Mexican American
women aged 75 years and older. The hypotheses are, first, that women with low socioeconomic
status (SES) tend to have lower screening rates compared to women with high SES, and second,
that older women who are US born tend to have higher cancer screening use rates than foreign
born.
Go to:
Method
Data set and sample
The Hispanic Established Population for the Epidemiologic Study of the Elderly is a community
based study that originally included 3,050 (1,758 women) Mexican Americans aged 65+ at the
1993-94 baseline survey. The sample was designed to be representative of approximately
500,000 older Mexican Americans living in five southwestern states including California,
Arizona, New Mexico, Colorado, and Texas (Markides, Rudkin, Angel, & Espino, 1997). The
study protocol was approved by the University of Texas Medical Branch Institutional Review
Board, and written consent forms were obtained from each participant. The surviving cohort at
Wave 5 in 2004-2005 includes 741 women (from a total of 1,167 persons) aged 75+. Also, at
Wave 5 a new representative cohort of 531 women (from a total of 902 persons) aged 75+ from
the same region was added to the original cohort. A total sample for this analysis includes 1,272
women aged 75+.
Measures
Our conceptual model is a modification of the Behavioral Model of Health Services Utilization
(Andersen, 1995), and proposes that cancer screening utilizations (as health outcomes) are
determined by predisposing characteristics of individuals and their environments (age, marital
status, education, country of birth, and language preference- as measure of acculturation); factors
that enable or impede utilization (income, financial strain, health insurance, functional status,
cognitive status, and affective status); and perceived and/or evaluated need for health services
(comorbidity, and history of cancer).
Outcomes
The outcomes were mammography use and Pap smear use (yes/no) during the two years prior to
the interview.
Independent Variables
Socioeconomic variables included education (0-5 years vs. >5), total annual household income
(<$10,000 vs. $10,000), health insurance (none, public (Medicare or Medicaid) or private
(HMO), and financial strain (difficulty in meeting monthly bills, yes/no). Acculturation refers to
the process by which immigrants adopt the attitudes, values, customs, beliefs, and behaviors of
their new culture. Among Hispanic immigrants to the US, these changes may include increases
in smoking, obesity, and alcohol intake and decreases in dietary quality and physical activity
(Lara, Gamboa, Kahramanian, Morales & Bautista, 2005). As a proxy measure of acculturation
we included place of birth (foreign or the US), and language at interview (Spanish or English).
We created these three categories for acculturation measure: foreign born (the less acculturated);
US born & Spanish; and US born & English. Other demographic variables included age and
marital status. A variable was created to distinguish the old versus the new cohort.
Medical conditions were assessed asking participants if they had ever been told by a doctor that
they had diabetes, heart attack, stroke, and hypertension. A summary score was created, from 0
to 4; and dichotomized as 0-1 vs. 2. Cancer was used as separated variable (yes/no). Functional
status was assessed by ten Instrumental Activities of Daily Living (IADL) items (range 0-10),
included use the telephone, drive the car or travel alone, go shopping for groceries or clothes,
prepare own meals, do light housework, take own medicine, handle own money, do heavy work
around the house, walk up and down stairs, and walk half a mile. IADL was dichotomized as 0-3
vs. 4 (Fillenbaum, 1985). Depressive symptoms were measured by the Center for
Epidemiologic Studies Depression Scale (CES-D) (Radloff, 1977), (range 0-60), and
dichotomized as depressed (16) vs. non-depressed (<16). Cognitive function was assessed
with the Mini-Mental State Examination (MMSE) (Folstein, Folstein, & McHugh, 1975), (range
0-30), and dichotomized as 18 vs. >18.
Data Analysis
We used the Chi-square/ Fisher test to assess bivariate associations between the outcomes
(mammography or Pap smear use) and other variables. A graphics was used to describe the
distribution of percentages of the outcomes by age and health insurance status. Multivariate
logistic regression analyses were used to test the association between the outcomes with the
independent variables. All analyses were performed using the SAS System for Windows, version
9.1.3 (SAS Institute, Inc., Cary, NC), significance level was set at p<0.05, two-tailed.
Go to:
Results
Table 1 shows the study population. A quarter (n=316; 25%) was aged 85+. Half of the
population (n=651; 51%) had up to 5 years of education, 27% (n=347) were married, 46%
(n=590) had income <$10,000/ year, 56% (n=711) reported financial strain, 4% (n=52) were
uninsured and 43% (n=550) were foreign born. A third (n=402; 32%) of women had 2 or more
medical conditions, 7% (n=84) had cancer, 50% (n=637) had 4 or more IADL limitations, 22%
(n=271) had high depressive symptoms, and 29% (n=365) had a MMSE of 18 or less.

Table 1
Study population, Mexican American women aged 75 and older, United States, 2004-2005
(N=1,272)
Figure shows the percentage of screening methods by age and insurance categories. There is an
association of insurance status with both Pap smear (p=0.0025) and mammography use
(p=0.0019) at age 75-79, where being uninsured had the lowest percentages of screening and
being on private insurance had the highest. In the other groups, there was only effect on
mammography use (p=0.0200) at age 80-84, and no effect at age 85+. When comparing the
uninsured group to the insured group (public or private), uninsured participants tend to be
younger (<85 yr vs. 85+, p=0.0419), foreign born (vs. US born Spanish or English speaking,
p=0.0019), part of the new cohort (containing more recent immigrants, p=0.0054), and in the
lower income category (p=0.0002).
Table 2 shows the prevalence of Pap smear and mammography use according to
sociodemographic and health variables. Women with higher Pap smear prevalence were
younger, married, highly educated, with higher income, without financial strain, on private
insurance, with lower number of functional limitations, with high MMSE score, and from the
new cohort. Women with higher mammography prevalence were younger, married, highly
educated, with higher income, without financial strain, on private insurance, with lower number
of functional limitations, with cancer or with a higher number of medical conditions, and with
high MMSE score. Thus, main factors associated with both Pap smear and mammography use in
bivariate analyses were predisposing factors such as age and education, enabling factors such as
income, financial strain, health insurance, functional status, and cognitive status, and health
needs perception factors such as history of cancer.

Table 2
Prevalence of Pap smear and mammography in the previous 2 years among Mexican American
women aged 75 and older, United States, 2004-2005
Table 3 shows the multivariate logistic regression analyses for predictors of Pap smear and
mammography use among older Mexican American women. Lower Pap smear use was
associated with older age (85+ vs. 75-79), lower education (<5 yr. vs. 5), financial strain, and
having public health insurance compared to private. Lower mammography use was associated
with older age (80-84 or 85+ vs. 75-79), lower education, lower income (<10,000/ yr vs.
10,000), having public health insurance compared to private, having 4 or more instrumental
activities of daily living limitations, or having a low MMSE score. In contrast, higher
mammography use was associated with having history of cancer, and higher depressive
symptoms. Immigration status and language use were not associated with either Pap smear or
mammography use. Thus, main factors associated with mammography use in multivariate
analyses were predisposing factors such as age and education, enabling factors such as income,
health insurance, functional status, depressive symptoms and cognitive status, and health needs
perception factors such as history of cancer. By contrast, factors associated with Pap smear use
in multivariate analyses were only predisposing factors such as age and education, and enabling
factors such as financial strain and health insurance.

Table 3
Multivariate logistic regression analyses, predictors of Pap smear and mammography use in the
previous 2 years among Mexican American women aged 75 and older, United States, 2004-2005
Go to:
Discussion
In this study we explored the relationship between socioeconomic factors and acculturation with
cancer screening utilization among Mexican American women aged 75+. According to our
conceptual model, predisposing characteristics of Mexican American older women such as age
and education have influences on both Pap smear and mammography use; enabling factors such
as insurance and socioeconomic status (income or financial strain) have influences on both Pap
smear and mammography use; however, other enabling factors such as functional status,
depressive symptoms and cognitive status have an influence on mammography use but not on
Pap smear use.
General guidelines for Pap smear use state that women who have an intact cervix and who are in
good health should continue cervical cancer screening until age 70; however, cancer screening
after age 70 is recommended for women in good health who have not been previously screened,
women for whom information about previous screening is unavailable, and for whom past
screening is unlikely (Smith, Cokkinides, Brooks, Saslow & Brawley, 2010). We have an overall
prevalence of 37% (n=454) for Pap smear in women aged 75+ in the past 2 years. In a
predominantly white population (79%, n=1,693; 8%, n=171 were Hispanic women), women
aged 70+ had a prevalence of 77% (n=1,659) for a Pap smear in the past 3 years (Walter,
Lindquist, & Covinsky, 2004). In a population of Mexican American women aged 50-74; there
was a prevalence of Pap smear for 64% (n=289) in the past two years (Randolph et al., 2002).
For mammography use, no specific upper age has been established. The decision to continue
mammography screening should be individualized base on the potential benefits and risks of
screening in the context of health status and estimated longevity (Smith et al., 2010; Walter &
Covinsky, 2001; Kapp, Lemaster, Zweig & Mehr, 2008). In our study we have an overall
prevalence of 49% (n=599) for a mammography; while the Medicare Current Beneficiary Survey
has a prevalence of 27% (n=628) for a mammography in the last 2 years among women 75+
(Blustein & Weiss, 1998); however, their data were collected when just Medicare instituted
biennial coverage for screening mammography for older women. In another study, 78%
(n=3,115) of women aged 70+ had a mammography in the past 2 years (Walter et al., 2004). By
age groups, women in our study tend to have lower breast cancer screening rates than in other
studies. Our prevalence for a mammography was 48% (n=176) for age 80-84 and 33% (n=100)
for age 85+, while the prevalence was of 58% (n=302) and 40% (n=145) in the National Health
Interview Survey during 2000 (Schonberg, McCarthy, Davis, Phillips, & Hamel, 2004), and 54%
(n=410) and 42% (n=319) in the Asset and Health Dynamics among the oldest old (AHEAD)
study during 2000 (Ostbye, Greenberg, Taylor, & Lee, 2003) respectively for those age ranges.
Having private insurance was an important predictor for both Pap smear and mammography use
in this study and agrees with other studies (Blustein, 1995; Ostbye et al., 2003; Rodriguez et al.,
2005; Reyes-Ortiz et al., 2006; Reyes-Ortiz, Velez, Camacho, Ottenbacher, & Markides, 2008).
In another study, lack of insurance coverage was associated with low utilization rates for Pap
smear and a mammogram among young Latinas in California (Rodriguez et al., 2005). Older
women from the AHEAD study (white and black population), where nearly all participants were
insured by Medicare, those who had additional private insurance were more likely to have a Pap
smear or a mammogram in the last two years (Ostbye et al., 2003). Similarly, women aged 65+
having Medicare coverage but lacking supplemental health insurance were less likely to undergo
mammography (Blustein, 1995).
In our study, there was not an effect of nativity status or language use at the interview as
measure of acculturation - on Pap smear or mammography use; in agreement with another study
(Borrayo & Guarnaccia, 2000), but in disagreement with other studies (Goel et al., 2003;
Rodriguez et al., 2005; Tsui, Saraiya, Thompson, Dey, & Richardson, 2007). At younger ages,
foreign-born Hispanic women had the highest rates of never being screened with mammography
and Pap smears when compared with US-born Hispanic women and non-Hispanic white women
(Rodriguez et al., 2005). In a predominantly younger sample (79% n=25,599 aged <60 years),
foreign-born Hispanic women were less likely to report cervical cancer screening than US-born
Hispanic women (Goel et al., 2003).
Our findings that lower education level and financial strain or low income was associated with
lower Pap smear or mammography use agree with other studies (Rodriguez et al., 2005; Ostbye
et al., 2003; Schonberg et al., 2004; Reyes-Ortiz et al., 2007). Our findings where history of
cancer, IADL limitations or lower cognition was associated with lower odds for a mammography
also agree with other studies (Caplan & Haynes, 1996; Marwill, Freund, & Barry, 1996; Blustein
& Weiss, 1998; Legg, Fauber, & Ozcan, 2003; Ostbye et al., 2003; Schonberg et al., 2004).
Very old age remained an important factor for lower cancer screening use in our study and
agrees with other studies including older women (Mandelblat et al., 1999; Randolph et al., 2002;
Reyes-Ortiz et al., 2006, 2008). According to Blustein and Weiss (1998), older women are less
likely to be screened because of womens preferences (low interest in potentially life-prolonging
medical procedures), access factors (fewer resources or social support), or physicians behaviors
(less offer of procedures to the oldest old). According to Ostbye et al. (2003), the age-related
pattern of decline for screening might be explained by other physicians factors such as
considering weak recommendations and little evidence of effect of screening in older women, or
diminishing importance of finding asymptomatic disease in participants with established illness.
In addition, randomized controlled trials do not provide evidence for or against screening
mammography in women who are 75+ because older women are not included in the trials
(Walter, Lewis, & Barton, 2005).
This study has some limitations. Data on mammography use and Pap smear use were self-
reported, and we could not distinguish between screening and diagnostic procedures. Our cross-
sectional analyses could not establish causal order between certain variables and screening use.
Also, income information was incomplete and we kept an additional category for missing values.
However, we used other socioeconomic measures such as education and financial strain that are
usually well correlated to income or other socioeconomic measures. On the other hand, our study
may help to understand that even in the very old population socioeconomic barriers may affect
screening utilization. Having public insurance is not enough to get a screening method, and
indicating that access to health care is a complex issue in the very old population. In addition, the
recent economic recession may make worst the influence of health insurance status or other SES
factors on screening utilization in these Mexican American women and perhaps in other
underserved populations (Lavarreda, Brown, Cabezas & Roby, 2009).
In conclusion, socioeconomic deprivation (low income or education, and financial strain), health
insurance coverage, functional status or cognitive and affective problems determine screening
utilization in very old Mexican American women but not acculturation. Further studies need to
explore the influence of insurance status coverage and other socioeconomic factors on cancer
screening utilization among older women in Latin American countries or other world areas.
Go to:
Acknowledgements
This project was supported by the Network for Multicultural Research on Health and Healthcare,
Department of Family Medicine, David Geffen School of Medicine, University of California Los
Angeles (U.C.L.A) funded by the Robert Wood Johnson Foundation. The sponsors had no role in
the design, methods, data collection, and analysis, interpretation of data, decision for submission
or writing of the manuscript. The interpretation and reporting of these data are the sole
responsibilities of the authors. Preliminary findings of this work were presented at the American
Public Health Association 136
th
Annual Meeting, San Diego, CA, October 28, 2008
Go to:
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Related citations in PubMed
Comparing acculturation scales and their relationship to cancer screening among older
Mexican-American women. [J Natl Cancer Inst Monogr. 1995]
Pap smear and mammogram screening in Mexican-American women: the effects of
acculturation. [Am J Public Health. 1994]
Prevalence and associated factors of cancer screening: why are so many older Mexican
American women never screened? [Prev Med. 2001]
Factors influencing cancer screening practices of underserved women. [J Am Acad Nurse
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Int J Prev Med >
v.3(8); Aug 2012 >
PMC3429807

Int J Prev Med. 2012 August; 3(8): 585590.
PMCID: PMC3429807
The Effect of Education on Women's Practice
Based on the Health Belief Model About Pap
Smear Test
Asiyeh Pirzadeh and Maryam Amidi Mazaheri
Author information Article notes Copyright and License information
Go to:
Abstract
Introduction:
Cervical cancer is the most common gynecological cancer in Iran. The single most effective tool
in reducing death due to cervical cancer is the use of pap smear as a screening tool. Therefore,
the aim of this study was to determine the effectiveness of education based on Health Belief
Model about giving pap smear in women.
Methods:
This quasi-experimental study was performed on 70 women who referred to two health center in
Kouhdasht (Lorestan- Iran). The samples were randomly divided in two groups (35 in
intervention group and 35 in control group). The data were collected by a validated and reliable
questionnaire. Interventions were run based on Health Belief Model during three sessions only
for intervention group. Each educational session was for 4560 min. The independent t-test and
paired t-test were used to analyze data. A two-tailed P value lower than 0.05 was considered
statistically significant.
Result:
According to results, the mean scores of knowledge were significantly different between two
groups after intervention (P < 0.001). The mean scores of the model variables (perceived
susceptibility and severity, perceived benefits, and barriers) had no significant difference in the
two groups before intervention, but after intervention had significant difference between the two
groups (P < 0.001).
Conclusion:
Designing and executing health education programs based on health belief model can promote
the practice of women regarding to pap smear tests.
Keywords: Health belief model, pap smear test, woman
Go to:
INTRODUCTION
Cervical cancer is one of the most common forms of carcinoma among women worldwide, and
80% of these cases occurring in developing and undeveloped countries.[1] Cervical cancer is
largely preventable by effective screening programs.
The single most effective tool in reducing death due to cervical cancer is the use of pap smear as
a screening tool.[2] Regular screening with the Papanicolaou (Pap) test may reduce cervical
cancer mortality by as much as 98%.[3,4]
Although other studies of Asian women found that lack of knowledge about cancer risk factors
resulted in failure to get pap smears.[5] In other hand, some of the other research found that
sociocultural barriers such as embarrassment for pelvic examination and individuals beliefs
about the causes and significance of cervical cancer may lead to lack of using pap smear test or
not.[57]
Cervical cancer is the most common gynecological cancer in Iran,[8] where various methods of
screening, diagnosis, and treatment have been reported.[9,10] However, since there is no lucid
system to document the data on cancers, there are no clear reports of incidence and prevalence of
cervical cancer in Iran.
Although cervical cancer is of high concern in Iran, and the level of screening test is
unacceptable, few studies have been carried out to determine why women do not refer to
participate in pap smear test, and education is efficient to persuade Iranian women to participate
in this test.
One of the behavioral models can describe this matter is Health Belief Model.
This model, which emerged in the late 1950s, was used as an exploratory model to assess why
people did not use preventive health services and eventually to understand why people use or fail
to use health services.[11] HBM consists of various constructs including perceived susceptibility,
severity, barriers, and benefits, cues to action, and health action.[11]
Many researchers now employ this model to guide the development of health interventions with
the aim of changing behaviors,[12] and effectiveness of this model has approved in many
research.[13,14] Shojaeezadeh et al. performed a quasi-experimental study in hamadanian
women which revealed that health education based on HBM can enhance women's knowledge of
cervical cancer, change their health beliefs, and improve their behaviors (giving pap smear
test).[15] Therefore, the aim of this study was to determine the effectiveness of education using
Health Belief Model on practice of women regarding pap smear in Kouhdasht (Lorestan-Iran),
20102011.
Go to:
METHODS
This is a quasi-experimental study, performed on 70 women who referred to two health center in
Kouhdasht (Lorestan- Iran).
Inclusion criteria of married women who never had a pap test and women who could not
understand the questions were excluded from study. The samples were randomly divided in two
groups (35 in intervention group and 35 in control group). There was no difference between the
two groups in age, job, and education level. A self-administered questionnaire was designed by
the researchers. The questionnaire was divided into four sections: demographic data (3
questions), knowledge (21 questions), HBM model constructs (57 questions) including 15
questions on perceived susceptibility, perceived severity, perceived benefits, each part (5
questions), perceived barriers (8 questions), cues to action (3 questions), and practice (1
question). Likert scoring method was used to assess the answers as follows: (certainly agree = 4,
agree = 3, no idea = 2, disagree = 1, and certainly disagree = 0) and the score range for every
section was 0 to 100.
For knowledge section, one score was given to each correct answer. The score for wrong
answers was zero. Finally, practice and behavior of participants were assessed by yes and no
question.
We allocated score 1 and 0 to yes and no answers about practice, respectively.
The reliability of questionnaire was determined by Cronbach's alpha, which was in the range of
0.600.83.
The questionnaires were distributed in two groups one week before the intervention and one
month after the intervention. Interventions were run based on Health Belief Model during three
sessions in health center only for intervention group. In first session, health educator informed
them about cervical cancer and causes of this cancer and tried to promote perceived
susceptibility and severity in women by showing cancer patients film. In second session, health
educators and midwifery specialist conduced group discussion about the benefit and barriers to
give pap smear test, also we used film about pap smear steps to decrease women's fear about test.
Finally, specialist informed their family as their mothers and husbands about the necessity of
having pap smear test for women. Women in both groups were intimated with detail of the study
and were asked to read and sign a consent form.
Each educational session lasted 4560 min. Statistical analysis was performed using SPSS
(version 18). Comparison between two groups was done by independent t-test. Paired t-test
analysis was used for comparison in one group before and after intervention. A two-tailed P
value lower than 0.05 was considered statistically significant.
Go to:
RESULTS
A total of 70 married women entered the study. The mean and standard deviation of participants
age was 31.64 7.5 years (range, 1949). The education level of 35.7% was diploma or
precollege degree, 21.4% went to guidance school, 7% just went to primary school, and a small
portion (2.9%) were illiterates. Majority of the participants (94.3%) were housewives.
There was no significant difference between age (P = 0.197), education level (P = 0.581), and
job (P = 0.483) in two groups before intervention.
The mean scores of knowledge in intervention group before and after intervention were 49.76
16.83, 93.06 5.92, respectively. There was significant difference between knowledge in
intervention group before and after intervention (P < 0.001). While in the control group has seen
a decline in knowledge score after intervention.
As presented in Table 1, there was a significant difference between the mean scores of all of the
constructs of HBM in intervention group after intervention compared to the before intervention
(P < 0.001). However, there was no significant difference between the constructs of HBM in
control group after intervention compared to the baseline values (P > 0.05).

Table 1
Mean SD of scores of constructs of Health belief model in women before and after intervention
About practice, from 35 participants in intervention group, 34 (97.14%) of them have done pap
smear test, but in control group only 1 (2.86%) of them has done test after intervention.
In control group, 10 (28.57%), 20 (57.14%), 5 (14.29%) of women known health staff, family
member specially spouse are most important cues to action before intervention, respectively, but
in intervention group 15 (42.86%) of women known health staff, 11 (31.43%) family member,
and 9 (25.71%) friend as cues to action before intervention but these percents had changed after
intervention.
Go to:
DISCUSSION
The mean score of knowledge before the intervention in both groups was indicative of the low
individual's knowledge of pap smear and cervical cancer. Other studies confirm this
matter.[14,1618]
Considering to the impact of knowledge on practice, lack of knowledge about benefits and the
purpose of the pap smear can be known as the reason for poor practice of pap smear. Consistent
with our study findings, Hazavehei and colleagues have also known the lack of knowledge as
one of the reasons of not doing the test.[14] After educational intervention, the level of
knowledge improved significantly that is emphasized on the impact of the education on
knowledge. Our study findings confirmed by other similar studies in our country.[14,19] Park
study has also confirmed the impact of educational intervention on increasing women's
knowledge and participation in cervical cancer screening program.[20]
Following the intervention, the mean score of perceived susceptibility has been increased in the
intervention group, but we are facing a decrease in the perceived susceptibility in control group.
This significant difference indicates that educational intervention on the basis of Health Belief
Model causing women to be awarded of being susceptible to cervical cancer. Significant increase
in perceived susceptibility also emphasized by Hazavehei, Yakhfrooshha, and Shojaeezadeh
studies.[14,15,19]
In contrast with our findings in park and colleagues study, the perceived susceptibility in both
intervention and control groups did not have any effect on participating in cervical cancer
screening program. They considered insufficient intervention time for changing the attitudes to
be the reason.[20]
With regards to perceived severity, the mean scores increased in intervention group following
education program. That is, educational intervention based on HBM increased perceived severity
regarding cervical cancer, which is similar with the result of other studies.[15,21]
Based on our study findings, perceived benefits in both groups were desirable before the
intervention. This showed that women in both groups were aware of the resulted benefits from
doing pap smear. These findings were also proved by other studies.[14,17] The emphasis on
perceived benefits has been emphasized in another study for women persuasion to do the
test.[2023]
According to the findings, difference between intervention and control groups about perceived
barriers was not significant before the intervention, but educational intervention increased
perceived barriers in intervention group. These findings were supported by Mc Farland and
colleagues study who stated that the women, who had more barrier perception, had less
performance regarding doing pap smear test during past 5 years.[18] Psychological barrier like
fear and embarrassment have been the most important barriers in women in lee study.[22] It may
refer to effectiveness of educational intervention based on the Health Belief Model that has
caused the individuals in the intervention group to overcome to barriers. In the other performed
studies based on the model, the education has been able to reduce the barrier on performing the
health activities.[24,25]
In relation to cues to action in the intervention group, 42.86% have chosen the health staff as the
performance guide which has been increased to 57.14% after education. This is similar with the
results of Enjzab and colleague study.[26] In Akbari study women who have done the pap smear
test regularly have considered the health care providers encouragements as the most important
cues to action[21] In the present study, majority of participants (97.4%) in intervention group
have done the test after intervention and the only one person avoided doing the test because of
financial ability to pay the cost. This indicates that financial support and providing free or low
cost services can improve health behavior of women regarding doing pap test. Also, in control
group, after the intervention, one person (2.85%) has done the test due to the sensitivity resulted
from answering the questionnaire. This study reveals the considerable increase in intervention
group practice as a result of educational intervention, which were also proved in other
studies.[2730] As general, the results of the study imply that education based on Health Belief
Model lead to giving pap smear test in women. By considering the benefit of giving pap smear as
a useful screening tools, educational intervention based on Health Belief Model is recommended
in health centers. The study was limited to women who referred to the health centers and had a
limited number of participants too. Further research must have participants from different groups
of women, increasing the number of participants would also allow for a more robust evaluation
and analysis. This study had pre- and postintervention measurements at two times, which showed
only the short-term effects of the intervention.
Go to:
ACKNOWLEDGEMENTS
The authors would like to thank the participants and health center employees who willingly
participated in the study.
Go to:
Footnotes
Source of Support: Nil.
Conflict of Interest: None declared.
Go to:
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The effectiveness of nutritional education on the knowledge of diabetic patients using the
health belief model. [J Res Med Sci. 2009]
The Effect of Educational Program on Increasing Cervical Cancer Screening Behavior
among Women in Hamadan, Iran: Applying Health Belief Model. [J Res Health Sci.
2011]
Cervical cancer and Pap smear screening in Botswana: knowledge and perceptions. [Int
Nurs Rev. 2003]
Effects of a cognition-emotion focused program to increase public participation in
Papanicolaou smear screening. [Public Health Nurs. 2005]
The Effect of Educational Program on Increasing Cervical Cancer Screening Behavior
among Women in Hamadan, Iran: Applying Health Belief Model. [J Res Health Sci.
2011]
Effects of a cognition-emotion focused program to increase public participation in
Papanicolaou smear screening. [Public Health Nurs. 2005]
The Effect of Educational Program on Increasing Cervical Cancer Screening Behavior
among Women in Hamadan, Iran: Applying Health Belief Model. [J Res Health Sci.
2011]
Knowledge and attitudes about human papillomavirus, Pap smears, and cervical cancer
among young women in Brazil: implications for health education and prevention. [Int J
Gynecol Cancer. 2006]
Effects of a cognition-emotion focused program to increase public participation in
Papanicolaou smear screening. [Public Health Nurs. 2005]
Cervical cancer and Pap smear screening in Botswana: knowledge and perceptions. [Int
Nurs Rev. 2003]
Korean American women's beliefs about breast and cervical cancer and associated
symbolic meanings. [Oncol Nurs Forum. 2007]
Development of a cervical cancer educational program for Chinese women using
intervention mapping. [Health Promot Pract. 2004]
Knowledge and practice about cervical cancer and Pap smear testing among patients at
Kenyatta National Hospital, Nairobi, Kenya. [Int J Gynecol Cancer. 2003]
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J Obstet Gynaecol India >
v.61(5); Oct 2011 >
PMC3257340

J Obstet Gynaecol India. 2011 October; 61(5): 558561.
Published online 2011 October 29. doi: 10.1007/s13224-011-0085-9
PMCID: PMC3257340
Incidence and Cytomorphological
Peculiarities of Lower Genital Tract
Infections in Vault (Post Hysterectomy)
Smears Versus Pap Smears from Non-
Hysterectomy Subjects: A Retrospective
Study
Veena Kashyap and Suresh Bhambhani
Author information Article notes Copyright and License information
Go to:
Abstracts
Objective
To evaluate morphology and frequency of lower genital infections in (post hysterectomy) vault
smears of women.
Methods
We analyzed vault smears from 500 women who had undergone hysterectomy, either for benign
diseases (230) or for carcinoma cervix (270) and findings were compared with Pap smear
diagnosis of non-hysterectomy subjects.
Results
Majority 432/500 (87%) of the vault smears were negative for squamous abnormality in
comparison to 381/500 (76%) Pap smears from non-hysterectomy subjects. It was observed that
48 (9.6%) vault smears showed lower genital tract infections, however frequency of infections
was reported significantly higher 101 (20.2%) in non-hysterectomy subjects. Gardenerella
vaginalis was the leading infection in vault smears 26 (5.2%) due to benign diseases and was
prevalent in the fifth and sixth decades of life of women in comparison to 43 (8.2%) in Pap
smears with higher prevalence in the fourth decade of life. Trichomonas vaginalis and Human
Papillomavirus infection were the second commonest infections in vault smears followed by
Candida albicans.
Conclusion
Cytologically diagnosed gynecological infections were remarkably low 48 (9.6%) in vault
smears as compared to 101/500 (20.2%) amongst non-hysterectomy subjects. Infections which
mainly thrive at the Squamo-columnar junction i.e. HPV, Chlamydia and HSV were absent or
rare in vault smears. Further incidence of infections in the vault smears where hysterectomy was
done due to carcinoma cervix was as low as 10 (3.7%) as compared to 38 (16.5%) where
hysterectomy was done due to benign uterine diseases.
Keywords: Post hysterectomy, Cervical infections, Vault smears
Go to:
Introduction
The Papanicolaou smear was originally designed to detect malignant cervical lesions,
subsequently used to diagnose not only cancerous lesions but precancerous lesions and other
lower genital tract infections of the uterine cervix including human papilloma virus infection [1].
Cytology is widely used as a rapid, cost effective, non-invasive technique in the evaluation and
follow up of patients subjected for hysterectomies [2]. It is estimated that by the age of 60 years
approximately 30% women undergo hysterectomy; approximately 85% of these hysterectomies
are performed for benign diseases and 15% for carcinoma cervix [3]. Any recurrence of
carcinoma after treatment can be detected by smearing the vault periodically and managing the
patients accordingly, likewise in case of hysterectomy done due to benign condition, status of
vault can be reflected by collecting smears [4]. It is not possible to predict the outcome of
treatment on clinical grounds alone and the routine vault smear, during follow up visit, is almost
mandatory for women who have undergone hysterectomies for any reason. Even the examination
of Pap smears during and after radiotherapy/chemotherapy offers a more precise determination
of the response of the individual patients [5, 6]. There is enough literature on the efficacy of
vaginal cuff testing [4, 7] but little information is available on the frequency of lower genital
tract infections in follow up cytologic examination after hysterectomy. We therefore performed a
retrospective study of 500 vault smears to evaluate cytologic findings in relation to cervical
infections in women undergone hysterectomy due to any reason (benign diseases or cancer
cervix) and at any age with the corresponding cervical Pap smears from non-hysterectomy
subjects.
Go to:
Material and Methods
The Papanicolaou stained vault smears of 500 women, who underwent hysterectomies due to
benign gynecologic diseases (230) or due to carcinoma cervix (270) were reviewed and analyzed
to predict the risk of squamous abnormality and specifically the frequency of lower genital
infections. For meaningful comparison same number of cervical Pap smears from non-
hysterectomy subjects attending Gynae OPD of Lok Nayak hospital of Delhi were also reviewed.
The details of patients age at the time of hysterectomy, clinical diagnosis, reason for
hysterectomy were also recorded and described in Table 1.

Table 1
Age wise prevalence and cause (benign and malignant indications) of hysterectomy in study
women
Go to:
Results
The mean age of 230 patients at the time of hysterectomy for benign uterine conditions was
41 years (median 48 years) with a range of 2362 years and mean age of the 270 patients at the
time of hysterectomy for carcinoma cervix was 50 years(median-50 years) with a range of 21
70 years. For this study all the subjects were categorized into five categories as/decades of life
(2130, 3140, 4150, 5160, 6170 years). Benign uterine diseases were found prevalent in
fifth decades of life in 105/230 (45.6%) followed by fourth decades in 71 (30.8%) women.
Fibroid uterus 135/230 (58.6%) was the most common indication for hysterectomy, followed by
Dysfunctional Uterine Bleeding 55 (23.9%) and prolapse uterus 40 (17.3%). Incidence of cancer
cervix was also found prevalent in the fifth decade of life 115 (42.5%) followed by fourth decade
70 (25.9%) and then sixth decade 53 (19.6%) of life. The age wise prevalence and indications for
hysterectomies are given in Table 1.
Majority of vault smears 437 (87%) were negative for any squamous abnormality and were
either normal 300 (60%) or inflammatory 137 (27%) however Pap smears from non-
hysterectomy subjects showed reverse findings where 150 (30%) smears were normal and 231
(46%) inflammatory. The lower genital tract infections which included Gardnerella vaginalis
(GV), Human Papillomavirus (HPV), Trichomonas vaginalis (TV), Candida were reported in 48
(9.6%) vault smears, however infections of Herpes Simplex virus (HSV) and Chlamydia were
not detected cytomorphologically. Infections including Chlamydia and HSV accounted for 98
(19.6%) in non-hysterectomy subjects during routine screening programme, the incidence being
more than double the test group. Low incidence of infection in vault smears was obvious even
though the women were in sexually active decades of life. Incidence of infection in the vault
smears where hysterectomy was done due to carcinoma cervix was as low as 10/270 (3.7%) as
compared to 38/230 (16.5%) where hysterectomy was done due to benign uterine diseases. The
infection of GV were seen in 26 (5.2%) vault smears as compared to 43 (8.6%) from routine Pap
smear. In non-hysterectomy subject the Pap smears showed blue colored short rods tending to
accumulate on the surface of epithelial cells, concentration being more on the margin thus
blurring the cell margins. These cells are commonly known as Clue cells. Fine granular
material gave overall dirty appearance of the smear. In vault smears clue cells were present in
small number and smears were cleaner as compared to non-hysterectomy subjects. The infection
of TV was prevalent in the sexually active phase of life of women i.e. 2150 years irrespective of
reason for hysterectomy. In vault smears TV appeared as small grey green round or elliptical
structures with eccentric nuclei without much cellular changes while cells in Pap smear from
non-hysterectomy subjects showed cytoplasmic eosinophilia, perinuclear halos, and excessive
cytolysis. The infection of HPV was reported in 8 (1.6%) vault smears however incidence was
three fold higher 24 (4.8%) in non-hysterectomy subjects. The HPV infection induces
cytomorphological changes in cervical epithelium in two forms: first classical changes reflects
formation of koilocytes i.e. epithelial squamous cells with cytoplasmic condensation at the
periphery with large paranuclear halo and eccentrically placed dark nucleus, and second non-
classical changes where full blown koilocytes are not formed but features of rounding of cells
with cytoplasmic condensation and eccentric/hanging nuclei are seen. Cells are seen in sheets
and chords. In vault smear we could see few round cells in small clusters with thickening of
borders, cytoplasmic vacuolation and eccentric nuclei depicting only non-classical category of
HPV induced changes while cells in Pap smears from non-hysterectomy subjects showed
classical as well as non-classical changes of HPV infection. Infection of Candida was reported in
4 (0.8%) vault smears but frequency was four times higher as 12 (2.4%) in non-hysterectomy
subjects. Infection of HSV and Chlamydia were totally absent in vault smears while observed in
few Pap smears from non-hysterectomy subjects. No more than one infection at a time was seen
in the vault smears and there was no low grade or high grade lesions seen in vault smears of
women subjected for hysterectomy. Non-hysterectomy subjects showed 0.6% Atypical
Squamous cells (ASC), 0.8% each LSIL-Mild dysplasia or HSIL. Malignant cells were only seen
in the 15/500 (3%) vault smears of women who underwent hysterectomy for carcinoma cervix on
follow up indicating recurrence. Age wise prevalence of infection and squamous abnormalities in
vault smears versus non-hysterectomy subjects are described in Table 2.

Table 2
Age wise prevalence of cytologic diagnosis and infections of vault smears after
hysterectomy/Pap smears from non-hysterectomy subjects
On comparing the diagnosis of vault smears due to benign diseases versus due to carcinoma
cervix it was observed that lower genital tract infections (including HPV) were frequently seen in
38 (16.5%) vault smears of women subjected for hysterectomy due to benign gynecologic
diseases in comparison to 10 (3.7%) vault smears due to carcinoma cervix. Vault smears after
hysterectomy for benign uterine diseases showed infection of GV four time higher, HPV three
time higher and TV two time higher when compared with vault smears after hysterectomy for
carcinoma cervix. No infection of Candida, HSV and chlamydia was seen after hysterectomy for
carcinoma cervix. No squamous abnormality was reported after hysterectomy for benign diseases
Table 3.

Table 3
Age wise prevalence of cytologic diagnosis of infections in vault smears due to benign uterine
diseases/carcinoma cervix
Go to:
Discussion
The lower genital tract infections of the uterine cervix are closely related with age, marital status,
promiscuity, socioeconomic status, malnutrition and genital hygiene. High incidence of
infections in general is also attributed by the lowered immune status of the females due to varied
physiological conditions of the body like diabetes and AIDS. Hygiene of the lower genital tract
is directly related to the infections and inflammation of genital organs of female [8]. In
developing countries where hygiene is poor incidence of infections is generally high as
compared to developed countries [9].
We investigated the frequency of lower genital tract infections in vault smears of women
subjected for hysterectomy due to any reason in her past and it was observed that 48 (9.6%) vault
smears showed infections of GV, HPV, TV and Candida, however these infections were
accounted for 101 (20.2%) in normal women during routine screening programme as reported
earlier also [10, 11]. The reason is related to sexual activity of women. After hysterectomy every
women reacts differently, and reactions are a combination of emotional and physical responses.
Some women enjoy sex more after hysterectomy, particularly if they had a lot of bleeding and
pain before surgery. Some women feel more relaxed not worrying about getting pregnant.
Infection like HSV, chlamydia and HPV which are more common in sexually active decades of
life were absent or rare in vault smears in comparison to non-hysterectomy subjects. These
infections grow by infecting delicate endocervical epithelium in endocervical canal at the place
of squamo-columnar junction and after hysterectomy, by removal of cervix uteri viz-a-viz
squamo-columnar junction; there are little chances of these infections. The GV was the leading
infection associated with inflammation and infected 21/230 (9.1%) women after hysterectomy
for benign diseases and more prevalent in the age group of 4150 years while cancer patients
showed only 5/270 (1.8%) cases having GV infection. The higher prevalence of GV as post
hysterectomy infection was also reported by Kristiansen et al. [12]. This difference in frequency
rate of GV with and without hysterectomy inflammation is highly significant and suggests a
causative role of organism. The morphological peculiarities of GV were different in vault smears
with less number of clue cells. The cellular changes, cytoplasmic eosinophilia, perinuclear halos,
and excessive cytolysis, induced by infestation of TV were not seen in vault smears however
organism seen adjacent to the cells as well as in the background. The frequency of HPV infection
was reported in 8/230 vault smears but it was reported in few vault smears 3/220 by Videlefsky
et al. [4]. As well as classical changes of HPV infection like koilocyte formation, large
perinuclear halo and large hyperchromatic nuclei were not found in vault smears after
hysterectomy, however cytoplasmic condensation and eccentric/hanging nuclei were supporting
features for the diagnosis of HPV infection and they proved for the positivity of HPV DNA and
HPV types 16 also. Gynecologic infections as well as dysplastic lesions, in vaginal cuff testing
after hysterectomy for benign uterine diseases, also reported by Videlefsky et al. [4] but
incidence was much higher in comparison to present results and in present study no squamous
abnormality was detected in vault smears due to benign uterine conditions. The low rate of
infection in women aging 5160 years and above may be explained on the basis that women by
the age of 50 years reached to the menopausal status of life and are less sexually active which
was a supporting factor towards lesser rate of infection. The present study revealed the
importance of follow up cytologic examination after hysterectomy as it is observed that lower
genital tract infections occur mainly in premenopausal age of women when the women are
usually sexually active irrespective of their hysterectomy for benign diseases and frequency of
infections decreased as the normal women gets older. It is concluded from the results that
examination of vault smears after hysterectomy due to benign diseases or cancer is important to
know the status of vault in relation to gynecologic infections as well as for detection of any
abnormality in the vault. More significantly HPV, chlamydia and HSV infections were absent or
rare in vault smear irrespective of any decade of life simply because of the fact that squamo-
columnar junction, site of infection, was no more in hysterectomy cases which is must for
initiation and proliferation of these infections.
Go to:
References
1. Koss LG. The papanicolaou test for cervical cancer detection. a triumph and a tragedy. JAMA.
1989;261:737743. doi: 10.1001/jama.1989.03420050087046. [PubMed] [Cross Ref]
2. Pearce KF, Haefner HK, Sarwar SF, et al. Cytopathologic findings on vaginal papanicolaou
smears after hysterectomy for benign gynecologic diseases. N Engl J Med. 1996;335:15591562.
doi: 10.1056/NEJM199611213352103. [PubMed] [Cross Ref]
3. Singh A, Arora AK. Profile of hysterectomy cases in rural North India. Climacteric.
2005;8:177184. doi: 10.1080/13697130500117920. [PubMed] [Cross Ref]
4. Videlefsky A, Grossl N, Denniston M, et al. Routine vaginal cuff smear testing in post-
hysterectomy patients with benign uterine conditions: when is it indicated? J Am Board Fam
Pract. 2000;13:233238. [PubMed]
5. Smith CJ, Heeren M, Nicklin JL, et al. Efficacy of routine follow-up in patients with recurrent
uterine cancer. Gynec Oncol. 2007;107:124129. doi: 10.1016/j.ygyno.2007.06.002. [PubMed]
[Cross Ref]
6. Cooper AL, Dornfeld-Finke JM, Banks HW, et al. Is cytologic screening an effective
surveillance method for detection of vaginal recurrence of uterine cancer? Obstet Gynae.
2006;107:716. doi: 10.1097/01.AOG.0000194206.38105.c8. [Cross Ref]
7. Lewis P. Vaginal cuff testing. J Am Board Fam Pract. 2000;13:470. [PubMed]
8. Singh V, Gupta MM, Satyanarayana L, et al. Association between reproductive tract infections
and cervical inflammatory epithelial changes. Sex Transm Dis. 1995;22:2330.
9. Singh V, Sehgal A, Satyanarayanan L, et al. Clinical presentation of gynecologic infections
among Indian women. Obstet Gynecol. 1995;85:215219. doi: 10.1016/0029-7844(94)00367-M.
[PubMed] [Cross Ref]
10. Kashyap V, Bhambhani S, Sharma S. Cervical cytology in postmenopausal women. J Cytol.
2001;18:163166.
11. Kashyap V, Bhambhani S. Coexistence of Human Papillomavirus and other lower genital
tract infection in cervical smears. J Cytol. 2002;19:171172.
12. Kristiansen FV, Oster S, Frost L. Gardnerella vaginalis in post hysterectomy infection. Eur J
Obstet Gynecol Repro Biol. 1990;35:6973. doi: 10.1016/0028-2243(90)90144-P. [Cross Ref]

Articles from Journal of Obstetrics and Gynaecology of India are provided here courtesy of Springer
Formats:
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Related citations in PubMed
Spectrum of genital human papillomavirus infection in a female adolescent population.
[Sex Transm Dis. 1995]
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albicans and actinomyces in Papanicolaou smears. [Clin Exp Obstet Gynecol. 2012]
[The correlation of inflammation and epithelial changes in the Pap smears of cervix
uteri]. [Acta Med Croatica. 2005]
Vaginal vault smears after hysterectomy for reasons other than malignancy: a systematic
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[Ano-genital lesions due to human papillomavirus infection in women]. [Med Mal Infect.
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NIHPA Author Manuscripts >
PMC3110214

Am J Public Health. Author manuscript; available in PMC 2012 July 1.
Published in final edited form as:
Am J Public Health. 2011 July; 101(7): 12971305.
Published online 2011 May 12. doi: 10.2105/AJPH.2010.300061
PMCID: PMC3110214
NIHMSID: NIHMS328049
Is health care system distrust a barrier to
breast and cervical cancer screening?
Evidence from Philadelphia
Tse-Chuan Yang, Stephen A. Matthews, and Marianne M. Hillemeier
Author information Copyright and License information
The publisher's final edited version of this article is available at Am J Public Health
See other articles in PMC that cite the published article.
Go to:
Abstract
Objectives
This study investigates whether health care system distrust is a barrier to breast and cervical
cancer screening and whether different dimensions of distrust values and competence have
different impacts on cancer screening.
Methods
We utilize data on 5,268 women 18 and older living in Philadelphia and analyze their use of
screening services via logistic and multinomial logistic regression.
Results
High levels of health care system distrust are associated with lower utilization of breast and
cervical cancer screening services. The associations differ by dimensions of distrust.
Specifically, high competence distrust is associated with a reduced likelihood of having Pap
smear tests, and women with high values distrust are less likely to have breast examinations
within the recommended time period. Independent of other covariates, individual health care
resources and health status are associated with utilization of cancer screening.
Conclusions
Health care system distrust is a barrier to breast and cervical cancer screening even after
controlling for demographic and socioeconomic determinants. Rebuilding confidence in the
health care system may improve personal and public health by increasing the utilization of
preventive health services.
Go to:
Introduction
Cancer is a leading cause of death in the United States. Approximately 1.5 million Americans are
diagnosed with cancer per annum and one in four deaths are due to cancer.
1
Among women, an
estimated 192,000 breast and 11,000 cervical cancer cases are detected each year and over
40,000 women die from breast cancer and approximately 4,000 from cervical cancer.
1
To be
effective in reducing the morbidity and mortality resulting from breast and cervical cancer,
efforts need to be made to increase the proportion of women who comply with screening
recommendations;
2
according to a recent report a third of women are not in compliance with
screening guidelines for breast cancer and over a fifth for cervical cancer.
3
The goal of this study
is to investigate whether health care system distrust (hereafter referred to as distrust) is a barrier
to breast and cervical cancer screening.
The late-Twentieth century saw many changes in the theoretical underpinnings of research on
health in general, and womens health in particular. The prevailing biomedical model was
criticized for ignoring social determinants of health, such as social class, gender roles, and
poverty,
4
and health determinants models that incorporated multiple social, economic and
demographic dimensions were embraced.
57
While the multiple determinants of health
perspective emphasizes the relationships between socioeconomic factors and health outcomes,
4

the role of psychological factors (i.e. depression and distrust) in cancer screening has only
recently been recognized.
811
Relatively little is known about whether distrust affects health
outcomes, and specifically whether it influences cancer screening behaviors among women.
11

Americans overall confidence in their health care system has declined markedly in recent
decades. In 2010 only 34 percent of adults reported a great deal of confidence in the health
system, down from over 70 percent in 1966.
12
More than 80 percent of the Americans, however,
held high levels of trust in their personal physicians or providers;
13
a paradox that has been
widely documented in the literature.
1417
Previous studies suggest trust in physicians is associated
with seeking timely medical care, maintaining appropriate health care, and adhering to medical
advice
1820
but it is unclear whether trust or its converse distrust affects the adoption of
preventive health services among women.
11

Of relevance to this study, the emerging distrust research in health care shows that distrust is a
multidimensional concept.
2123
For example, Shea et al. used focus groups, pilot testing, and a
telephone survey to develop a highly reliable 9-item distrust scale that includes 2 subscales:
competence distrust and values distrust.
22
Competence distrust is expected to be high when the
quality of service fails to meet patient expectations and does not improve health. Values distrust
is expected to be high when the integrity of the health care system is questioned (e.g., ethical
issues, financial priorities, transparency of care). While it is possible that dimensions of distrust
may influence the use of preventive health services in different ways, little research has
addressed this issue explicitly.
A range of individual characteristics have been found to be associated with the use of breast and
cervical cancer screening, including age,
5, 24
race/ethnicity,
11, 25
socioeconomic factors,
5, 24

marital status,
5, 11, 24
and availability and utilization of health care resources.
11, 24
Access to
insurance and health care providers is associated with higher likelihood of interaction with the
health care system, and has been hypothesized to be related to levels of distrust and to
individuals health-related behaviors.
26
Personal health status has been found to be related to
levels of distrust,
27
although the underlying causal mechanisms have not been well-documented.
Evidence concerning the association of health status with use of preventive health services is
inconclusive.
11
An important contribution of our study is the investigation of the association of
distinct aspects of distrust-- values distrust and competence distrust--with receipt of two
preventive health services for adult women: the Papanicolaou (Pap) test for cervical cancer and
clinical breast examination to screen for breast cancer. We test the following two hypotheses:
after controlling for individual socioeconomic and demographic characteristics, (1) high levels of
distrust are associated with low utilization of cancer screening services; and (2) the negative
relationship between distrust and cancer screening utilization holds for both the values and
competence dimensions of distrust.
Go to:
Data and Methods
Data Source
This study is based on data collected on all women aged 18 and older (n = 5,268) in the
Philadelphia Health Management Corporations (PHMC) 2008 Southeastern Pennsylvania
Household Health Survey; a survey covering five counties in southeastern Pennsylvania, Bucks,
Chester, Delaware, Montgomery, and Philadelphia counties. The interviews were conducted
between June and October 2008 via computerized telephone random digit dialing based on a
stratified sampling frame to ensure representation from the 5 counties.
28
The response rate for the
PHMC 2008 was 25% based on criterion #3 of the American Association for Public Opinion
Research.
29
While the response rate appears low it is important to note that this in and of itself is
not an indicator of survey quality. Recent research finds no significant biases as a result of
response rate.
30, 31
Moreover, the PHMC 2008 sample closely matches the demographic and
socioeconomic structure of the study counties as reported in the U.S. Census Bureau in their 3-
year 20062008 release of the American Community Survey (ACS)
32
and health screening rates
in the PHMC 2008 mirror those in the BRFSS 2008 data for Philadelphia. For example, 81
percent of women aged 50+ have had a mammogram within the past year according to the
BRFSS and 82 percent in PHMC.
33
A balancing weight is used in the statistical analysis.
Measures
We are interested in three outcomes. The first is whether a woman had a Pap smear test within
the past 2 years (coded 1 = Yes, 0 = No). The PHMC asked women How long has it been since
your last Pap test? and the response categories were one year or less, 12 years, 25
years, 510 years, more than 10 years, and never. At the time of the study, the American
College of Obstetricians (ACOG) and Gynecologists recommended Pap testing every 23
years.
34
Since the 25 year interval choice would include many women who were not screened
within the recommended interval, we chose to code only those reporting one year or less or
12 years as having received recommended screening. The second outcome of interest is
whether a woman had a breast examination by a doctor or health professional within the past
year as recommended (coded 1 = Yes, 0 = No).
34
The correlation between Pap testing and breast
examination in the PHMC sample is 0.45 (p<0.001). The third outcome included in the analyses
is a trichotomized variable measuring whether a woman had both tests (coded 2), had only
one of the two tests (coded 1), or no test (coded 0, reference group) according to the
recommended schedule. These three outcomes allow us to construct a more complete picture of
cancer screening behaviors among women and the role, if any, of health care system distrust.
We have five groups of independent variables. The primary predictor of interest is distrust,
which is measured by a 9-item scale developed by Shea et al.
22
The nine questions are rated on a
5-level Likert scale (strongly disagree, disagree, neither agree/disagree, agree, or strongly agree)
producing a possible distrust score range between 9 and 45. The reliability of the distrust scale
and subscales has been tested and reported elsewhere.
22
Using the 2008 PHMC data and factor
analysis with the varimax rotation method, we generated two standardized factor scores based on
the regression method capturing two different dimensions of distrust of health care system:
values distrust and competence distrust (the eigenvalues were 3.86 and 1.10 respectively and the
total variance explained was 55%). The regression method applies factor weights to create the
distrust scores centered on zero with a standard deviation of 1 (see Table 1). We categorized
each item into one of the two dimensions when the factor loading for that assigned dimension
was 0.5 or higher and the other factor loading was lower than 0.5. Table 1 includes the nine
questions and their factor loadings on each sub-scale, as well as the distributions of the factor
scores. Factor analysis not only takes into account the interdependency among the questions, but
also gives weights to each question to yield scales based on the empirical data. Our grouping is
similar to the original paper.
22
We imputed missing values based on an EM algorithm for
continuous variables
35
and the imputed scores were rounded to the nearest whole number to
reflect the Likert scales.

Table 1
Factor loadings with Varimax rotation.
A second group of variables are demographic predictors. Age was reported by the women and
treated as a continuous variable. Race/ethnicity is based on four categories (three dummy
variables in analysis): White (reference group), Black, Hispanic, and other race/ethnicity. Marital
status is based on three categories (two dummy variables): single (reference group), married or
cohabiting, and widowed, divorced, or separated.
Socioeconomic status (SES) factors form our third group of variables. Poverty status was based
on the 2008 federal poverty guideline where those women in households with incomes below the
poverty line are classified as poor (coded 1) and others (coded 0). Employment status was
trichotomized into employed, unemployed, and others (i.e. disabled or retired; reference group).
Educational attainment is measured by four dummy variables based on a five-category variable:
did not graduate high school (reference group), high school diploma, some college, an
associate/bachelor degree, and post college degree.
The fourth group of predictors relate to health care resources and insurance status. The women
were asked about their primary source of care grouped into: no regular health care provider,
private doctors office, public and community health center, and other source of care (e.g.,
outpatient clinic). Three dummy variables were created with no regular health care provider
serving as the reference group. Health insurance status was dichotomized into insured (coded 1)
and uninsured (coded 0).
The final group of variables concerns the womans health status. Self-rated health is based on a
question with four choices: excellent (reference group), good, fair, or poor. We also include self-
rated stress; in the PHMC this is a single scale from 1 to 10 to assess the experience of day-to-
day stress, where 1 indicated no stress and 10 extreme amount of stress. This measure has
been used in the absence of a complete inventory of stressful events.
36, 37
Including these
measures in the analyses captures aspects of both mental and physical health.
Analytical strategy
Our analysis is based on the use of both logistic and multinomial logistic regression models. For
the binary dependent variables (whether the women had a Pap smear, whether the women had a
clinical breast exam), we model the likelihood that the response is equal to 1 given a set of
explanatory covariates. For the trichomized dependent variable (the women had both tests, one
test, or no test), we use a multinomial logistic regression, comparing those women who report
both tests or just one test with the comparison category (no test), respectively.
Go to:
Results
Eighty percent of PHMC women 18 and older had a Pap test within two years and more than 70
percent had a breast examination by a doctor or health professional within a year (results not
shown). Table 2 presents descriptive statistics for all variables used in this study by the number
of screening services used (for dummy variables the proportions can be interpreted as
percentages). We provide data on the mean value of each variable for the overall sample and we
compare mean values between three subsamples: those women who had neither the Pap test nor
breast examination within the recommended time, those women who had one screening test, and
those women who had both. The comparisons of means between samples are shown in the last
column of Table 2. Several patterns are worth noting. First, both values and competence distrust
scores are lower among women with greater utilization of screening services. Specifically, the
values distrust of the women who reported having one or both tests is significantly lower than the
group of women who did not have either a Pap test or a breast examination (Both 0.083 vs. One
0.020 vs. Neither 0.103). Second, higher SES women utilize preventive health services more
than other women. For example, almost 17 percent of women who reported having both a Pap
test and a breast examination had a post college degree compared to 9 percent of women who
had no screening test, a difference that is statistically significant. Third, respondents whose usual
source of care was a private physicians office were more likely to have both Pap and breast
cancer screening tests than those with other types of sources of care. Finally, women with less
stress or better self-rated health also reported more utilization of cancer screening tests.

Table 2
Descriptive statistics overall and by number of screening services obtained in recommended time
interval


Table 3 presents the logistic regression results for utilization of Pap tests and clinical breast
examination. Competence distrust was associated with the odds of having a Pap test.
Specifically, a unit increase in competence distrust was associated with an 8 percent decrease in
the likelihood of having a Pap test (OR=0.916; 95% CI= 0.851, 0.986). The odds of having a Pap
test also was related to age, race/ethnicity, marital status, employment status, education, health
care resources, and personal health. For instance, having a regular source of care (regardless of
type) was associated with a 68~77 percent increase in the odds of having a Pap test. Controlling
for other covariates, each 10-year increase in age was related to a 24 percent decrease in the odds
of having a Pap test in the recommended time interval (0.973^10= 0.761).

Table 3
Logistic regression results modeling receipt of pap smear screening test and clinical breast
examination within the recommended time interval, N=5,268
With respect to breast cancer screening, only higher levels of values distrust are associated with
lower odds of receiving a clinical breast examination. Other things equal, the odds of having a
breast cancer screening decreased by roughly 8 percent with each one unit increase in values
distrust (OR=0.923; 95% CI= 0.864, 0.986). The determinants of having a clinical breast
examination are similar to those of having a cervical cancer test, i.e., demographic features and
health care resources. One of the potentially modifiable factors is insurance status. The odds of
having a breast examination among insured women were almost triple those of women without
insurance (OR=2.757; 95% CI= 2.179, 3.489).
Next, we used multinomial logistic regression to investigate whether distrust was related to the
number of preventive screening tests (Table 4). Compared to women without any screening tests,
values distrust was related to the likelihood of having one of these two tests, and both values and
competence distrust scores were negatively associated with the odds of receiving both services.
Specifically, one unit increase in values distrust would result in a 12.5 percent decrease
(OR=0.875; 95% CI= 0.790, 0.970) in the likelihood of having only one of the two preventive
tests. This association remained when comparing women with both tests (OR= 0.875; 95% CI=
0.800, 0.958). An association for competence distrust was found among those utilizing both
services; specifically, the odds of taking two tests would be reduced by almost 10 percent
(OR=0.914; 95% CI= 0.838, 0.997) if competence distrust increased by one unit.

Table 4
Multinomial regression results modeling the number of receipt of screening tests in the
recommended time interval versus none, N=5,268
There are several noteworthy additional findings. Economic factors and health status do not
appear to be associated with differences between having no screening test and having one; i.e.,
poverty, employment status, educational attainment, self-rated health, and stress were not
significant. Marital status, race/ethnicity, health insurance and source of care, however, were
associated with the difference between having no test and one test. When comparing those
women having both tests with those with none, we find that socioeconomic and health conditions
were important. Employed women and those with a college degree were more likely to have had
both recent breast and cervical cancer screenings. Self-rated health was also associated with
having both tests. Women who rated their health as fair or poor were about 35 to 40 percent less
likely to receive breast and cervical cancer screening. Moreover, employment status, having at
least a college education, and reporting fair/poor health are the main factors that account for the
differences between the two models in Table 4.
Go to:
Discussion
Our findings support the first hypothesis that high levels of health care system distrust among
women are associated with low utilization of cancer screening services, specifically Pap smears
and clinical breast examinations. However, our second hypothesis that both the values and
competence distrust scores were negative associated with cancer screening utilization was not
fully supported. Results suggest that different dimensions of distrust play a unique role in
understanding cancer screening usage; that is, high competence distrust was associated with low
odds of receiving Pap test screening and values distrust was negatively associated with the
likelihood of receiving a clinical breast examination. This difference is intriguing, and warrants
further investigation. Since women can be screened for breast cancer by both clinical breast
exam and mammogram, it could be the case that those who distrust their health care providers
integrity or ethics are more likely to opt to rely on the objective screening provided by
mammography. On the other hand, women who have doubts about the technical competence of
their health care provider may be reluctant to submit to an office-based laboratory test like a Pap
smear.
Independent of other covariates, health care resources and personal health were associated with
womens utilization of cancer screening. If women have a regular source of care they are more
likely to receive and act on the recommendation to have a regular Pap test and clinical breast
examination.
38
Women with a regular source of care may have frequent interactions with the
health care system (i.e. insurance company and health providers) and these interactions may
promote the trustworthiness of health care environment and hence lessen competence distrust.
26

As mentioned above, the differences between the two models in Table 4 indicate that
employment status, education and self-rated health are important factors associated with the
utilization of cancer screening. Consistent with other research we find that higher educational
attainment is associated with the dissemination and adoption of information on the importance of
preventive health services;
39, 40
respondents with at least college education are more likely to
receive both, rather than one of, cervical and breast cancer screenings than their counterparts.
Similarly, perhaps women with fair/poor self-rated health may not seek screening because of
concerns about the discovery of cancers.
This study of Philadelphia women documents a significant association between distrust and
utilization of breast and cervical cancer screening tests, net of other factors. While employing
different measures of distrust, this study corroborates a recent paper that concluded that different
dimensions of trust in the health care system had unique relationships with the use of preventive
health services among older black and white adults in Pittsburgh.
11
Our findings are consistent
with studies exploring determinants of cancer screening. For example, we found that Black
women were 1.5 to 2 times and 50 percent more likely than White women to have Pap tests or
breast examinations. Hispanic women were also 50 percent more likely to have a Pap test (Table
3) than White. These findings echo those of a recent study.
25
Being married or living with a
partner facilitated the use of cancer screening services. Again, similar findings have been
documented elsewhere.
5, 11, 41, 42

This study has several limitations. First, the survey data come from women in the Philadelphia
metropolitan area and the findings may not be generalizable to women in other areas, although
the findings are in line with research conducted in similar settings. Second, the PHMC does not
provide specific information on levels of respondents trust in their primary health providers and
thus the intertwined association between trust in physicians and health care system distrust
cannot be separated. Third, as noted earlier, the wording and classification of time intervals for
the Pap test question does not permit a direct comparison with recommended screening
guidelines. Fourth, this study is cross-sectional, which precludes looking at cause and effect
relationships over time. Fifth, while the balancing weights were constructed accounting for
phone type and sociodemographic features,
43
non-response bias is another possible source of
errors. Finally, the data are self-report and therefore subject to recall bias and other measurement
errors.
44, 45

Several policy implications emerge from this study. As distrust plays an important role in the
utilization of cancer screening tests, rebuilding levels of trust in the health care system among the
American public should be a priority. The values and competence distrust in the health care
system has been a barrier to public health research.
46
Maintaining a high level of service quality
and responsiveness (i.e. reducing medical errors, providing transparency to patients) may reduce
both competence and values distrust
47
and in turn may increase the utilization of cancer
screening tests. This could be an example of how macro-level changes can influence individual
behaviors.
As found in this study, having a regular source of care, regardless of type, may increase the
opportunity for advice and compliance with cancer screening test recommendations. Even
though there is an increased vulnerability to cancer with age, older women are less likely to
receive screening tests. Promoting earlier and regular screening can lead to early detection and
will reduce cancer morbidity and mortality within American women.
This study used a recently developed health care system distrust scale to investigate the effects of
different dimensions of distrust on breast and cervical cancer screening. The results indicate that
competence and values distrust are associated with the likelihood of recommended use of
screening tests, even after controlling for other competing covariates. Health care system distrust
was found to be a barrier in the utilization of preventive health services. In addition to traditional
demographic and socioeconomic determinants, future research should include measures of
distrust so as to better understand patterns and determinants of cancer screening.
Go to:
Contributor Information
Tse-Chuan Yang, The Social Science Research Institute, The Pennsylvania State University, 601
Oswald Tower, University Park, PA 16802, Email: tuy111/at/psu.edu, Tel: 814-865-5553.
Stephen A. Matthews, The Department of Sociology, The Pennsylvania State University, 601
Oswald Tower, University Park, PA 16802.
Marianne M. Hillemeier, The Department of Health Policy and Administration, The
Pennsylvania State University, 601 Oswald Tower, University Park, PA 16802.
Go to:
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Int J Prev Med >
v.3(8); Aug 2012 >
PMC3429807

Int J Prev Med. 2012 August; 3(8): 585590.
PMCID: PMC3429807
The Effect of Education on Women's Practice
Based on the Health Belief Model About Pap
Smear Test
Asiyeh Pirzadeh and Maryam Amidi Mazaheri
Author information Article notes Copyright and License information
Go to:
Abstract
Introduction:
Cervical cancer is the most common gynecological cancer in Iran. The single most effective tool
in reducing death due to cervical cancer is the use of pap smear as a screening tool. Therefore,
the aim of this study was to determine the effectiveness of education based on Health Belief
Model about giving pap smear in women.
Methods:
This quasi-experimental study was performed on 70 women who referred to two health center in
Kouhdasht (Lorestan- Iran). The samples were randomly divided in two groups (35 in
intervention group and 35 in control group). The data were collected by a validated and reliable
questionnaire. Interventions were run based on Health Belief Model during three sessions only
for intervention group. Each educational session was for 4560 min. The independent t-test and
paired t-test were used to analyze data. A two-tailed P value lower than 0.05 was considered
statistically significant.
Result:
According to results, the mean scores of knowledge were significantly different between two
groups after intervention (P < 0.001). The mean scores of the model variables (perceived
susceptibility and severity, perceived benefits, and barriers) had no significant difference in the
two groups before intervention, but after intervention had significant difference between the two
groups (P < 0.001).
Conclusion:
Designing and executing health education programs based on health belief model can promote
the practice of women regarding to pap smear tests.
Keywords: Health belief model, pap smear test, woman
Go to:
INTRODUCTION
Cervical cancer is one of the most common forms of carcinoma among women worldwide, and
80% of these cases occurring in developing and undeveloped countries.[1] Cervical cancer is
largely preventable by effective screening programs.
The single most effective tool in reducing death due to cervical cancer is the use of pap smear as
a screening tool.[2] Regular screening with the Papanicolaou (Pap) test may reduce cervical
cancer mortality by as much as 98%.[3,4]
Although other studies of Asian women found that lack of knowledge about cancer risk factors
resulted in failure to get pap smears.[5] In other hand, some of the other research found that
sociocultural barriers such as embarrassment for pelvic examination and individuals beliefs
about the causes and significance of cervical cancer may lead to lack of using pap smear test or
not.[57]
Cervical cancer is the most common gynecological cancer in Iran,[8] where various methods of
screening, diagnosis, and treatment have been reported.[9,10] However, since there is no lucid
system to document the data on cancers, there are no clear reports of incidence and prevalence of
cervical cancer in Iran.
Although cervical cancer is of high concern in Iran, and the level of screening test is
unacceptable, few studies have been carried out to determine why women do not refer to
participate in pap smear test, and education is efficient to persuade Iranian women to participate
in this test.
One of the behavioral models can describe this matter is Health Belief Model.
This model, which emerged in the late 1950s, was used as an exploratory model to assess why
people did not use preventive health services and eventually to understand why people use or fail
to use health services.[11] HBM consists of various constructs including perceived susceptibility,
severity, barriers, and benefits, cues to action, and health action.[11]
Many researchers now employ this model to guide the development of health interventions with
the aim of changing behaviors,[12] and effectiveness of this model has approved in many
research.[13,14] Shojaeezadeh et al. performed a quasi-experimental study in hamadanian
women which revealed that health education based on HBM can enhance women's knowledge of
cervical cancer, change their health beliefs, and improve their behaviors (giving pap smear
test).[15] Therefore, the aim of this study was to determine the effectiveness of education using
Health Belief Model on practice of women regarding pap smear in Kouhdasht (Lorestan-Iran),
20102011.
Go to:
METHODS
This is a quasi-experimental study, performed on 70 women who referred to two health center in
Kouhdasht (Lorestan- Iran).
Inclusion criteria of married women who never had a pap test and women who could not
understand the questions were excluded from study. The samples were randomly divided in two
groups (35 in intervention group and 35 in control group). There was no difference between the
two groups in age, job, and education level. A self-administered questionnaire was designed by
the researchers. The questionnaire was divided into four sections: demographic data (3
questions), knowledge (21 questions), HBM model constructs (57 questions) including 15
questions on perceived susceptibility, perceived severity, perceived benefits, each part (5
questions), perceived barriers (8 questions), cues to action (3 questions), and practice (1
question). Likert scoring method was used to assess the answers as follows: (certainly agree = 4,
agree = 3, no idea = 2, disagree = 1, and certainly disagree = 0) and the score range for every
section was 0 to 100.
For knowledge section, one score was given to each correct answer. The score for wrong
answers was zero. Finally, practice and behavior of participants were assessed by yes and no
question.
We allocated score 1 and 0 to yes and no answers about practice, respectively.
The reliability of questionnaire was determined by Cronbach's alpha, which was in the range of
0.600.83.
The questionnaires were distributed in two groups one week before the intervention and one
month after the intervention. Interventions were run based on Health Belief Model during three
sessions in health center only for intervention group. In first session, health educator informed
them about cervical cancer and causes of this cancer and tried to promote perceived
susceptibility and severity in women by showing cancer patients film. In second session, health
educators and midwifery specialist conduced group discussion about the benefit and barriers to
give pap smear test, also we used film about pap smear steps to decrease women's fear about test.
Finally, specialist informed their family as their mothers and husbands about the necessity of
having pap smear test for women. Women in both groups were intimated with detail of the study
and were asked to read and sign a consent form.
Each educational session lasted 4560 min. Statistical analysis was performed using SPSS
(version 18). Comparison between two groups was done by independent t-test. Paired t-test
analysis was used for comparison in one group before and after intervention. A two-tailed P
value lower than 0.05 was considered statistically significant.
Go to:
RESULTS
A total of 70 married women entered the study. The mean and standard deviation of participants
age was 31.64 7.5 years (range, 1949). The education level of 35.7% was diploma or
precollege degree, 21.4% went to guidance school, 7% just went to primary school, and a small
portion (2.9%) were illiterates. Majority of the participants (94.3%) were housewives.
There was no significant difference between age (P = 0.197), education level (P = 0.581), and
job (P = 0.483) in two groups before intervention.
The mean scores of knowledge in intervention group before and after intervention were 49.76
16.83, 93.06 5.92, respectively. There was significant difference between knowledge in
intervention group before and after intervention (P < 0.001). While in the control group has seen
a decline in knowledge score after intervention.
As presented in Table 1, there was a significant difference between the mean scores of all of the
constructs of HBM in intervention group after intervention compared to the before intervention
(P < 0.001). However, there was no significant difference between the constructs of HBM in
control group after intervention compared to the baseline values (P > 0.05).

Table 1
Mean SD of scores of constructs of Health belief model in women before and after intervention
About practice, from 35 participants in intervention group, 34 (97.14%) of them have done pap
smear test, but in control group only 1 (2.86%) of them has done test after intervention.
In control group, 10 (28.57%), 20 (57.14%), 5 (14.29%) of women known health staff, family
member specially spouse are most important cues to action before intervention, respectively, but
in intervention group 15 (42.86%) of women known health staff, 11 (31.43%) family member,
and 9 (25.71%) friend as cues to action before intervention but these percents had changed after
intervention.
Go to:
DISCUSSION
The mean score of knowledge before the intervention in both groups was indicative of the low
individual's knowledge of pap smear and cervical cancer. Other studies confirm this
matter.[14,1618]
Considering to the impact of knowledge on practice, lack of knowledge about benefits and the
purpose of the pap smear can be known as the reason for poor practice of pap smear. Consistent
with our study findings, Hazavehei and colleagues have also known the lack of knowledge as
one of the reasons of not doing the test.[14] After educational intervention, the level of
knowledge improved significantly that is emphasized on the impact of the education on
knowledge. Our study findings confirmed by other similar studies in our country.[14,19] Park
study has also confirmed the impact of educational intervention on increasing women's
knowledge and participation in cervical cancer screening program.[20]
Following the intervention, the mean score of perceived susceptibility has been increased in the
intervention group, but we are facing a decrease in the perceived susceptibility in control group.
This significant difference indicates that educational intervention on the basis of Health Belief
Model causing women to be awarded of being susceptible to cervical cancer. Significant increase
in perceived susceptibility also emphasized by Hazavehei, Yakhfrooshha, and Shojaeezadeh
studies.[14,15,19]
In contrast with our findings in park and colleagues study, the perceived susceptibility in both
intervention and control groups did not have any effect on participating in cervical cancer
screening program. They considered insufficient intervention time for changing the attitudes to
be the reason.[20]
With regards to perceived severity, the mean scores increased in intervention group following
education program. That is, educational intervention based on HBM increased perceived severity
regarding cervical cancer, which is similar with the result of other studies.[15,21]
Based on our study findings, perceived benefits in both groups were desirable before the
intervention. This showed that women in both groups were aware of the resulted benefits from
doing pap smear. These findings were also proved by other studies.[14,17] The emphasis on
perceived benefits has been emphasized in another study for women persuasion to do the
test.[2023]
According to the findings, difference between intervention and control groups about perceived
barriers was not significant before the intervention, but educational intervention increased
perceived barriers in intervention group. These findings were supported by Mc Farland and
colleagues study who stated that the women, who had more barrier perception, had less
performance regarding doing pap smear test during past 5 years.[18] Psychological barrier like
fear and embarrassment have been the most important barriers in women in lee study.[22] It may
refer to effectiveness of educational intervention based on the Health Belief Model that has
caused the individuals in the intervention group to overcome to barriers. In the other performed
studies based on the model, the education has been able to reduce the barrier on performing the
health activities.[24,25]
In relation to cues to action in the intervention group, 42.86% have chosen the health staff as the
performance guide which has been increased to 57.14% after education. This is similar with the
results of Enjzab and colleague study.[26] In Akbari study women who have done the pap smear
test regularly have considered the health care providers encouragements as the most important
cues to action[21] In the present study, majority of participants (97.4%) in intervention group
have done the test after intervention and the only one person avoided doing the test because of
financial ability to pay the cost. This indicates that financial support and providing free or low
cost services can improve health behavior of women regarding doing pap test. Also, in control
group, after the intervention, one person (2.85%) has done the test due to the sensitivity resulted
from answering the questionnaire. This study reveals the considerable increase in intervention
group practice as a result of educational intervention, which were also proved in other
studies.[2730] As general, the results of the study imply that education based on Health Belief
Model lead to giving pap smear test in women. By considering the benefit of giving pap smear as
a useful screening tools, educational intervention based on Health Belief Model is recommended
in health centers. The study was limited to women who referred to the health centers and had a
limited number of participants too. Further research must have participants from different groups
of women, increasing the number of participants would also allow for a more robust evaluation
and analysis. This study had pre- and postintervention measurements at two times, which showed
only the short-term effects of the intervention.
Go to:
ACKNOWLEDGEMENTS
The authors would like to thank the participants and health center employees who willingly
participated in the study.
Go to:
Footnotes
Source of Support: Nil.
Conflict of Interest: None declared.
Go to:
REFERENCES
1. Cervical cancer screening in developing countries: Report of a WHO Consultation. Geneva:
WHO; 2002. World Health Organization.
2. Dell DL, Chen H, Ahmad F, Stewart DE. Knowledge about human papillomavirus among
adolescents. Obstet Gynecol. 2000;96:6536. [PubMed]
3. Koss LG. The Papanicolaou test for cervical cancer detection: A triumph and a tragedy.
JAMA. 1989;261:73743. [PubMed]
4. Blackman DK, Bennett EM, Miller DS. Trends in self-reported use of mammograms (1989
1997) and Papanicolaou tests (19911997)- Behavioral Risk Factor Surveillance System.
MMWR CDC Surveill Summ. 1999;48:122.
5. Chen MS, Jr, Hawks BL. A debunking of the myth of healthy Asian Americans and Pacific
Islanders. Am J Health Promot. 1995;9:2618. [PubMed]
6. Pitts M, Clarke T. Human papillomavirus infections and risks of cervical cancer: What do
women know? Health Educ Res. 2002;17:70614. [PubMed]
7. Bingham A, Bishop A, Coffey P, Winkler J, Bradley J, Dzuba I, et al. Factors affecting
utilization of cervical cancer prevention services in low-resource settings. Salud Pblica de
Mxico. 2003;45:28391.
8. Behtash N, Ghaemmaghami F, Ayatollahi H, Khaledi H, Hanjani P. A case control study to
evaluate urinary tract complications in radical hysterectomy. World J Surg Oncol. 2005;3:12.
[PMC free article] [PubMed]
9. Mousavi A, Karimi Zarchi M, Gilani MM, Behtash N, Ghaemmaghami F, Shams M, et al.
Radical hysterectomy in the elderly. World J Surg Oncol. 2008;6:38. [PMC free article]
[PubMed]
10. Ghaemmaghami F, Karimi Zarchi M, Mousavi A, Mohammad ZA, Fallahi A. Results of
cervical cone excision biopsy in iran. Asian Pac J Cancer Prev. 2008;9:457. [PubMed]
11. Glanz K, Rimer BK, Viswanath K. Health behavior and health education: Theory, research,
and practice. 4th ed. San Francisco: John Wiley and Sons; 2008.
12. Stretcher VJ, Rosenstock IM. The Health Belief Model. In: Glanz K, Lewis FM, Rimer BK,
editors. Health behavior and health education. San Francisco: Jossey-Bass; 1997. pp. 4159.
13. Sharifirad Gh, Entezari MH, Kamran A, Azadbakht L. The effectiveness of nutritional
education on the knowledge of diabetic patients using the health belief model. J Res Med Sci.
2009;14:16. [PMC free article] [PubMed]
14. Rahmati M. The effect of educational program based on H.B.M Model on the women
practice about Pap smear test [dissertation] Isfahan: Isfahan University of Medical Sciences;
2008.
15. Shojaeizadeh D, Hashemi SZ, Moeini B, Poorolajal J. The Effect of Educational Program on
Increasing Cervical Cancer Screening Behavior among Women in Hamadan, Iran: Applying
Health Belief Model. J Res Health Sci. 2011;11:205. [PubMed]
16. Baghyani-moghaddam MH. Survey on knowledge, attitude and practice of 15-49 years age
group married women related to Pap smear test in Yazd city in 2001. J Mazandaran Univ Med
Sci. 2003;13:7985.
17. Moreira ED, Oliveira BG, Ferraz FM, Costa S, Costa Filho JO, Karic G. Knowledge and
attitude about human papilloma Virus, Pap Smear and Cervical cancer among young Woman in
brazil: Implieation for health education and prevention. Int J Gynecol Cancer. 2006;16:599603.
[PubMed]
18. Macfrland DM, William F. Cervical cancer and pap smear Screening in Botswana:
Knowledge and perceptions. Int Nurs Rev. 2003;50:16775. [PubMed]
19. Yakhforoshha A, Solhi M, Ebadifard-Azar F. Effects of education via health belief model on
knowledge and attitude of voluntary health workers regarding pap smear in urban centers of
qazvin. Faculty Nurs Midwifery Q. 2008;18:2530.
20. Park S, Chang S, Chung C. Effects of a cognition-emotion focused program to increase
public participation in Papanicolaou smear screening. Public Health Nurs. 2005;22:28998.
[PubMed]
21. Akbari F, Shakibazadeh E, Pourreza A, Tavafian SS. Barriers and Facilitating Factors for
Cervical Cancer Screening: A Qualitative Study from Iran. Iran J Cancer Prev. 2010;4:17884.
22. Lee E, Tripp-Reimer T, Miller A, Sadler G, Lee S. Korean American Women's Beliefs About
Breast and Cervical Cancer and Associated Symbolic Meanings. Oncol Nurs Forum.
2007;34:71320. [PMC free article] [PubMed]
23. Mobaraki A, Mahmoudi F, Mohebi Z. The Knowledge, Attitude & Practice of Women
Working at Yasouj Hospitals Regarding Pap Smear Test. J Gorgan Bouyeh Fac Nurs Midwifery.
2008;5:2935.
24. Karimi M, Ghofranipour FA, Heidarnia A. The effect of health education based on health
belief model on preventive actions of aids on addict in zarandieh. J Guilan Univ Med Sci.
2009;18:6473.
25. Sharifi-rad GR, Hazavei MM, Hasanzadeh A, Danesh-amouz A. The effect of health
education based on health belief model on preventive actions of smoking in grade one, middle
school students. Arak Med Univ J. 2007;10:18.
26. Enjezab B, Faraj Khoda T, Bokaei M. Barriers and motivators related to cervical and breast
cancer screening. J Shahid Sadoughi Univ Med Science Health Serv. 2004;12:1414.
27. Hou SI, Fernandez ME, Parcel GS. Development of a Cervical cancer Educational Program
for Chinese Woman using Intervention Mapping. Health Promot Pract. 2004;5:807. [PubMed]
28. Papa D, Moore Simas TA, Reynolds M, Melnitsky H. Assessing the role of education in
women's knowledge and acceptance of adjunct high-risk human Papillomavirus testing for
cervical cancer screening. J Low Genit Tract Dis. 2009;13:6671. [PubMed]
29. Nguyen TT, McPhee SJ, Nguyen T, Lam T, Mock J. Predictors of cervical Pap smear
screening awareness, intention, and receipt among Vietnamese-American women. Am J Prev
Med. 2002;23:20714. [PMC free article] [PubMed]
30. Gichangi P, Estambale B, Bwayo J, Rogo K, Ojwang S, Opiyo T, et al. Knowledge and
practice about cervical cancer and pap smear testingamong patients at Kenyatta National
Hospital, Nairobi, Kenya. Int J Gynecol Cancer. 2003;13:82733. [PubMed]

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CMAJ >
v.183(5); Mar 22, 2011 >
PMC3060184

CMAJ. 2011 March 22; 183(5): 563568.
doi: 10.1503/cmaj.101156
PMCID: PMC3060184
Management of Papanicolaou test results
that lack endocervical cells
Lizette Elumir-Tanner, MD and Meghan Doraty, BHSc, for the Southern Alberta Primary Care Research
Network (SAPCReN)
Author information Copyright and License information
Go to:
The case
Mrs. McTavish is a 25-year old patient whose Papanicolaou (Pap) test results have come back
from the laboratory. The smear is described as satisfactory for evaluation; however, it is noted
that an inadequate number of endocervical cells were present in the sample. The results of the
patients past Pap tests have been satisfactory for evaluation and negative for abnormality. She is
otherwise well. Her physical examination, including pelvic examination, showed nothing
unusual.
Rates of cervical cancer have been declining in Canada since the implementation of the
Papanicolaou (Pap) smear, with reduction in both incidence (from 11.1 per 100 000 in 1970
1972 to 5.2 per 100 000 in 19941996) and mortality (7.9 per 100 000 in 19531955 to 1.9 per
100 000 in 19951997).
1
Further improvements will depend on the continuance of screening for
cervical cancer and the effectiveness of screening tools. The Bethesda System the
conventional system for reporting cervical cytologic diagnoses provides feedback about
specimen adequacy using the categories satisfactory or unsatisfactory.
2
Primary health care
providers may receive Pap test results that are identified as satisfactory but accompanied by a
note that indicates a sample from the transformation zone is lacking. Some provincial and
national guidelines are unclear about how clinicians should respond to this type of report.
Because of this uncertainty, we sought to review the current evidence on the topic. How should a
care provider proceed with screening when faced with an otherwise satisfactory Pap smear that
lacks sampling from the transformation zone? If physicians continue with regular screening
intervals without special attention to the lack of endocervical cells, are cervical abnormalities
being missed?
Go to:
Literature review
We searched MEDLINE from 1975 to the end of July 2010 using the following combination of
keywords and subject headings: unsatisfactory Pap smear, endocervical component,
endocervical status, endocervical cells and Pap smear, Pap smear and quality and
abnormal Pap smear. Bibliographies from the identified articles were manually searched.
Summary sites such as Towards Optimal Practice (Alberta) and Cancer Care Manitoba were also
reviewed in July 2010. We identified 462 citations, and reviewed 53 full-text articles. Papers
were excluded if they were written in a language other than English, if they did not discuss the
topic of Pap smear quality and presence or absence of endocervical cells, and if there were
insufficient data to draw conclusions. Twenty-four articles were included in our review and are
summarized in Appendix 1 (available at www.cmaj.ca/cgi/content/full/cmaj.101156/DC1).
The level of evidence was determined by the hierarchy developed by the Canadian Task Force
on the Periodic Health Examination,
3
according to which the highest level of evidence (Level I)
derives from at least one randomized controlled trial, and the lowest level derives from the
opinion of experts (Level III). The evidence identified in our search was predominantly Level II,
indicating that the literature contained mainly cohort, cross-sectional and casecontrol studies.
No randomized controlled trials, systematic reviews or meta-analyses were found.
Go to:
What is an adequate sample?
The effectiveness of screening using the Pap smear relies on adequate sampling from the cervix.
1

Although a conclusive definition of adequate sample remains elusive, the retrieval of
endocervical cells from an area of the cervix known as the transformation zone or
squamocolumnar junction, from which most abnormalities arise,
4
has historically been
considered an indication of quality.
5
Some older studies
514
have shown a relationship between
the presence of endocervical cells and the identification of cervical abnormality. Such findings
are consistent with the hypothesis that samples with endocervical cells are more likely to detect
atypia. However, more recent research
1528
has shown that the absence of endocervical cells is
not necessarily associated with a higher risk of cervical abnormality.
Go to:
What do the guidelines recommend?
Not all provinces and territories in Canada have guidelines for screening for cervical cancer or a
screening program (Table 1). Of those that do,
2935
most do not definitively address how to
respond to a Pap smear result when it lacks a sample from the transformation zone. Guidelines in
Nova Scotia
34
and in Manitoba
32
suggest early repeat testing may not be necessary. The recently
revised guidelines in Alberta
29
note that the sample may still be satisfactory if endocervical cells
are missing.

Table 1:
Clinical guidelines for treatment when transformation zone cells are not present in sample
International guidelines vary. Recent guidelines from the United Kingdom
36
recommend testing
every three years for women aged 25 to 49 years, but make no mention of what to do should
results not include endocervical cells. Australian guidelines,
37
which recommend screening every
two years, cite retrospective cohort studies and note that the quality of a smear is not determined
by the presence or absence of endocervical cells. The American Cancer Society
38
recommends
annual repeat screening for women whose Pap smears show no endocervical cells, or earlier
repeat testing for certain women. These guidelines do not clarify which women qualify for early
repeat testing; this ambiguity may cause confusion for physicians about who and when to retest.
Go to:
What is the evidence?
The debate regarding the significance of endocervical cells was sparked when initial research
found that the presence of endocervical cells on a smear was related to an increase in detection of
abnormalities of the cervix.
510,12,13
One study
8
assessing the cytologic histories of 376 women
diagnosed with invasive carcinoma of the cervix found that endocervical cells were seen less
often in smears reported as negative (45.5%) than in those with atypia (84.4%) and those with
cervical intraepithelial neoplasia (97.8%). This difference was significant (p < 0.001), suggesting
that the composition of the smear was related to the detection of abnormalities. To best identify
atypia, the authors argued, a repeat test is necessary.
Further studies verified this finding. Another study
10
reviewed 36 853 Pap smears to investigate
the effect of the presence or absence of endocervical cells on the detection rate of abnormalities,
with the result that cervical intraepithelial neoplasia (CIN) was detected 2.3 times more often in
smears with endocervical cells. Two further studies reviewed false-negative Pap smears from
patients who had a confirmed diagnosis of cervical cancer. Many of these smears (35 of 94
[37%]
12
and 30 of 47 [64%]
13
) were missing endocervical cells. Based on this evidence, it
became standard practice for physicians to sample endocervical cells to improve the chances that
abnormalities were caught and to test repeatedly as deemed necessary when endocervical cells
were not present.
However, recent retrospective studies
15,21,23,24
assessed the effect of the presence or absence of
endocervical cells on the rate of detection of abnormalities by comparing the concordance
between cytology (assessed by Pap smear) and histology (assessed by colposcopic examination).
One study
23
examined 151 instances of histologically diagnosed CIN II and III and retrieved the
Pap tests to determine discordant, or false-negative, cases. Of the 13 Pap tests lacking an
endocervical component, only 3 (23%) were discordant, whereas of the 138 Pap tests with an
endocervical component, 38 (27%) were discordant. There was no significant difference between
these groups (p > 0.5), suggesting that the inclusion of an endocervical component within a
smear does not guarantee that an existing abnormality will be detected. Other casecontrol
studies
17,18,20,25
support this finding. Thus an endocervical component may not be a good
indicator of specimen quality, and its lack may not indicate that early repeat testing is necessary.
The most convincing evidence, however, is found in longitudinal studies in which patients were
prospectively evaluated for the presence of endocervical cells and for subsequent abnormal Pap
smears.
16,22,26,27
Methods of reporting cervical atypia have changed over the years, so among
these studies, the measured outcome varied (i.e., CIN v. low-grade squamous intraepithelial
lesion v. atypia). As well, the length of follow-up differed among studies. However, the essence
of the findings was consistent: women whose Pap smears did not contain endocervical cells were
not at higher risk for subsequent detection of cervical abnormalities than those whose smears did
contain endocervical cells.
Perhaps the most convincing longitudinal study was performed by Mitchell in 2001.
22
Four
cohorts of women who had an initial negative Pap smear and a subsequent Pap smear three years
later were studied. Endocervical cells were present in both entry and exit smears in cohort A (n
=18618); endocervical cells were absent in the entry smear and present in the exit smear in
cohort B (n = 16 632); endocervical cells were present in the entry smear and absent in the exit
smear in cohort C (n = 16 291); and both smears had absent endocervical cells in cohort D (n =
8603). One would expect a higher incidence of disease in cohort B compared with cohort A,
given that cohort B would be more likely to exhibit missed abnormalities in the entry smear
because of the lack of endocervical cells. This was not the case; cohort B had no more histologic
high-grade disease than cohort A (standardized incidence ratio for cohort B compared with
cohort A 0.89, 95% confidence interval [CI] 0.671.12). This result suggests that the absence of
an endocervical component is not linked to increased rates of subsequent abnormality for both
histologic and cytologic outcomes. The author concluded that early repeat testing is unnecessary.
Another key finding in Mitchells study was that cohorts B, C and D showed less disease than
cohort A. This finding raises a new question: Does the presence of endocervical cells actually
indicate a greater risk of cervical abnormality? Mitchell and Medley suggested in an earlier
study
17
that the transformation zone may be more easily sampled when abnormality is present
because of the reduced adhesiveness of cells. A recent blinded, comparative cross-sectional
study
14
showed that cervical smears with a higher number of endocervical cells (> 50 cells) was
significantly associated with the presence of at least 10 squamous atypical cells (odds ratio 2.87,
95% CI 1.545.35). This finding suggests that there is a positive association between the number
of endocervical cells and the number of atypical cells in a smear, and supports the hypothesis
that endocervical cells may be more accessible in cervices with abnormalities. The presence of
these cells may be a marker in women with a greater risk of cervical abnormality, indicating a
higher risk for disease. However, more research is needed to explore this hypothesis.
Although the longitudinal studies described present the strongest evidence available, some
limitations do exist with this type of study. Other explanations for their findings are possible. For
example, in longitudinal studies with cytologic follow-up, Pap smears without endocervical cells
may be less sensitive than those with endocervical cells. Thus, abnormalities may be missed on
subsequent Pap tests that do not include an endocervical component. In longitudinal studies with
histologic data, only positive cytologic results are usually verified. If Pap tests without
endocervical cells are less sensitive, these test results are less likely to be subject to histologic
verification. As a consequence, verification bias may occur, giving the impression that such
women are at low risk for cervical abnormalities when they are actually not. Studies with shorter
follow-up periods are more prone to this bias. More research is required to address these
concerns.
Go to:
Should women whose Pap smears lack endocervical cells be
retested?
Studies using multiple methodologies have attempted to determine the role of endocervical cells
in Pap tests in the detection of cervical cancer, but the conclusions of these studies have often
been contradictory. According to the criteria of the Canadian Task Force on Preventive Health
Care,
39
contradictory evidence receives a C grade, meaning that no recommendation can be
made. However, the majority of recent, rigorous and validated studies support the view that the
presence of endocervical cells is not necessary for a Pap smear result to be valid and may
possibly be a risk factor for cervical abnormality. As such, this body of research represents fair
evidence to recommend avoiding early repeat testing for those women whose Pap smears are
negative and do not contain an endocervical component.
Go to:
Are there differences among Pap smear sampling
techniques?
Efforts have been made to improve the sampling methodology for the collection of adequate Pap
smear samples. Over the years, accepted sampling techniques have changed. Studies included in
our review used a variety of sampling techniques, such as wooden spatula and cotton swab
19,25

and Thin-Prep Pap tests.
23
Many of the studies we reviewed did not differentiate among
sampling techniques. However, Mitchell and Medley
16
found that using a combination of
cytobrush and spatulae, compared with just using spatulae, improved the probability of having
endocervical cells reported in the sample. It is not known, however, whether different sampling
techniques affect detection rates of atypia depending on the presence or absence of endocervical
cells. Therefore, we suggest that clinicians continue to use the sampling technique recommended
by guidelines in their area.
There may be other factors that influence the collection of an adequate sample. For instance, the
Alberta guidelines
29
suggest some conditions for optimal collection, including the stipulation that
patients refrain from use of contraceptive creams or jellies, douching, intravaginal medication
and sexual intercourse for 24 hours before the test. However, a review of the evidence
underlying these recommendations is beyond the scope of this paper. To optimize the collection
of a specimen, clinicians should follow the manufacturers directions.
Go to:
Gaps in knowledge
This review is not designed to posit a biological mechanism that might explain the contradictory
claims of the studies examined. Future inquiry may seek to validate the hypothesis of Mitchell
and Medley
17
that when atypia is present, endocervical cells slough off the transformation zone
more readily, which accounts for their frequent presence in positive samples. Testing other
hypotheses that seek to reconcile the contradictory evidence is also important for a full
understanding of the role of endocervical cells in the development of cervical cancer. Various
sampling methods were used in the studies examined by this review, but this paper does not
address the effectiveness of different sampling techniques.
More studies are needed to determine whether there is a higher incidence of invasive cervical
cancer among women whose Pap smears lack endocervical cells. Prospective, longitudinal
studies of longer duration, encompassing the onset of atypia to the development of cervical
cancer, would also benefit this area of study. A close examination of regional guidelines is also
recommended to ensure that the most accurate and up-to-date information from rigorous research
is being relayed to practitioners.
Go to:
The case revisited
Mrs. McTavish returns to review her Pap test results. Her physician assures her that the result is
normal and that there will be no change in the scheduling of her screening Pap tests. She
wonders about the meaning of the phrase inadequate number of endocervical cells present
included in the report. The physician explains that there is a zone in the cervix from which most
abnormalities arise. There has been some suggestion that, when there is a lack of these
endocervical cells on a Pap smear, perhaps this zone was not adequately sampled. However, a
balance of research articles shows that a lack of endocervical cells on a Pap test result does not
lead to an increased risk of abnormality for someone like Mrs. McTavish. Therefore, Mrs.
McTavish can continue with regularly scheduled Pap tests. Local guidelines should be consulted
to determine the timing of the next Pap test.
Go to:
Conclusion
Based on the strongest evidence available, when a physician is confronted with a Pap smear
result lacking endocervical cells, an appropriate course of action would be to schedule the patient
for regular testing unless there is suspicion of abnormality, such as abnormal bleeding or other
clinical indicators of cervical abnormality. The patient would not be required to undergo an
uncomfortable and invasive procedure a second time. Minimizing unnecessary procedures can
save the health system considerable expenditures in the form of physician time, testing supplies,
laboratory analyses and other costs. It would be helpful for clinicians if provincial and national
guidelines were updated to reflect recent research in this area. Local guidelines, however, are an
excellent resource for best practices in Pap smear techniques.
Key points
Some provincial, national and international guidelines are unclear about how to proceed when a
Papanicolaou smear result is reported as lacking a sample from the transformation zone.
Although controversy exists in the literature, the majority of recent rigorous studies do not
support early repeat testing for women whose smears lack a sample from the transformation
zone.
Unless abnormality is suspected or there are risk factors for cervical dysplasia, such patients may
be scheduled for testing at regular screening intervals.
Go to:
Supplementary Material
[Online Appendix]
Click here to view.
Go to:
Acknowledgements
The authors thank Neil Drummond, Tyler Williamson, Behnaz Somji and members of the
Southern Alberta Primary Care Research Network for their help in the development of this
paper.
Go to:
Footnotes
Competing interests: None declared.
This article has been peer reviewed.
Contributors: Both of the authors contributed to the planning and design of the article, the
review of the literature, and the drafting and revision of the manuscript. Both of them approved
the final version of the manuscript submitted for publication.
Go to:
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cc/media/cancercare/CCPPManual09WEB.pdf (accessed 2010 July 14).
35. Steban M. Clinical manifestation and diagnosis of HPV-related disease In: Canadian consensus
guidelines on human papillomavirus. J Obstet Gynaecol Can 2007;29Suppl 3:S114.
36. Cervical Screening Wales quality manual. Section 2 core reference section. National Health
Service; London (UK): 2009. Available:
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37. Screening to prevent cervical cancer: guidelines for the management of asymptomatic women with
screen detected abnormalities. Canberra (Australia): National Health and Medical Research Council;
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38. Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society Guideline for the early detection
of cervical neoplasia and cancer. CA Cancer J Clin 2002;52:34262. [PubMed]
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Can Fam Physician >
v.53(8); Aug 2007 >
PMC1949259

Can Fam Physician. 2007 August; 53(8): 13281329.
PMCID: PMC1949259
Papanicolaou smears
To swab or not to swab
Narpinder Hans, MD CCFP
Family physician at the Meadowbrook Medical Clinic and is Associate Clinical Professor in the
Department of Family Medicine at the University of Alberta in Edmonton
Andrew J. Cave, MB MClSc CCFP FRCGP
Professor in the Department of Family Medicine at the University of Alberta in Edmonton
Olga Szafran, MHSA
Research Coordinator in the Department of Family Medicine at the University of Alberta
Gordon Johnson, MD FRCPC
Director of Cytopathology at Dynacare Kasper Medical Laboratories in Edmonton
Ann Glass, RN
Manager of the Family Medicine Clinic at the University of Alberta Hospital in Edmonton
G. Richard Spooner, MD CCFP FCFP
Professor and the Chair in the Department of Family Medicine at the University of Alberta. At
the time of the study
Philip J. Klemka, MD CCFP
Assistant Professor in the Department of Family Medicine at the University of Alberta. He is
now a family physician in Edmonton
Shirley Schipper, MD CCFP
Author information Copyright and License information
Go to:
Abstract
OBJECTIVE
To determine whether cleaning the cervix with a cotton swab affects the quality of the
conventional Papanicolaou smear.
DESIGN
Prospective, single-blinded randomized case-control study.
SETTING
Two academic family medicine teaching units and 1 community family practice site.
PARTICIPANTS
Female patients, 18 to 65 years of age, who presented for a routine Pap smear in the family
practice setting were randomized into the Swab Group (n = 300) or the No Swab Group (n =
316).
INTERVENTION
Before the Pap smear, the cervix of patients in the Swab Group was wiped with a cotton swab
until visibly free of mucus. In the No Swab Group, the cervix was not cleaned with a cotton swab
before the Pap smear.
MAIN OUTCOME MEASURES
The quality of the conventional Pap smear was determined by the presence or absence of
endocervical cells noted on the pathology report.
RESULTS
There was no major difference in the quality of the Pap smear in terms of the adequacy of
endocervical cells between the Swab and No Swab Group.
CONCLUSION
Cleaning the cervix with a cotton swab does not appear to affect the quality of the conventional
Pap smear in terms of adequacy of endocervical cells. This implies that the practice of wiping or
not wiping the mucus from the cervix before taking the Pap smear can be employed at the
discretion of the clinician.
Go to:
RSUM
OBJECTIF
Dterminer si le fait de nettoyer le col de lutrus avec un couvillon affecte la qualit du test
conventionnel de Papanicolaou.
CONCEPTION
Une tude cas-tmoins randomise prospective simple insu.
CONTEXTE
Deux units denseignement universitaire en mdecine familiale et 1 cabinet de pratique
familiale dans la communaut.
PARTICIPANTES
Des patientes de 18 65 ans qui se sont prsentes pour un test de Pap routinier dans un milieu
de pratique familiale ont t choisies au hasard pour faire partie du groupe avec couvillon (n =
300) ou de celui sans couvillon (n = 316).
INTERVENTION
Avant le frottis de Pap, le col de lutrus des patientes du groupe avec couvillon tait essuy
avec un coton-tige pour enlever le mucus visible. Dans le groupe sans couvillon, le col ntait
pas nettoy avec un coton-tige avant le frottis de Pap.
PRINCIPALES MESURES DES RSULTATS
La qualit du frottis de Pap conventionnel tait dtermine par la prsence ou labsence de
cellules endocervicales dans le rapport du pathologiste.
RSULTATS
Il ny avait pas de diffrences majeures entre le groupe avec couvillon et celui sans couvillon
dans la qualit du frottis de Pap en ce qui avait trait au nombre suffisant de cellules
endocervicales.
CONCLUSION
Le nettoyage du col de lutrus avec un coton-tige ne semble pas affecter la qualit du frottis de
Pap conventionnel en ce qui a trait au nombre suffisant de cellules endocervicales. La pratique
dessuyer ou non le mucus du col avant le frottis de Pap est donc laisse la discrtion du
clinicien.
The purpose of the Papanicolaou smear is to obtain cell samples from the endocervical-
squamous cell junction of the cervix (ie, the area in which cervical cancer most frequently
develops). During the routine performance of Pap smears, physicians often note the presence of
mucus on the cervix. The effect of removing this mucus before sampling the cervical epithelium
is debated. Some clinicians believe that the mucus contains a valuable proportion of the
diagnostic cells that are being sampled.
1
However, sampling large quantities of thick mucus onto
the slide can make it difficult for the screening technician to identify the cellular component.
Evidence that wiping the mucus from the cervix removes diagnostic cells and produces an
inadequate sample is lacking.
Inadequate tests can result in false-negative conclusions or, if the test is repeated, cause patients
anxiety, inconvenience, and resource overexpenditure. Many Pap tests are not repeated promptly,
putting patients at risk of delayed diagnosis.
2
In a primary care setting in British Columbia (BC),
Kotaska and Matisic
3
investigated the adequacy of samples after swabbing of the cervix. Using
the patients last test as a historical control and also comparing the results with the BC statistical
averages, they found a lower frequency of smears with inadequate endocervical cells in women
who had the cervix cleaned with a cotton swab before the Pap smear was taken. The authors
called for a prospective, randomized controlled trial to be conducted. Researchers from
Wisconsin performed an analysis of adequacy using a broom (as is used in colonoscopy) and
alternative specimen preservation techniques, dry slide or liquid immersion,
1
but did not relate
their results to swabbing. Addition of the cytologybrush as a routine augment to the spatula has
been shown to result in a 30% decrease in the number of inadequate samples.
4

No prospective, randomized controlled trial of cleaning of cervical mucus has been reported in
the literature. We designed such a study to determine whether cleaning the cervix with a cotton
swab affects the quality of the Pap smear performed in the family practice setting.
Go to:
METHODS
Study design and setting
This was a prospective, single-blinded randomized case-control study. Using an odd-even
numbering system, female patients presenting for a routine Pap smear were randomly assigned to
the Swab Group or the No Swab Group. Randomization was performed by the family practice
nurse after patient consent was obtained and before a doctor saw the patient. Neither the
physicians nor the patients were blinded to the study procedure; only the pathologist was blinded
to the study. The study was conducted at 2 academic family medicine teaching units in the
Department of Family Medicine at the University of Alberta in Edmonton and 1 community
family practice site in Edmonton, Alberta. The clinicians performing the Pap test included 13
family physicians, 24 family medicine residents, and 1 nurse practitioner. The study was
conducted from June 2002 to May 2003. Ethical approval for the study was obtained from the
Health Research Ethics Board at the University of Alberta.
Patients and study procedures
The study sample consisted of consecutive female patients, 18 to 65 years of age (including
prenatal patients), who presented for a routine Pap smear and consented to participate in the
study. Women who had a previous hysterectomy were excluded. Before the Pap smear was
taken, the cervix of each patient in the Swab Group was wiped with a cotton swab until free of
visible mucus. Each patient in the No Swab Group did not have her cervix wiped with a cotton
swab before the Pap smear, regardless of the amount of mucus present on the cervix. Orientation
sessions on the study were provided to all physicians and the nurse practitioner. This included
standardization of the Pap smear procedure using both spatula and cytology brush in sequence
for each test.
Data collection and outcome measures
Data were collected prospectively on a data-collection form clipped on top of patients charts.
The family practice nurse noted on the form the patients age, menopausal status, and the study
group into which the patient had been randomized. At the time of the Pap smear, the physician
recorded the appearance of the cervix in terms of its redness (normal, moderately red, or beefy
red), friability (normal, friable, or very friable), and atrophy (yes or no), as well as the amount of
mucus present on the cervix (dry cervix, light mucus, or heavy mucus). The degree of severity of
these conditions of the cervix was based on the subjective clinical assessment by the physician.
When the pathology report was available, the study nurse obtained from the specimen report the
following data: the quality of the Pap smear, the result of the Pap smear, and whether a repeat
Pap smear was required. The quality of the Pap smear was determined by the presence or
absence of adequate numbers of endocervical cells noted on the pathology report. An
inadequate specimen report indicated that no or very few cells of any kind were present, and
adequate, but limited was defined as having good cellular component (presence of other cells
sampled), but no or very few endocervical cells seen. The former would suggest that a repeat
smear be performed, and the latter would require a clinical decision on risk to determine how
soon the next smear test would be indicated. Either case was reported by the pathologist as
repeat Pap smear required.
Data analysis
Data analysis was performed using SPSS 12.0 for Windows and consisted of frequencies and
summary statistics. Differences between the 2 groups were tested using
2
and the Fisher exact
test, where appropriate. An level of .05 was used to test for statistical significance. With a
power of 80% and an level of .05, our study sample size was sufficient to detect a reduction of
greater than 46% in inadequate smears from the 1998 Alberta provincial baseline of 15%.
4

Go to:
RESULTS
There were 772 consecutive patients approached to take part in the study. A total of 156 (20%)
declined or were excluded. Seventy (45%) of these 156 were excluded because of previous
hysterectomy. A total of 616 patients were recruited into the study (ie, 300 in the Swab Group
and 316 in the No Swab Group). The 2 groups were similar in age, menopausal status, the
redness, friability and atrophy of the cervix, and the amount of mucus on the cervix (Table 1).
There was no significant difference in the quality of the Pap smear in terms of the adequacy of
endocervical cells between the Swab and No Swab Groups (Figure 1). The rate of repeat Pap
smears, as recommended by the pathologist, was similar between the groups (ie, 28.3% in the
Swab Group and 25.0% in the No Swab Group). The main reason for recommended repeat Pap
smears was limited cellular component (14.3% and 10.8%). Cellular changes accounted for 7.7%
and 9.5% and other factors, such as patients previous history, for 6.3% and 4.7% (Table 2).

Table 1
Characteristics of Papanicolaou smear patients by study group

Figure 1
Adequacy of sample

Table 2
Repeat Papanicolaou smears
Swabbing or not swabbing in the presence of varying degrees of mucus present did not affect the
adequacy of endocervical cells (Table 3). There was also no difference between the groups in
terms of adequacy of endocervical cells controlling for age, menopausal status, and friability,
redness, or atrophy of the cervix.

Table 3
Laboratory report by group for various amounts of mucus
Go to:
DISCUSSION
This prospective, single-blinded randomized trial found that cleaning the cervix with a cotton
swab before taking the Pap smear sample did not affect the adequacy of endocervical cells on the
conventional Pap smear. These findings are consistent with another study that reported no
statistically significant difference in the quality of the Pap smear, in terms of adequacy of
endocervical cells, when using a Weck-cel sponge to collect endocervical secretions.
5
Our
findings differ, however, from those of a recent Canadian study that found an association
between cleaning with an oversized cotton swab and a lower frequency of smears with
inadequate endocervical cells.
3

Current guidelines of the Alberta Medical Association are undecided on the wiping of the cervix.
They state that excess mucus on the cervix may be removed with a cotton swab prior to
sampling if this is a problem.
6
Our study findings do not refute this position.
The necessary repeat of Pap tests because endocervical cells are absent from the sample is not a
minor problem. Patients are inconvenienced by having to return and also by undergoing the
procedure again. Their anxiety about the importance of the inconclusive result often must be
addressed by clinicians. The repeat test rates of 14.3% and 10.8% because of sampling issues are
a marker of considerable patient distress.
It seems that the risk of removing diagnostic cells by swabbing is balanced by removing thick
impenetrable mucus that the technician cannot see through. It might seem reasonable to advise
removing heavy mucus and not swabbing a dry cervix, but the number of dry cervices in our
study does not allow us to comment on this (Table 3).
This study had some limitations. The specific elements of the study design are strengths of this
clinical trial. However, the numerous clinicians who performed the Pap smears, while reflecting
the real-world situation, might have jeopardized the standardization of the Pap smear technique.
Despite clinicians standardized training, heterogenous Pap smear techniques among clinicians
might have contributed to non-significant findings. There might have been interobserver
discrepancy in the subjective assessment by each clinician of the friability, redness, and amount
of mucus on the cervix, thereby resulting in non-significant findings for these characteristics.
The study findings apply only to conventional Pap smears and not to those obtained using liquid-
based cytology. Furthermore, the study examines only a single outcome (smear adequacy) and
not the comparative sensitivity of samples taken with or without swabbing.
Future studies should include randomization, multiple clinicians, and a larger sample size. If
heterogenous techniques did jeopardize standardization of Pap smear techniques, better training
might be required. The study should be repeated in another setting to confirm our findings.
Go to:
CONCLUSION
Cleaning the cervix with a cotton swab does not appear to affect the quality of the Pap smear in
terms of adequate samples of endocervical cells. This implies that the practice of wiping or not
wiping the mucus from the cervix before taking the Pap smear can be at the discretion of the
clinician.
Go to:
Acknowledgment
We thank Mary Wittenberg for data entry and Shufen Edmondstone for secretarial assistance.
The findings of this study were presented at the North American Primary Care Research Group
(NAPCRG) meeting in Orlando, Fla, on October 12, 2004.
Go to:
Notes
EDITORS KEY POINTS
When performing conventional Papanicolaou smears, physicians frequently encounter
mucus overlying the cervix. Some believe that the mucus contains valuable diagnostic
cells, while others believe that the mucus will obscure the cellular component on the
slide.
This randomized study found that swabbing or not swabbing made no difference in the
quality of the conventional Pap smear.
The authors caution that there are some limitations to their study, which include possible
heterogeneity in Pap smear technique by the numerous physicians who participated in the
study. They recommend that the study be repeated in another centre with a larger sample
size.
POINTS DE REPRE DU RDACTEUR
Lors dun frottis de Papanicolaou conventionnel, les mdecins sont souvent en prsence
de mucus sur le col de lutrus. Certains croient que le mucus contient des cellules utiles
dans le diagnostic, tandis que dautres sont davis que le mucus brouille la composante
cellulaire sur la lame.
Dans cette tude randomise, on a constat quavec ou sans couvillon, la qualit du
frottis de Pap conventionnel tait la mme.
Les auteurs avertissent les lecteurs que leur tude comporte certaines limites, notamment
lhtrog-nit de la technique du frottis de Pap, tant donn le grand nombre de
mdecins qui ont particip ltude. Ils recommandent que cette tude soit refaite dans
un plus grand centre, auprs dun plus important chantillonnage.
Go to:
Footnotes
This article has been peer reviewed.
Contributors
Dr Hans was involved in the conceptualization of the study, development of the study design,
data analysis and interpretation, and review of the manuscript. Dr Cave was involved in the
conceptualization of the study, development of the study design, development of the data-
collection form, data analysis and interpretation, and writing and reviewing the manuscript. Ms
Szafran provided methodological support to the project and was involved in the development of
the data-collection form, data anlaysis, and writing and reviewing the manuscript. Dr Johnson
participated in the conceptualization of the study, development of the study design, overseeing
the pathology testing, and reviewing the manuscript. At the time of the study, Ms Glass was the
research nurse who collected the data and reviewed the manuscript. Drs Spooner, Klemka, and
Schipper participated in the conceptualization of the study, development of the study design,
interpretation of the study findings, and review of the manuscript.
Competing interests
This project was funded by the Grey Nuns Family Medicine Research and Education Fund.
Go to:
References
1. Marchand L, Van Dinter M, Mundt M, Dingel W, Klein G. Current cervical cancer screening
practices of Dane County, Wisconsin primary care clinicians. WMJ. 2003;102(3):3540.
[PubMed]
2. British Columbia Cancer Agency. British Columbia Cancer Agency Annual Report 2000.
Vancouver, BC: British Columbia Cancer Agency; 2000.
3. Kotaska AJ, Matisic JP. Cervical cleaning improves Pap smear quality. CMAJ.
2003;169(7):6669. [PMC free article] [PubMed]
4. Dynacare Kasper Medical Laboratories. Pap smear reporting guidelines. Edmonton, Alta:
Dynacare Kasper Medical Laboratories; 2002.
5. Hildesheim A, Concepcion Bratti M, Edwards RP, Schiffman M, Rodriguez AC, Herrero R, et
al. Collection of cervical secretions does not adversely affect Pap smears taken immediately
afterward. Clin Diagn Lab Immunol. 1998;5(4):4913. [PMC free article] [PubMed]
6. Toward Optimized Practice. Screening for cervical cancer. Edomonton, Alta: Toward
Optimized Practice; 2007. [Accessed 2007 Mar 16]. Available from:
http://www.topalbertadoctors.org/top/cpg/cervicalcancer/cervicalcancer.htm.

Articles from Canadian Family Physician are provided here courtesy of College of Family Physicians of Canada
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Related citations in PubMed
Cervical cleaning improves Pap smear quality. [CMAJ. 2003]
[Prevention of cervix cancer. Comparison of the sample quality obtained using cotton
swab or cervical brush]. [Aten Primaria. 2000]
A randomized clinical trial comparing the Cytobrush and cotton swab for Papanicolaou
smears. [Obstet Gynecol. 1992]
Cervicovaginal involvement in pemphigus vulgaris: a clinical study of 77 cases. [Br J
Dermatol. 2008]
Computerized scanning devices for Pap smear screening: current status and critical
review. [Clin Lab Med. 1997]
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PMC3089673

Cancer Epidemiol Biomarkers Prev. Author manuscript; available in PMC 2012 May 1.
Published in final edited form as:
Cancer Epidemiol Biomarkers Prev. 2011 May; 20(5): 835843.
Published online 2011 March 23. doi: 10.1158/1055-9965.EPI-10-0880
PMCID: PMC3089673
NIHMSID: NIHMS282255
Evaluating the Efficacy of Lay Health
Advisors for Increasing Risk-appropriate
Pap Test Screening: A randomized controlled
trial among Ohio Appalachian women
Electra D. Paskett, Ph.D.,
1,2,3
John M. McLaughlin, M.S.,
1,2
Amy M. Lehman, M.A.S.,
4
Mira L.
Katz, Ph.D.,
1,5
Cathy M. Tatum, M.A.,
1
and Jill M. Oliveri, Dr.P.H.
1

Author information Copyright and License information
The publisher's final edited version of this article is available free at Cancer Epidemiol
Biomarkers Prev
Go to:
Abstract
Background
Cervical cancer is a significant health disparity among women in Ohio Appalachia. The goal of
this study was to evaluate the efficacy of a lay health advisor (LHA) intervention for improving
Pap testing rates, to reduce cervical cancer, among women in need of screening.
Methods
Women from 14 Ohio Appalachian clinics in need of a Pap test were randomized to receive
either usual care or an LHA intervention over a ten-month period. The intervention consisted of
two in-person visits with an LHA, two phone calls, and four post cards. Both self-report and
medical record review (MRR) data (primary outcome) were analyzed.
Results
Of the 286 women, 145 and 141 were randomized to intervention and usual care arms,
respectively. According to MRR, more women in the LHA arm had a Pap test by the end of the
study compared to those randomized to usual care (51.1% vs. 42.0%; OR=1.44, 95%CI: 0.89,
2.33; p=0.135). Results of self-report were more pronounced (71.3% vs. 54.2%; OR=2.10,
95%CI: 1.22, 3.61; p=0.008).
Conclusions
An LHA intervention showed some improvement in the receipt of Pap tests among Ohio
Appalachian women in need of screening. While biases inherent in using self-reports of
screening are well known, this study also identified biases in using MRR data in clinics located
in underserved areas.
Impact
LHA interventions show promise for improving screening behaviors among non-adherent
women from underserved populations.
Keywords: lay health advisor, natural helpers, cervical cancer, screening, Pap test, risk-
appropriate, Appalachia, health disparities
Go to:
Introduction
Rates of cervical cancer incidence have decreased roughly 75% since the introduction of the
Papanicolaou (Pap) test in 1950 (1). Although persistent infection with human papillomavirus
(HPV) causes the majority of cervical cancer, today, remaining morbidity and mortality caused
by cervical cancer is almost entirely the result of nonparticipation in screening and the absence
of proper and timely follow-up for abnormalities diagnosed by screening (27). Thus, efforts to
reduce the costs, both human and economic, of cervical cancer should focus on increasing
adherence to recommended cervical cancer screening guidelines and ensuring compliance with
treatment among women with abnormal findings, especially among women at higher risk for
developing cervical cancer.
Women in Appalachia comprise a U.S. population that is at notably higher risk for developing
and dying of cervical cancer. Rates of cervical cancer incidence and mortality are 12% and 21%
higher, respectively, in Appalachian Ohio counties compared to non-Appalachian counties in
Ohio (8). Many factors indicative of women living in this geographic region may contribute to
cervical cancer disparities, including unique values, beliefs, and attitudes about cervical cancer,
the social environment (limited healthcare access and public transportation, low socioeconomic
status), higher prevalence of HPV, providerpatient communication issues (including lack of
recommendation for screening), psychosocial factors (fear of cancer, stress), behavioral factors
(tobacco use, risky sexual activity), and lower rates of Pap test completion (812). Innovative
strategies to reach underserved populations that address these multiple levels should be tested in
Appalachian populations.
Lay Health Advisors (abbreviated LHA and synonymously referred to as promoters, community
health workers, natural helpers, or patient navigators) have emerged as a viable way to promote
the uptake of proper risk-appropriate screening and facilitate proper post-diagnostic follow-up in
vulnerable populations (1324). Risk appropriate cervical cancer screening (annually vs. every
23 years) is based on a womans risk (high vs. low) of developing cervical cancer as determined
by the presence of risk factors (e.g. history of sexually transmitted disease, smoking). In the
current complex and fragmented health care system, LHAs, especially in underserved
populations, can serve as a bridge between the formal health care system and the community-
based system of care and support. Utilizing LHAs has been previously effective in lowering rates
of infant mortality and low birthweight, increasing childhood immunization, helping patients
control hypertension, promoting smoking cessation, helping individuals with human
immunodeficiency virus (HIV) or mental illness find needed services, increasing the use of
screening tests for breast, cervical, prostate, and colorectal cancer, and promoting the use of
genetic counseling, preventive, and primary care services in various settings (13, 14, 1641).
LHAs typically are trusted individuals from the same community as participants and, in the
context of cervical cancer, have been trained to educate women about cervical health and the
importance of having a routine Pap test (15, 16, 25, 33, 42). In addition to providing education,
LHAs provide advice and advocacy, tangible aid, and emotional and logistical support women
may need to act on what they have been taught about screening. Working with health
practitioners, LHAs address contextual multi-level barriers to cancer screening and abnormal Pap
test follow-up, enhance access to screening, and reinforce tailored messages about risk-
appropriate screening guidelines (15, 16, 25, 32, 33, 42).
Few of these prior studies have been conducted among Appalachian populations, and
information about who benefits from LHA interventions and who is likely to be adherent to Pap
testing guidelines in Appalachia is sparse. The primary objective of this study was to evaluate the
efficacy of an LHA intervention program (versus usual care) designed to increase adherence to
risk-appropriate cervical cancer screening guidelines in Ohio Appalachiaa population at
elevated risk for the disease (8). Additionally, we examined other predictors of Pap test receipt
and compared the results of medical record review (MRR) with self-reports of Pap test receipt.
Go to:
Materials and Methods
Study Population
The Community Awareness Resources and Education (CARE) initiative was conducted from
March 2005 through February of 2009 as one of eight Centers for Population Health and Health
Disparities (P50) funded by the National Institutes of Health with the goal of addressing high
cervical cancer incidence and mortality rates in Ohio Appalachia (43). All participants in this
study (one of three studies comprising the CARE initiative) were from one of 14 participating
health clinics in Ohio Appalachia and were recruited in two phases. During the first phase
(March 2005 through June 2006), potential participants were asked to complete a baseline cross-
sectional interview to determine eligibility for this study as well as two other components of the
P50, and eligible participants were invited to participate. To increase efficiency, during the
second phase (July 2006 through February 2009) participants potential eligibility was
determined first by telephone survey, and only participants who were potentially eligible for this
study were asked to complete the baseline interview to determine final eligibility. Baseline
interviews were completed in person unless the participant requested that the interview be
completed by telephone.
To be eligible for the study, participants had to be female, age 18 or older, not pregnant, and a
resident of Ohio Appalachia. At the time the study was conducted, Ohio Appalachia comprised
29 (33.0%) counties in the state. Additionally, participants had to have been seen by a physician
in the clinic from which they were selected within the previous two years and have no history of
invasive cervical cancer or hysterectomy. Finally, to be eligible, participants had to be in need of
a Pap test based on risk-appropriate guidelines described previously (4445). Specifically,
women with any risk factors for cervical cancer (i.e., smoking, early age at first intercourse, five
or more sexual partners in a lifetime, or having a personal history or partner with a history of
HPV or a sexually transmitted infection) should have a Pap test annually, while women with no
identified risk factors should have a Pap test at least every three years. Although recommended
screening guidelines (46) do not stratify by behavioral risk factors, previous research suggests
that this may be important (44, 45). Women in Appalachia Ohio often to not visit healthcare
providers on a regular basis, live in a geographic region that has an increased HPV prevalence
rate, and have many behavioral factors which put them at increased risk for developing cervical
cancer. Informed consent procedures and study protocols were approved by the Institutional
Review Boards of The Ohio State University and the University of Michigan.
Randomization and Intervention Design
Participants were randomized to either the LHA intervention group or the usual care control
group via permuted block randomization that was stratified by clinic and administered through a
central database system. Clinical research nurses who performed the MRR, participant
interviewers, and the primary investigators were blinded to the treatment arm assignment,
however, the LHAs and participants unavoidably were not. After the baseline interview, women
randomized to usual care received a letter from their physician and a National Cancer Institute
brochure that encouraged them to have a Pap test (47). The intervention design followed the
framework set forth in the PRECEDEPROCEED program planning model which incorporates
constructs of the Health Belief Model (e.g. perceived severity), Social Learning (Social
Cognitive) Theory (e.g. expectancies; the values that a person places on an outcome), and a
number of general models of health behavior (48, 49). The design of the educational program,
namely how messages were presented, was based primarily on Social Learning Theory (i.e.,
behavior is determined by expectancies and incentives) (50, 51). Additionally, the
Transtheoretical Model (TTM) was used as a template to stage each participants readiness to
change cervical cancer screening behaviors (52), and the Communication-Behavior Change
model (e.g. addressing the personal relevance of the behavior by tailoring the message to a
specific individuals barriers) was used as a foundation for choosing what communication
approach to take with individual women in the intervention group (53).
Participants in the intervention arm received two in-person visits, two telephone calls, and four
postcards from an LHA over ten months. In this study, LHAs were women indigenous to the
Ohio Appalachian region and were between 40 and 50 years old, had no post-secondary
education, and were trained to deliver the intervention and subsequently observed by study
coordinators in the field. Within four weeks of randomization to the intervention group, LHAs
visited women either in their home or at a convenient site in the community. During the first 45
60 minute visit, LHAs provided information designed to increase knowledge about cervical
cancer, Pap test screening, and the importance of follow-up after an abnormal test. LHAs also
assessed each womans personal risk of developing cervical cancer in her lifetime, obtained
information on barriers to screening, and then provided individualized counseling for reported
barriers to having a Pap test.
LHAs followed the initial visit with two telephone calls at one and five months later, and a series
of four postcards mailed at two, three, six, and seven months after the initial visit to provide
continuous contact and screening reminders. Postcards were targeted to each participant based
upon their current stage of change in the TTM (52). The intervention period concluded with a
second in-person visit approximately ten months after the first. At the final visit, the LHA
provided additional barriers counseling, if necessary, and encouraged the participant to continue
to be proactive about her health care.
Measures
As part of the CARE initiative, baseline information was collected based on the Social
Determinants of Health (SDH) model (54) and described social and cultural factors, material
factors, health and health behaviors, psychological factors, and environmental factors related to
cervical cancer screening behavior (43, 45). For this intervention study, it was determined a
priori that only variables describing age, race, marital status, employment status, occupation,
education, annual household income, type of health insurance, and history of previous abnormal
Pap tests would be examined for potential confounding or effect modification of the intervention
effect. A measure of socioeconomic status (SES), loosely based on the Hollingshead scale (55),
was calculated and was derived by combining information about occupation, education, and
income. For analysis purposes, SES was grouped into three levels: SES scores of 01, 23, and
46 represent low-, middle-, and high-level SES, respectively (45).
The primary outcome in this study was whether or not a woman who was in need of a Pap test,
based upon risk-appropriate guidelines, actually received one in the time between randomization
and the 12-month follow-up interview based on information in the medical record. As a
secondary outcome, self-report of receipt of Pap test was obtained in the follow-up survey
conducted at the end of the study. To obtain medical record information, a form requesting
patient information along with a copy of the medical record release form was faxed to the clinic
listed by each participant. At least three attempts (calls or another fax) were made to obtain the
information from the clinic.
Statistical Analysis
Based on previous research, we estimated that approximately 40% of women in the control
group would be screened at follow-up, and between 55% 65% would be screened if they were
in the intervention group. Anticipating a 30% attrition rate, 140 women were needed per
treatment arm to detect a 20% difference in screening rates assuming a two-sided chi-square (1
d.f.) test for detecting differences in proportions in independent data with a type I error rate of
0.05. Descriptive statistics were used to provide overall characteristics by treatment arm and to
ensure balancing of covariates after randomization. Initial unadjusted likelihood ratio chi-square
tests were used to compare differences in rates of Pap test utilization between intervention and
control groups at follow-up. Both the primary and secondary endpoints were tested at the 0.05
level of significance. Logistic regression models were constructed to evaluate the intervention
effect (i.e., having had a Pap test during the study period) and to assess the confounding
influences of clinic (random effect) and other pre-specified, potentially confounding fixed effects
measured at baseline. Interaction effects were assessed to determine if the effect of the
intervention was moderated by specific characteristics of the women. Separate exploratory
logistic regression models were constructed to identify significant predictors (among factors
listed in Table 1) of obtaining a Pap test after controlling for treatment arm. Differential loss to
follow-up was assessed by comparing characteristics of participants who did not provide self-
reported Pap test status with those who did. For logistic regression analyses, likelihood ratio chi-
square tests were used to determine improved statistical fit. All statistical analyses were
conducted using SAS version 9.2 (SAS Institute Inc., Cary, NC).

Table 1
Baseline participant demographics by treatment arm (n=280
*
)
Go to:
Results
Study Participants
Figure 1 displays the number of women selected, assessed for eligibility, accrued, randomized,
and assessed for the primary outcome. The main reasons women were ineligible were: currently
pregnant (76%), not speaking English (54%), not an active patient at the clinic (55%), and not
living in Appalachia (12%) [note, participants at screening could be ineligible for more than one
reason]. After the baseline interview, the most common reason for ineligibility (145/423) was not
needing a Pap test. The overall response rate was 81.9% (286 of 349 eligible women). Of the 286
women who met all eligibility criteria and consented, 145 were randomized to the LHA
intervention and 141 were allocated to usual care. Six women were later found to be ineligible
after randomization and were not included in the analysis.

Figure 1
Study Flow of Participants from Sampling to Analysis, CONSORT diagram.
Baseline characteristics of intervention and usual care groups are shown in Table 1. The mean
age of the participants was 43.7 years, and nearly all of the participants (95.4%) were white,
which is typical of the Ohio Appalachian area. Most had household incomes less than $50,000
(74.7%) and were either married or part of a couple (63.4%). A majority of participants had
some type of health care coverage (82.4%), and more than half of the population (52.1%) had
completed at least some college. Approximately a quarter of the participants (27.6%) had a
history of an abnormal Pap test, and more than a third (36.4%) had CES-D scores16, indicative
of clinical depression. Although a notably higher proportion of participants in the intervention
group had a history of abnormal Pap tests, there were no statistically significant differences in
baseline characteristics between intervention and usual care groups at p<.05.
Pap Test Screening Rates at Study Completion
MRR data pertaining to Pap test status at the end of the study were available for 270 (96.4%)
participants. Four and six participants were missing MRR data from the intervention and control
groups, respectively. No significant differences in baseline characteristics were found between
women with and without MRR data. At follow-up, 47 women were missing data about self-
reported Pap test status. Those without self-reported Pap test status were significantly younger
(35.3 vs. 45.5 years, p<.0001) and more likely to have a history of abnormal Pap test (42.6% vs.
24.6%, p=0.012). Participants with and without self-reported Pap test status were similar across
other measured demographic factors. A larger proportion of participants from the intervention
group did not provide Pap test information at the follow-up survey although this difference was
not statistically significant (19.6% vs. 13.9%%; p= 0.201).
Table 2 shows the proportion of women who, at study completion, had a Pap test according to
MRR and self-reported having had a Pap test by study arm. According to MRR, a greater
proportion of women in the intervention group had a Pap test at study completion when
compared to women in the control group (51.1% vs. 42.0%, p=.135). Overall, a notably larger
proportion of participants self-reported having had a Pap test by the end of the study than was
confirmed by MRR (62.7% vs. 46.7%, respectively). Like MRR, however, a greater proportion
of participants self-reported having had a Pap test by the end of the study in the intervention
group compared to those receiving usual care (71.3% vs. 54.2%, p=.008). This difference,
however, may be a reflection of the missing data from women who did not complete the follow-
up interview.

Table 2
Pap test status by treatment arm and report type
Logistic regression modeling showed that over the course of the study, participants receiving the
LHA intervention were 1.44 (95%CI: 0.89, 2.33; p=0.135) times as likely to have had a Pap test
based on MRR. According to participant self-report, those in the intervention group were 2.10
(95%CI: 1.22, 3.61; p=0.008) times as likely to report having had a Pap test during the study
period (Table 3). There was no evidence of confounding or effect modification by any of the pre-
specified variables collected at baseline for either reporting type, therefore, we report crude
results. Additionally, results of exploratory analyses suggested that after controlling for the
intervention effect, women who reported having had a Pap test in the past three years were more
than twice as likely (OR: 2.13; 95%CI: 1.09, 4.16; p=0.028) to receive a Pap test by the end of
the study based on MRR. According to self-report, women who reported having had sex before
age 18 or having had a previous sexual partner with an STI were 2.92 (95%CI: 1.53, 5.55) and
2.85 (1.23, 6.60) times as likely to have a Pap test during the study period, respectively. No
significant interactions with treatment arm were found.

Table 3
Odds ratios and 95% confidence intervals for receiving Pap tests within the 12-month follow-up
period for participants in the intervention group by report type
Agreement between MRR and Self-report
Overall agreement between MRR and self-report data was good (74.4%; =0.728), and
agreement was similar between intervention and control groups (74.8% vs. 74.1%) (Table 4).
The largest discrepancy was in the control group, where 34.4% of participants who reported
having had a Pap test within the study period did not according to MRR, compared to 30.4% of
the participants in the intervention group. Among women who reported not having had a Pap
test, only a minority of women in both intervention (12.5%) and control (15.7%) groups actually
did according to MRR.

Table 4
Agreement between medical record review and self-report methods of assessing Pap test uptake
(n=223
*
)
Go to:
Discussion
Cervical cancer is largely preventable through Pap testing with prompt and proper follow-up for
abnormal results. Not all women, however, receive Pap tests at appropriate intervals, and
Appalachia Ohio is an area where women are particularly at risk for Pap test non-adherence (8).
In this randomized trial, we tested the efficacy of an LHA intervention designed to increase the
uptake of Pap test screening among women in need of the test who were recruited from 14
separate health clinics in Ohio Appalachia. The LHA intervention was hypothesized to promote
Pap test screening by improving knowledge, reducing barriers, and increasing positive beliefs
about screening. The impact of the intervention on knowledge, barriers, and beliefs is the topic of
another manuscript; however, evidence from previous studies of LHA interventions documents
this process (40, 41).
Overall, the results demonstrate an increase in screening among women who received the LHA
intervention, although results from MRR and self-report differed in effect size and level of
statistical significance of the intervention effect. Participants in the intervention group were more
than twice as likely to report having had a Pap test within the study period (p=0.008). However,
according to MRR, although a higher proportion of participants in the intervention group
received a Pap test, the difference between the two arms was not significant (p=0.135). The
effect size for our LHA intervention was similar to that reported by several previous studies
using medical record review (17), however, other studies have shown an even larger intervention
effect (19, 22, 33, 40, 41). Perhaps the lack of statistical significance for the intervention effect
based on MRR in our analysis stemmed also from our definition of usual care. We defined usual
care as receiving an NCI brochure and a letter from the participants physician. In reality,
however, usual care may include neither, and we may have watered down our intervention
effect by defining usual care in such a manner.
Self-report bias in screening has been extensively studied, and likely explains why the overall
proportion of women who reported having had a Pap test during the study period was notably
higher than that confirmed by MRR (5661). However, self-report and MRR discordance
between the intervention and control groups did not appear to be differential among those who
had information for both report types. That is, a slightly higher proportion of women in the
control group who did not have a Pap test according to MRR reported having had a Pap test. For
self-report bias to explain the difference in magnitude and significance of the intervention effect
between self-report and MRR data in this study, the opposite would have had to be true.
Therefore, we sought alternate explanations for the discordance of results in MRR and self-
report. It is likely that women who did not complete the follow-up survey were less likely to
have had a Pap test within the study period. This fact may be particularly important among the
women in the intervention group who may have refused the follow-up survey because they did
not want to indirectly disappoint the LHA who had spent time trying to assist them during the
past year. Thus, social desirability bias may have been introduced into the self-report population,
and the self-reported intervention effect may have been artificially inflated.
Another possibility stems from the MRR of Pap test completion in the clinics in which this study
was conducted. While in most settings MRR is the gold standard, Ohio Appalachia represents a
unique setting. Many clinics in our study had inadequate resources to maintain complete and up-
to-date medical records. Most of the clinics lacked computerized records, and many were
understaffed in administrative positions. Still another site was damaged by local flooding and
reported losing a portion of their medical records in the natural disaster. Thus, there is the
possibility that for some of the women who reported having had a Pap test, but for whom there
was no medical record of the test, a Pap test was performed but the record was lost or destroyed.
In this scenario, the intervention effect in the MRR analysis could have been underestimated.
The latter possibility should be considered in future studies that plan to use MRR as the gold
standard in highly rural, understaffed, and underfunded clinics where lack of computerized
medical record technology is prevalent.
Secondary outcomes showed that based on MRR data, having a Pap test in the previous three
years was the strongest predictor of obtaining a Pap test over the course of the intervention. This
underscores the importance of promoting regular screening by health care providers to establish
patterns of healthy behavior. In addition, based on self-report, women in this study with a history
of risky-sexual behavior (i.e., having had sex before age 18 or with a partner with an STI) were
more likely to adhere to risk-appropriate screening guidelines, suggesting that providers may
stress the importance of regular screening to high-risk women or that women who engage in
risky sexual behavior may be more acutely aware of their cervical cancer risk. The finding that
significant predictors of Pap adherence for MRR were dissimilar than those of self-report further
highlights the need to examine outcomes of studies conducted in rural populations using a
variety of methods.
This study is not without limitations. Primarily, medical records in the Appalachian Ohio clinics
included in our study may have been incomplete. Computerized medical records were used in
only two (14.3%) of the participating clinics, and other clinics reported having had problems
finding or maintaining medical records for all of the women enrolled in our study. If records of
Pap tests for participants were differentially lost, the effect of the intervention could have been
dampened. Additionally, we did not have follow-up survey data or MRR data for all women
which could have introduced bias, although we obtained this information for the great majority
of participants. However, internal validity of this study was likely protected by randomization
and statistical control for measured baseline demographics. Furthermore, results are not
generalizable to populations outside of Ohio Appalachia and, specifically, the clinics who
participated in our study.
In spite of limitations, this study is one of the few LHA interventions conducted in Appalachia,
an area which suffers from health disparities. Moreover, we recruited women from 14 clinics
across four regions of Ohio Appalachia, representing the great variation in this area.
Additionally, we captured information on participant characteristics to assess factors associated
with both the intervention and outcome. Lastly, this is one of few studies that compared MRR to
self-reported Pap test receipt among an underserved population served by rural health clinics.
Because Pap tests must be obtained from a health care provider, the use of medical records to
verify receipt of Pap tests has traditionally been the gold standard for research. Data about Pap
testing from Appalachian clinics have never been evaluated for use in research studies nor
compared to self-reported Pap test adherence.
Ultimately, results from our study suggest increased uptake in Pap testing among women who
were randomized to receive an LHA intervention. Thus, the LHA intervention appears to be
transferable to the Ohio Appalachian population in need of Pap testing; however, future studies
should explore methods to strengthen Pap test uptake in the Ohio Appalachian region. Indeed,
results of MRR, which is typically considered the gold standard, were not significant. Future
studies should continue to assess the effect and cost-effectiveness of LHAs on uptake of cervical
cancer screening in vulnerable populations, evaluate the effect of varying definitions of usual
care, and examine the reliability of MRR in clinic populations with poor administrative
oversight, funding, and access to computerized medical charting.
Go to:
Acknowledgments
P50 CA105632, P30 CA016058, UL1-RR025755, K07 CA107079 (MLK)
Go to:
Footnotes
Clinical Trials Registration #: NCT01172561
Go to:
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J Gen Intern Med >
v.25(11); Nov 2010 >
PMC2947627

J Gen Intern Med. 2010 November; 25(11): 11981204.
Published online 2010 July 21. doi: 10.1007/s11606-010-1450-6
PMCID: PMC2947627
Barriers to Follow-Up of an Abnormal Pap
Smear in Latina Women Referred for
Colposcopy
Sanja Percac-Lima, MD, PhD,
1,2,3
Leslie S. Aldrich, MPH,
2
Gloria B. Gamba, MA,
1,2
Adriana M. Bearse,
BA,
2
and Steven J. Atlas, MD, MPH
3

Author information Article notes Copyright and License information
Abstract
BACKGROUND
Lower rates of follow-up after an abnormal Pap smear in racial and ethnic minorities may
contribute to the higher incidence and mortality rates of cervical cancer seen in these groups.
OBJECTIVE
To identify patient-perceived barriers to follow-up after an abnormal Pap smear result among
Latina women.
DESIGN, PARTICIPANTS AND APPROACH
Qualitative, semi-structured, one-on-one interviews were conducted with patients from an
academic hospital-affiliated urban community health center. Three groups of women were
interviewed: new colposcopy clinic patients, patients who had previous colposcopies and patients
enrolled in the health center's patient navigator program. Open-ended questions explored their
knowledge, beliefs and experiences with colposcopy. Content analysis of transcripts was
performed using established qualitative techinques.
RESULTS
Of 40 Latina women recruited, 75% spoke only Spanish. The average age was 31.5 (range 18
55). Personal and system barriers identified were categorized into four themes: (1) anxiety/fear
of procedure and diagnosis; (2) scheduling/availability of appointments interfering with work
and/or child care; (3) inadequate communication about appointments, including lack of
explanation regarding diagnosis, procedure and results; and (4) pain. New patients more
commonly reported problems with scheduling and communication. Follow-up patients were
more concerned about pain, and navigated women most often reported fear of results but had
fewer concerns about inadequate communication.
CONCLUSION
Anxiety/fear was the most common personal barrier, while difficulty scheduling appointments
and inadequate communication were the major systems barriers identified in these Latina
women. Interventions to lower these barriers to colposcopy among Latina women may increase
adherence to follow-up of abnormal Pap smears.
KEY WORDS: colposcopy, Latino, health disparities, patient navigation
BACKGROUND
The likelihood that a woman will develop or die from cervical cancer in the US has steadily
declined, but the National Cancer Institute SEER predicted that 11,270 women would still be
diagnosed with and 4,070 would die from cervical cancer in 2009
1
. According to SEER data,
there is a marked disparity in incidence and mortality rates across racial and ethnic groups
2
. The
incidence of cervical cancer in Latina women per 100,000 is 12.7 compared to 7.1 for non-Latina
white women. More Latinas are dying from cervical cancer compared to non-Latina whites (3.1
vs. 2.1 per 100,000)
2
. Since effective screening is available to prevent cervical cancer, higher
incidence and mortality may be attributed to lapses in screening, failure of the Pap test to detect
an abnormality, or inadequate follow-up after an abnormal Pap test result
3,4
. Pap smear rates and
adherence to follow-up after an abnormal test are also lower in Latina women
5,6
. Differences in
screening and abnormal follow-up could be due to language barriers, foreign birth/acculturation,
limited education, poverty and lack of insurance
711
. All these factors are more common in
Latinas and could influence their compliance with recommended care.
There have been studies exploring patient barriers to cervical cancer screening
1115
, attitudes and
beliefs about human papilloma virus (HPV) and the HPV vaccine
1618
; however, few have
focused on barriers to follow-up of an abnormal Pap smear
3,6,7,16
. Del Carmen and colleagues
explored sociodemographic and knowledge differences between Latina and non-Latina women
referred to colposcopy
7
. Little is known about patients perspectives regarding experiences with
or possible barriers to colposcopy
19
.
The objective of this study was to examine barriers to colposcopy reported by Latina patients
receiving care in an urban community health center. We sought the perspective of new patients,
patients who had already had a colposcopy and patients who were part of a cervical outreach
(patient navigator) program. By better matching barriers to colposcopy with potential
interventions, our goal is to increase adherence rates in low-income Latina women.
METHODS
Design
We conducted a qualitative, descriptive study of Latina patients with abnormal Pap smears
referred for colposcopy to obtain in-depth information about potential barriers to receiving
recommended follow-up care. The study was approved by our institutional review board.
Setting and Participants
Participants included women referred from the Massachusetts General Hospital Chelsea Health
Care Center (MGH Chelsea). This urban, multi-specialty community health center in Chelsea,
MA, serves a multiethnic, low-income, heavily immigrant and refugee community. Over 23% of
Chelseas 35,080 residents live below the poverty level, and it has the second largest percentage
of Latinos (48%) of any city in the state
20
. The cervical cancer incidence is two and a half times
the state average (16.3 vs. 6.5 per 100,000)
21
, and mortality is 1.8 vs. 1.5 per 100,000
22
.
Interviews were conducted at the MGH colposcopy clinic located on the main hospital campus.
The clinic sees around 1,800 patients per year (21% from MGH Chelsea). Women were eligible
for the study if they received their primary care at MGH Chelsea, were referred to colposcopy
because of an abnormal Pap smear and identified themselves as Latinas. A convenience sample
of patients meeting these criteria was identified using the colposcopy clinics scheduling system.
Patients were called by a bilingual research assistant to schedule an interview during their
colposcopy visit, and were excluded if they did not speak English or Spanish, or had major
physical or mental co-morbidities.
Interviews
An interview guide (Text Box 1) was developed based on previous studies of barriers to
colposcopy in racial and ethnic minorities
6,7,19
, as well as informal interviews with MGH Chelsea
navigators and health care providers. A research assistant was trained to conduct semi-structured
one-on-one patient interviews of approximately 10-15 min using this guide. The interview
collected demographic information, followed by questions on how participants were informed
about needing a colposcopy and their knowledge of and beliefs about colposcopy. If this was the
participants first visit to the colposcopy clinic, she was classified as a new patient, and further
open-ended questions were asked to explore her experiences, problems and concerns to date. If
this was a follow-up visit, the participant was classified as a follow-up patient and further
questions explored both previous and current experiences, problems and concerns. Participants
enrolled in the MGH Chelsea Cervical Outreach Program because of missed colposcopy
appointments or identified by a clinician as at-risk were classified as navigated patients and
asked the same questions as follow-up patients. The study sought to recruit equal numbers of
women from each of these three groups to ensure a broad range of experiences and insights, and
for comparison purposes. The research assistant described the study to participants, provided a
fact sheet about the study, answered questions and obtained verbal consent. Interviews were
performed from September to December of 2008.

Analysis
All interviews were tape recorded, transcribed verbatim, and translated by a certified medical
interpreter if needed. Transcripts were analyzed after 5, 12, 18, 30 and 40 interviews were
completed. After analyzing 40 interviews, it was determined that saturation was achieved since
no new themes emerged from the last ten transcripts.
Content analysis of the transcripts was performed to synthesize findings and identify key themes.
The data were analyzed using the framework method described by Ritchie and Spencer
23
. To
become familiar with the data, the interview transcripts were independently reviewed by the two
research assistants, with senior researcher oversight. Preliminary themes began to emerge during
the familiarization phase, leading to the development of an initial thematic framework. Theme
counts were performed through indexing of transcripts, and data were subsequently charted and
organized by overarching theme. In the mapping and interpretation phases, patterns and
differences among the three categories of interviewed women were explored. The analysis team
met bi-monthly to review data, discuss new insights, confirm existing and generate new themes.
Interrater reliability about the themes and supporting data were always greater than 90%.
Disagreements were resolved through discussion until the group achieved consensus.
RESULTS
Study Participants
Sociodemographic characteristics of the 40 participants are shown in Table 1. Three women
approached declined to be interviewed (93% response rate). All self-identified as Latinas, with
most speaking only Spanish. The average age was 31.5 (range 1855). Less than a third (28%)
reported being married, and close to two-thirds (63%) had children in their care. Twenty-five
participants (63%) were employed at the time of the interview. For 12 participants (30%), it was
their first colposcopy clinic visit (classified as new patients). Fifteen (38%) were there for a
follow-up visit (follow-up patients), and 13 (33%) were enrolled in Chelseas Cervical
Outreach Program (navigated patients). Most women (60%) had lived in the US for 5 or more
years, eight were recent immigrants, and eight had lived in the US their whole lives.

Table 1
Patient Demographic Characteristics
Findings Overview
A range of barriers were identified, and four main themes emerged: (1) anxiety/fear of the
procedure and/or of diagnosis; (2) scheduling difficulties including appointments interfering with
work and/or childcare, and transportation-related issues; (3) inadequate communication about
appointments and lack of explanation about the diagnosis, procedure and/or results; and (4) pain
associated with the procedure. These themes were categorized as personal barriers (anxiety/fear,
and concerns about pain) or systems barriers (inadequate communication and scheduling
difficulties) (Table 2). Follow-up and navigated patients more commonly reported concerns
about pain, and new and navigated patients more commonly reported anxiety/fear, particularly of
results (navigated patients). Systems issues were more common in new patients.

Table 2
Barriers to Follow-Up of Abnormal Pap Smear Results
Personal Barriers
Anxiety/Fear
For all women, anxiety/fear regarding the colposcopy and/or its results was a common theme.
Diagnosis/Results Anxiety/fear around diagnosis/results was the most frequently expressed type
of anxiety/fear: about half of participants shared a fear that the procedure would result in a
cancer diagnosis. As one woman stated, theres always a little bit of fear when they tell you
they are going to do a colposcopyI think maybe I could have cancer. Many participants fear
the unknown since they have no experience with and little knowledge of colposcopy or cervical
cancer: at the beginning I was scared, I was nervous, I did not know what was going onI
thought I had cancer. Some participants also feared an HPV diagnosis. As stated by one,
Before all of this I was cryingI dont know, maybe I just overreacted on what the nurse told
me who called to explain the possible HPV. Thats what you hear a lot about now. Before, you
never really heard too much about that. That made me nervous. It scared me, you know?
Fear of Procedure Several participants expressed fear of the procedure, although less
commonly than fear of diagnosis: Im more afraid of the results than the procedure. Fear of the
procedure was often connected to fear of physical pain (see below). One participants comment
demonstrated this link: I was worried. I was afraid. I thought it would hurt and I was afraid of
what they might find.
Embarassment Anxiety/fear was often coupled with feelings of surprise or embarrassment
regarding possible diagnoses, and/or confusion due to lack of knowledge or understanding about
why the procedure is done and what the results might mean. This connection is exemplified in
the following quote: I was embarrassed because of what I have. The girl who called said I have
an abnormal Pap. I think maybe I have an infection or bacteria, and I dont know why. She also
mentioned cancer, and I was worriedI am very confused and worried. I thought I might have
something serious. Embarrassment was most commonly reported among new patients.
Childbearing Concerns Another source of anxiety and fear for participants was uncertainty
about whether the test results would influence their health in the future, particularly pregnancy.
I worry that they keep coming back abnormal. I am also trying to get pregnant, so I dont
knowwell, I worry about these results and how they will affect my pregnancy.
Pain
Although the least commonly reported barrier was concern about, fear of and prior experiences
with pain/discomfort, for one participant it was a main reason for missing a prior appointment: I
didnt want to come, because its uncomfortable and I just put it off. A few participants felt
misinformed about how painful the procedure would be: They said it would be like a pinch, but
its a bit more than that. Pain during previous colposcopies was a more often reported barrier in
follow-up compared to navigated patients.
System Barriers
Scheduling Difficulties
Many participants identified scheduling and transportation difficulties as barriers to care,
including lack of timely colposcopy appointments and clinic hours that conflicted with work
schedules or childcare responsibilities. These barriers were most common in new patients.
Work Conflicts Work-related issues were cited by a third of participants. In order to attend
appointments scheduled during work hours, participants often had to request uncompensated
time off work: I am a single mom, and if I lose two hours of work then I cant make it upI
need to feed my children. Work-related issues were most common among new patients. Three
participants who had missed past appointments cited work-related reasons.
Childcare Conflicts Scheduling difficulties associated with childcare were cited by almost a
quarter of participants. As stated by one participant, I leave them with my husband, so he needs
to take time [from work] to stay with them while I come to the appointment. Some participants
bring their children to appointments: I kept her [daughter] from schoolI had to bring her with
me. I had no one to pick her up from school. She was in the room when I had the appointment.
Lack of Appointment Availability Several participants, particularly new patients, identified
lack of availability of timely appointments as a barrier: I just tried to get an earlier appointment.
I didnt want to waitthey had none. Waiting to get an appointment after being told of an
abnormal test result was a source of stress: I was cryingI was a bit nervousI wanted to be
seen tomorrow. I wanted to hurry up and get seen you know? I thought I had cancer.
Transportation Issues Transportation represented a barrier for a quarter of all participants.
Although Chelsea is only 5 miles from the colposcopy clinic, for some: The commute is too
longIts about an hour to get here. I wish there were something easier. The clinic is also
outside of the participants community: I was late because Im not familiar with the area. Even
patients familiar with the hospital still felt overwhelmed: They said if I knew how to get to the
hospital then I would know where to go. Well, I know the hospitalbut I did not know where to
go. New patients were particularly prone to experiencing transportation issues, with half getting
lost or arriving late for an appointment. Navigated patients rarely experienced these issues: Last
time the navigator took me, so no problems.
Inadequate Communication
The other system-related theme was inadequate communication. Communication breakdowns
were related to three main areas: (1) lack of explanation about the procedure, diagnosis or
results, (2) inadequate appointment or results notification and (3) language barriers.
Lack of Adequate Explanation Lack of adequate explanation about the procedure, diagnosis or
results was the main form of inadequate communication reported. Close to half of new patients
felt the colposcopy was inadequately explained. Conversely, only one navigated patient did not
receive adequate explanation of the procedure/diagnosis. One patients experience highlights this
issue: They did not tell me anything. They just said I had an appointment and that I had to come
here. When asked if anyone explained why she needed a colposcopy, another said: They didnt
say. I just got the appointment by letter. They didnt tell me anythingI did receive a pamphlet
explaining the appointment and it said that I probably had an abnormal Pap. Some participants
received an explanation but did not clearly understand it.
Inadequate Appointment/Results Notification Some participants, especially new patients,
reported inadequate notification from the clinic regarding their appointments or colposcopy
results, which often contributed to anxiety: well, if there were something wrong, Im sure they
would have told me by nowbut I worry. One participant expressed frustration about both her
appointment and results notification: I was very upset at how I found out I needed to come here.
I got the appointment for the colpo before the doctor even told me something was up. I got the
letter in the mail, no call, no resultsno nothingWhen you get bad results, you just dont get it
in the mail, and thats how I got it. I wanted a callThree days later I got a letter from the nurse
telling me what the results were.
Language Barriers Language barriers, such as receiving materials in English when needed in
Spanish, were mentioned by only two participants. Most women had Spanish-speaking staff and
interpreters available at the colposcopy clinic when needed.
DISCUSSION
Lowering the incidence of cervical cancer requires understanding why women do not get
screened for cervical cancer and why women with abnormal screening tests do not complete
follow-up evaluations, including colposcopy. This is the first qualitative study exploring patient-
perceived barriers to colposcopy in low-income Latina women, some of whom received
navigation services to help reduce barriers to care. We focus specifically on Latina women
because this group is known to have the highest cervical cancer incidence and mortality rates
2,24
.
Many of the barriers perceived by the Latina women in our sample have been previously
described in the literature as possible reasons for non-adherence to colposcopy in other women.
Anxiety/fear is often due to insufficient knowledge and understanding about the purpose of
colposcopy
25,26
. Studies show that anxiety in women referred to colposcopy can be significantly
decreased by sending a one-page handout or culturally tailored educational brochure prior to the
appointment
2729
. Anxiety/fear about the diagnosis as well as potential for cancer in particular is
one of the most commonly cited possible barriers to colposcopy, especially in low-income
minority women
25,30,31
. As described by Reynolds, Latina women may be torn between wanting
to know and being afraid to find out if they have cancer
9
. In our study, anxiety/fear about cancer
was more common in older participants, while younger women were more concerned about
HPV. Misinformation or misunderstanding of available information about HPV and cervical
cancer is common and variable in multiethnic low income populations
1618
. Childbearing issues
post-colposcopy are also described in the literature
31,32
.
The most common systems barrier identified by our participants, particularly new patients, was
scheduling difficulties and lack of timely appointments. Work and child-care responsibilities also
contribute to missed appointments
32,33
. Inadequate communication, our second most prominent
systems barrier, was recognized and targeted in Project SAFe, which was designed to improve
abnormal cervical screen follow-up among low-income Latinas
33
.
Low English proficiency in Latinas is described in the literature as a barrier to receiving
physician recommendations to have a Pap smear
31
, but further studies among immigrant
populations are needed to determine its influence on adherence to colposcopy. The majority of
our participants did not speak English but did not mention language as a barrier.
Comparing barriers perceived by new, follow-up and navigated patients enabled us to recognize
the needs of each group and design appropriate interventions. Navigated women enrolled in
MGH Chelseas Cervical Outreach Program reported similar levels of anxiety/fear and concerns
about pain compared to new and follow-up patients, but reported fewer systems barriers. By
including navigated women who were targeted because of their increased risk of missing follow-
up appointments, barriers reported might be overrepresented due to their higher risk status or
underrepresented as a result of receiving navigation services that strive to change attitudes and
reduce barriers. It is also possible that womens attitudes/barriers to colposcopy may be
influenced by the education they receive from the navigator. Women may experience either more
or less anxiety/fear because of the increased knowledge received through the program about
cervical health and about the importance of appointment adherence to detect abnormalities.
Only by understanding the common barriers to follow-up can strategies be implemented to
increase successful colposcopy evaluations. Matching participants personal and system barriers
with interventions to improve abnormal Pap smear follow-up is a goal of outreach programs
3439
.
Based upon our findings, we propose changes that could improve our cervical outreach
(navigator) program and adherence to colposcopy (Text Box 2).

Our study has several limitations. We focused on Latina women because they represent 75% of
all patients referred from our health center to the colposcopy clinic. Though Latina women have
the highest cervical cancer incidence and mortality rates, other low-income minority groups are
also at risk, and our results may not apply to them. Latina women in this small study represented
a range of countries of origin, years in the US and ages, but these results may not generalize to
all Latina populations. The study setting, an urban community health center that already has a
program to assist Latina patients, may result in underestimating the challenges faced by women
in settings without such efforts. We also did not interview patients who failed to follow-up on an
abnormal Pap test, and their issues may have differed from those of the patients who were
interviewed. However, a third of the women (navigated patients) had missed at least one
colposcopy appointment in the past, and their concerns were similar to the other groups.
Nevertheless, future studies that focus on the women who have not yet completed a follow-up
visit might provide additional insights into barriers associated with not evaluating an abnormal
Pap result. To compare the groups interviewed, we heavily relied on counts of themes. For
personal barriers that emerged spontaneously, it is difficult to know whether some themes were
not mentioned by women because they were not important, they just did not come to mind or
were so obvious to the participant that she did not think she should mention them. Thus, these
barriers might be underreported in our study. On the other hand, systems barrier items were
explicitly suggested in questions 3a and 3b (Text Box 1). Because of differences in ascertaining
personal and systems barriers, it may not be appropriate to compare frequencies between them.
Finally, though we developed an interview guide and used a highly trained interviewer, the use
of two or more interviewers may have decreased bias associated with individual style or
emphasis.
Understanding why some Latina women are not receiving colposcopy after an abnormal Pap
smear is important to reduce racial and ethnic disparities in cervical cancer mortality and
morbidity. Our findings add to those previously reported and support directed interventions to
address these barriers in low-income Latina patients in urban settings to improve adherence to
follow-up after abnormal Pap smear results.
Acknowledgements
The authors would like to thank Sarah Abernathy-Oo, Joan Quinlan and Diana Maldonado for
assisting in the early conceptualization of the study and for their ongoing support. The authors
are very thankful to Elyse Park, Ph.D, MPH, for review of the manuscript and help with the
qualitative methodology. This paper was presented at the 32nd Annual Meeting of the Society of
General Medicine in Miami, May 2009.
The study was funded by a grant from Gillette Corporation to the MGH Chelsea Cervical
Outreach Program and the MGH Center for Community Health Improvement. Drs. Percac-Lima
and Atlas were supported in part by a grant from the Agency for Healthcare Research and
Quality (1R18 HS019161-01).
Conflict of interest None disclosed.
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v.7(7); 2012 >
PMC3393696

PLoS One. 2012; 7(7): e40766.
Published online 2012 July 10. doi: 10.1371/journal.pone.0040766
PMCID: PMC3393696
Knowledge and Acceptability of Pap Smears,
Self-Sampling and HPV Vaccination among
Adult Women in Kenya
Anne F. Rositch,
1,*
Ann Gatuguta,
2
Robert Y. Choi,
3
Brandon L. Guthrie,
4
Romel D.
Mackelprang,
4,5
Rose Bosire,
6
Lucy Manyara,
7
James N. Kiarie,
8
Jennifer S. Smith,
9
and Carey
Farquhar
3,4,5

Author information Article notes Copyright and License information
Go to:
Abstract
Objectives
Our study aimed to assess adult womens knowledge of human papillomavirus (HPV) and
cervical cancer, and characterize their attitudes towards potential screening and prevention
strategies.
Methods
Women were participants of an HIV-discordant couples cohort in Nairobi, Kenya. An
interviewer-administered questionnaire was used to obtain information on sociodemographic
status, and sexual and medical history at baseline and on knowledge and attitudes towards Pap
smears, self-sampling, and HPV vaccination at study exit.
Results
Only 14% of the 409 women (67% HIV-positive; median age 29 years) had ever had a Pap
smear prior to study enrollment and very few women had ever heard of HPV (18%). Although
most women knew that Pap smears detect cervical cancer (69%), very few knew that routine Pap
screening is the main way to prevent ICC (18%). Most women reported a high level of cultural
acceptability for Pap smear screening and a low level of physical discomfort during Pap smear
collection. In addition, over 80% of women reported that they would feel comfortable using a
self-sampling device (82%) and would prefer at-home sample collection (84%). Nearly all
women (94%) reported willingness to be vaccinated to prevent cervical cancer if offered at no or
low cost.
Conclusions
These findings highlight the need to educate women on routine use of Pap smears in the
prevention of cervical cancer and demonstrate that vaccination and self-sampling would be
acceptable modalities for cervical cancer prevention and screening.
Go to:
Introduction
Cervical cancer is a preventable disease, yet the number of cases globally is expected to almost
double by the year 2025 [1]. Infection with high-risk genotypes of human papillomavirus (HR-
HPV) is the primary cause of invasive cervical cancer; over 70% of all cervical cancers are
attributable to infection with HPV-16 and 18 [2], [3]. Cervical cancer is the third most common
cancer among women worldwide with an estimated 529,000 new cases in 2008, 85% of which
occur in developing countries [4]. In 2008, WHO estimated that cervical cancer was the second
most common cancer among Kenyan women [1], yet screening coverage is currently very low,
according to the Kenyan national cervical cancer prevention strategic plan for 20122015
released in January of 2012 [5].
Traditionally, Pap smear, combined with treatment of cervical precancer and early stage cancer,
has been successful in preventing up to 80% of invasive cervical cancer cases in developed
countries [6], [7], [8]. In developing countries, however, high rates of cervical cancer mortality
persist due to lack of effective screening programs and low uptake of Pap smear testing [9].
Reasons cited for the low uptake of screening include lack of awareness, inadequate access,
exam discomfort, fear of finding cancer and logistical issues associated with obtaining screening
[10], [11]. Newer technologies such as the careHPV DNA test (QIAGEN, Gaithersburg, MD,
USA), cervico-vaginal self-sampling, and HPV vaccination have the potential to increase
screening and reduce cervical cancer in developing countries [12], [13], [14].
Uptake of self-sampling has been shown to be successful and HPV testing from self-collected
samples is highly sensitive for detection of cervical intraepithelial neoplasia grade 2/3 in both
clinic and home settings [15], [16], [17]. Previous studies have shown that African women find
self-sampling acceptable; for example, 80% of Ugandan women were willing to collect their own
samples at home [18]. However, knowledge of new screening and cervical cancer prevention
technologies remains low among most women, with studies documenting almost no awareness of
HPV infection, HPV screening for women 30 years and older and adolescent vaccination for the
prevention of future disease [10], [19], [20], [21], [22], [23], [24]. Awareness is even low among
healthcare workers who are expected to provide preventative health services [25], [26], [27].
With the increase in technology and opportunity to prevent cervical cancer worldwide, it is
important to understand attitudes and barriers of screening among women at high-risk of
invasive cervical cancer in low-resource settings. Therefore, our study aimed to assess womens
knowledge of HPV and cervical cancer, and their attitudes towards potential screening strategies,
including routine Pap smears, self-sampling for HPV DNA testing, and HPV vaccination. These
data will be critical for successful implementation and high uptake of community-level cervical
cancer screening programs.
Go to:
Methods
Study Population and Design
Women were recruited into a cohort of HIV-1-discordant couples identified in voluntary
counseling and testing centers in Nairobi, Kenya, from May 2007 to October 2009. Couples were
eligible to enroll in the study if they reported 3 sex acts in the previous 3 months, planned to
stay in Nairobi in their current relationship for at least 2 years, and if one member of the couple
was HIV-1-infected and the other HIV-1 susceptible. Women who were pregnant and
participants using antiretroviral therapy at the time of enrollment were excluded. At enrollment
and at quarterly follow-up visits, the HIV status of the uninfected partner was determined using
the Determine HIV1/2 Rapid Test (Abbott Laboratories, Abbott City, IL, USA) or Bioline
Recombigen HIV Test (Standard Diagnostics, Suwon City, Korea), with confirmation by the
Vironostika HIV Uni-form II Ag/Ab ELISA kit (bioMrieux Inc., Durham, NC, USA). In the
HIV-1-infected partner, CD4+ T-cell counts were taken at enrollment and every six months
using a FACSCaliber flow cytometer (BD Biosciences, Franklin Lakes, NJ, USA).
At enrollment, clinical staff administered a questionnaire to obtain information on
sociodemographic characteristics, sexual history and behavior, history of Pap screening, and
medical history. Questionnaires were presented in English or Kiswahili, depending on participant
preference, and were administered individually to ensure confidentiality. A medical examination
was also conducted during biannual study visits, which included collection of a cervical Pap
smear. All participants with abnormal cervical cytology were followed up with a repeat Pap test
or colposcopy and biopsy as recommended.
Assessment of Womens Knowledge and Beliefs Regarding Cervical Cancer
At the final study visit, up to two years after study enrollment, clinical staff administered an
extended questionnaire to obtain additional information on male circumcision, pregnancy
history, domestic violence, ARV medication history, and cervical cancer and screening. Relevant
questions fell into three categories to assess womens: 1) knowledge of HPV and the causes and
prevention of cervical cancer, 2) attitudes towards Pap smear screening after having had biannual
screening in the study, and 3) attitudes towards routine Pap smear screening, self-sampling and
HPV vaccination. Specifically, participants were asked if they had ever heard of HPV and if they
knew the cause of cervical cancer or how to prevent it. Participants gave detailed histories of Pap
smear screening prior to the study or the reasons why they had never had any screening, and
were also asked about future intentions for Pap smear screening. Women rated their level of pain
during study-conducted Pap smears, beliefs of cultural acceptability, and feelings of necessity of
Pap smear screening. Finally, women were asked if they would feel comfortable collecting their
own vaginal samples at home and if they would consider HPV vaccination if it were offered at
no or low cost. No intervention or education on cervical cancer and screening was provided
during the study unless medically indicated, and all responses were based on womens one-time
self-report.
Written informed consent was obtained from all participants. The study was conducted according
to procedures approved by the University of Washington Institutional Review Board and the
Kenyatta National Hospital Ethics and Research Committee.
Statistical Analysis
A descriptive summary of knowledge and acceptability overall and stratified by HIV-status is
presented. The numbers and percentages of each response are presented. Measures of Pap smear
acceptability, necessity and pain-level are based on a scale of 0 to 100 and womens responses
are summarized by the mean, median and interquartile range. Exact logistic regression was used
to calculate unadjusted odds ratios and 95% confidence intervals to describe the associations
between baseline socioeconomic indicators and medical and sexual history and: 1) having ever
had a Pap smear prior to study enrollment, 2) having ever heard of human papillomavirus, 3)
knowing that Pap smear screening is conducted to prevent invasive cervical cancer, and 4)
feeling that Pap smears are completely acceptable (rating of 100) versus less than completely
acceptable. All analyses were conducted using SAS version 9.2 (SAS, Cary, NC, USA).
Go to:
Results
Study Population
We interviewed 409 women from HIV-1-discordant couples, 268 (65%) of whom were HIV-
positive at baseline with a median CD4+ T-cell count of 463 (interquartile range [IQR] 311681;
Table 1). The median age in the study population was 29 years (IQR 2534), and the majority of
women (97%) were married and had completed at least primary education (8 years). HIV-
negative and positive participants were very similar, although HIV-negative women were
slightly more likely to be married (99% vs. 95%), earn an income (35% vs. 28%), have never
smoked (94% vs. 92%), be on hormonal contraceptive (24% vs.16%) and have fewer lifetime
sexual partners (median 2 vs. 3) compared to HIV-positive women.

Table 1
Baseline characteristics of 409 HIV-negative and HIV-positive adult women.
Knowledge and Beliefs Regarding Cervical Cancer
We assessed knowledge of cervical cancer, HPV, and screening among both HIV-negative and
HIV-positive women (Table 2). HIV-positive women tended to be more aware that HPV, a
virus, or a sexually transmitted infection causes cervical cancer compared to HIV-negative
women (24% vs. 18%). While a substantial number of women did not know the cause of cervical
cancer (78%), most women (69%) knew that Pap smears are used to test for cervical cancer.
However, 82% of women did not know that Pap smear screening is an important part of
preventing, not just detecting, cervical cancer. Nearly a quarter of women cited condom use and
13% reported being faithful to their partners as ways in which cervical cancer can be prevented.
Only 18% of women had ever heard of HPV, and of these, 64% knew that HPV is transmitted
through sexual intercourse and 35% did not know any mode of HPV transmission.

Table 2
HPV, Pap, and screening knowledge and acceptability by HIV infection status among adult
women
1
.
Very few women (19% HIV-negative and 11% HIV-positive) reported having had a Pap smear
prior to the study. Of those who reported having a Pap smear prior to enrollment in the study,
most had been done as part of routine care (42%) or as part of a prior research study (19%) and
the remaining were conducted for unknown reasons (23%). Those who had never had a Pap
smear reported that they did not get screened because they did not know what a Pap smear was
or why they needed one (77%). After having at least two Pap smears as part of the study
protocol, nearly all women (93%) said that they would seek out Pap screening in the future, with
the hospital being the most commonly cited place at which they can be screened. Three-quarters
of women said they would be willing to pay up to 400 Kenyan shillings for a Pap smear
(approximately 5 US dollars).
When asked about methods of screening and prevention, including self-sampling for HPV testing
and HPV vaccination, the majority of the women (82%) reported that they would be comfortable
using an at-home cervico-vaginal self-sampling device. In fact, 84% of all women said they
would prefer this method over having a sample collected in a clinic. Despite their willingness to
consider self-sampling, the majority of women (91%) had concerns regarding self-sampling,
with the ability to properly collect the sample being the most commonly cited concern (67%).
HIV-negative women were slightly more likely to report no concerns (16%) as compared to
HIV-positive women (5%). Nearly all HIV-negative (94%) and HIV-positive women (94%) said
they would get a vaccine to prevent cervical cancer if offered to them in the future at no or low
cost.
When asked about the level of acceptability, pain, and necessity that they felt towards Pap smear
screening, nearly all women (95%) gave Pap smears the highest possible rating for necessity
(Figure 1). About half of women (47%) gave Pap smears the highest possible rating for
acceptability (100 on a scale from 0 to 100; median =80 (IQR 10100)), while 21% felt they
were completely unacceptable. When the women, who had undergone biannual screening as part
of the study, were asked to rate the level of pain associated with Pap smears, 73% of the women
reported the lowest level of pain (0 on a scale from 0 to 100; n =300) and only 3% (n =12) gave
a rating of 50.

Figure 1
Womens response regarding their feelings of Pap smear acceptability, feelings of necessity,
and how painful they found Pap smears to be over two years of biannual screening.
Correlates of Pap Smear, Knowledge and Acceptability
Women age 30 years and older (odds ratio [OR]: 3.6, 95% confidence interval [CI]: 1.9, 7.2),
with at least a secondary education (OR=2.0, 95% CI: 1.1, 3.7), who had ever heard of HPV
(OR=2.2, 95% CI: 1.1, 4.2) or knew that Pap smears were used to prevent invasive cervical
cancer (OR=1.7, 95% CI: 0.8, 3.5) were more likely to have ever had a Pap smear prior to
enrolling in the study (Table 3). Women who were HIV-seropositive (OR=0.5, 95% CI: 0.3,
1.0) or used a condom the last time they had sex prior to baseline (OR=0.2, 95%CI: 0.1, 0.6)
were less likely to have a history of Pap smear screening. Education, knowledge of HPV, HIV-
status and condom use remained significantly associated with ever having a previous Pap smear
after adjusting for age.

Table 3
Association between womens baseline characteristics and previous pap testing and
knowledge and acceptability of Pap screening.
Women with at least a secondary education compared to less than a secondary education (OR=
3.2, 95%CI: 1.8, 5.8), those who had ever had a Pap smear prior to enrollment in the study
compared to never previously screened (OR=2.2, 95%CI: 1.1, 4.2), and those who knew
compared with those who did not know that Pap smears were conducted to as part of preventing
cervical cancer (OR=2.4, 95%CI: 1.3, 4.4) were more likely to have heard of HPV. Similarly,
women with at least a secondary education compared to less than a secondary education (OR=
2.2, 95%CI: 1.3, 3.9) and those who had ever versus never heard of HPV (OR=2.4, 95%CI: 1.3,
4.4) were more likely to know that Pap smears can identify cervical abnormalities before cancer
develops in order to prevent the development of invasive cancer. A womans history of Pap
smear screening (OR=1.9, 95%CI: 1.1, 3.6), knowledge of HPV (OR=1.7, 95%CI: 1.0, 3.0) and
knowledge that Pap smears are a tool to prevent invasive cervical cancer (OR=1.8, 95%CI: 1.1,
3.2) were associated with giving routine Pap smear screening the highest possible rating for
acceptability. Although education was associated with a history of Pap smear screening,
knowledge of HPV and knowledge that Pap smears are used in the prevention of cervical cancer,
education was not associated with acceptability of Pap smears (OR=1.0, 95% CI: 0.7, 1.5).
Go to:
Discussion
The majority of women knew that Pap smears are used to detect cervical cancer (69%), but very
few knew that routine Pap screening is the main way to prevent cervical cancer (18%). Most
women did not know the cause of cervical cancer (78%) and only 18% had ever heard of HPV.
However, it was reassuring to find that most women held positive attitudes towards future Pap
smear screening, self-sampling, and HPV vaccination. Our findings highlight the need to educate
and reinforce to women that routine Pap smear screening is a key part of preventing invasive
cervical cancer so that the fear of being diagnosed with cancer is not a barrier to screening.
Despite the fact that knowledge of HPV was very low in our cohort, almost all women reported
that they would be willing to be vaccinated against HPV if the vaccine was available at no or low
cost. This finding is similar to other studies [28], [29], including one from Kenya which found
that 95% of women would likely vaccinate their daughters to prevent cervical cancer [9].
However, this previous comprehensive vaccine assessment study found that only 31% of those
women still said they would vaccinate their daughter if it took three injections and 75% of
women said they would only pay 100 Kenyan shillings (approximately 1.25 United States
Dollars [USD]) out of pocket to vaccinate their daughter. Current generation prophylactic HPV
vaccines cost approximately 375 USD in developed countries and require three injections over a
6 month period. However, the GAVI Alliance now includes the HPV vaccine on its list of
childhood vaccines available for funding in resource-limited countries. Also, studies are
currently underway to assess the efficacy of a shortened 1 or 2 dose vaccine administration
schedule.
Consistent with previous studies that document low uptake of Pap smear screening in sub-
Saharan Africa, previous Pap smear screening was low in our cohort, with most women (86%)
reporting never having had a Pap smear prior to joining the study [30], [31]. It was interesting to
find that even though HIV-positive women are generally more likely to be in contact with the
healthcare system, and despite the recognized link between HIV and cervical precancer [32],
[33] and the recommendation for women to have biannual screening during the first year after
HIV diagnosis, HIV-positive women were less likely to have had a previous Pap smear
compared to HIV-negative women. This highlights the importance of integrating cervical cancer
screening and management with routine HIV care and treatment programs, as suggested by the
2011 national guidelines for antiretroviral therapy in Kenya [34].
Without an intervention or educational campaign, it is likely that the strongest predictor of future
screening is having been screened in the past. Identifying the characteristics of women who have
and have not had previous screening can help to target screening and outreach efforts. In this
cohort, women with less education, who were HIV-positive, or didnt have knowledge of HPV
or Pap smears, were less likely to have had previous Pap smear screening. Given the cross-
sectional study design, it is unclear whether women learned of HPV during Pap smear screening
or whether they learned about HPV from other sources and thus sought out cervical cancer
screening. However, in a setting such as Nairobi, where Pap smear screening is available,
although access and campaigns are limited, and where HPV testing is now being advertised, it is
likely that women who had previous Pap smears for a research study, routine care or diagnostic
purposes learned of HPV during or in response to screening. In addition, these findings are
consistent with a previous study of cervical cancer patients and non-patients in Nairobi, which
found a lower level of education and lack of knowledge of cervical cancer to be associated with a
decreased likelihood of having had previous pap screening [9]. Previous studies have also shown
that knowledge of cervical cancer and Pap smears can influence the uptake of cervical cancer
screening services [35], [36]. In our study, women who had heard of HPV and knew that Pap
smears are used to prevent invasive cervical cancer were far more likely to find Pap screening
100% acceptable and necessary as compared to women without knowledge of HPV and the role
of Pap smears in cervical cancer prevention.
Womens knowledge and attitudes were self-reported when they exited the study so there was no
follow-up to confirm their feelings or intentions. Pap smear screening conducted during the study
may have influenced womens perception towards Pap smear acceptability, as compared to
women who have never been screened. However, after having at least one Pap smear during the
study, women reported little physical discomfort associated with Pap smear screening and most
responded positively toward future use of a self-sampling device and HPV vaccination. All
women in our cohort were in stable, HIV-discordant partnerships and so their responses may not
be generalizable to other HIV-negative and HIV-positive women in the general population.
However, this is a very relevant population of women since they are of screening age, HIV-
positive or at risk for HIV, and many are mothers with daughters potentially eligible for HPV
prophylactic vaccination. Furthermore, very little data exist on womens knowledge and attitudes
towards cervical cancer and prevention, especially from East Africa where the incidence and
mortality rate of cervical cancer are one of the highest worldwide [1]. Our ability to examine
within one population attitudes towards both traditional screening methods, such as Pap smears,
and towards new alternative methods, such as the use of self-sampling and HPV vaccination,
does differentiate this study from previous surveys by providing new data on acceptability and
correlates of several modalities of cervical cancer prevention. These data are an important first
step to developing and successfully implementing effective and acceptable screening programs.
Community-based assessment of knowledge and acceptability, including women who have never
had Pap smear screening and women who have used self-sampling devices, is an important next
step to obtain information that reflects the diversity of the target population.
Despite low levels of knowledge of HPV and that the fact that Pap smears are a tool to prevent,
not just detect, cervical cancer, women reported a high-level of acceptability for cervical cancer
prevention measures, including Pap screening, HPV vaccination, and self-sampling. Our findings
highlight the need for education regarding the cause and prevention of cervical cancer. Currently
over 100 sites in Kenya offer regular screening, however, awareness is low and cervical cancer
screening coverage for all women age 1869 years is only 3.2% [5]. Therefore, start-up of a
successful screening program requires bringing the resources into the community but also
mobilizing the unscreened population to participate in the program. Data from this study can
help inform educational and outreach programs to target high-risk women, with the goal of
eliminating cervical cancer worldwide through the use of various screening and prevention tools.
Go to:
Acknowledgments
We thank the women and couples who participated in this research study and the clinical,
laboratory, and data management personnel who made this research possible.
Go to:
Footnotes
Competing Interests: Dr. Smith has received consultancy and research grants from GSK and
Merck Corporation over the past five years. The remaining authors have no competing interests
to declare. This does not alter the authors' adherence to all the PLoS ONE policies on sharing
data and materials.
Funding: This research was funded by US National Institutes of Health (NIH) National Institute
of Allergy and Infectious Diseases (R01 AI068431) and the University of Washington Center for
AIDS Research (P30 AI027757). Dr. Rositch and Dr. Gatuguta were supported by the Fogarty
International Clinical Research Scholars/Fellows program funded by the NIH Fogarty
International Center grant (R24 TW007988) and Dr. Rositch by the Institutional Research
Cancer Epidemiology Fellowship funded by the NIH National Cancer Institute (T32
CA0009314). The funders had no role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Go to:
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Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. [J
Pathol. 1999]
Human papillomavirus type distribution in invasive cervical cancer and high-grade
cervical lesions: a meta-analysis update. [Int J Cancer. 2007]
Review Screening for cervical cancer. [Ann Intern Med. 1990]
Cancer of the cervix--old and young, now and then. [Gynecol Oncol. 1991]
Annual report to the nation on the status of cancer, 1975-2007, featuring tumors of the
brain and other nervous system. [J Natl Cancer Inst. 2011]
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HPV DNA testing of self-collected vaginal samples compared with cytologic screening
to detect cervical cancer. [JAMA. 2000]
Comparison of human papillomavirus testing and cytology for cervical cancer screening
in a primary health care setting in the Democratic Republic of the Congo. [Gynecol
Oncol. 2012]
Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer
prevention (MARCH): a community-based randomised controlled trial. [Lancet. 2011]
Assessing women's willingness to collect their own cervical samples for HPV testing as
part of the ASPIRE cervical cancer screening project in Uganda. [Int J Gynaecol Obstet.
2011]
See more ...
Review Predictors of HPV vaccine acceptability: a theory-informed, systematic review.
[Prev Med. 2007]
HPV vaccine acceptability in Ghana, West Africa. [Vaccine. 2011]
Knowledge and practice about cervical cancer and Pap smear testing among patients at
Kenyatta National Hospital, Nairobi, Kenya. [Int J Gynecol Cancer. 2003]
Evaluation of cervical cancer screening program at a rural community of South Africa.
[East Afr J Public Health. 2008]
Knowledge of cervical cancer screening and use of cervical screening facilities among
women from various socioeconomic backgrounds in Durban, Kwazulu Natal, South
Africa. [Int J Gynecol Cancer. 2002]
Review HIV, human papillomavirus, and cervical neoplasia and cancer in the era of
highly active antiretroviral therapy. [Eur J Cancer Prev. 2008]
Knowledge and practice about cervical cancer and Pap smear testing among patients at
Kenyatta National Hospital, Nairobi, Kenya. [Int J Gynecol Cancer. 2003]
Breast and cervical cancer screening practices among Hispanic women in the United
States and Puerto Rico, 1998-1999. [Prev Med. 2002]
Beliefs and attitudes as determinants of cervical cancer screening: a community-based
study in Singapore. [Prev Med. 1995]
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v.10; 2010 >
PMC2904281

BMC Cancer. 2010; 10: 310.
Published online 2010 June 21. doi: 10.1186/1471-2407-10-310
PMCID: PMC2904281
Self-reported history of Pap-smear in HIV-
positive women in Northern Italy: a cross-
sectional study
Luigino Dal Maso,
1,2
Silvia Franceschi,
3
Mauro Lise,
1
Priscilla Sassoli de' Bianchi,
4
Jerry
Polesel,
1
Florio Ghinelli,
5
Fabio Falcini,
6
and Alba C Finarelli
4
, the Screening of HIV-positive
women in Emilia-Romagna (SHER) Study epidemiology@cro.it
Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background
The incidence of invasive cervical cancer in HIV-positive women is higher than in the general
population. There is evidence that HIV-positive women do not participate sufficiently in cervical
cancer screening in Italy, where cervical cancer is more than 10-fold higher in women with
AIDS than in the general population. The aim of the present study was to evaluate the history of
Pap-smear in HIV-positive women in Italy in recent years. We also examined the
sociodemographic, clinical, and organizational factors associated with adherence to cervical
cancer screening.
Methods
A cross-sectional study was conducted between July 2006 and June 2007 in Emilia-Romagna
region (Northern Italy). All HIV-positive women who received a follow-up visit in one of the 10
regional infectivology units were invited to participate. History of Pap-smear, including
abnormal smears and subsequent treatment, was investigated through a self-administered
anonymous questionnaire. The association between lack of Pap-smear in the year preceding the
interview and selected characteristics was assessed by means of odds ratios (OR) and 95%
confidence intervals adjusted for study centre and age.
Results
A total of 1,002 HIV-positive women were interviewed. Nine percent reported no history of Pap-
smear, and 39% had no Pap-smear in the year prior to the date of questionnaire (last year). The
lack of Pap-smear in the last year was significantly associated with age <35 years (OR = 1.4,
compared to age 45 years), lower education level (OR = 1.3), first HIV-positive test in the last 2
years (OR = 1.4), and CD4 count <200 cells/l (OR = 1.6). Conversely, when women were
advised by a gynecologist rather than other health workers to undergo screening, it significantly
increased adherence. Non-significantly higher proportions of lack of Pap-smear in the last year
were found in women born in Central-Eastern Europe (OR = 1.8) and Africa (OR = 1.3). No
difference in history of Pap-smear emerged by mode of HIV-acquisition or AIDS status.
Three hundred five (34%) women reported a previous abnormal Pap-smear, and of the 178
(58%) referred for treatment, 97% complied.
Conclusions
In recent years the self-reported history of Pap-smear in HIV-positive women, in some public
clinics in Italy, is higher than previously reported, but further efforts are required to make sure
cervical cancer screening is accessible to all HIV-positive women.
Go to:
Background
The incidence of invasive cervical cancer in HIV-positive women is higher than in the general
population [1]. This elevated incidence varies from country to country depending on study site
and characteristics of the populations under study [2-4]. The weaker association between HIV-
infection and cervical cancer risk in some countries seems to be explained by competing risks of
death (e.g.: in Africa), or early detection of pre-invasive lesions (e.g.: in the United States) [5].
Effective screening and early treatment of precancerous cervical lesions are key factors in
preventing the progression to invasive cervical cancer in both HIV-positive and -negative women
[6]. Recent guidelines recommend that, following two initial normal Pap-smears at a 6-month
interval, all HIV-positive women should undergo annual cervical cytologic examination [7]. In
addition, it is recommended that all immunosuppressed women with atypical squamous cells
undergo colposcopy [7].
In the United States, approximately 80% of HIV-positive women reported a history of Pap-smear
in the past year [8,9]. Low incidence rates of invasive cervical cancer, similar to those among
HIV-negative women, were found among adequately screened HIV-positive women [10]. In
contrast, there is evidence that HIV-positive women do not participate sufficiently in cervical
cancer screening in Southern European countries such as Italy and Spain, where cervical cancer
incidence is more than 10-fold higher in women with AIDS than in general population
[3,5,11,12].
In Italy, one-half of women with invasive cervical cancer as the AIDS-defining illness (3% of all
women with AIDS) had their first HIV-positive test 10 years before cancer diagnosis [12]. This
long interval suggests a failure to stop the progression of precancerous lesions through screening,
despite the knowledge of HIV infection.
A large cross-sectional study showed not only a scanty use of Pap-smear among HIV-positive
Italian women, but also that these women did not know that a Pap-test was used to prevent
cervical cancer [13]. In addition, a survey conducted among clinicians in 27 Italian HIV centers
showed low compliance with the published guidelines on gynecologic follow-up of HIV-positive
women in Italy [14].
The aim of the present study was to evaluate the recent history of Pap-smear in HIV-positive
women in Italy followed in public HIV clinics. We also examined the sociodemographic,
clinical, and organizational factors associated with the lack of adherence to screening
recommendations.
Go to:
Methods
Study population
A cross-sectional study was conducted between July 2006 and June 2007 the in Emilia-Romagna
Region (Northern Italy). At end of 2006, this region covered an area of more than 22.000 km
2
(7% of Italy), with a population of 4.2 million inhabitants (7% of Italian population).
Approximately 1,500 HIV-positive women are estimated to live in the Emilia-Romagna Region
[15,16]. All HIV-positive women who underwent a follow-up visit (recommended every 6-
months) in one of the 10 regional infectivology units were invited to participate. The study
period was limited to one year in order to reduce the possibility of duplication.
A total of 1,108 HIV-positive women were invited and 1,002 (90.4%) accepted to participate.
Study aims were explained and written informed consent was obtained from study women, who
subsequently completed a self-administered anonymous questionnaire. History of Pap-smear was
investigated in detail to assess lifetime screening, including dates of first and last Pap-smear, and
number of Pap-smears in the three years preceding the questionnaire. The questionnaire included
additional items on the place where Pap-smear was taken, HPV testing, history of abnormal
smears, and treatment of cervical lesions. Other collected data included sociodemographic
factors (e.g., age, education level, and country of birth), smoking and reproductive history,
sexual habits (e.g., age at first intercourse, lifetime number of sexual partners, and use of
contraceptive methods), and history of HIV infection (e.g., date of first HIV-positive test and
most probable route of HIV acquisition). In a separate form, the attending infectivologist
reported information on the course of HIV-infection (e.g.: HIV-related hospitalization, last CD4
count and HIV RNA values, AIDS status, and AIDS-defining conditions).
The Ethical Committees of all participating centers approved the study protocol.
Statistical analysis
Odds ratios (ORs) and 95% confidence intervals (CIs) were used as the measures of association
between history of Pap-smear and women's characteristics, and were estimated using logistic
regression models adjusted for study centre and age [17,18]. Estimates were also calculated
including further adjustment for area of birth, mode of HIV acquisition, and time since first HIV-
positive test.
Go to:
Results
A total of 1,002 HIV-positive women completed the questionnaire. The median age was 41 years
and the vast majority of women (87%) fell in the 30-to-49-year age range. Eighty percent of our
study women were born in Italy and nearly two-thirds reported sexual intercourse as the route of
HIV acquisition. One hundred eighty (18%) women had a previous AIDS diagnosis and 56% had
their first HIV-positive test 10 or more years prior to the questionnaire.
Nine percent of women reported no history of Pap-smear and 305 (34%) had abnormal Pap-
smear results (Figure (Figure1).1). Women with no history of Pap-smear were younger and more
likely to be born in Central-Eastern Europe (15%) or Africa (29%) than women reporting
previous Pap-smears (3% and 9%, respectively) (data not shown). HPV test was reported by only
27% of women (Figure (Figure11).

Figure 1
Pap-smear practice and treatment after a positive Pap-smear in HIV-positive women.
Emilia-Romagna Region, Italy, 2006-2007
Overall, 607 (61%) of the 1,002 HIV-positive women had a Pap-smear in the year prior to
questionnaire (last year, Table Table1).1). Women younger than 35 years (OR, compared to age
45 = 1.4; 95%CI: 1.0-2.0), those with lower education level (OR = 1.3; 95%CI: 1.0-1.7), those
with recent first HIV-positive test (OR for 2 years vs 10 years = 1.4; 95%CI: 1.0-2.1), or a
CD4 count of <200 cells/l (OR compared to 500 = 1.6; 95%CI: 1.0-2.5) were more likely to
have no history of Pap-smear in the year before questionnaire. Non-significantly higher
proportions of lack of Pap-smear in the last year were found in women born in Central-Eastern
Europe (OR = 1.8; 95%CI: 0.9-3.6) and Africa (OR = 1.3; 95%CI: 0.8-2.0). No difference in
Pap-smear history emerged by mode of HIV acquisition, or AIDS status.

Table 1
Odds ratio (OR) and corresponding 95% confidence intervals (CI) for lack of Pap-smear in the
last year by selected characteristics
Receiving screening advice from a gynecologist rather than an infectivologist (OR = 0.6; 95%CI:
0.4-0.9) and history of abnormal Pap-smear (OR = 0.5; 95%CI: 0.3-0.6) were associated with
better screening participation (Table (Table1).1). The multivariate models, including additional
terms for area of birth, mode of HIV acquisition, and time since first HIV-positive test, did not
materially modify the risk estimates even if associations with age and first HIV-positive test
were not statistically significant (Table (Table11).
Among the 305 women who reported a previous abnormal Pap-smear, treatment was
recommended for 178 (58%); of whom, 173 (97%) complied. Among the 127 (42%) women
who were referred for further testing but not treatment, 84 (66%) underwent all the
recommended follow-up tests.
Among the 178 women to whom treatment was recommended, 145 (81%) reported colposcopy
and all follow-up tests. Conization was the surgical procedure most frequently reported by
patients (122, 69%), followed by hysterectomy (19, 11%), and cryotherapy (8, 4%).
Go to:
Discussion
This study was the first attempt to provide estimates of self-reported Pap-smear history in HIV-
positive women attending infectivology units of a large Italian region. We found that 91% of
women had had at least one Pap-smear in their lifetime, and 61% reported a Pap-smear in the last
year. These proportions are similar to the ones reported by the general population of the same
age and geographical area (95% and 47%, respectively) (Carrozzi and Bertozzi, personal
communication), and substantially higher than those reported (43%) in 2001 by a physician-
based Italian survey [14]. Increase in the number of Pap-smears performed, however, is difficult
to evaluate, given the different study designs of previous studies conducted in Italy [13,14]. The
proportion of women who had a Pap-smear in the last year, however, remains suboptimal with
respect to current guidelines regarding HIV-positive women (annual Pap-smear recommended to
all patients), and is lower than the estimates (approximately 80%) reported in the USA [8,9].
Factors associated with lack of recent Pap-smear were young age (<35 years), recent HIV
diagnosis (2 years), and more advanced diseases (CD4 count at last visit <200 cells/L).
Conversely, receiving screening advice from a gynecologist significantly improved the
adherence to Pap-smear. We found less influence of education level or country of birth than a
previous cross-sectional study conducted in Rome [13]. As expected, study women reported a
high proportion of previous abnormal Pap-smears (34%), in agreement with previous reports
among HIV-positive women in Italy [13] and the United States [8,9].
Overall, our study highlights the difficulties in following the recommended protocol of
combining routine follow-up of HIV infection with gynecological examination, which is
generally not performed in infectivology units [5,10]. In addition, patient compliance needs to be
improved [14] and health professionals (e.g., infectious disease specialists and gynecologists)
should thoroughly inform HIV-positive women (particularly the disadvantaged ones) of the
importance of Pap-smear to their health.
The present study has strengths and weaknesses. Strengths included the high participation among
unselected women attending infectivology units. Approximately 1,500 HIV-positive women are
estimated to live in the Emilia-Romagna Region [15,16] and all women attending HIV follow-up
(recommended every 6 months) were contacted in a 1-year period. A previous study in Northern
Italy [19] showed that patients infected with HIV through injecting drug use, patients without
AIDS diagnosis, or patients with higher CD4 counts are more likely to miss medical
appointments and discontinue their follow-up. It is unlikely that HIV-positive women in the
region received their follow-up visits elsewhere, given the high standard of medical care
provided (free of charge) in Emilia-Romagna in comparison with other Italian areas. However,
the possibility of some socio-demographic bias in women who did not attend regularly follow-up
cannot be totally ruled out.
The number of self-reported Pap-smears among HIV-positive women in our study may be an
overestimate as women tend to over-report their participation in cervical cancer screening in a
given timeframe [20]. Confidentiality prevented us from linking women's reports with
gynecological and cytological records, thus leaving substantial uncertainty about the actual
additional tests and treatments performed. To validate self-reported Pap-smear use and to follow-
up the treatment of HIV-positive women diagnosed with gynaecological lesions, a new study is
being planned, which will adopt broader confidentiality rules and obtain a written consent to
follow-up. The most important limitation of our survey, however, is the restriction to HIV-
positive women followed by public clinics in one of the best organized regions of Italy, in terms
of participation and quality of cervical cancer screening [21,22].
Go to:
Conclusions
Our study showed that progresses have been made to screen adequately HIV-positive women in
Italy and that such efforts can also reach the most vulnerable populations (e.g.: immigrants). The
opportunity to prevent cervical cancer in women living with HIV infection should not be missed;
successful implementation of such screening programs will also teach valuable lessons that could
then be applied to all women [5]. There is, however, still some scope for improvement,
especially in the completeness of treatment and follow-up of HIV-positive women with an
abnormal Pap-smear. Most importantly, much remains to be done to make sure that the
experience of the Emilia-Romagna Region can be extended to other parts of Italy.
Go to:
Competing interests
The authors declare that they have no competing interests.
Go to:
Authors' contributions
LDM, SF, PSdB, and ACF conceived the study and were involved in data interpretation. PSdB
coordinated the data collection. ML and JP collaborated with LDM in the acquisition of data and
statistical analyses. LDM drafted the manuscript. FG and FF supervised the study. All members
of the "Screening of HIV-positive women in Emilia-Romagna (SHER) Study" actively
collaborated to all the phases of the study. All Authors critically revised the manuscript for
important intellectual contents. All authors read and approved the final manuscript.
Go to:
Authors' information
LDM is a Senior Scientist at Aviano Cancer Institute and coordinated a surveillance study on
cancer in people with HIV/AIDS in Italy. SF is Head of Infections and Cancer Epidemiology
Group at International Agency for Research on Cancer (Lyon, France) and has been carrying out
numerous international studies on the association between infection and cancer. ACF is Head of
Public Health department of Emilia-Romagna Region. ML and JP collaborated with LDM, PSdB
collaborated with ACF. FG is president of AIDS Commission, Emilia-Romagna Region, FF is
Chief of Romagna Cancer Registry.
Go to:
Pre-publication history
The pre-publication history for this paper can be accessed here:
http://www.biomedcentral.com/1471-2407/10/310/prepub
Go to:
Acknowledgements
Funding: This work was supported by grants from Emilia-Romagna Region, National Institute of
Health, Rome (No. 20G.3), and OncoSuisse (ICP OCS 01355-03-2003). Mauro Lise was
supported, while at the International Agency for Research on Cancer, by a fellowship from the
Italian Association for Cancer Research (AIRC).
The authors wish to thank Mrs Luigina Mei for editorial assistance. All the HIV-positive women
who took part in this research are gratefully acknowledged.
Members of the SHER Study also include:
Lucia Droghini (Emilia-Romagna Region), Diego Serraino (CRO Aviano), Francesco Alberici
(Piacenza), Anna Degli Antoni (Parma), Giacomo Magnani (Reggio Emilia), Giovanni Guaraldi
(Modena), Francesco Chiodo (Bologna); Laura Sighinolfi (Ferrara), Giacomo Ballardini
(Ravenna), Claudio Cancellieri (Forl), Alessandro Stagno (Cesena), Massimo Arlotti (Rimini),
Alessandra Govoni (Imola).
Go to:
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[J Acquir Immune Defic Syndr. 2001]
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Acquir Immune Defic Syndr. 2009]
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Evidence for lack of cervical cancer screening among HIV-positive women in Italy. [Eur
J Cancer Prev. 2006]
Knowledge and use of papanicolaou test among HIV-positive women. [Int J Cancer.
2005]
Access to gynecological services and Papanicolau tests in HIV-infected Italian women: a
questionnaire survey. [AIDS Care. 2006]
Access to gynecological services and Papanicolau tests in HIV-infected Italian women: a
questionnaire survey. [AIDS Care. 2006]
Knowledge and use of papanicolaou test among HIV-positive women. [Int J Cancer.
2005]
Screening for cervical cancer in HIV-infected women receiving care in the United States.
[J Acquir Immune Defic Syndr. 2001]
Prevalence of cervical cancer screening of HIV-infected women in the United States. [J
Acquir Immune Defic Syndr. 2009]
Knowledge and use of papanicolaou test among HIV-positive women. [Int J Cancer.
2005]
Screening for cervical cancer in HIV-infected women receiving care in the United States.
[J Acquir Immune Defic Syndr. 2001]
Prevalence of cervical cancer screening of HIV-infected women in the United States. [J
Acquir Immune Defic Syndr. 2009]
Cervical cancer screening of women living with HIV infection: a must in the era of
antiretroviral therapy. [Clin Infect Dis. 2007]
Low incidence of invasive cervical cancer among HIV-infected US women in a
prevention program. [AIDS. 2004]
Access to gynecological services and Papanicolau tests in HIV-infected Italian women: a
questionnaire survey. [AIDS Care. 2006]
Factors associated with the failure of HIV-positive persons to return for scheduled
medical visits. [HIV Clin Trials. 2002]
Review Accuracy of self-reports of Pap and mammography screening compared to
medical record: a meta-analysis. [Cancer Causes Control. 2009]
Performance indicators of organized cervical screening in Romagna (Italy). [Eur J Cancer
Prev. 2003]
Cervical cancer screening of women living with HIV infection: a must in the era of
antiretroviral therapy. [Clin Infect Dis. 2007]
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Int J Circumpolar Health >
v.71; 2012 >
PMC3417708

Int J Circumpolar Health. 2012; 71: 10.3402/ijch.v71i0.17996.
Published online 2012 March 19. doi: 10.3402/ijch.v71i0.17996
PMCID: PMC3417708
Inuit women's attitudes and experiences
towards cervical cancer and prevention
strategies in Nunavik, Quebec
Helen Cerigo,
1
Mary Ellen Macdonald,
2
Eduardo L. Franco,
1,3
and Paul Brassard
1,4,*

Author information Article notes Copyright and License information
Go to:
Abstract
Objectives
To describe the attitudes about and experiences with cervical cancer, Pap smear screenings and
the HPV vaccine among a sample of Inuit women from Nunavik, Quebec, Canada. We also
evaluated demographic and social predictors of maternal interest in HPV vaccination.
Study design
A mixed method design was used with a cross-sectional survey and focus group interviews.
Methods
Women were recruited through convenience sampling at 2 recruitment sites in Nunavik from
March 2008 to June 2009. Differences in women's responses by age, education, and marital
status were assessed. Unconditional logistic regression was used to determine predictors of
women's interest in HPV vaccination for their children.
Results
Questionnaires were completed by 175 women aged 1863, and of these women a total of 6
women aged 3155 participated in 2 focus groups. Almost half the survey participants had heard
of cervical cancer. Women often reported feelings of embarrassment and pain during the Pap
smear and older women were more likely to feel embarrassed than younger women. Only 27% of
women had heard of the HPV vaccine, and 72% of these women were interested in vaccinating
their child for HPV. No statistically significant predictors of maternal interest in HPV
vaccination were found.
Conclusions
Our findings indicate that health service planners and providers in Nunavik should be aware of
potential barriers to Pap smear attendance, especially in the older age groups. Given the low
awareness of cervical cancer, the Pap smear and the HPV vaccine, education on cervical cancer
and prevention strategies may be beneficial.
1

Keywords: cervical cancer, human papillomavirus, attitudes, experiences, Inuit, vaccine
The inclusion of cervical cytology screening in the Canadian health care system has led to a great
reduction in cervical cancer incidence and mortality (1). Non-compliance to screening guidelines
continues to be a major risk factor for invasive cervical cancer (2). In 1998, about 20% of
Canadian women aged 2069 reported not having had a Papanicolaou (Pap) test within the
previous 3 years and the majority of cervical cancer cases occur among unscreened or
underscreened women (1). Factors that predict underutilization of cervical cancer screening in
Canada include older age, lower educational attainment, lower socio-economic status, single
marital status, birth place outside Canada, Aboriginal identity, rural residence and negative
health and lifestyle characteristics, such as infrequent physical activity and not having a regular
family doctor (35). Further, Pap smear screening among Aboriginal women has been found to
be limited by a lack of knowledge about Pap smears and their importance, feelings of
embarrassment and a lack of continuity of care due to a high turnover of health professionals
(6,7).
The discovery that the human papillomavirus (HPV) is a necessary cause of cervical cancer has
allowed for the development of HPV vaccines as an additional means of cervical cancer
prevention (8). Although HPV vaccination has the potential to reduce cervical cancer incidence
worldwide by 70%, regular cervical cancer screening is still important to prevent the remaining
30% of cancers.
The historically high incidence of cervical cancer among the Canadian Inuit population has
declined greatly since the 1990s; however, the Inuit continue to suffer a disproportionate burden
of the disease compared to the general population (9). Among the Canadian Inuit, the age-
standardized incidence rate of cervical cancer between 1989 and 2003 was 14.7 per 100,000,
which was about three times higher than the Canadian average (9,10).
Approximately one-fifth of the Canadian Inuit population resides in the geographic region of
Nunavik, the Subarctic and arctic region of northern Quebec (11). In Quebec, the Aboriginal
populations face both a higher cervical cancer incidence and mortality rate than the general
population (12). Consistent with the high risk of cervical cancer in the Inuit populations of
Canada, a high prevalence of HPV has been found among the predominately Inuit populations of
Nunavik and the Arctic federal territory of Nunavut (13,14). In Quebec there is no organized
cervical cancer screening program and thus in Nunavik, Pap smear screening is done
opportunistically. The Pap test is available in all 14 Nunavik communities, and is generally
performed by nurse practitioners. Colposcopy, the standard follow-up for abnormal Pap smears,
is available at the main health centres located in Kuujjuaq and Puvirnituq, which implies that
women from the other 12 communities have to fly to attend referral appointments. In the 2004
Nunavik Health Survey, not having a Pap test in the previous 2 years was associated with a lower
level of education and older age (15).
The HPV vaccination program in Nunavik was implemented in 2008 and was linked to the
successful school-based hepatitis B vaccination program. First dose vaccine coverage for girls 9
to 17 years was 78.3% for all of Nunavik (Lise Lapierre, Clinical Nurse of Infectious Diseases,
personal communication, June 2010).
Despite the higher incidence and mortality rates of cervical cancer among Aboriginal women
worldwide, there have been relatively few studies describing Aboriginal women's knowledge,
attitudes and experiences regarding cervical cancer and its prevention (1618). This paper aims
to describe the attitudes about and experiences with cervical cancer, Pap smear screening and the
HPV vaccine among a sample of Inuit women from Nunavik, Quebec. We also evaluate
demographic and social predictors of women's interest in HPV vaccination for their children.
Such knowledge can assist in the planning of future cervical cancer screening and vaccination
programs.
Go to:
Material and methods
From March 2008 through June 2009, a convenience sample of 175 Inuit women aged 1869
years was recruited from common gathering places in 2 communities of Ungava Bay, Nunavik.
Nurse practitioners from the communities were responsible for recruitment and questionnaire
administration. The survey contained 59 questions divided into 7 sections: (1) sociodemo-
graphics, health and lifestyle characteristics; (2) use of health services; (3) knowledge, attitudes
and beliefs about HPV; (4) knowledge, attitudes and beliefs about cervical cancer; (5)
knowledge, attitudes and beliefs about the Pap test; (6) sexual behaviour and self-perceived risk
of STI; and (7) knowledge and purpose of HPV vaccines. This paper focuses on outcome
variables from sections 4, 5 and 7 and on the covariates measured in sections 1, 2 and 6. Analysis
of the outcome variables from section 3 has been presented elsewhere and includes details about
the questionnaire administration, validation and translation (19).
Previous awareness of cervical cancer was defined as a response of Yes to the question Have
you heard of cervical cancer? whereas a response of Yes to the question Have you heard of a
vaccine against HPV? defined awareness of the HPV vaccine. Maternal interest in HPV
vaccination was defined as a response of Yes to the question As a parent, would you be
interested in having your child/children vaccinated for HPV?
Women's attitudes and knowledge about cervical cancer and the HPV vaccine were only
determined among women who reported being previously aware of cervical cancer and the HPV
vaccine, respectively. Likewise, women's previous experiences with Pap smears were only
reported for women who stated that they had a previous history of cervical cancer screening.
Basic descriptive statistics and frequency calculations were performed on all variables. As age,
education and marital status have been shown to affect women's cervical cancer and HPV
vaccine awareness and knowledge (20,21) and as it was hypothesized that women's attitudes and
experiences would vary by these factors,
2
tests were used to explore differences in women's
responses to questionnaire items by these stratifying variables. Fisher's exact tests were used
when the cell count was less than 5. Variables were stratified as follows: age (less than 35 years
vs. 35 years and older), education (13 years of education or more vs. less than 13 years of
education) and marital status (married or living with a partner vs. not married or living with a
partner).
Unconditional logistic regression was used to determine predictors of maternal interest in HPV
vaccination. Odds ratios and their respective 95% confidence intervals were calculated.
Statistical significance was set at 5% for all tests and regressions. Statistical analysis was carried
out with SAS version 9.2.
In conjunction with the questionnaire data, focus groups were conducted in the 2 recruitment
communities between June and October 2008. Recruitment into the focus groups was based on
convenience sampling and was advertised via radio broadcast, a popular medium in these
communities. Focus groups lasted about 45 minutes and were facilitated by 1 investigator (PB).
The focus group guide included the following domains: barriers/facilitators to Pap smear
attendance, use of safe-sex practices, awareness of cervical cancer, purpose of Pap smears,
perceptions about HPV vaccination and ways to promote the vaccine. Each session was
recorded, transcribed and then coded with NVivo computer software. Thematic content analysis
of the transcripts was used to organize the data.
Written informed consent was obtained from all participants. Women were compensated with
$20 after they completed the survey and after they participated in the focus group. Ethical
approval was obtained from the McGill Institutional Review Board and the Tulattavik Health
Centre.
Go to:
Results
Selected demographic characteristics are displayed in Table I. A complete description of the
study sample has been reported previously (19). The mean age of the sample was 34.3 with a
range of 1863 years. The two focus groups consisted of a total of 6 participants; 1 group had 2
participants and 1 group had 4 participants. The average age of focus group participants was 40.7
years (range: 3155).

Table I
Selected demographic characteristics of study participants, Nunavik, 20082009 (n =175)
Experiences, attitudes and beliefs about cervical cancer
Almost half of the survey study sample reported having previously heard about cervical cancer
(47%). The cervical cancer attitudes and beliefs among these women are summarized in Table II.
Most women who had heard of cervical cancer correctly identified a risk factor for the disease
(73%), with the largest proportion of women identifying the risk of multiple sexual partners
(42%). The majority of women reported that they thought early detection of cervical cancer
would increase the chances for a cure (59%), although another 38% of women did not know if it
would make a difference. About 45% of the subgroup of women who were aware of cervical
cancer believed they were at average risk for developing cervical cancer.

Table II
Experiences, attitudes and beliefs about cervical cancer among those women participants who
had heard of cervical cancer, Nunavik, 20082009 (n=85)
A significantly higher proportion of women 35 years and older thought they were at a higher risk
for cervical cancer (17%) than did women under 35 years (0%) (p=0.009). No statistically
significant associations were found when responses to questionnaire items on women's
experiences, attitudes and beliefs about cervical cancer were stratified by education and marital
status.
Pap smear history, understanding and experiences
Almost all women reported a history of previous Pap smear (96%), with 80% of all study
participants reporting that their last Pap smear was within the past year (Table III). The majority
of women intended to go for a Pap smear in the coming year (72%). The correct purpose of the
Pap smear (cervical cancer screening) was known by 46% of study participants, but another 30%
believed that it is a test for sexually transmitted infections (STIs).

Table III
Study participants Pap smear history, intentions, understanding and experiences, Nunavik,
20082009 (n=175)
Responses to the questionnaire items regarding experiences with Pap smears are displayed in
Table III for the subset of women who reported a previous history of Pap smears. Previous
abnormal Pap smears were reported by 20% of the women who reported having a Pap smear;
however, almost one-third of these women were unsure of their results. Feelings of
embarrassment during Pap smears were experienced by 37% of women who reported having a
previous Pap smear. Over 60% of women would prefer if the nurse or doctor explained each step
of the examination during the test. Pain during Pap smear tests was reported by 49% of women,
although 41% experienced pain only sometimes.
The majority of women would be most comfortable undergoing a Pap smear if it was
administered by a female practitioner, although another 19% reported that they did not have a
preference. This sentiment was also described by one women from one focus group, who said,
Some people don't go [to get Pap smears], maybe they're shy all of my friends don't go
probably because they are shy or sometimes they don't want to [be] checked by a man, if it is a
man that is a nurse.
Feelings of embarrassment were more commonly reported among women 35 years and older
(45%) than those under 35 (29%) (P=0.028). When women's responses to questions about Pap
smears were stratified by educational and marital status, no statistically significant associations
were found.
Attitudes towards the HPV vaccine
A total of 47 (27%) study participants reported previously hearing about the HPV vaccine prior
to this study. The attitudes towards the HPV vaccine among women who had heard about the
vaccine are displayed in Table IV. Of the women who were aware of the vaccine, almost 70%
knew that the potential benefits of the vaccine were protection from cervical cancer and 87%
knew that Pap smear tests would still be necessary after the vaccine.

Table IV
Attitudes towards the HPV vaccine among study participants who had heard of the HPV vaccine,
Nunavik, 20082009 (n=47)
Women would most likely go to their health practitioner for further information about HPV and
the HPV vaccine (68%), and 81% of the women reported that their decision to get the vaccine, if
indicated, would be influenced by a health professional. The majority of women believed that the
vaccine should be given to teenagers before the onset of sexual activity (68%). Maternal interest
in HPV vaccination was reported by 72% of the participants, but about one-quarter were either
unsure or were not interested in having their child vaccinated.
There were no significant associations when responses to questionnaire items concerning
attitudes to the HPV vaccine were stratified by age, educational status and marital status. None
of the demographic characteristics measured in our study significantly predicted the mothers'
interest in having their children vaccinated.
Go to:
Discussion
The components of the survey addressed in this paper assessed women's awareness, attitudes and
experiences with cervical cancer, the Pap smear and the HPV vaccine. A low awareness of
cervical cancer and the HPV vaccine was found, but almost 80% of the participants stated that
they had a Pap smear in the previous year, and 72% intended to get one within the coming year.
A similarly high cervical cancer screening coverage rate was reported by the 2004 Nunavik
Health Survey, where 82% of respondents reported having a Pap smear in the previous 2 years
and 60% in the past 12 months (15). Both our survey and the Nunavik Health Survey used self-
reported data and these data may show an overestimation of the coverage rate, given that a
previous chart review conducted between 2002 and 2007 showed that 71% of women in Nunavik
had a Pap test within the previous 3 years (14).
A sizable proportion of the women were unable to identify a cervical cancer risk factor and were
unsure if detecting cervical cancer early would affect the chance for a cure. Further, we found
that some women did not fully understand the purpose of the Pap smear as a method of cervical
cancer screening, as 30% reported that the purpose of the Pap smear test is to screen for STIs.
These results suggest that further education about cervical cancer and its prevention may be
beneficial to increase awareness. Higher knowledge about Pap smears has been shown to be
associated with higher cervical cancer screening adherence (20,22).
Feelings of embarrassment and pain during Pap smears were common among our study
population and others (23). Among our population, older women reported more feelings of
embarrassment than the young women. Health care providers in Nunavik should be aware of this
difference in Pap smear experience by age, especially given that older age is associated with a
decline in cervical cancer screening in the Canadian population and cervical cancer incidence is
the highest among women in their 40s (3,24). Additionally, more women over the age of 35 in
our population perceived themselves to be at a higher risk of cervical cancer than women who
were younger than 35. We found that Inuit women had a strong preference for having cervical
cancer screening performed by female health practitioners and that they wanted explanations to
be given to them throughout the Pap smear examination. These preferences were also shown
among Aboriginal populations in Canada and the United States (17,25). When planning health
services these concepts should be kept in mind, as Coe et al. (16) found that Pap smear
adherence was lower among women who reported that they would refuse a male provider.
Inuit women who had heard of the HPV vaccine generally reported positive views towards the
HPV vaccine with the majority of women reporting a belief in the vaccine's safety. However,
many women may want further information about the vaccine, as evidenced by those who
answered with the unsure category to many questionnaire items. Most women agree that the
vaccine should be given to younger women before they engage in sexual activity.
The majority of women who had heard of the HPV vaccine were interested in having their
children vaccinated, which was also found among the general Canadian population (26) and in a
population of Alaska Native parents (18). Although we only measured maternal interest, there
was in fact a very high first-dose HPV vaccination uptake in Nunavik. This suggests that the
high interest in vaccination reported by mothers was indeed predictive of the future behaviour of
parents in Nunavik to provide consent for their children to be vaccinated. The high uptake of the
vaccine may be related to the trust in health professionals reported by women in our study, where
most women report that they would seek further information on the vaccine from and have their
decision to be vaccinated influenced by their doctor or nurse. We were unable to determine if a
woman's relationship with her health provider influenced her interest in vaccinating her children,
but general trust in doctors and government was previously found to be predictive of vaccine
acceptance in a study of British parents (27). It is important to note that the strong acceptance of
the vaccine in this population may not be specific to concerns about HPV and cervical cancer,
but that it may be more indicative of a general acceptance of vaccination due to the active role
nurses play in communities and schools (where the vaccination program occurs) and the
historical power differential between the Inuit and health providers. This may be especially true
as there is a low level of understanding about HPV and its relation to cervical cancer in this
population (19).
No predictors of maternal interest in vaccination were found in our study population. This result
may be due to our small sample and that few mothers were definitively uninterested in the
vaccination for their children. Despite this, it is possible that there are no predictors of
acceptance in this population given the high uptake rate. Previous studies have shown factors
such as parental cervical cancer screening behaviour (19,28) and younger parental age (26) to be
associated with parental interest in vaccination and adolescent vaccine uptake. Further, vaccine
acceptance has been shown to be associated with acceptance of general vaccines (26,27,29) and
vaccination rates of hepatitis B are very high in Nunavik.
The main limitation of this study was the non-random recruitment strategy. Women were
recruited into this study through convenience sampling. They were frequent health care users
and, given their interest in the study, may have a higher understanding of cervical cancer, Pap
smears and the HPV vaccine compared to less frequent health services users. It was not feasible
to collect information about the women who chose not to participate in the study. Despite our
sampling method, our sample had a similar age distribution (30), health behaviours (31,32),
health service use (15,33) and educational attainment (30) as the female population of Nunavik.
It is possible that our study underestimated women's awareness of cervical cancer and the HPV
vaccine, given that the Inuit are often modest about their knowledge and experiences (34). If this
was the case, we may have unnecessarily reduced our sample size by focusing our reporting of
attitudes and knowledge of cervical cancer, the HPV vaccine and Pap smears on women who had
respectively stated they had heard of cervical cancer and the vaccine and on those who had a
history of Pap smears. It was decided that this restriction was important to reduce the influence
of chance guessing on the estimates. Additionally, these data are self-reported, so we do not
actually know what women will do or have done.
Although unintended, participants of both focus groups directed the conversation towards an
educational focus due to the limited knowledge about HPV, cervical cancer and Pap smears
among participants. This shows that these women have an interest in gaining further knowledge
about women's health issues, such as cervical cancer and STI prevention, and further
opportunities for education should be made available. As a result of the educational focus of the
interviews, we were unable to assess the effect that factors such as a lack of knowledge about
Pap smears and their importance and the lack of continuity of care due to a high turnover of
health professionals had on Pap smear attendance among women in Nunavik.
This is the first study to attempt to describe women's awareness, attitudes and experiences of
cervical cancer, Pap smears and the HPV vaccine in a Canadian Inuit population. Although
questionnaire items were of a sensitive nature, there was very little missing information. As
almost all study participants stated they had a history of Pap smears, we were unable to assess
demographic predictors of Pap smear attendance. Future research such should focus on
determining if there are certain subsets of the female population who are underscreened for
cervical cancer in Nunavik and how screening coverage can be increased within these groups.
Go to:
Acknowledgements
Funding for this research was provided by the Social Sciences and Humanities Research Council
(SSHRC) and a Team Grant on HPV Infection and Associated Diseases from the Canadian
Institutes of Health Research (CIHR). P. Brassard was supported by a clinician scientist career
award from the Fonds de Recherche en Sante du Quebec (FRSQ).
The authors thank the Tulattavik Health Centre, collaborating nurse practitioners, especially
Johanne Blouin, the participating communities, and the Nunavik Regional Board of Health and
Social Services for making this research possible.
Go to:
Footnotes
1
Published ahead-of-print 26 October 2011 (at www.ijch.fi) in accordance with previous
publisher's routines.
Go to:
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acceptance. Hum Vaccin. 2007;3(5):1715. [PubMed]
28. Chao C, Slezak JM, Coleman KJ, Jacobsen SJ. Papanico-laou screening behavior in mothers
and human papil-lomavirus vaccine uptake in adolescent girls. Am J Public Health.
2009;99(6):113742. [PMC free article] [PubMed]
29. Lenselink CH, Gerrits MM, Melchers WJ, Massuger LF, van Hamont D, Bekkers RL.
Parental acceptance of Human Papillomavirus vaccines. Eur J Obstet Gynecol Reprod Biol.
2008;137(1):1037. [PubMed]
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Qubec (table). Aboriginal Population Profle, 2006 Census.
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Regional Board of Health and Social Services; 2007. Tobacco Use; p. 9.
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de Qubec, Nunavik Regional Board of Health and Social Services; 2010. Alcohol, drug use and
gambling among the Inuit of Nunavik: epidemiological profle; p. 17.
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Inuit of northern Quebec, 19821996: a case-control study. CMAJ. 2001;165(6):74955. [PMC
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PMC2734064

Int J Epidemiol. 2008 August; 37(4): 862869.
Published online 2008 July 23. doi: 10.1093/ije/dyn118
PMCID: PMC2734064
Who is getting Pap smears in urban Peru?
Valerie A Paz Soldan,
1,*
Frank H Lee,
2
Cesar Carcamo,
3
King K Holmes,
4
Geoff P Garnett,
5
and
Patricia Garcia
3

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background Cervical cancer, although usually preventable by Pap smear screening, remains the
leading cause of cancer-related deaths among women in Peru. The percentages and
characteristics of women in Peru who have or have not had a Pap smear have not been defined.
Methods In an urban community randomized trial of sexually transmitted infection (STI)/HIV
prevention in Peru, 6712 randomly selected women between the ages of 18 and 29 from 20 cities
were interviewed regarding having had cervical Pap smears.
Results Among women sampled, only 30.9% had had a Pap smear. By multivariate analysis, the
main predictors of having a Pap smear were having had sex, having had children, completion of
secondary education and increasing age. Regional variations were also found: women from the
highlands and rainforest were less likely to have had Pap smears than women from the coast.
Conclusion A norm of seeking and receiving Pap smears has not been established among
sexually active young Peruvian women. To improve Pap smear coverage in Peru, promotion
efforts should target underserved women and regions with less coverage.
Keywords: Vaginal smear, Peru
Go to:
Background
Cervical cancer is one of the most preventable cancers. We can screen for pre-cancerous and
early cervical neoplasia, which progresses slowly if at all to invasive cancer; and cervical
neoplasia can be effectively treated if caught in time.
1
Despite this, cervical cancer is a leading
cause of cancer-related deaths among women in many developing countries, including Peru.
1,2
In
Peru, the annual cervical cancer incidence is one of the highest in the Americans at 40/100 000
women, resulting in a cause-specific mortality rate of 22/100 000 women per year.
3

To date, cervical cancer prevention efforts worldwide have relied on using cervical Pap smears
to screen at-risk women for cellular abnormalities, and then treating any pre-cancerous lesions
identified.
24
This secondary prevention has successfully decreased cervical cancer in high- and
middle-income countries,
2
and reduced cervical cancer mortality in these countries, including
some in Latin America.
57
In Peru, reducing cervical cancer has been a national priority for
several decades; in 1998, a National Plan for the Prevention of Gynecological Cancer outlined
strategies for cervical cancer prevention.
8
In 2000, the Ministry of Health published its Manual
of Standards and Procedures for the Prevention of Cervical Cancer, recommending Pap smear
screening for women between the ages of 30 and 49 every 3 years, starting at age 25 if possible,
as recommended by the World Health Organization and U.S. Preventive Services Task Force.
911

However, for various reasons, many women in developing countries never get tested.
12
In Latin
America, many programmes have not been effectively or adequately implemented,
1215
and
screening is infrequent.
16
Various estimates indicate Pap smear coverage rates of 742.9% in
Peru or certain Peruvian cities,
13,1719
but data on nationwide coverage are scarce.
Low coverage results from several factors, including limited facilities and few personnel for
screening and follow up, unaffordable treatment options and women's inadequate preventive
health seeking behaviours.
8
Many Peruvian women do not seek reproductive health services even
when experiencing abnormal symptoms.
2023

Information about women in Peru who do not get screened is limited. In developed countries,
such women tend to be older and single, have less education, fewer children and lower income
levels than those who do get screening.
7,24
Additionally, they tend to have had less previous
contact and experience with the health care system, lack regular health providers and have little
knowledge about screening, but feel anxious or fearful about it.
2325

This study seeks to: (i) determine Pap smear coverage among young women (1829 years) in 20
of the largest cities of Peru and (ii) examine the socio-economic and demographic determinants
associated with having received Pap smears in those 20 cities.
Go to:
Study design
Data for this analysis comes from the PREVEN study, an urban community randomized trial
aimed at controlling gonorrhoea, chlamydial infection, trichomoniasis and syphilis through
improved syndromic management of STIs, and through screening of sex workers for these
curable infections. Outcomes were assessed through three household-based surveys of young
men and women 18 to 29 years of age, with a baseline survey in 2002 and subsequent surveys in
2005 and 2006. The 2006 survey provided the data for this current analysis. The study was
carried out in 20 of the largest cities in Peru (which has a total population of 29 million
26
)each
city with a population of more than 50 000.
Sampling
Within these 20 cities, sampling sets of approximately 80 houses were defined by the National
Statistics Office for other unrelated work. Since these predefined sets were larger than needed for
this study, they were split into clusters of 40 contiguous houses, randomly selected to provide
approximately 10 eligible households per cluster. Thus, a total of 108 neighbourhood clusters
were randomly selected per city and surveyed until a target sample size of 600 people per city
was achieved. All eligible households within the cluster were identified based on residents age
(1829 years) and residence status (lived in that city for at least the past 6 months). Eligible
households were selected to participate, for up to a maximum of 10 households per cluster. If
more than 10 households had eligible participants in that cluster, then 10 households were
randomly selected using a random number table. If more than one household member was
eligible, the member with the most recent birthday was selected. The participation rate for this
study was 92.8%. For the remaining 7.2%, either the household, or eligible household member,
refused to participate. Without more information on more participants, we can not determine
how they differed from those who did participate.
The total sample size for the PREVEN 2006 survey was 13 602 men and women. Of the 7106
women who participated in the study, 6712 had complete data for all relevant questions and are
included in this analysis. Remaining participants skipped some questions, especially in the self-
administered portion of the survey. Those dropped for missing data were mostly similar for
demographic and behavioural variables with those that remained, except that those who dropped
were less likely to have had sex (23.1% vs. 18.5%, P < 0.001).
Consent process and survey instruments
All consent processes and subsequent interviews were conducted in Spanish, although research
assistants who spoke other languages (based on location) were hired where needed to assist.
After giving written consent, participants provided demographic information in face-to-face
interviews, then used a palm pilot for a self-administered questionnaire, focusing on reproductive
health and sexual behaviours. In the self-administered survey, women responded to questions
regarding age of sexual debut, lifetime number of sexual partners, symptoms of different STIs,
having ever had a Pap smear, having ever had an abnormal Pap smear and the advice given by
their doctor if the smear had been abnormal.
Ethical approval
The PREVEN study obtained IRB approval for the first round from the Universidad Peruana
Cayetano Heredia, the University of Washington in Seattle and the United States Navy Medical
Research Center Detachment in Lima (NMRCD). This IRB approval has been renewed every
year since. IRB approval was also obtained from Tulane University School of Public Health and
Tropical Medicine and Vanderbilt University for use of these data.
Data analysis
Using STATA 8.0 software, means and frequencies for variables of interest were estimated, and
Chi-square and t-tests were used to compare the distribution of variables between those who had
had Paps and those who had not. Odds ratios were estimated to examine unadjusted associations
between independent variables and the dependent variable of interest (having had a Pap smear)
and the P-value for the Chi-square test for trend was estimated using StatCalc for some variables.
The adjusted associations between the various social, economic and demographic variables, and
having had a Pap smear, were estimated using logistic regression. It was also hypothesized that
certain community level factors were associated with women's Pap smear seeking behaviours.
Hence, the 20 cities were grouped into the three main geographic regions of Peru (coast,
highlands, rainforest) and the coastal cities were used as a reference group. Odds ratios and 95%
CIs were reported for unadjusted and adjusted associations estimated through these models.
Finally, multicollinearity in the models were assessed by analysing correlations of the parameters
and coefficients with one another, as well as by computing the variance inflation factor.
Go to:
Results
Pap smear coverage for this sample of women was 30.9%. Of women who reported having had a
Pap smear, 2.2% reported being told they had had an abnormal Pap, 3% did not remember or
know what they were told and the rest reported being told their Pap smears were normal.
Mean age for women in the sample was 23.2 years (Table 1). About half had completed high
school; over 40% had gone on to some type of post-secondary schooling; 53.7% were single;
43.8% were married or cohabiting; a very small percentage were separated, divorced or widowed
(2.5%); 16% also spoke an indigenous language (predominantly Quechua or Aymara). About
half had had at least one child. Most (66%) had lived their whole lives in the city where the
interview took place. Economically, 42.2% were unemployed, 32.9% were students and a quarter
worked. About two-thirds obtained most income from themselves or their parents, while about
one-third depended on their partners. Overall, 81.6% reported having experienced sex, with a
mean age of first sex of 18.2 years and a median age of 18 years.

Table 1
Description of study sample (n = 6712)
By unadjusted analyses, women who did and did not report having had Pap smears differed for
all of the demographic characteristics, as well as for selected sexual behaviours and risks (Tables
1 and and2).2). Women who had had a Pap smear were much more likely than those who had not
been married or cohabiting (76.5 vs 29%), and to have had children (88 vs 32.8%). Among
women over age 25, 53.5% had had a Pap smear, compared with 16.8% of those ages 1824.
Among sexually experienced women, 37.8% had had a Pap smear, including 22.7% of those 18
to 24 years of age vs. 56.8% of those 25 to 29 years of age; only 0.5% of those who denied
sexual experience reported having had a Pap smear. Moreover, women who had lived in the
same city all their lives were less likely than others to have had a Pap smear. Of those who have
had sex, 37.8% have had a Pap smear (compared with 0.5% who have had a Pap but not had
sex). Those who had had Pap smears had a slightly younger age at first sex (17.7- vs 18.5-years-
old), and reported more STI symptoms than women who had never had a Pap smear.
Surprisingly, in the unadjusted analyses, those with higher education were less likely to have had
Pap smears than those with less education, and those who were studying or working (vs the
unemployed) were also less likely to have had a Pap smear. However, after adjusting for other
variables, including employment status, the direction of the association for education was
reversed.

Table 2
Socio-demographic determinants of having had a Pap smear, reporting unadjusted and adjusted
odds ratio and 95% CI (n = 6712)
In multivariate analyses, the most significant determinant (other than sexual experience) of
having had a Pap for women ages 18 to 29 in these cities was parity (see Table 2). Compared
with women with no children, women with one child were 3.7 times more likely to have had a
Pap smear (P < 0.001) and women with two or more children were 4.7 times more likely to have
had a Pap (P < 0.001). Age and education remained important determinants of coverage: women
in the oldest age group (2529 years), as well as women in the middle age group (2124 years),
were more likely to have had a Pap than the youngest women (1820 years) (25- to 29-year-olds:
OR = 5.5, P < 0.001; 21- to 24-year-olds: OR = 2.3, P < 0.001); Chi-square test for trend, P <
0.001, and those with at least some secondary education were more likely to have had a Pap
smear than women with only primary education (OR = 1.4, P = 0.001). Women's employment
status or monthly family income did not remain significantly associated with having had a Pap
smear after adjusting for other variables.
Those sexually active at a younger age (17 years or less, and 18- to 20-year-olds) were more
likely to have had a Pap smear than women whose first sexual intercourse occurred when older
than 21 (17 years or less: OR = 2.2, P < 0.001; 1820: OR = 1.9, P < 0.001). Women who had
experienced an abnormal vaginal discharge in the past year were also more likely to have had
Pap smears than women who had not (OR = 1.2, P = 0.002). However, no significant
associations of having had a Pap smear were found with having experienced genital ulcers in the
past year or having ever had genital warts.
Regional variations were also observed. Women interviewed in the highlands (OR = 0.8, P =
0.001) and rainforest (OR = 0.8, P = 0.037) were less likely to have had Pap smears than women
from the coast.
Go to:
Discussion
Pap smear coverage in this study, 30.9%, was higher than expected based on other available
numbers for Peru's general population.
13,1719
However, this study took place in 20 of the largest
cities of Peru, where coverage would be expected to be higher than smaller cities or rural areas
due to accessibility. Additionally, urban people tend to be more educated and affluent than rural
dwellers, and these factors have been associated with seeking Pap smears in other settings.
7,13,24

Despite higher coverage than expected, the coverage also indicates that most women in these age
groups are in fact not getting screened.
The most significant predictors of having received a Pap smear were demographic: number of
children, education and age. Because many providers do Pap smears during antenatal pelvic
exams, more children equals more opportunities to have been offered a Pap smear, and perhaps
more opportunities to learn about them. The association between more education and having had
a Pap has also previously been reported.
7,24

Though Pap smear costs have been identified as a barrier for women in Latin America,
3,27
and a
separate study in Peru found an association between higher income and health service
utilization,
28
we found no association between family income, nor a woman's current
employment status and having had a Pap smear. Data on family income may not represent the
best measure of readily available resources to pay for a test, and it may be that the low cost of the
Pap smear at public facilities in Peru was within budgetary limits to most women despite income.
Though we did not specifically ask women about their perceived risk for cervical cancer or
exposure to human papilloma virus (HPV), the general lack of association we found between Pap
seeking behaviour and STI risk or symptoms is consistent with some reports from low-resource
settings that describe a lack of understanding about prevention in some populations: one goes to
a health centre when one feels ill.
24,29
In addition, some have found that many women from Latin
America or other resource settings undergoing Pap smear do not know what the exam was for,
nor have much knowledge about cervical cancer and what causes it.
3,29
To what extent the
relatively low coverage of Pap smearsespecially for those ages 25 to 29reflects health care
seeking, or low provision of Pap smears by clinicians for those who do obtain health care,
remains undetermined.
Interestingly, regional effects on Pap smear utilization were observed. Though the observed
difference may be due to less geographic barriers (lack of mountains, road quality during rainy
seasons) along the coast than in the mountains or rainforest, this study took place in urban areas,
where accessibility would be somewhat similar from region to region. Centralization both of
population (one-third of the population lives in the capital city of Lima on the coast) and of
resources are one possible explanation. Despite the Peruvian government's development and
implementation of strategies to prevent cervical cancer, outside Lima, resources for treating
abnormal lesions are limited: few hospitals outside of Lima can perform cone biopsies or
colposcopies. The large reference hospital in Lima, the Instituto Nacional de Enfermedades
Neoplsicas, is well equipped and has well-trained doctors, so many women with abnormal Paps
are referred there for treatment. However, costs associated with travel to and treatment in Lima,
and the associated loss of income from work, are too high for most women.
27
A survey
conducted in the rainforest region of San Martn found that only 23% of women with abnormal
Pap smears actually received any follow up treatment.
30
Thus, motivation to seek screening to
detect pre-cancerous lesions may be outweighed by the knowledge or belief that treatment of a
pre-cancerous lesion would not be available or affordable; this may be determined by where one
lives, and access to a facility that can offer appropriate follow up or treatment if necessary. A
successful cervical cancer screening programme must link screening, follow up procedures, and
services to manage women with abnormal Pap smears.
1,13,14,31,32

Further research can determine to what extent lower Pap smear coverage in highlands and
rainforest cities, where indigenous people are more concentrated, reflect cultural differences (i.e.
modesty about one's body, anxiety towards male providers; less exposure to Western models of
care) and/or structural barriers (i.e. types and quality of services within the cities, availability of
appropriate labs or trained personnel). However, we did find a negative association between
speaking an indigenous language and having had Pap smears. Perhaps, because women in our
sample were surveyed in Peru's largest cities, they had become relatively acculturated to city life
and the type of medical care available, and the regional differences observed have explanations
other than cultural factors. Regardless, in this resource limited country, efforts to improve
coverage of Pap smear screening should focus on the Andean region, where coverage is currently
lowest, as well as on rainforest.
The main limitation of this analysis is that, due to the design and objectives of the study from
which data were used, the women sampled were 29 years of age or younger and many might get
Pap smears in the future, so Pap smear coverage should rise as women age, have children, learn
more about Pap smears and/or have providers who recommend a Pap smear. Although Peru and
WHO recommend Pap smears at age 25 if resources are available, only 53% of those 25- to 29-
years old had received a Pap smear and this percentage decreased among those in the highlands
and rainforest, those with only elementary education and especially among women without
children (both when examining these numbers for all women and for all sexually experienced
women), indicating the need for outreach to such women.
Recall bias is possible: some women may have forgotten about their screening if it was part of a
routine obstetrics/gynaecological examination. Conversely, some women screened for STIs or
who have had vaginal examinations might think they have had a Pap when they have not.
Newly available HPV vaccines could greatly decrease incidence of cervical cancer over time and
raises new issues in a country like Peru regarding efforts to increase cervical cancer screening.
Cervical cancer screening through Pap smears would remain essential to comprehensive cervical
cancer approaches because it allows for early detection and treatment of cases in women who
have not received the vaccine, in those already infected with oncogenic HPV types before
receiving an HPV vaccine, and in those infected with oncogenic HPV types not included in
existing HPV vaccines. Although the cost-effectiveness of Pap smears will decrease as cervical
cancer incidence decreases due to HPV vaccine program implementation, this decrease is not
expected for at least a decade after HPV vaccine introduction, and possibly not for 30 years.
34

Additionally, though the vaccine is available and there are indications of interest among women
in Peru,
33
it is for now unaffordable for most Peruvians. Finally, as the vaccine becomes
accessible to more women, it will be essential to monitor its impact on cervical cancer incidence
and mortality through screening. This monitoring will also provide the data needed to apply new
models to determine the most cost-effective guidelines for Pap smear frequency in the coming
era of HPV vaccines. In sum, HPV vaccine availability does not diminish the importance of
improving Pap smear coverage in Peru: HPV vaccines and cervical cancer screening are both key
to preventing cervical cancer.
34

In Peru, cervical cancer incidence is one of the highest in the Americas.
3
Increased cervical
screening has tremendously impacted morbidity and mortality of women in other regions, and
would be expected to influence morbidity and mortality of women in Peru as well. Our study of
women 1829 years of age reveals that the main predictors of getting screened are having had
children and age, likely indicating that women are receiving Pap smears as part of their antenatal
care. Efforts to increase Pap smear coverage among other Peruvian women should include its
promotion during other types of health visits, such as those for family planning, and encouraging
preventive health seeking behaviours among women in general. Finally, more research to
determine causes of significant regional variations in coverage will help us determine ways to
improve Pap smear coverage in undercovered regions, such as the Andes highlands and
rainforest.
Go to:
Acknowledgements
We would like to thank the field team, as well as the women who participated in this study. The
data analysed was from the PREVEN study, a research project supported in part by the
Wellcome Trust Foundation (059131/Z/99/Z) and the University of Washington Center for AIDS
Research (CFAR), a National Institutes of Health funded program (P30 AI27757).
Conflict of interest: None declared
KEY MESSAGES
Pap smear coverage among 18- to 29-year-olds in urban Peru is only 30.9%, and is
associated with having had sex, having children, higher education, increasing age and
being from the coast as opposed to the highlands or rainforest.
Increased Pap smear coverage in Peru requires promotion during different types of
women's health visits, and targeted at young women with no children and low education
levels.
Regional variations in coverage suggest the need to examine differences in infrastructure
and resources for follow up and treatment that influence whether or not women go for
and receive screening.
Go to:
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Prevention Issues in Depth, No. 4.
25. Coughlin SS, Uhler RJ, Hall HI, Briss PA. Non-adherence to breast and cervical cancer
screening: what are the linkages to chronic disease risk? Preventing Chronic Disease. [Accessed
June 11, 2008];serial online. 2004 Jan;1 Available online at:
http://www.cdc.gov/pcd/issues/2004/jan/03_0015.htm.
26. US Census Bureau. International data base summary demographic data for Peru. [Accessed
June 11, 2008]; Available at: http://www.census.gov/cgi-bin/ipc/idbsum?cty=PE.
27. Hunter JL. Cervical cancer in Iquitos, Peru: local realities to guide prevention planning. Cad
Saude Publica. 2004;20:16071. [PubMed]
28. Valdivia M. Public health infrastructure and equity in the utilization of outpatient health care
services in Peru. Health Policy Plan. 2002;17(Suppl):1219. [PubMed]
29. Bingham A, Bishop A, Coffey P, et al. Factors affecting utilization of cervical cancer
prevention services in low-resource settings. Salud Publica Mex. 2003;45:S40816. [PubMed]
30. Shaw T. Peru tries vinegar against cervical cancer. News Sect Bull World Health Organ.
2003;81:7374.
31. Bradley J, Barone M, Mahe C, Lewis R, Luciani S. Delivering cervical cancer prevention
services in low-resource settings. Int J Gynaecol Obstetr. 2005;89(Suppl 2):S2129.
32. Goldhaber-Fiebert JD, Denny LE, De Souza M, Wright TC, Jr, Kuhn L, Goldie SJ. The costs
of reducing loss to follow-up in South African cervical cancer screening. Cost Eff Resour Alloc.
2005;3 Available online at: http://www.resource-allocation.com/content/pdf/1478-7547-3-11.pdf
(Accessed June 11, 2008)
33. Lee F, Paz Soldan V, Carcamo C, Vermund SH, Ferris DG, Garcia PJ. Knowledge and
attitudes of Peruvian women vis--vis Human Papillomavirus (HPV), cervical cancer, and the
HPV vaccine. Unpublished manuscript currently being reviewed.
34. World Health Organization. Preparing for the Introduction of HPV Vaccines: Policy and
Programme Guidance for Countries. Geneva, Switzerland: World Health Organization and
United Nations Population Fund; 2006.

Articles from International Journal of Epidemiology are provided here courtesy of Oxford University Press
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Related citations in PubMed
Low knowledge of cervical cancer and cervical pap smears among women in Peru, and
their ideas of how this could be improved. [Int Q Community Health Educ. 2010]
[Attendance rate in the Polish Cervical Cancer Screening Program in the years 2007-
2009]. [Ginekol Pol. 2010]
Adolescent and young adult women's misunderstanding of the term Pap smear. [Arch
Pediatr Adolesc Med. 2004]
Abnormal Pap test results and the rurality factor. [Aust J Rural Health. 2003]
Paying for prevention standardizing the measurement of the value of health care
interventions. [Obstet Gynecol Clin North Am. 2002]
See reviews... See all...
Cited by other articles in PMC
HBV Infection in Relation to Consistent Condom Use: A Population-Based Study in Peru
[PLoS ONE. ]
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v.7; 2010 >
PMC2926920

Cytojournal. 2010; 7: 16.
Published online 2010 August 5. doi: 10.4103/1742-6413.67112
PMCID: PMC2926920
Colposcopic evaluation of cervix with
persistent inflammatory Pap smear: A
prospective analytical study
Papa Dasari,
*
S Rajathi, and Surendra V Kumar
1

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Abstract
Background:
Inflammatory Pap smear is the most common report received by a gynecologist. The cervical
screening algorithm for benign cellular changes on the Pap smear recommends treatment of
infection if indicated and a repeat Pap smear in 4 to 6 months time. If the inflammatory changes
still persist, subject the patient to colposcopy. However, in practice, this is not followed,
especially in developing countries like ours where proper screening protocols are not available.
Hence, a good number of patients in the premalignant stage are being missed. This study was
undertaken to evaluate patients with persistent inflammatory Pap smears without atypia using
colposcopy.
Methods:
A prospective analytical study of 150 gynecologial patients with persistent inflammatory Pap
smear between 2006 and 2008 in an out-patient setting. All of them were subjected to
colposcopy and biopsy from the abnormal areas. The incidence of cervical intraepithelial
neoplasia (CIN)/invasive carcinoma was calculated by proportions/percentages.
Results:
The incidence of invasive carcinoma was <1%. But, the incidence of pre-malignant lesions
(CIN) was high (20.9%). CIN 2/3 and carcinoma in situ were present in 6.9% of the cases.
Conclusions:
Patients with persistent inflammatory Pap smears can harbour a high proportion of CIN and
hence these patients will need further evaluation.
Keywords: Invasive carcinoma, non-specific inflammation, persistent inflammatory cellular
changes, squamous intraepithelial lesion
INTRODUCTION
Chronic inflammation, either specific or non-specific, has been shown to be associated with
malignancy and was thought to be one of the factors responsible for carcinogenesis. Persistent
inflammation leads to increased cellular turnover, especially in the epithelium, and provides a
selection pressure that results in the emergence of cells that are at a high risk for malignant
transformation[1] Inflammatory Pap smear is the most common report the gynecologist receives
even when the cervix appears normal. The original Papanicolau classification of class 2 smears
denotes inflammation and the recommendation is to repeat the smear after treating the
infection[2] However, this does not specify the type of infection, and the present reporting of Pap
smear by the Bethesda system reports on specific infections and classifies it under benign
cellular changes.[3] The cervical screening algorithm for benign cellular changes recommends
treatment of infection if indicated and performing a repeat Pap smear in 4 to 6 months time and,
if the inflammatory changes persist, to subject the patient to colposcopy.[4] In practice, however,
this is not always followed, especially in developing countries. The significance of cervical
cytology with atypia has been extensively studied. There is a great controversy regarding the
optimal management of women with persistent inflammatory changes without atypia, some
considering it less likely to be associated with dysplasia[5] and others recommending further
evaluation as it is associated with a high incidence of cervical intraepithelial neoplasia
(CIN).[6,7] Hence, we have undertaken this study with the following objectives: (1) to study the
colposcopic features in the cervices of persistent inflammatory cellular changes on Pap smear (2)
to study epithelial cell abnormalities by colposcopic biopsy of abnormal areas in such cases and
(3) to determine the existence of significant cervical intraepithelial lesions or invasive carcinoma
in patients with persistent inflammatory Pap smear.
MATERIALS AND METHODS
This is a prospective analytical study conducted in the Department of Obstetrics and Gynecology
between August 2006 and June 2008. One hundred and fifty women who showed persistent
inflammatory changes on Pap smear were included in the study. Patients with persistent
inflammatory changes with atypical or dysplastic cells, patients with Diabetes mellitus, pregnant
women and patients with previous cervical surgery were e



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v.7; 2010 >
PMC2926920

Cytojournal. 2010; 7: 16.
Published online 2010 August 5. doi: 10.4103/1742-6413.67112
PMCID: PMC2926920
Colposcopic evaluation of cervix with
persistent inflammatory Pap smear: A
prospective analytical study
Papa Dasari,
*
S Rajathi, and Surendra V Kumar
1

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background:
Inflammatory Pap smear is the most common report received by a gynecologist. The cervical
screening algorithm for benign cellular changes on the Pap smear recommends treatment of
infection if indicated and a repeat Pap smear in 4 to 6 months time. If the inflammatory changes
still persist, subject the patient to colposcopy. However, in practice, this is not followed,
especially in developing countries like ours where proper screening protocols are not available.
Hence, a good number of patients in the premalignant stage are being missed. This study was
undertaken to evaluate patients with persistent inflammatory Pap smears without atypia using
colposcopy.
Methods:
A prospective analytical study of 150 gynecologial patients with persistent inflammatory Pap
smear between 2006 and 2008 in an out-patient setting. All of them were subjected to
colposcopy and biopsy from the abnormal areas. The incidence of cervical intraepithelial
neoplasia (CIN)/invasive carcinoma was calculated by proportions/percentages.
Results:
The incidence of invasive carcinoma was <1%. But, the incidence of pre-malignant lesions
(CIN) was high (20.9%). CIN 2/3 and carcinoma in situ were present in 6.9% of the cases.
Conclusions:
Patients with persistent inflammatory Pap smears can harbour a high proportion of CIN and
hence these patients will need further evaluation.
Keywords: Invasive carcinoma, non-specific inflammation, persistent inflammatory cellular
changes, squamous intraepithelial lesion
Go to:
INTRODUCTION
Chronic inflammation, either specific or non-specific, has been shown to be associated with
malignancy and was thought to be one of the factors responsible for carcinogenesis. Persistent
inflammation leads to increased cellular turnover, especially in the epithelium, and provides a
selection pressure that results in the emergence of cells that are at a high risk for malignant
transformation[1] Inflammatory Pap smear is the most common report the gynecologist receives
even when the cervix appears normal. The original Papanicolau classification of class 2 smears
denotes inflammation and the recommendation is to repeat the smear after treating the
infection[2] However, this does not specify the type of infection, and the present reporting of Pap
smear by the Bethesda system reports on specific infections and classifies it under benign
cellular changes.[3] The cervical screening algorithm for benign cellular changes recommends
treatment of infection if indicated and performing a repeat Pap smear in 4 to 6 months time and,
if the inflammatory changes persist, to subject the patient to colposcopy.[4] In practice, however,
this is not always followed, especially in developing countries. The significance of cervical
cytology with atypia has been extensively studied. There is a great controversy regarding the
optimal management of women with persistent inflammatory changes without atypia, some
considering it less likely to be associated with dysplasia[5] and others recommending further
evaluation as it is associated with a high incidence of cervical intraepithelial neoplasia
(CIN).[6,7] Hence, we have undertaken this study with the following objectives: (1) to study the
colposcopic features in the cervices of persistent inflammatory cellular changes on Pap smear (2)
to study epithelial cell abnormalities by colposcopic biopsy of abnormal areas in such cases and
(3) to determine the existence of significant cervical intraepithelial lesions or invasive carcinoma
in patients with persistent inflammatory Pap smear.
Go to:
MATERIALS AND METHODS
This is a prospective analytical study conducted in the Department of Obstetrics and Gynecology
between August 2006 and June 2008. One hundred and fifty women who showed persistent
inflammatory changes on Pap smear were included in the study. Patients with persistent
inflammatory changes with atypical or dysplastic cells, patients with Diabetes mellitus, pregnant
women and patients with previous cervical surgery were excluded. The study was approved by
the Institute Scientific and Ethical Committee.
Patients with a report of inflammatory Pap smear were selected at random for initial recruitment.
These patients were advised to use Clotimazole or Betadine vaginal pessaries for a minimum of
6 days. Those with a clinical diagnosis of chronic pelvic inflammatory disease and showing
inflammatory Pap smear were given Doxycycline and Metronidazole for a minimum period of
14 days along with vaginal pessaries. A repeat Pap smear was performed after a period of 2
weeks with Ayer's wooden spatula. No preparation of the cervix was undertaken at the time of
sampling and women were not menstruating or using any vaginal douche or vaginal
contraceptives at the time of sampling. If inflammatory cellular changes were reported again on
the repeat Pap smear, these patients were subjected to colposcopic examination after taking
informed consent.
The woman was kept in a dorsal position and the cervix was exposed by inserting a Cusco's
speculum. Excess mucus was wiped off with a cotton swab soaked in saline. Five percent acetic
acid was applied to the cervix and it was visualized using a binocular colposcope (OLYMPUS
OSC 3FLA, M/s Olympus Optical Co. Ltd., Tokyo, Japan) under 40X magnification. Biopsies
were taken from the abnormal areas (acetowhite areas and vascular abnormalities like fine
punctuations, coarse punctuations, mosaic and areas showing atypical vasculature) and an
endocervical curettage was performed. All the specimens were subjected to histopathological
examination. The incidence of pre-malignant and malignant lesions was calculated as
percentages.
Go to:
RESULTS
The clinical profile of the patients is shown in Table 1. The mean age was 37 years and the mean
parity was 2.6. The most common symptom was vaginal discharge followed by pelvic pain and
in 45% of the patients the clinical diagnosis was pelvic inflammatory disease. Abnormal uterine
bleeding and erosion of the cervix also contributed to inflammatory smear in approximately 20%
of the patients. The colopscopic features of patients with persistent inflammatory Pap smears are
shown in Table 2. The most common feature was acetowhiteness (41.3%) followed by a
combination of acetowhiteness and vascular abnormality (24.7%). Colposcopy was normal in
nine patients and hence no biopsy was taken. Erosion was confirmed by colposcopy in 12% of
the patients. Biopsy was also not performed when the margins of erosion were regular and these
accounted for five cases. The correlation of inflammatory Pap smear with coloposcopic biopsy
results is shown in Table 3. The most common biopsy result in patients with inflammatory Pap
smear was chronic cervicitis (28.7%). Human papilloma virus (HPV) lesions accounted for
21.2% CIN 1 for 14.7% and CIN 2/3 for 4.4% of the cases. The two cases of carcinoma in situ
and one case of invasive carcinoma also showed non-specific inflammation on Pap test. Ten
percent (14/150) did not require biopsy.

Table 1
Clinical profile

Table 2
Colposcopic features of patients with inflammatory Pap smear

Table 3
Correlation of inflammatory Pap smear with colposcopic biopsy
The correlation between clinical symptomatology and colposcopic features is shown in Table 4.
The most common colposcopic feature is acetowhiteness followed by a combination of
acetowhite areas and vascular abnormality, irrespective of the symptoms. Of the patients who
presented with pelvic pain, 46% showed acetowhite areas and 24% showed a combination of
acetowhite areas and vascular abnormality. This is slightly higher than the patients presenting
with vaginal discharge per vaginum who showed acetowhite areas in 34% of the cases and a
combination of acetowhite areas and vascular abnormality in 28% of the cases. Erosion was
more common in patients with vaginal discharge than in those with pelvic pain.

Table 4
Correlation of clinical symptoms and colposcopic findings
Table 5 shows the results of colposcopic biopsy in correlation with symptomatology. The patient
with invasive carcinoma presented with pelvic pain and two patients with carcinoma in situ
presented with post-coital bleeding. In patients who presented with vaginal discharge, the most
common diagnosis was chronic cervicitis followed by HPV lesions in 17% and CIN 1 in another
17% of the cases. Patients with abnormal uterine bleeding also showed a significantly increased
incidence of CIN (22.2%).

Table 5
Clinical symptoms and colposcopic biopsy results
Of the benign lesions, chronic cervicitis and HPV changes were common. Acanthosis,
koilocytosis, chronic cervicitis with koilocytosis, squamous metaplasia with koilocytosis,
acanthosis with koilocytosis and koilocytic atypia were grouped under HPV changes. The
incidence of invasive carcinoma was <1%. But, the incidence of pre-malignant lesions was high
(20.9%). CIN 2/3 and carcinoma in situ together contributed to 6.9% of the cases.
Go to:
DISCUSSION
Cervical cancer screening was proved to be an important part of preventive health care of
women. Attempts are being made to improve the efficacy of the screening programme to
decrease the morbidity and mortality due to cervical cancer. The cervical screening algorithm for
benign cellular changes on Pap smear recommends treatment of infection if indicated and a
repeat Pap smear in 4 6 months time, and, if the inflammatory changes still persist, to subject
the patient to colposcopy. However, in practice, this is not followed, especially in developing
countries like ours, where proper screening protocols are not available/followed. Hence, a good
number of patients in the pre-malignant stage are being missed. Most Obstetrician Gynecologists
do not review the Pap smear result with the cytologists and 41% do nothing when inflammatory
Pap smear is reported. Only 11% treat the infection and repeat Pap smear and 24% treat infection
and do not repeat Pap smear.[8]
There are very few studies in the literature where the incidence of premalignant and malignant
lesions was looked into in cases of inflammatory Pap smear. Inflammation can obscure few
malignant cells and may result in high false negative rates and the same may be reduced by
employing liquid based cytology.[8] However, it was reported that liquid based cytology was not
cost-effective for developing countries and the recent studies did not report a statistically
significant difference of accuracy between conventional Pap test and liquid based cytology.[9]
The main reason for false-negative reports of cytology were found to be sampling errors, with
sampling errors as high as 42.5% being suboptimal and 17.5% being inadequate for
interpretation.[10] Mc Lachlan and colleagues studied the colposcopic features and biopsy
results of 102 women with persistent inflammatory Pap smears and found 19% cases of CIN 2 or
worse.[11] This is almost similar to the present study.
The mean age and parity in the present study was higher (37 years and 2.6) than that of Seckin
and colleagues, where the mean age was 30.2 years and the parity was 1.7. The most common
persistent inflammatory Pap smear subjected to colposcopy was presumed to be non-specific in
the study of Seckin and collegues, as they did not specify on the type of inflammatory smear.[6]
In the present study, 92% were non-specific inflammation and only 8% were specific
inflammation due to Trichomonas vaginalis, Candida albicans and bacterial vaginosis. Wilson
and colleagues included bacteriological cultures of cervicovaginal smears to diagnose specific
infections and found an increased incidence of sexually transmitted infections in patients <25
years of age and in many showing abnormal colposcopic features in this age group7. Colposcopy
was normal in 9.3% of the patients in the present study, which was much lower than that of
Seckin and collegues, who reported 29.1% to be normal. A very high percentage (62.5%) of
normal colposcopic findings was reported by Wilson and colleagues in 96 patients of
inflammatory Pap smears. This is in contrast with the results of the present study.
Colposcopic biopsy showed benign lesions in 48.2% of the cases in the study done by Seckin
and collegues, which was lower than that reported in the present study. Seckin reported a very
high incidence of HPV-related lesions (64.5%) where as Frisch reported an incidence of only
8%.[12] HPV related lesions constituted only 19.4% in the present study. The incidence of pre-
malignant lesions in the present study (20.9%) was closer to that of Frisch (23.5%) but much
higher than that of Seckin and colleagues (8% - 18 out of 224). There were no cases of
malignancy in the series of Seckin and Frisch but in the present study, one case was found.
Recently, Hammes and colleagues evaluated the population of macrophages during the cervical
malignant transformation and its influence on CIN in cervical biopsy specimens. They concluded
that macrophage count and inflammation increased linearly with disease progression.
Inflammation was present in 25%, 46.1%, 58.4% and 89.3% of normal, Low grade squamous
intraepithelial lesion (LGSIL), (High grade squamous intraepithelial lesion) HGSIL and
squamous cell carcinoma, respectively.[13]
Seckin recommends colposcopic evaluation of patients with persistent inflammatory Pap smear
despite therapy in any population in any part of the World. Frisch is of the opinion that
colposcopy of women with cytologic diagnosis of inflammatory epithelial changes may be a
useful way to detect otherwise unrecognized cases of CIN, and the present study highlights these
statements.
Go to:
CONCLUSIONS
Patients with persistent inflammatory Pap smears can harbour a high proportion of CIN and HPV
infection and hence these patients will need further evaluation by colposcopy.
Go to:
COMPETING INTEREST STATEMENT BY ALL
AUTHORS
No competing interest to declare by any of the authors.
Go to:
AUTHORSHIP STATEMENT BY ALL AUTHORS
Each author acknowledges that this final version was read and approved. All authors of this
article declare that we qualify for authorship as defined by ICMJE http://www.icmje.org/#author.
Each author has participated sufficiently in the work and take public responsibility for
appropriate portions of the content of this article.
Go to:
ETHICS STATEMENT BY ALL AUTHORS
This study was conducted with approval from Institutional Review Board (IRB) (or its
equivalent) of all the institutions associated with this study. Authors take responsibility to
maintain relevant documentation in this respect.
Go to:
EDITORIAL / PEER-REVIEW STATEMENT
To ensure integrity and highest quality of CytoJournal publications, the review process of this
manuscript was conducted under a double blind model(authors are blinded for reviewers and
reviewers are blinded for authors) through automatic online system.
Go to:
Footnotes
Available FREE in open access from: http://www.cytojournal.com/text.asp?2010/7/1/16/67112
Go to:
REFERENCES
1. Moss SF, Blaser MJ. Mechanisms of Disease: Inflammation and origins of cancer. Nat Clin
Pract Oncol. 2005;2:907.
2. Kiviat NB, Paavonen JA, Brockway J, Critchlow CW, Brunham RC, Stevens CE, Cytologic
manifestations of cervical and vaginal infections. I. Epithelial and Inflammatory changes.
JAMA. 1985;253:98996. [PubMed]
3. Atikson KM. benign cellular changes. In: Bonfigilo T, Erogen YS, editors. Gynaecologic
Cytopathology. Philadelphia: Lppincot Raven Publishers; 1997. pp. 3342.
4. ACOG Practice Bulletin. clinical management guidelines for Obstetrician and Gynecologist
Cervical Cytology screening Obstet Gynecol. 2003;102:41727.
5. Swinker M, Cutlip AC, Ogle D. A comparison of uterine cervical cytology and biopsy results:
Indications and outcome of Colposcopy. J Fam Pract. 1994;38:404.
6. Seckin NC, Turban NO, Ozmen S, Ersan F, Avsar F, Ustin H. Routine evaluation of patients
with persistent inflammatory cellular changes on Pap smear. Int J Gynaecol Obstet. 1997;59:25
9. [PubMed]
7. Wilson JD, Robinson AJ, Kinghorn SA, Hicks DA. Implications of inflammatory changes on
cervical cytology. BMJ. 1990;300:63840.
8. Marchand L, Van Dinter M, Mundt M, Dingel W, Klein G. Current cervical cancer screening
practices of Dane Country, Wsconsin Primary care clinicians. WMJ. 2003;102:3540.
9. ACOG Committee on Practice Bulletins--Gynecology. ACOG Practice Bulletin no. 109:
Cervical cytology screening. Obstet Gynecol. 2009;114:140920. [PubMed]
10. Vassilakos P. Management of Suboptimal Cytologic smears: Persistent inflammatory smears.
Acta Cytol. 1998;42:1481. [PubMed]
11. McLachalan N, Patwardhan JR, Ayer B, Pacey NF. Management of suboptimal cytologic
smears: Persistent inflammatory smears. Acta Cytol. 1994;38:5316.
12. Frisch LE, Parmar H, Buckley LD, Chalem SA. Colposcopy of patients with Cytologic
Inflammatory epithelial changes. Acta Cytol. 1990;34:1335.
13. Hammes LS, Tekamal RR, Naidu P, Edelweiss MI, Kirma N, Valentene PT, et al.
Macrophages, inflammation and risk of cervical intraepithelial neoplaia (CIN) progression -
Clinicopathological correlation. Gynecol Oncol. 2007;105:15765. [PubMed]

Articles from CytoJournal are provided here courtesy of Medknow Publications
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|
Full Text
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Related citations in PubMed
Routine colposcopic evaluation of patients with persistent inflammatory cellular changes
on Pap smear. [Int J Gynaecol Obstet. 1997]
Comparison of visual inspection of cervix and Pap smear for cervical cancer screening. [J
Coll Physicians Surg Pak. 2003]
Clinical evaluation of follow-up methods and results of atypical glandular cells of
undetermined significance (AGUS) detected on cervicovaginal Pap smears. [Gynecol
Oncol. 1999]
Cervical cytology and the evaluation of the abnormal Papanicolaou smear. [Prim Care.
1988]
Present standards for cervical cancer screening. [Curr Opin Oncol. 2002]
See reviews... See all...
Cited by other articles in PMC
Thank you CytoJournal reviewers and authors - 2008 through 2010 [CytoJournal. ]
See all...
Links
PubMed
Taxonomy
Taxonomy Tree
Recent activity
Clear Turn Off
Colposcopic evaluation of cervix with persistent inflammatory Pap smear: A prosp...
PMC
Who is getting Pap smears in urban Peru?
PMC
Inuit women's attitudes and experiences towards cervical cancer and prevention s...
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Self-reported history of Pap-smear in HIV-positive women in Northern Italy: a cr...
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See more...
Cytologic manifestations of cervical and vaginal infections. I. Epithelial and
inflammatory cellular changes. [JAMA. 1985]
Routine colposcopic evaluation of patients with persistent inflammatory cellular changes
on Pap smear. [Int J Gynaecol Obstet. 1997]
ACOG Practice Bulletin no. 109: Cervical cytology screening. [Obstet Gynecol. 2009]
Management of suboptimal cytologic smears: persistent inflammatory smears. [Acta
Cytol. 1998]
Routine colposcopic evaluation of patients with persistent inflammatory cellular changes
on Pap smear. [Int J Gynaecol Obstet. 1997]
Macrophages, inflammation and risk of cervical intraepithelial neoplasia (CIN)
progression--clinicopathological correlation. [Gynecol Oncol. 2007]
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BMC Cancer >
v.11; 2011 >
PMC3144456

BMC Cancer. 2011; 11: 257.
Published online 2011 June 17. doi: 10.1186/1471-2407-11-257
PMCID: PMC3144456
Sociodemographic gradients in breast and
cervical cancer screening in Korea: the
Korean National Cancer Screening Survey
(KNCSS) 2005-2009
Mi Jin Park,
1
Eun-Cheol Park,
2
Kui Son Choi,
1
Jae Kwan Jun,
1
and Hoo-Yeon Lee
1

Author information Article notes Copyright and License information
This article has been cited by other articles in PMC.
Go to:
Abstract
Background
Cancer screening rates in Korea for five cancer types have increased steadily since 2002. With
regard to the life-time cancer screening rates in 2009 according to cancer sites, the second
highest was breast cancer (78.1%) and the third highest was cervical cancer (76.1%). Despite
overall increases in the screening rate, disparities in breast and cervical cancer screening, based
on sociodemographic characteristics, still exist.
Methods
Data from 4,139 women aged 40 to74 years from the 2005 to 2009 Korea National Cancer
Screening Survey were used to analyze the relationship between sociodemographic
characteristics and receiving mammograms and Pap smears. The main outcome measures were
ever having had a mammogram and ever having had a Pap smear. Using these items of
information, we classified women into those who had had both types of screening, only one
screening type, and neither screening type. We used logistic regression to investigate
relationships between screening history and sociodemographic characteristics of the women.
Results
Being married, having a higher education, a rural residence, and private health insurance were
significantly associated with higher rates of breast and cervical cancer screening after adjusting
for age and sociodemographic factors. Household income was not significantly associated with
mammograms or Pap smears after adjusting for age and sociodemographic factors.
Conclusions
Disparities in breast and cervical cancer screening associated with low sociodemographic status
persist in Korea.
Go to:
Background
Cancer screening rates in Korea for five cancer types have increased steadily since 2002 [1].
Regarding the life-time cancer screening rates in 2009, according to cancer site, the second
highest was breast cancer (78.1%), and the third highest was cervical cancer (76.1%) [1]. A
comparison of the cancer screening rates in Korea with those in other countries showed that the
rates for breast (78.1%) and cervical cancer screening (76.1%) in Korea were lower than those in
Great Britain (93 and 91%, respectively) [1,2].
In 1999, Korea began organized screening as part of the National Cancer Screening Program
(NCSP), covering the entire population. NCSP invites women in Korea over the age of 40 years
for breast cancer screening every 2 years, and women over the age of 30 years for cervical cancer
screening every 2 years [1]. NCSP provides screening services free of charge for Medical Aid
enrollees and people with National Health Insurance (NHI) with a contribution below 50%.
Additionally, NCSP provides cancer screening to people with a contribution over 50% and has
subsidized 90% of the costs of these services. The insurance contribution is calculated based on
the individual's income level. In addition to the NCSP, cancer screening is conducted in
outpatient clinics and private health assessment centers for opportunistic screening. However,
individuals must pay for all procedure-related costs associated with such opportunistic screening
[1].
Various studies have identified sociodemographic and health system-related characteristics that
are barriers to or facilitators of breast and cervical cancer screening [3-10]. Well-established
barriers to screening include sociodemographic characteristics, such as lower income, lower
educational attainment, lack of appropriate health information, distance to services, fear of
cancer, lack of health care insurance, and factors related to the healthcare system, such as lack of
a recommendation for screening by a healthcare provider, poor coordination of services, poor
access to transport, and lack of a patient or provider reminder system . Data from the USA
indicated that the breast cancer screening rates of women in lower sociodemographic status were
low, and that their morbidity and death rates have not been reduced [11-15]. A similar pattern
emerges for cervical screening, with sociodemographic characteristics appearing to influence
cervical screening rates in France and the United Kingdom (UK) as well as in urban areas of
Australia [12,13,15-17].
Despite the overall increase in the screening rates, disparities in breast and cervical cancer
screening based on sociodemographic characteristics still exist [3-10,18]. The objective of this
study was to examine the relationships between sociodemographic characteristics and breast and
cervical cancer screening among women in Korea.
Go to:
Methods
Data sources
This study was performed using the Korean National Cancer Screening Survey (KNCSS) data
from 2005 to 2009. KNCSS is a continuous national interview survey, conducted by the Korean
National Cancer Center. KNCSS is conducted to investigate Korean participation rates in cancer
screening for five common cancers: gastric, liver, colorectal, breast, and cervical cancer. Men
and women were selected based on the Resident Registration Population data using a stratified,
multistage, and random sampling procedure according to geographic area, age, and gender. The
Resident Registration Population data are published annually by the Korea National Statistical
Office after data are gathered from residents of the registration population every December 31.
The publication provides data about changes in population size and structure and identifies
population changes by administrative district. For the present study, investigators from a
professional research agency conducted face-to-face interviews at the participants' homes. Study
recruitment involved door-to-door contact. We made at least three attempts to contact a resident
at each dwelling. Eligible participants were asked about their experiences of screening for five
common cancers; health behaviors, health status, family history of cancer, and socioeconomic
and demographic information. We included people from the age of 40 to 74 years in the KNCSS
because those older than 75 years have difficulty recalling and answering many questions (n =
4,139). All subjects provided informed consent for participation in the study. This study was
approved by the Institutional Review Board (IRB) of the National Cancer Center, Korea.
Measures
For this study, variables of interest included age (40-49, 50-59, and 60-74), marital status
(married or other (widowed, divorced, separated, or never married)), region of residence
(metropolitan, urban, or rural), and private health insurance member (yes or no).
Education and household income were used to determine socioeconomic status. Education was
classified into four categories: less than middle school (level 1), middle school graduate or some
high school (level 2), high school graduate or some college (level 3), and college graduate or
higher (level 4). Household income was categorized into four groups: < 1 million won per month
(level 1), 1-2.5 (level 2), 2.5-4 (level 3), and > 4 (level 4) million won per month (1000 won
US $0.84).
Those who did not attend were asked to choose one of eight reasons: had not heard about cancer
screening, did not feel it was necessary, lacked time, could not afford cancer screening, feared
the exam procedure, feared detecting cancer, had no faith in cancer screening, and no medical
facilities in the neighborhood.
The main outcome measures were having ever had a mammogram and having ever had a Pap
smear. Using these items of information, we classified women into those who had had both types
of screening (that is, at least one mammogram and at least one Pap smear), only one screening
type (a mammogram or a Pap smear, but not both), and neither screening type. We adopted this
approach because women who have had one type of screening are known to be more likely to
attend another screening program. We did not exclude women who had had a hysterectomy since
the most recent Pap smear.
We analyzed data using the SAS software (ver. 9.1 for Windows). We calculated differences in
breast and cervical cancer screening rates by age and sociodemographic factors. We used logistic
regression to investigate relationships between screening history and sociodemographic
characteristics of the women. We derived odds ratios (ORs) and 95% confidence intervals (CI)
for categorical values. We regarded a p-value less than 0.05 as indicating statistical significance.
We present both odds ratios adjusted for age only and fully adjusted odds ratios.
Go to:
Results
The response rates were 55.8-58.3% from 2005 to 2009 [18]. Of the participants, 55.8% reported
having ever had a mammogram, and 75.5% reported having ever had a Pap smear (Table
(Table1).1). Women with higher screening rates (having ever had a mammogram or Pap smear)
were more likely to be age 50 or older, married, have a household income level of 4, and have
private health insurance.

Table 1
Screening history by sociodemographic characteristics of respondents, 2005-2009
Table Table22 shows the odds ratio of receiving a mammogram or Pap smear, adjusted for age
and sociodemographic factors (marital status, region of residence, education, household income,
and private health insurance). Positive associations were found between education and both
mammogram and Pap smear screenings. For example, those with an education level of 4 were
more likely to have had screening procedures than were those with an education level of 1; after
adjustment for age, the odds ratios were 1.62 (95% CI = 1.24-2.13) for mammograms and 1.60
(95% CI = 1.17-2.20) for Pap smears. Those with a household income level of 4 were more
likely to have had screening procedures than were those with a household income level of 1;
after adjustment for age, the odds ratios were 1.54 (95% CI = 1.20-1.97) for mammograms and
1.91 (95% CI = 1.43-2.54) for Pap smears. After adjusting for age and sociodemographic factors,
private health insurance was the only significant predictor when we compared women who had
had mammograms with those who had not (p < 0.0001). Marital status (p < 0.0001) and private
health insurance (p < 0.0001) were significant predictors of having had a Pap smear versus
having had none.

Table 2
Odds ratios of screening history (ever had a mammogram, ever had a Pap smear) by
sociodemographic characteristics, 2005-2009
Being married, having a rural residence, having an education level of 4, and being a private
health insurance member were significant predictors of having had both a mammogram and Pap
smear, compared with having had only one or neither of these screenings, after adjustment for
age and sociodemographic factors. In particular, an education level of 4 had an odds ratio of 1.51
(95% CI = 1.10-2.08) compared with an education level of 1 in ever having had both a
mammogram and Pap smear versus having had only one or neither screening, after adjustment
for age and sociodemographic factors. Marital status (p = 0.003) and private health insurance (p
< 0.0001) were significant predictors of having had some screening compared with having had
none, after adjustment for age and sociodemographic factors. These results enable us to
investigate who was likely to participate in screening (Table (Table33).

Table 3
Odds ratios of screening history (ever had both screenings, ever had some screening) by
sociodemographic characteristics, 2005-2009
The three most common reasons women gave for not having had a mammogram or Pap smear
were, in all age groups: 1) they did not feel it was necessary, 2) they did not have enough time,
and 3) they could not afford it (Figure (Figure11).

Figure 1
Reasons for not having had a mammogram (a), and a Pap smear (b), women aged 40-74
years.
Go to:
Discussion
The findings of this study contribute to our understanding of the sociodemographic
characteristics associated with the use of breast and cervical cancer screening. Being married and
having a higher education level, rural residence, and private health insurance were significantly
associated with higher rates of breast and cervical cancer screening, after adjusting for age and
sociodemographic factors. Household income was not significantly associated with
mammograms or Pap smears.
Of the sociodemographic factors, household income was not shown to be significantly associated
with mammograms or Pap smears by multivariate logistic regression after full adjustment. Other
studies have suggested that household income affects mammogram and Pap smear participation,
with women from low-income households less likely to participate than those from high-income
households [2,5,19-21]. Inequalities in breast and cervical cancer screening still exist in the UK,
despite free screening for the entire population [2]. Many studies have suggested that having
access to a physician who performs mammograms and Pap smears was a powerful predictor of
breast and cervical cancer screening [2,5,21-26]. A possible cause of this difference in study
results is that in 1999, Korea began screening for cancer as part of the NCSP, which covers the
entire population. NCSP provides screening services free of charge for Medical Aid enrollees
and NHI participants with a contribution below 50%. Since 2010, the NCSP has included a
subsidy of 90% for people with NHI with a contribution over 50%. Such government support
might have reduced the effect of household income on breast and cervical cancer screening
participation [1,18,27].
Our finding of higher rates of having ever had a mammogram and Pap smear among women with
a rural residence differs from the results of other studies that have indicated low rates among
women with a rural residence [5,23-25]. This may have resulted partly from the mobile screening
service now provided by the NCSP. The mobile screening service is helpful for target
populations who are not able to access medical institutions to obtain appropriate screening, and it
may contribute to improving compliance with the screening program. The increase in the
compliance rate for the cancer screening program might have resulted from the provision of
accessible and acceptable screening services, such as mobile screening.
A disparity in mammogram and Pap smear use was found among women of different education
levels after adjusting for age and sociodemographic factors. Other studies have used multivariate
logistic regression analysis to show that women were more likely to undergo a mammogram and
Pap smear if they had a higher education level [2,5,19-21]. To date, a low education level is a
known barrier to breast and cervical cancer screening. Some studies have indicated that routine
monitoring of coverage of screening and information polices affect breast and cervical cancer
screening rates at various education levels [2,18,22,24]. Additionally, the perception of not
needing the test due to good health or an absence of symptoms was the most frequently reported
barrier to participation in breast and cervical cancer screening in all age groups. Thus, we need to
increase the knowledge and awareness of cancer in the target population to increase the
participation rate in cancer screening programs [22,24,26,28-30]. Attempts to promote cancer
screening have used a public health model that targets entire communities, e.g., mass-media
campaigns about the organized screening system in Korea. Additional individual-directed
interventions in health care settings regarding cancer screening use are required, such as
individualized in-person or telephone counseling, individualized letters and reminders, or other
individual-directed strategies, to increase participation and reduce the disparity in cancer
screening [18,27,30].
There may be other reasons for the low perceived risk of breast and cervical cancer in addition to
perceptions of good health or an absence of symptoms. There could be no experience of cancer
among friends and family, misperceptions about the causes of cancer, or not feeling at risk of
cervical cancer because of sexual experience [22,24,25]. Alternative reasons could include the
fact that the service offered is unattractive to women or promoted in an unattractive manner.
However, we did not investigate these reasons in this study. We need to study these reasons
further. The rate of not undergoing screening of breast and cervical cancer due to a lack of time
was high in the women between 40 and 49 years old compared with other age groups. Officials
are discussing whether to give a holiday for cancer screening or to provide cancer screening
service at the employee's place of work while on duty.
Private health insurance was the strongest predictor of breast and cervical cancer screening.
Koreans can take cancer screening through organized or opportunistic systems. Even if they can
take cancer screening free of charge or for a small fee, which is only 10% of the cost, when they
want to take organized cancer screening, some people prefer opportunistic screening to
organized screening. In this case, having private health insurance is a necessary precondition for
improving the use of cancer screening, because private health insurance can remove economic
and practical barriers to screening in opportunistic settings [31].
This study has several limitations, based on the KNCSS data that we used. First, KNCSS data
were self-reported, which may have introduced a bias because several studies have suggested
that self-reports overestimate the prevalence of participation in cancer screening. Second, we
were unable to explore the influence of other important correlates, such as test-specific
characteristics (e.g., preparation, cost, time constraints, and transportation for screening) and
psychological factors (e.g., discomfort, concern about complications, or anxiety about the
procedure) involved in the use of breast and cervical cancer screening. Third, we focused on
women who have ever had screening in this study. It is difficult to compare the life-time
screening rates with screening rates with recommendations directly.
Go to:
Conclusions
In summary, we found that married marital status, higher educational level, rural residence, and
private health insurance were significantly associated with higher rates of breast and cervical
cancer screening after adjustment for age and sociodemographic factors. To improve the
participation rate for breast and cervical cancer screening, more attention should be given to
women in lower sociodemographic groups. Future analyses of the use of breast and cervical
cancer screening for women could include the influence of other important correlates, such as
test-specific characteristics (e.g., preparation, cost, time constraints, or transportation for
screening) and psychological factors (e.g., discomfort, concern about complications, or anxiety
about the procedure) in greater detail in the Korean National Cancer Screening Survey data.
Go to:
Competing interests
The authors declare that they have no competing interests.
Go to:
Authors' contributions
MP participated in the design of the study and drafted the manuscript. EP participated in the
design of the study. KC participated in the sequence alignment. JJ performed the statistical
analyses. HL participated in the design of the study and drafted the manuscript. All authors read
and approved the final manuscript.
Go to:
Pre-publication history
The pre-publication history for this paper can be accessed here:
http://www.biomedcentral.com/1471-2407/11/257/prepub
Go to:
Acknowledgements
Support for this research was provided by the National Cancer Control Research Institute, grant
1010200.
Go to:
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PMC2788032

Ethn Health. Author manuscript; available in PMC 2010 December 1.
Published in final edited form as:
Ethn Health. 2009 December; 14(6): 575589.
doi: 10.1080/13557850903111589
PMCID: PMC2788032
NIHMSID: NIHMS132822
PAP SMEAR RECEIPT AMONG
VIETNAMESE IMMIGRANTS: THE
IMPORTANCE OF HEALTH CARE
FACTORS
Victoria M. Taylor, MD, MPH,
1
Yutaka Yasui, PhD,
2
Tung T. Nguyen, MD,
3
Erica Woodall,
MPH,
1
H. Hoai, Do, MPH,
1
Elizabeth Acorda, MA,
1
Lin Li, MD, MS,
1
John Choe, MD, MPH,
4

and J. Carey Jackson, MD, MPH
4

Author information Copyright and License information
The publisher's final edited version of this article is available at Ethn Health
See other articles in PMC that cite the published article.
Go to:
Abstract
Objective
Recent US data indicate that women of Vietnamese descent have higher cervical cancer
incidence rates than women of any other race/ethnicity, and lower levels of Pap testing than
white, black, and Latina women. Our objective was to provide information about Pap testing
barriers and facilitators that could be used to develop cervical cancer control intervention
programs for Vietnamese American women.
Design
We conducted a cross-sectional, community-based survey of Vietnamese immigrants. Our study
was conducted in metropolitan Seattle, Washington. A total of 1,532 Vietnamese American
women participated in the study. Demographic, health care, and knowledge/belief items
associated with previous cervical cancer screening participation (ever screened and screened
according to interval screening guidelines) were examined.
Results
Eighty-one percent of the respondents had been screened for cervical cancer in the previous three
years. Recent Pap testing was strongly associated (p<0.001) with having a regular doctor, having
a physical in the last year, previous physician recommendation for testing, and having asked a
physician for testing. Women whose regular doctor was a Vietnamese man were no more likely
to have received a recent Pap smear than those with no regular doctor.
Conclusion
Our findings indicate that cervical cancer screening disparities between Vietnamese and other
racial/ethnic groups are decreasing. Efforts to further increase Pap smear receipt in Vietnamese
American communities should enable women without a source of health care to find a regular
provider. Additionally, intervention programs should improve patient-provider communication
by encouraging health care providers (especially male Vietnamese physicians serving women
living in ethnic enclaves) to recommend Pap testing, as well as by empowering Vietnamese
women to specifically ask their physicians for Pap testing.
Keywords: Cervical cancer, Immigrants, Pap testing, Vietnamese
Go to:
INTRODUCTION
The number of Asian Americans in the United States (US) increased from approximately one
million in 1970 to over 12 million in 2000 (Lin-Fu 1993; US Census Bureau 2007). Asian
Americans are not homogeneous. Rather, they are a diverse ethnic group originating from the Far
East, Indian subcontinent, and Southeast Asia (Asian American Health Initiative 2005). They
have different economic characteristics, religious backgrounds, and health practices. For
example, some Asian American groups (e.g., Chinese and Japanese) have higher educational
levels and household incomes than non-Latino whites, while other Asian American groups (e.g.,
groups of Southeast Asian descent) are very educationally and economically disadvantaged (Ro
2002). Therefore, data collection efforts should focus on individual Asian sub-groups and
intervention approaches should be tailored to specific Asian communities (Truman et al. 1994).
Eleven percent of Asian Americans are of Vietnamese descent, and the Vietnamese population
now exceeds 1,400,000 (Pfieifer 2008; US Census Bureau 2007). A majority of Vietnamese
Americans came to the US during one of three immigration waves. The first wave occurred in
1975, following the fall of Saigon, while the second wave started in 1979 as political turmoil
escalated in Southeast Asia. Finally, the third wave of immigrants began in 1989 when the
Vietnamese government began allowing emigration under the auspices of the Orderly Departure
Program and Family Reunification Program (Pham 1999).
Nearly one-third (30%) of Vietnamese Americans have less than a high school education and
only about one-quarter (24%) have a Bachelors degree. Vietnamese American households have
an average income of $46,000 (compared to $56,000 among all Asian American households) and
14% of Vietnamese Americans live below the Federal poverty level. Notably, 55% of
Vietnamese Americans have limited English proficiency and 88% speak Vietnamese (rather than
English) at home (US Census Bureau 2007). Forty-nine percent of Vietnamese Americans live in
the West, 30% live in the South, 11% live in the Northeast, and 10% live in the Midwest.
Washington State has the third largest Vietnamese population in the US (after California and
Texas) (Pfeifer 2008).
Vietnamese have higher rates of invasive cervical cancer than any other racial/ethnic group in the
US (Cockburn and Deapen 2004). Recent data show the cervical cancer incidence rate among
Vietnamese women is over twice the cervical cancer incidence rate among non-Latina white
women (16.8 versus 8.1 per 100,000) (Miller et al. 2008). The Presidents Advisory Commission
on Asian Americans recently identified cervical cancer among Vietnamese women as one of the
most important health disparities experienced by Asian American populations. This group also
specified that the research community should support community-based studies to specifically
address health disparities experienced by Asian American sub-groups, as well as to identify
barriers and facilitators to disease prevention among each Asian sub-group (Presidents Advisory
Commission on Asian Americans and Pacific Islanders 2003).
Humanpapilloma virus (HPV) infection has been identified as a universal risk factor for cervical
cancer (American Cancer Society 2005; Parkin 2006). While little is known about HPV infection
among Vietnamese women living in the US, the limited available data indicate that the cervical
cancer disparity is more likely to be due to low Papanicolaou (Pap) testing levels than variations
in HPV infection rates and/or types (Vo et al. 2004).
National guidelines specify that women should be screened for cervical cancer every one to three
years, depending on their risk factors for disease and previous screening history (Saslow et al.
2002). National cervical cancer screening goals for the year 2010 specify that at least 97% of
women should have been screened on at least one occasion, and 90% should have received a Pap
smear within the previous three years (US Department of Health and Human Services 2000).
However, an analysis of 2003 California Health Interview Survey responses showed that only
70% of Vietnamese women had received a Pap smear in the last three years. In contrast, the
proportions of white, black, and Latina women reporting recent Pap smear receipt were 84%,
87%, and 85%, respectively (Holtby et al. 2006).
Over a 12-month period during 2006 and 2007, we conducted a community-based survey of
Vietnamese women aged 2079 years living in metropolitan Seattle. For this analysis, we used
our survey data to examine the influence of both cognitive and contextual factors on Pap testing
use. The goal of the analysis was to provide information about Pap testing barriers and
facilitators that could be used to develop future cervical cancer control intervention programs for
Vietnamese women.
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METHODS
Sampling Methods
Two validated lists of Vietnamese last names have previously been published (Lauderdale and
Kestenbaum 2000; Nguyen et al. 2002). We compiled a list of 55 Vietnamese names that were
included in one or both of these published lists. Our name list was applied to an electronic
version of the 2005 telephone book for metropolitan Seattle. We identified all households, with
one of the 55 Vietnamese names, which were listed in the telephone book. Then, we identified
zip codes that included at least 50 households with one of the 55 names. Our study sample
included 4,436 households in these 33 zip codes. Households in zip codes with relatively few
Vietnamese residents were excluded for interviewer travel cost reasons, and those with
incomplete address information were excluded because the Institutional Review Board required
an introductory letter.
Household Recruitment
The Fred Hutchinson Cancer Research Center Institutional Review Board approved our study
procedures. Households received an introductory mailing from the project. The letter explicitly
stated that the project aimed to interview Vietnamese/Vietnamese American women in the
Seattle area, and asked households to contact the project if they did not consider themselves to be
Vietnamese or Vietnamese American. Bilingual, bicultural, female survey workers conducted
interviews in womens homes. Before completing surveys, the interviewers verified that women
self-identified as being Vietnamese or Vietnamese American. Women who completed the survey
were given a $15 grocery store card as a token of appreciation for their time. Each respondent
was given the option of completing her survey in Vietnamese or English, and interviews took
about 45 minutes to complete. Up to five door-to-door attempts were made to contact each
household.
Participant Selection
We aimed to interview one woman aged 20 to 79 years in each household. Our previous
experience indicates that survey response rates, in Vietnamese communities, are negatively
effected by attempts to list household members and then randomly select one respondent in
households with two or more eligible respondents. However, to ensure our sample was
representative of different age-groups, we randomly assigned households to one of two groups:
Households where we initially asked to speak with a woman in the 2049 age-group (and then
asked to speak with a woman aged 5079 if there were no women in the younger age-group);
and those where we initially asked to speak with a woman in the 5079 age-group (and then
asked to speak with a woman aged 2049 if there were no women in the older age-group).
Survey Instrument
The survey instrument was developed in English, translated into Vietnamese using double-
forward methods, and pre-tested (Eremenco et al. 2005). We used findings from an earlier
qualitative study and the Health Behavior Framework to guide our survey instrument
development (Burke et al. 2004; Curry and Emmons 1994; Gritz and Bastani 1992). The
theoretical perspective of the Health Behavior Framework has recently been described in detail
elsewhere (Bastani et al. 2007; Jo et al. 2007). Briefly, it specifies that factors influencing the
use of preventive health procedures include demographic characteristics (including acculturation
in foreign-born individuals), health care and physician factors (including communication with
providers), and knowledge and beliefs (including cultural beliefs).
Women were read the following statement: A Pap test is when a doctor does a pelvic exam and
also takes a scraping of tissue from the cervix inside the vagina and sends it to a laboratory.
They were then asked whether they had ever had a Pap test and, if so, when they were last
screened. Survey participants were queried about their age, marital status, educational level,
household income, length of time in the US, and English language proficiency.
Each woman was asked to specify if she had a history of hysterectomy, had received obstetric
services in the US, had received family planning services in the US, and had completed a
physical exam in the last year. Women indicated whether they had health insurance and if there
was one doctor who usually provided their care. Those with health insurance specified if they
had Medicare, Medicaid, the Basic Health Plan (a Washington insurance program for lower
income families), or private insurance. Similarly, those with a regular physician provided
information about their doctors gender and ethnicity. Finally, respondents were asked whether a
doctor had ever recommended Pap testing, and whether they had ever asked a doctor for testing.
Each woman specified whether she thought Vietnamese are more likely than whites to get
cervical cancer; and cervical cancer can be prevented by using traditional Vietnamese washes,
cervical cancer can be prevented by observing the sitting month, and cervical cancer can be
prevented by getting regular Pap tests. (Our earlier qualitative study found that Vietnamese
women believe that maintaining female hygiene by washing regularly with alum and observance
of a set of traditional post-partum practices, known as the sitting month, both protect women
from gynecologic problems.) Participants were also asked whether they thought Pap testing is
necessary for asymptomatic women, Pap testing is necessary for sexually inactive women, and
Pap testing is necessary for post-menopausal women.
Data Analysis
We compared the characteristics of women who had received at least one Pap test and those who
had not, as well as the characteristics of women who had received a Pap test in the previous three
years and those who had not. Household income was classified as $30,000, <$30,000, or
unknown. We chose to use this classification for income because 17% of the respondents either
did not know their household income or refused to answer the income question. Medicare,
Medicaid, and the Basic Health Plan were combined into a public insurance category for the
purpose of this analysis. To examine the effect of physician gender and ethnicity on Pap testing
behavior, we created a physician characteristics variable (Vietnamese man, Vietnamese woman,
Non-Vietnamese man, non-Vietnamese woman, and no regular physician).
Statistical methods included chi-square tests and unconditional logistic regression. Three
multivariable analyses were conducted, for each of our Pap testing outcomes, using pre-specified
explanatory variables. The first of these models included demographic variables, the second
included health care variables (adjusted for demographics), and the third included
knowledge/belief variables (adjusted for demographics). Additionally, we conducted summary
backward selection multivariable analyses for our two Pap testing outcomes. All study variables
(demographic, health care, and knowledge/belief) were included in the backward selection
analyses and p<0.05 was the criterion for retention.
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RESULTS
Survey Response
A total of 1,532 women completed interviews and 596 eligible households refused participation.
The cooperation rate (i.e., response among reachable and eligible households) was 72%. Table 1
provides the dispositions of the other addresses in our original sample. For 1,177 of the
addresses, we were unable to establish if the household was Vietnamese (either because the
interviewer was unable to access a secure building or there was no-one home after five attempts).
We verified that 888 of the households were ineligible (either because the household was not
Vietnamese or did not include an age-eligible Vietnamese woman).

Table 1
Survey Response
One woman was excluded from this analysis because she was in her early eighties and should not
have been interviewed. As this analysis focused on immigrants, nine women were excluded
because they were born in the US. Finally, we excluded six women who reported a personal
history of cervical cancer. Therefore, the study group included 1,516 women.
Pap Testing History
Ninety-three percent of the respondents had received cervical cancer screening on at least one
occasion. The proportions reporting Pap smear receipt in the last year, last two years, and last
three years were 53%, 72%, and 81%, respectively.
Demographic Characteristics
As shown in Table 2, about one-half of the study group were younger than 50 years of age
(50%), had less than 12 years education (51%), and reported an annual household income of less
than $30,000 (48%). Approximately four-fifths were currently married (80%) and had been in
the US for at least 10 years (79%). Only 12% spoke English very well or fluently. In bivariate
comparisons, both the Pap testing outcomes (ever received Pap testing and received Pap testing
in the last three years) were associated with age, marital status, household income, and English
language proficiency. Length of time in the US was associated with ever having received a Pap
smear and educational level was associated with recent Pap testing.

Table 2
Demographic Characteristics and Cervical Cancer Screening
Health Care Factors
Table 3 gives information about health care factors. Only 6% had a history of hysterectomy. The
proportions reporting obstetric and family planning services in the US were 42% and 26%,
respectively. A majority had received a physical in the last year (77%), had some form of health
insurance (89%), and had a regular provider (85%). Eighty-two percent reported a previous
physician recommendation for testing and 68% had asked a doctor for testing. As would be
expected, women with a previous hysterectomy were less likely to have been screened in the
previous three years. The following variables were strongly correlated with both our cervical
cancer screening outcomes in bivariate analyses: Obstetric services in the US, family planning
services in the US, physical in the last year, health insurance, physician characteristics, and the
two communication with provider variables.

Table 3
Health Care Factors and Cervical Cancer Screening
Knowledge and Beliefs
Information about knowledge and beliefs is provided in Table 4. Less than one-quarter (21%) of
our participants knew that Vietnamese women are more likely to get cervical cancer than white
women. The proportions who thought cervical cancer can be prevented by traditional
Vietnamese washes, observing the sitting month, and getting regular Pap tests were 81%, 74%,
and 92%, respectively. A majority knew that Pap testing is necessary for women who are
asymptomatic (95%), sexually inactive (86%), and post-menopausal (91%). Respondents who
knew that Vietnamese women are at increased risk of cervical cancer and the disease can be
prevented by regular Pap tests were more likely to have ever been screened and to have been
screened in the previous three years. Additionally, the three Pap testing knowledge variables
were all strongly associated with our two cervical cancer screening outcome variables.

Table 4
Knowledge, Beliefs, and Cervical Cancer Screening
Results of Regression Analyses
Table 2 presents results of our multivariable analyses of demographic variables associated with
the two Pap testing outcomes. Independent associations between health care factors and cervical
cancer screening (after adjustment for demographics) are given in Table 3, and independent
associations between knowledge/beliefs and cervical cancer screening (after adjustment for
demographics) are given in Table 4.
Table 5 shows the summary backward elimination models. Never married women were less
likely to have ever received a Pap smear than currently and previously married women. Women
with a female Vietnamese doctor, a male non-Vietnamese doctor, and a female non-Vietnamese
doctor were more likely to have received at least one Pap smear than women without a regular
doctor. However, women with a male Vietnamese doctor were no more likely to have been
recently screened than those with no regular doctor. Finally, having received obstetric services in
the US and our provider communication variables were strongly associated with cervical cancer
screening on at least one occasion. The following variables were strongly associated with a Pap
smear in the last three years: Age, physician characteristics, physical in the previous 12 months,
doctor had recommended Pap testing, and had asked doctor for Pap testing.

Table 5
Factors Independently Associated with Cervical Cancer Screening
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DISCUSSION
We previously completed a survey of Vietnamese women in Seattle during 2002. This earlier
survey found that 71% of women without a history of hysterectomy had been screened for
cervical cancer at least once and 68% had been screened in the last three years (Taylor et al.
2004b). In the five years since our prior survey, Pap testing rates have increased substantially.
Specifically, in 20062007, we found that 92% of women without a history of hysterectomy had
ever received a Pap smear and 82% had received a recent Pap smear (in the last three years).
Over the last five years, Seattles Vietnamese community has been the focus of cervical cancer
control efforts by the National Breast and Cervical Cancer Early Detection Program, as well as a
community clinic system serving limited English speaking Asian Americans. Our findings
indicate that these efforts may have been successful in increasing Pap testing levels among
Vietnamese women.
This study identified sub-groups of women who could usefully be the focus of future cervical
cancer control efforts in Vietnamese communities. For example, over one-quarter of never
married women had not received a Pap smear, and the odds of ever having been screened were
about four times higher among currently/previously married women than among never married
women in our backward elimination model. Similarly, the odds of Pap test receipt on at least one
occasion were estimated to be four times higher among women who had been in the US for at
least 20 years than those who had been in the US for less than 10 years.
Current cervical cancer screening guidelines specify that women aged 70 years and older who
have had three or more normal Pap smears and no abnormal Pap smears in the last 10 years may
choose to stop cervical cancer screening. They also specify that screening is not necessary after
hysterectomy with removal of the cervix (Saslow et al. 2002). Therefore, it is not surprising that
women in their seventies had lower levels of recent Pap testing than younger women, and
women with a history of hysterectomy had lower levels of recent Pap testing than women
without a history of hysterectomy. Interestingly, nearly three-quarters of our respondents with a
history of hysterectomy did report a recent Pap smear. While a proportion of these women may
have received a hysterectomy without removal of the cervix, this finding suggests that some
physicians may be performing unnecessary Pap testing.
Some authors have speculated that traditional health beliefs may act as barriers to utilization of
preventive health services (Jenkins et al. 1996). A majority of our respondents believed cervical
cancer can be prevented by traditional Vietnamese washing procedures and proper observance of
the sitting month; however, these beliefs were not important correlates of Pap testing behavior.
Nonetheless, it is important that health educational programs for Vietnamese and other
immigrant groups recognize communities cultural beliefs and incorporate them into intervention
programs. Indeed, decontextualization of a health problem from the belief systems and daily
routines of the target population may diminish the effectiveness of health education efforts
(Hubbell et al. 1995).
Levels of knowledge about Pap testing were relatively high and over 80% of our participants
knew that Pap testing is necessary for asymptomatic women, Pap testing is necessary for
sexually inactive women, and Pap testing is necessary for post-menopausal women. Our
multivariable analyses of knowledge/beliefs and Pap testing suggest that educational programs
might usefully focus on the role of Pap testing in the prevention of cervical cancer and the
necessity of Pap testing for all women.
Our summary multivariable analyses indicate that health care factors are the most important
determinants of cervical cancer screening participation. Findings with respect to physician
patient communication about Pap testing were very similar to those reported from a recent study
of Vietnamese women in California and Texas. Specifically, Nguyen and colleagues found that
women who had requested a Pap test were nine times more likely to have ever been screened
than women who had never requested the test, and women who had received a physician
recommendation were eight times more likely to have ever been screened than those who had not
received a recommendation (Nguyen et al. 2002).
Previous research has consistently demonstrated that women of Southeast Asian descent who
have a female doctor are more likely to receive cervical cancer screening than those who have a
male doctor (McPhee et al. 1997a; McPhee et al. 1997b; Nguyen et al. 2002; Taylor et al. 1999;
Taylor et al. 2004a). However, previous findings with respect to physician ethnicity have been
inconsistent (McPhee et al. 1997a; McPhee et al. 1997b; Nguyen et al. 2002; Taylor et al.
2004a). In this study, multivariable analyses indicated that women with a male Vietnamese
doctor were no more likely to have been recently screened than those with no regular doctor.
However, screening rates among women with a female Vietnamese physician were comparable
to those among women with a non-Vietnamese physician. Low levels of Pap smear use among
Vietnamese male physicians may be attributable to a lack of emphasis on prevention during
medical training in Vietnam, as well as a cultural sensitivity to personal modesty issues among
female patients (Lai et al. 2004). If male Vietnamese physicians are uncomfortable performing
Pap tests, they could be advised to refer their patients to an appropriate provider. Finally, our
results suggest that positive associations between physician-patient racial/ethnic concordance
and quality of care cannot be assumed (Cooper and Powe 2004).
Coyne and colleagues conducted a literature review of factors associated with cervical cancer
screening among women in the US. This review found that individual barriers to screening, as
well as their relative importance, differ markedly between population subgroups. For example,
Spanish-speaking Latina women are more likely to report that they find Pap smears embarrassing
and frightening than do English-speaking Latina women. As might be expected, logistic issues
such as transportation, childcare, and concern about using scarce resources for unnecessary tests
are most important among socially disadvantaged and racial/ethnic minority women. For the
female population as a whole, these authors concluded that the most important barriers to Pap
testing are perceptions that it is unnecessary, fear of embarrassment, and lack of physician
recommendation (Coyne et al. 1992).
A group of researchers recently described perceived barriers to cervical cancer screening from
the perspectives of women, men, and healthcare providers in five Latin American countries
(Ecuador, El Salvador, Mexico, Peru, and Venezuela). The main barriers were accessibility and
availability of quality health services, medical facilities that lacked comfort and privacy, the
financial costs of screening, and levels of courtesy among providers (Agurto et al. 2004).
Similarly, the following have been reported to be barriers to Pap testing among Mexican women
from urban (Mexico City) and rural (the State of Oaxaca) areas of the country: Problems in
doctor/medical institution-patient relationships, long waits for sample collection and receiving
results, and perceived high costs for care (Lazcano-Ponce et al. 1999).
The recently completed Vietnamese REACH for Health Initiative evaluated a multifaceted
cervical cancer control intervention program for Vietnamese women in Santa Clara County,
California (Nguyen et al. 2006). Intervention components included continuing medical education
sessions for Vietnamese physicians (Lai et al. 2004; Nguyen et al. 2006). Doctors who
participated in the educational sessions were asked to complete pre-education and post-education
surveys. Results showed that the sessions were effective in improving knowledge about cervical
cancer and Pap testing (Lai et al. 2004). Indirect evidence, from surveys of women, also
suggested that levels of physician recommendation for cervical cancer screening increased as a
result of the continuing medical education sessions (Nguyen et al. 2006).
During 19982002, the cervical cancer incidence rate among Cambodian women in California
and Washington was 15.0 per 100,000 women, compared to 7.7 per 100,000 among non-Latina
white women (Kem and Chu 2007). Additionally, the incidence rate among Hmong women in
California during 19962001 was 33.7 per 100,000 (Yang et al. 2004). While these other
Southeast Asian groups come from the same geographic area and have similar immigration
histories to the Vietnamese, there are many cultural differences. Therefore, it is important that
future efforts to increase Pap testing focus on these communities.
The reported study has several limitations that warrant discussion. Our findings with respect to
Pap testing rates may not be applicable to all geographic areas. For example, we documented
relatively high rates of health insurance coverage, compared to other studies (Nguyen et al. 2002;
Nguyen et al. 2006). Only households with listed telephone numbers were eligible for the study.
Also, survey respondents may have had different preventive behavior patterns than those who
were unreachable or refused participation. Finally, Pap testing self-reports may be faulty due to
inaccurate recall or desirability bias. Since racial/ethnic minority women tend to over-report
screening test receipt when compared to non-Latina white women, it is possible that our study
over-estimated levels of Pap testing use (McPhee et al. 2002).
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Conclusion
A recent analysis indicated that disparities in Pap smear use among black, white, and Latina
women no longer exist in California (De Alba et al. 2004). While nearly 20% of our survey
participants had not received a recent Pap smear, our study findings indicate that disparities
between Vietnamese and other racial/ethnic groups are decreasing. Our findings also suggest
that, as in other disadvantaged groups, the cervical cancer disparity among Vietnamese women is
likely a marker for health care access inequities, and efforts to further increase screening
participation in Vietnamese communities should enable women without a source of health care
to find a regular provider (Freeman and Wingrove 2005). Additionally, intervention programs
should improve patient-provider communication by encouraging health care providers
(especially male Vietnamese physicians serving women living in ethnic enclaves) to recommend
Pap testing, as well as by empowering Vietnamese women to specifically ask their physicians for
Pap testing. Finally, healthcare providers, particularly Vietnamese males, need to be informed
about the value of Pap tests for women with an intact cervix, and continuing medical education
programs should focus on clarifying cultural beliefs and US cancer screening recommendations.
Go to:
Acknowledgments
This publication was supported, in part, by grant R01-CA-115564 from the National Cancer
Institute, cooperative agreement U01-CA-114640 from the National Cancer Institute, and
cooperative agreement U48-DP-000050 from the Centers for Disease Control and Prevention.
The contents of the article are solely the responsibility of the authors and do not necessarily
represent the views of the National Cancer Institute nor the Centers for Disease Control and
Prevention.
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41. Vo PD, Nguyen TT, Nguyen P, Hilton JF, Palefsky JM, Ma Y, McPhee SJ. Human
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J Gen Intern Med >
v.25(11); Nov 2010 >
PMC2947642

J Gen Intern Med. 2010 November; 25(11): 11861192.
Published online 2010 July 7. doi: 10.1007/s11606-010-1434-6
PMCID: PMC2947642
Community Health Worker Intervention to
Decrease Cervical Cancer Disparities in
Hispanic Women
Matthew J. OBrien, MD, MSc,
1,4
Chanita Hughes Halbert, PhD,
3
Rebecca Bixby, RN,
4
Susana
Pimentel,
4
and Judy A. Shea, PhD
2

Author information Article notes Copyright and License information
Abstract
INTRODUCTION
U.S. Hispanic women suffer a disproportionate burden of cervical cancer, with incidence and
mortality rates almost twice that of whites. Community health workers, or promotoras, are
considered a potential strategy for eliminating such racial and ethnic health disparities. The
current study is a randomized trial of a promotora-led educational intervention focused on
cervical cancer in a local Hispanic community.
METHODS
Four promotoras led a series of two workshops with community members covering content
related to cervical cancer. Sociodemographic characteristics, cervical cancer risk, previous
screening history, cervical cancer knowledge, and self-efficacy were measured by a pre-
intervention questionnaire. The post-intervention questionnaire measured the following
outcomes: cervical cancer knowledge (on a 06 scale), self-efficacy (on a 05 scale), and receipt
of Pap smear screening during the previous 6 months (dichotomous). Univariate analyses were
performed using chi square, t-test, and the MannWhitney test. Multivariate logistic regression
was used to model the association between explanatory variables and receipt of Pap smear
screening.
RESULTS
There were no statistically significant differences between the two experimental groups at
baseline. Follow-up data revealed significant improvements in all outcome measures: Pap smear
screening (65% vs. 36%, p-value 0.02), cervical cancer knowledge (5.4 vs. 3.5, p-value <0.001),
and self-efficacy (4.7 vs. 4.0, p-value 0.002). In multivariate analysis, cervical cancer knowledge
(OR 1.68, 95% CI 1.10-2.81) and intervention group assignment (OR 6.74, 95% CI 1.77-25.66)
were associated with receiving a Pap smear during the follow-up period.
DISCUSSION
Our randomized trial of a promotora-led educational intervention demonstrated improved Pap
screening rates, in addition to increased knowledge about cervical cancer and self-efficacy. The
observed association between cervical cancer knowledge and Pap smear receipt underscores the
importance of educating vulnerable populations about the diseases that disproportionately affect
them. Future research should evaluate such programs on a larger scale, and identify novel targets
for intervention.
Electronic supplementary material
The online version of this article (doi:10.1007/s11606-010-1434-6) contains supplementary
material, which is available to authorized users.
KEY WORDS: cervical cancer, health disparities, community health worker, promotora
INTRODUCTION
As the largest and fastest-growing minority group in the United States, Hispanics represent an
important target population for health interventions
1
. The U.S. Census projects that Hispanic
Americans will number 47.8 million in 2010, and will represent 25% of the U.S. population by
2050
2
. A large body of medical literature demonstrates the vulnerability of this growing
population to poor health outcomes when compared to other racial and ethnic groups. Two recent
reports summarize disparities between Hispanics and whites with respect to disease-specific
outcomes, healthcare quality, and access to medical services and treatments
3,4
. The persistence of
racial and ethnic disparities in health and health care necessitates novel strategies for reducing,
and ultimately eliminating them
5
.
Cervical cancer represents one of the starkest health disparities facing U.S. Hispanic women.
Cervical cancer incidence among U.S. Hispanic women is nearly twice that of white women, and
mortality is 42% higher in this population
6
. More recent data suggest that these disparities are
increasing
7
. The excess mortality observed in U.S. Hispanics is due, in part, to low Pap smear
screening rates
8
. Estimates of annual screening rates in this population vary widelyfrom 42%
to 83%
911
, compared with 88% among all U.S. women
12
. Disparities in cervical cancer
screening and outcomes are influenced by individual factorscultural beliefs
13,14
, linguistic
barriers
15
, socioeconomic status
16
, and levels of health literacy
17
. Systemic factors, such as low
levels of insurance
18
, lack of a usual source of care
19,20
, and fear of discrimination
21
, also play an
important role in producing cervical cancer disparities. Foreign-born Hispanic women are less
likely than their U.S.-born counterparts to receive Pap smears, which may partially reflect the
impact of immigration status on utilization of cancer screening
22,23
.
Community health workers (CHWs) may provide a novel and culturally-appropriate model for
addressing such health disparities in underserved populations. CHWs are community members
who work almost exclusively in community settings and who serve as connectors between
healthcare consumers and providers to promote health.
24
This lay medical workforce emerged
in Latin America in the 1950s and has since performed a wide range of health promotion and
disease prevention activities, both domestically and internationally
25
. Examples of CHW roles
include providing health education, performing patient navigation, and directly delivering
medical services, such as immunizations
26
. CHW programs have targeted many diseases
diabetes
2730
, cancer
3135
, cardiovascular disease
3639
, and asthma
4044
in addition to focusing on
general health promotion
45
and maternal/child health
4648
.
A recent review of the domestic community health worker literature (CHW) revealed that such
programs were most prevalent in Hispanic communities, where these lay workers are often called
promotoras
49
. The same review reported that cancer screening was the most common focus of
CHW programs
49
. The evidence base for promotora interventions in Hispanic communities is
weak, with most studies using quasi-experimental designs to evaluate their effectiveness
5052
. But
despite the lack of rigorous evidence
53
, many stakeholders have advocated for CHWs to help
lower healthcare costs and reduce racial and ethnic health disparities
4,54,55
.
In an effort to generate more rigorous evidence supporting CHW efforts to address an important
health disparity, we implemented and evaluated a promotora-led educational intervention
focused on cervical cancer. Based on our literature review, this study represents the first
randomized trial of a promotora-led cervical cancer program involving a community-dwelling
cohort. The only other previous randomized trial of a similar intervention recruited and
randomized participants in a clinic setting
56
. Three previous studies randomized communities
57
59
, and two studies were randomized at the level of the CHW
60,61
. Our program was adapted from
a curriculum that has been previously studied and reported elsewhere
6163
. Our primary objective
was to evaluate the impact of the experimental intervention on participants receipt of Pap smear
screening, cervical cancer knowledge, and self-efficacy. We hypothesized that this educational
interventionbased on the Health Belief Model
64
would increase participants self-efficacy
and knowledge about cervical cancer, and thereby increase Pap smear screening rates. A
secondary objective was to examine other predictors of Pap smear receipt among members of
study cohort.
METHODS
The University of Pennsylvania institutional review board (IRB) approved the experimental
protocol. The current study followed the principles of community-based participatory research,
involving the South Philadelphia Hispanic community throughout
65
. An advisory board was
established at the outset, consisting of representatives from the following organizations that serve
the target community: the Mexican Consulate, the Catholic Archdiocese, a primary-care clinic,
and a social service organization. These organizations guided the research through regular
feedback provided in both formal and informal settings. This groupcomposed of individuals
from the target population and advocates who were not community membersmet quarterly and
participated actively in the conceptualization, development, implementation, evaluation, and
dissemination of the study.
120 Hispanic women aged 18-65 were recruited and enrolled in the community by 4 female
promotoras. Exclusion criteria included age older than 65 or younger than 18, current pregnancy,
prior history of cervical cancer, and prior history of hysterectomy. Recruitment and enrollment
efforts took place in local faith-based and community-based organizations, the Philadelphia
Mexican Consulate, and participants homes. This sampling approach was chosen to more
accurately reflect the target population, rather than recruiting subjects in healthcare institutions
where baseline health knowledge and behaviors may be greater. Eligible women were invited to
participate in the study, and received two $20 gift cards as an incentive.
All participants took a baseline questionnaire, which was administered in Spanish by the
promotoras and lasted approximately 30 minutes. The promotoras training in research methods
has been reported elsewhere
49
. The personal and professional backgrounds of our promotoras are
also described elsewhere
66
. The baseline questionnairepreviously piloted in the community
included 55 questions measuring the following constructs: health status, history of Pap smear
screening and general health care use, and risk profile for cervical cancer. Sociodemographic
characteristics measured in the baseline questionnaire included age, marital status, educational
attainment, employment, insurance status, country of origin, length of residence in the U.S., and
acculturation. Our primary outcome was receipt of cervical cancer screening following the
intervention; our secondary outcomes were knowledge about cervical cancer and self-efficacy to
undergo Pap smear screening. All outcome measures were assessed in the baseline questionnaire
and in a 28-question follow-up questionnaire, which was also administered in Spanish by the
promotoras in approximately 15 minutes.
Self-reported health status was measured with a single question using a five-point Likert scale
from 1 (Excellent) to 5 (Poor). Previous Pap smear screening history was assessed by asking
the month and year of the participants last Pap smear. This question was dichotomized as having
received a Pap within 1 year (i.e. up-to-date) or not. Knowledge about cervical cancer was
measured using a 6-item questionnaire developed by the research team. (See
Online Appendix
). These
six questions covered the pathogenic role of HPV, methods for prevention, screening
recommendations, the meaning of a positive Pap smear, the relevant epidemiology of cervical
cancer in Hispanics, and anatomy of the cervix. Self-efficacy was measured using a previously
validated scale that contains 19 close-ended questions with a 5-point Likert scale describing the
participants likelihood of undergoing Pap smear screening under different scenarios
67
.
Responses range from 1 (I would definitely not have a Pap smear) to 5 (I would definitely
have a Pap smear). Acculturation was measured using the Short Acculturation Scale for
Hispanics developed by Marin et al, and is represented as a numeric average of the responses to
the five questions, which range from 1 (least acculturated) to 5 (most acculturated)
68
.
All 120 participants were randomized to receive a promotora-led cervical cancer educational
intervention or usual care. At the suggestion of community members involved in the design of
the study, control-group participants crossed over to receive the experimental intervention after
completion of the follow-up evaluation. A random number sequence was generated by the PI to
guide group assignment. Subjects were allocated to either the intervention or control group by
the promotoras based on whether their study number was odd or even. We determined a priori
that 60 participants in each group were necessary to detect a 25% difference in the percentage of
women who received Pap screening between the two groups, assuming a baseline screening level
of 50%, an of 0.05, and 80% power.
The intervention consisted of two 3-hour workshopsincluding between 4 and 10 women in
each groupwhich were led by a pair of promotoras. These workshops followed a previously-
studied curriculum, which was modified by the study team for the purposes of the current
study
62
. The curriculum employs an interactive format and includes information about female
genital anatomy, risk factors for cervical cancer, common myths about cervical cancer, screening
procedures and recommendations, the implications of screening, and the epidemiology of
cervical cancer in Hispanic women. All participants were given a copy of this curriculum, in
addition to other program materials including informational pamphlets from the American
Cancer Society and U.S. Department of Health and Human Services.
The intervention was delivered in several rounds over a 4-month period. We used multiple
process measures to ensure that the intervention was implemented uniformly. A basic set of
questions was filled out by the promotoras at the end every workshop documenting the number
of participants, the length of time spent on each portion of the curriculum, and the total time for
each session. The principal investigator and study coordinator randomly observed 20% of the
workshop sessions to confirm adherence to the curriculum and to verify the promotoras
responses to the process measures outlined above. Follow-up of all study participants occurred
approximately 6 months following the delivery of the educational intervention, consisting of a
second questionnaire that included a question about whether the participants underwent Pap
smear screening during the follow-up period, and if so, where they received it. Self-reported data
on Pap smear receipt were verified by chart review for 83% of participants who reported
undergoing screening at three local health centers.
Baseline characteristics were compared between the two study groups using chi-square tests for
dichotomous variables and t-tests for continuous variables. The MannWhitney test was used to
compare continuous variables with non-normal distributions, which was assessed using the
ShapiroWilk test. Receipt of Pap smear screening during the follow-up period was expressed as
the percentage of women in each group that underwent Pap screening. This outcome was
compared between the two groups using the chi-square test. The secondary outcome of a cervical
cancer knowledge score was calculated using the number of questions answered correctly; and a
self-efficacy score was expressed as the numerical average of participants answers to the 19
self-efficacy questions. Post-intervention knowledge and self-efficacy were expressed both as t-
test comparisons of these scores between the groups, and as a difference in differences from
baseline scores using t-tests. We used multivariate logistic regression to estimate the influence of
the following predictors on receiving a Pap smear among the follow-up cohort: age, education,
having a usual source of care, parity, acculturation, self-efficacy, cervical cancer knowledge, and
group assignment.
RESULTS
Figure 1 shows the flow of participants through the study. The intervention was ultimately
delivered to 43 of the intervention-group participants (72%), 9 of whom were lost to follow-up at
6 months. The overall 6-month follow-up rate was 58%. The only significant difference between
those who followed-up and those who did not was a slightly better self-reported health status
among the follow-up cohort (3.0 vs. 3.3, P=0.04). The baseline sociodemographic
characteristics of all 120 study subjects are presented in Table 1. There were no significant
differences between the intervention- and control-group participants with respect to any of these
factors. Overall, the study cohort consisted of young women with low levels of formal education
and acculturation, who were at modest risk for developing cervical cancer. Our outcome
measures demonstrated no significant differences at baseline.

Figure 1
Flow diagram of participants through study.

Table 1
Baseline Characteristics of the Study Cohort (N=120)
Table 2 presents the 6-month follow-up results. Excluding the 17 intervention and 18 control
subjects who were already up-to-date with Pap smear screening at baseline, the difference in
screening rates between the two groups was significant at 6 months (71% vs. 22%, P=0.004).
Cervical cancer knowledge was significantly higher among intervention participants at 6 months,
and was also significant as a difference in differences from baseline (2.2 vs. 0.2, P <0.001). Self-
efficacy also demonstrated a significant increase among intervention participants.

Table 2
Study Outcomes at 6 Months
Table 3 displays the results from our exploratory multivariate logistic regression model
describing the association of multiple predictors with Pap smear receipt in the follow-up cohort.
Only post-intervention cervical cancer knowledge and group assignment were predictive of
receiving a Pap smear during the 6-month follow-up period. There was an association between
acculturation and Pap smear receipt, which was not statistically significant.

Table 3
Adjusted Odds Ratios of the Association between Explanatory Variables and Receipt of Pap
Smear Screening in the Follow-up Cohort (N=70)
DISCUSSION
The study findings support our primary hypothesis, demonstrating the effectiveness of this
promotora-led intervention on increasing participants self-efficacy and knowledge about
cervical cancer, in addition to significantly improving Pap smear screening rates at 6 months.
Perhaps these findings reflect some of the proposed benefits of using a promotora model for
cancer education
69
, despite the inherent challenges of implementing and evaluating such
programs
70
. This approach is culturally competent and interactive, allowing more time for
learning than physicians are able to accommodate during brief office visits. Our study also
provides preliminary evidence that knowledge about cervical cancer predicts receipt of Pap
smear screening. Our model also revealed a significant association between group assignment
and Pap receipt. The odds ratio for acculturation was large as was the CI.
There are several strengths of the current study. First, randomizing participants at the individual
level represents a methodological improvement over much of the existing CHW literature, where
weaker experimental designs are more prevalent
57,58,62,7173
. Second, the community-based
recruitment strategies employed here produced a study cohort that is likely more representative
of the overall population than a clinic-based cohort. Our unique cohort with low levels of
acculturation provides an important contribution to the existing literature, which has either
studied more acculturated Hispanic women
58,61
or not reported acculturation levels
59,71,73
. Third,
the current study enrolled new Hispanic immigrants, the majority of whom (92%) did not have
health insurance coverage. Since lack of insurance is a well-recognized barrier to Pap smear
receipt
18
, our intervention might have an even larger impact on cervical cancer screening in
insured populations than was observed in the current study. Finally, our validation of Pap self-
report using chart data represents another strength of the current study.
There are also obvious limitations to the current study. The unique nature of our study cohort
limits the generalizability of our findings to more established Hispanic immigrants and U.S.-born
Hispanics. Although we did not gather data about participants immigration status, the collective
experience of the investigators and community partners suggests that a majority of the target
population is undocumented. This did not affect study recruitment but likely had an impact on
the large drop-out rate observed here, which was similar to other studies evaluating promotora-
led cervical cancer interventions in the community setting
58,59,61
. Nevertheless, even with these
small samples, we had sufficient power to detect the observed difference in Pap smear screening
rates between the two groups at a significance level of P=0.1.
A sensitivity analysis was performed assuming that all participants who were lost to follow-up
did not receive a Pap smear, which revealed a consistent but insignificant result for Pap receipt
(37% vs. 21%, P=0.07). The participants who followed-up reported better overall health status
than those who did not, which may have introduced bias away from the null since those with
better health may undergo cancer screening more regularly than those who report poor health
74
.
Although our 6-month follow-up period is consistent with several studies in the existing
literature
58,61,72
, a 1-year assessment would have provided a more medically relevant interval for
follow-up. This shorter follow-up period may have underestimated the effect of the intervention
on screening behavior, since it was not indicated at 6 months for many participants.
The current study is the first trial of a promotora-led cervical cancer intervention involving a
randomized community-based sample. Our intervention demonstrated a larger effect on Pap
smear screening rates than most previous non-randomized studies, and those that randomized
either CHWs or communities
56,60,61,72,73
. Perhaps this reflects the effectiveness of the curriculum
in motivating behavior change; although the original study on which our curriculum was based
reported a more modest effect
61
. The promotoras skill may also help explain our interventions
large impact on Pap screening rates, and future research might examine the effectiveness of
individual CHWs to identify the qualities that promote success in this role. Our intervention also
demonstrated a greater impact on the participants knowledge about cervical cancer than others
in the existing literature
58,60
. Self-efficacy was measured in only one previous study, which
reported a modest, but statistically significant increase following their intervention
58
.
An important finding of the current study is the observed association between knowledge about
cervical cancer and receipt of Pap screening. Although the association between cervical cancer
knowledge and screening is consistent with several theoretical models of health behavior
75
and
has been suggested in observational studies
7682
, our study is the first to report this result in the
context of an intervention trial. This finding has important implications for reducing cancer
disparities in communities where cancer-related knowledge is poor. Future research should
examine the impact of knowledge on screening behavior in larger, more diverse cohorts; and
efforts to improve screening among the underserved must consider the importance of educational
outreach as a component of such programs.
Another interesting finding from our multivariate analysis is the large, though statistically
insignificant association between acculturation and receipt of Pap smear. Several observational
studies have examined the impact of acculturation on Pap smear receipt in Hispanics, many
using proxy measures for acculturation
8386
. Studies analyzing NHIS data and using a modified
acculturation measure similar to the current study have failed to show a consistent association
between acculturation and Pap smear receipt
8789
. Further research is necessary to clarify the
relationship between acculturation and Pap smear screening, which may suggest new strategies
for improving cancer screening in Hispanic women. In conclusion, our community health worker
intervention carries promise to reduce cervical cancer disparities in Hispanics. Future research
should both evaluate such programs in larger randomized cohorts, and help identify new
intervention components to improve upon existing programs.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(367K, doc)

(DOC 366 kb)
Acknowledgments
The authors thank the promotoras whose work is the subject of this article, and whose dedication
to this study has been essential to its success. Their names are Susana Pimentel, Irma Zamora,
Bertha Gonzalez, and Guadalupe Canchola. The authors would like to thank Giselle Dutcher and
Darryl Powell for their help in the implementation of this study. We also thank Dr. Steven
Larson for helping conceptualize and develop our community health worker program. We
acknowledge our community partners involved in the design and ongoing implementation of the
study: Puentes de Salud Health Center, the Mexican Consulate of Philadelphia, the Catholic
Archdiocese of Philadelphia, and Juntos Mexicanos. The current study was supported by Grant
Number UL1RR024134 from the National Center for Research Resources. The content is solely
the responsibility of the authors and does not necessarily represent the official views of the
National Center for Research Resources or the National Institutes of Health. This paper was
presented at the SGIM 33rd Annual Meeting in April 2010.
Conflict of Interest None disclosed.
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PMC3110214

Am J Public Health. Author manuscript; available in PMC 2012 July 1.
Published in final edited form as:
Am J Public Health. 2011 July; 101(7): 12971305.
Published online 2011 May 12. doi: 10.2105/AJPH.2010.300061
PMCID: PMC3110214
NIHMSID: NIHMS328049
Is health care system distrust a barrier to
breast and cervical cancer screening?
Evidence from Philadelphia
Tse-Chuan Yang, Stephen A. Matthews, and Marianne M. Hillemeier
Author information Copyright and License information
The publisher's final edited version of this article is available at Am J Public Health
See other articles in PMC that cite the published article.
Go to:
Abstract
Objectives
This study investigates whether health care system distrust is a barrier to breast and cervical
cancer screening and whether different dimensions of distrust values and competence have
different impacts on cancer screening.
Methods
We utilize data on 5,268 women 18 and older living in Philadelphia and analyze their use of
screening services via logistic and multinomial logistic regression.
Results
High levels of health care system distrust are associated with lower utilization of breast and
cervical cancer screening services. The associations differ by dimensions of distrust.
Specifically, high competence distrust is associated with a reduced likelihood of having Pap
smear tests, and women with high values distrust are less likely to have breast examinations
within the recommended time period. Independent of other covariates, individual health care
resources and health status are associated with utilization of cancer screening.
Conclusions
Health care system distrust is a barrier to breast and cervical cancer screening even after
controlling for demographic and socioeconomic determinants. Rebuilding confidence in the
health care system may improve personal and public health by increasing the utilization of
preventive health services.
Go to:
Introduction
Cancer is a leading cause of death in the United States. Approximately 1.5 million Americans are
diagnosed with cancer per annum and one in four deaths are due to cancer.
1
Among women, an
estimated 192,000 breast and 11,000 cervical cancer cases are detected each year and over
40,000 women die from breast cancer and approximately 4,000 from cervical cancer.
1
To be
effective in reducing the morbidity and mortality resulting from breast and cervical cancer,
efforts need to be made to increase the proportion of women who comply with screening
recommendations;
2
according to a recent report a third of women are not in compliance with
screening guidelines for breast cancer and over a fifth for cervical cancer.
3
The goal of this study
is to investigate whether health care system distrust (hereafter referred to as distrust) is a barrier
to breast and cervical cancer screening.
The late-Twentieth century saw many changes in the theoretical underpinnings of research on
health in general, and womens health in particular. The prevailing biomedical model was
criticized for ignoring social determinants of health, such as social class, gender roles, and
poverty,
4
and health determinants models that incorporated multiple social, economic and
demographic dimensions were embraced.
57
While the multiple determinants of health
perspective emphasizes the relationships between socioeconomic factors and health outcomes,
4

the role of psychological factors (i.e. depression and distrust) in cancer screening has only
recently been recognized.
811
Relatively little is known about whether distrust affects health
outcomes, and specifically whether it influences cancer screening behaviors among women.
11

Americans overall confidence in their health care system has declined markedly in recent
decades. In 2010 only 34 percent of adults reported a great deal of confidence in the health
system, down from over 70 percent in 1966.
12
More than 80 percent of the Americans, however,
held high levels of trust in their personal physicians or providers;
13
a paradox that has been
widely documented in the literature.
1417
Previous studies suggest trust in physicians is associated
with seeking timely medical care, maintaining appropriate health care, and adhering to medical
advice
1820
but it is unclear whether trust or its converse distrust affects the adoption of
preventive health services among women.
11

Of relevance to this study, the emerging distrust research in health care shows that distrust is a
multidimensional concept.
2123
For example, Shea et al. used focus groups, pilot testing, and a
telephone survey to develop a highly reliable 9-item distrust scale that includes 2 subscales:
competence distrust and values distrust.
22
Competence distrust is expected to be high when the
quality of service fails to meet patient expectations and does not improve health. Values distrust
is expected to be high when the integrity of the health care system is questioned (e.g., ethical
issues, financial priorities, transparency of care). While it is possible that dimensions of distrust
may influence the use of preventive health services in different ways, little research has
addressed this issue explicitly.
A range of individual characteristics have been found to be associated with the use of breast and
cervical cancer screening, including age,
5, 24
race/ethnicity,
11, 25
socioeconomic factors,
5, 24

marital status,
5, 11, 24
and availability and utilization of health care resources.
11, 24
Access to
insurance and health care providers is associated with higher likelihood of interaction with the
health care system, and has been hypothesized to be related to levels of distrust and to
individuals health-related behaviors.
26
Personal health status has been found to be related to
levels of distrust,
27
although the underlying causal mechanisms have not been well-documented.
Evidence concerning the association of health status with use of preventive health services is
inconclusive.
11
An important contribution of our study is the investigation of the association of
distinct aspects of distrust-- values distrust and competence distrust--with receipt of two
preventive health services for adult women: the Papanicolaou (Pap) test for cervical cancer and
clinical breast examination to screen for breast cancer. We test the following two hypotheses:
after controlling for individual socioeconomic and demographic characteristics, (1) high levels of
distrust are associated with low utilization of cancer screening services; and (2) the negative
relationship between distrust and cancer screening utilization holds for both the values and
competence dimensions of distrust.
Go to:
Data and Methods
Data Source
This study is based on data collected on all women aged 18 and older (n = 5,268) in the
Philadelphia Health Management Corporations (PHMC) 2008 Southeastern Pennsylvania
Household Health Survey; a survey covering five counties in southeastern Pennsylvania, Bucks,
Chester, Delaware, Montgomery, and Philadelphia counties. The interviews were conducted
between June and October 2008 via computerized telephone random digit dialing based on a
stratified sampling frame to ensure representation from the 5 counties.
28
The response rate for the
PHMC 2008 was 25% based on criterion #3 of the American Association for Public Opinion
Research.
29
While the response rate appears low it is important to note that this in and of itself is
not an indicator of survey quality. Recent research finds no significant biases as a result of
response rate.
30, 31
Moreover, the PHMC 2008 sample closely matches the demographic and
socioeconomic structure of the study counties as reported in the U.S. Census Bureau in their 3-
year 20062008 release of the American Community Survey (ACS)
32
and health screening rates
in the PHMC 2008 mirror those in the BRFSS 2008 data for Philadelphia. For example, 81
percent of women aged 50+ have had a mammogram within the past year according to the
BRFSS and 82 percent in PHMC.
33
A balancing weight is used in the statistical analysis.
Measures
We are interested in three outcomes. The first is whether a woman had a Pap smear test within
the past 2 years (coded 1 = Yes, 0 = No). The PHMC asked women How long has it been since
your last Pap test? and the response categories were one year or less, 12 years, 25
years, 510 years, more than 10 years, and never. At the time of the study, the American
College of Obstetricians (ACOG) and Gynecologists recommended Pap testing every 23
years.
34
Since the 25 year interval choice would include many women who were not screened
within the recommended interval, we chose to code only those reporting one year or less or
12 years as having received recommended screening. The second outcome of interest is
whether a woman had a breast examination by a doctor or health professional within the past
year as recommended (coded 1 = Yes, 0 = No).
34
The correlation between Pap testing and breast
examination in the PHMC sample is 0.45 (p<0.001). The third outcome included in the analyses
is a trichotomized variable measuring whether a woman had both tests (coded 2), had only
one of the two tests (coded 1), or no test (coded 0, reference group) according to the
recommended schedule. These three outcomes allow us to construct a more complete picture of
cancer screening behaviors among women and the role, if any, of health care system distrust.
We have five groups of independent variables. The primary predictor of interest is distrust,
which is measured by a 9-item scale developed by Shea et al.
22
The nine questions are rated on a
5-level Likert scale (strongly disagree, disagree, neither agree/disagree, agree, or strongly agree)
producing a possible distrust score range between 9 and 45. The reliability of the distrust scale
and subscales has been tested and reported elsewhere.
22
Using the 2008 PHMC data and factor
analysis with the varimax rotation method, we generated two standardized factor scores based on
the regression method capturing two different dimensions of distrust of health care system:
values distrust and competence distrust (the eigenvalues were 3.86 and 1.10 respectively and the
total variance explained was 55%). The regression method applies factor weights to create the
distrust scores centered on zero with a standard deviation of 1 (see Table 1). We categorized
each item into one of the two dimensions when the factor loading for that assigned dimension
was 0.5 or higher and the other factor loading was lower than 0.5. Table 1 includes the nine
questions and their factor loadings on each sub-scale, as well as the distributions of the factor
scores. Factor analysis not only takes into account the interdependency among the questions, but
also gives weights to each question to yield scales based on the empirical data. Our grouping is
similar to the original paper.
22
We imputed missing values based on an EM algorithm for
continuous variables
35
and the imputed scores were rounded to the nearest whole number to
reflect the Likert scales.

Table 1
Factor loadings with Varimax rotation.
A second group of variables are demographic predictors. Age was reported by the women and
treated as a continuous variable. Race/ethnicity is based on four categories (three dummy
variables in analysis): White (reference group), Black, Hispanic, and other race/ethnicity. Marital
status is based on three categories (two dummy variables): single (reference group), married or
cohabiting, and widowed, divorced, or separated.
Socioeconomic status (SES) factors form our third group of variables. Poverty status was based
on the 2008 federal poverty guideline where those women in households with incomes below the
poverty line are classified as poor (coded 1) and others (coded 0). Employment status was
trichotomized into employed, unemployed, and others (i.e. disabled or retired; reference group).
Educational attainment is measured by four dummy variables based on a five-category variable:
did not graduate high school (reference group), high school diploma, some college, an
associate/bachelor degree, and post college degree.
The fourth group of predictors relate to health care resources and insurance status. The women
were asked about their primary source of care grouped into: no regular health care provider,
private doctors office, public and community health center, and other source of care (e.g.,
outpatient clinic). Three dummy variables were created with no regular health care provider
serving as the reference group. Health insurance status was dichotomized into insured (coded 1)
and uninsured (coded 0).
The final group of variables concerns the womans health status. Self-rated health is based on a
question with four choices: excellent (reference group), good, fair, or poor. We also include self-
rated stress; in the PHMC this is a single scale from 1 to 10 to assess the experience of day-to-
day stress, where 1 indicated no stress and 10 extreme amount of stress. This measure has
been used in the absence of a complete inventory of stressful events.
36, 37
Including these
measures in the analyses captures aspects of both mental and physical health.
Analytical strategy
Our analysis is based on the use of both logistic and multinomial logistic regression models. For
the binary dependent variables (whether the women had a Pap smear, whether the women had a
clinical breast exam), we model the likelihood that the response is equal to 1 given a set of
explanatory covariates. For the trichomized dependent variable (the women had both tests, one
test, or no test), we use a multinomial logistic regression, comparing those women who report
both tests or just one test with the comparison category (no test), respectively.
Go to:
Results
Eighty percent of PHMC women 18 and older had a Pap test within two years and more than 70
percent had a breast examination by a doctor or health professional within a year (results not
shown). Table 2 presents descriptive statistics for all variables used in this study by the number
of screening services used (for dummy variables the proportions can be interpreted as
percentages). We provide data on the mean value of each variable for the overall sample and we
compare mean values between three subsamples: those women who had neither the Pap test nor
breast examination within the recommended time, those women who had one screening test, and
those women who had both. The comparisons of means between samples are shown in the last
column of Table 2. Several patterns are worth noting. First, both values and competence distrust
scores are lower among women with greater utilization of screening services. Specifically, the
values distrust of the women who reported having one or both tests is significantly lower than the
group of women who did not have either a Pap test or a breast examination (Both 0.083 vs. One
0.020 vs. Neither 0.103). Second, higher SES women utilize preventive health services more
than other women. For example, almost 17 percent of women who reported having both a Pap
test and a breast examination had a post college degree compared to 9 percent of women who
had no screening test, a difference that is statistically significant. Third, respondents whose usual
source of care was a private physicians office were more likely to have both Pap and breast
cancer screening tests than those with other types of sources of care. Finally, women with less
stress or better self-rated health also reported more utilization of cancer screening tests.

Table 2
Descriptive statistics overall and by number of screening services obtained in recommended time
interval


Table 3 presents the logistic regression results for utilization of Pap tests and clinical breast
examination. Competence distrust was associated with the odds of having a Pap test.
Specifically, a unit increase in competence distrust was associated with an 8 percent decrease in
the likelihood of having a Pap test (OR=0.916; 95% CI= 0.851, 0.986). The odds of having a Pap
test also was related to age, race/ethnicity, marital status, employment status, education, health
care resources, and personal health. For instance, having a regular source of care (regardless of
type) was associated with a 68~77 percent increase in the odds of having a Pap test. Controlling
for other covariates, each 10-year increase in age was related to a 24 percent decrease in the odds
of having a Pap test in the recommended time interval (0.973^10= 0.761).

Table 3
Logistic regression results modeling receipt of pap smear screening test and clinical breast
examination within the recommended time interval, N=5,268
With respect to breast cancer screening, only higher levels of values distrust are associated with
lower odds of receiving a clinical breast examination. Other things equal, the odds of having a
breast cancer screening decreased by roughly 8 percent with each one unit increase in values
distrust (OR=0.923; 95% CI= 0.864, 0.986). The determinants of having a clinical breast
examination are similar to those of having a cervical cancer test, i.e., demographic features and
health care resources. One of the potentially modifiable factors is insurance status. The odds of
having a breast examination among insured women were almost triple those of women without
insurance (OR=2.757; 95% CI= 2.179, 3.489).
Next, we used multinomial logistic regression to investigate whether distrust was related to the
number of preventive screening tests (Table 4). Compared to women without any screening tests,
values distrust was related to the likelihood of having one of these two tests, and both values and
competence distrust scores were negatively associated with the odds of receiving both services.
Specifically, one unit increase in values distrust would result in a 12.5 percent decrease
(OR=0.875; 95% CI= 0.790, 0.970) in the likelihood of having only one of the two preventive
tests. This association remained when comparing women with both tests (OR= 0.875; 95% CI=
0.800, 0.958). An association for competence distrust was found among those utilizing both
services; specifically, the odds of taking two tests would be reduced by almost 10 percent
(OR=0.914; 95% CI= 0.838, 0.997) if competence distrust increased by one unit.

Table 4
Multinomial regression results modeling the number of receipt of screening tests in the
recommended time interval versus none, N=5,268
There are several noteworthy additional findings. Economic factors and health status do not
appear to be associated with differences between having no screening test and having one; i.e.,
poverty, employment status, educational attainment, self-rated health, and stress were not
significant. Marital status, race/ethnicity, health insurance and source of care, however, were
associated with the difference between having no test and one test. When comparing those
women having both tests with those with none, we find that socioeconomic and health conditions
were important. Employed women and those with a college degree were more likely to have had
both recent breast and cervical cancer screenings. Self-rated health was also associated with
having both tests. Women who rated their health as fair or poor were about 35 to 40 percent less
likely to receive breast and cervical cancer screening. Moreover, employment status, having at
least a college education, and reporting fair/poor health are the main factors that account for the
differences between the two models in Table 4.
Go to:
Discussion
Our findings support the first hypothesis that high levels of health care system distrust among
women are associated with low utilization of cancer screening services, specifically Pap smears
and clinical breast examinations. However, our second hypothesis that both the values and
competence distrust scores were negative associated with cancer screening utilization was not
fully supported. Results suggest that different dimensions of distrust play a unique role in
understanding cancer screening usage; that is, high competence distrust was associated with low
odds of receiving Pap test screening and values distrust was negatively associated with the
likelihood of receiving a clinical breast examination. This difference is intriguing, and warrants
further investigation. Since women can be screened for breast cancer by both clinical breast
exam and mammogram, it could be the case that those who distrust their health care providers
integrity or ethics are more likely to opt to rely on the objective screening provided by
mammography. On the other hand, women who have doubts about the technical competence of
their health care provider may be reluctant to submit to an office-based laboratory test like a Pap
smear.
Independent of other covariates, health care resources and personal health were associated with
womens utilization of cancer screening. If women have a regular source of care they are more
likely to receive and act on the recommendation to have a regular Pap test and clinical breast
examination.
38
Women with a regular source of care may have frequent interactions with the
health care system (i.e. insurance company and health providers) and these interactions may
promote the trustworthiness of health care environment and hence lessen competence distrust.
26

As mentioned above, the differences between the two models in Table 4 indicate that
employment status, education and self-rated health are important factors associated with the
utilization of cancer screening. Consistent with other research we find that higher educational
attainment is associated with the dissemination and adoption of information on the importance of
preventive health services;
39, 40
respondents with at least college education are more likely to
receive both, rather than one of, cervical and breast cancer screenings than their counterparts.
Similarly, perhaps women with fair/poor self-rated health may not seek screening because of
concerns about the discovery of cancers.
This study of Philadelphia women documents a significant association between distrust and
utilization of breast and cervical cancer screening tests, net of other factors. While employing
different measures of distrust, this study corroborates a recent paper that concluded that different
dimensions of trust in the health care system had unique relationships with the use of preventive
health services among older black and white adults in Pittsburgh.
11
Our findings are consistent
with studies exploring determinants of cancer screening. For example, we found that Black
women were 1.5 to 2 times and 50 percent more likely than White women to have Pap tests or
breast examinations. Hispanic women were also 50 percent more likely to have a Pap test (Table
3) than White. These findings echo those of a recent study.
25
Being married or living with a
partner facilitated the use of cancer screening services. Again, similar findings have been
documented elsewhere.
5, 11, 41, 42

This study has several limitations. First, the survey data come from women in the Philadelphia
metropolitan area and the findings may not be generalizable to women in other areas, although
the findings are in line with research conducted in similar settings. Second, the PHMC does not
provide specific information on levels of respondents trust in their primary health providers and
thus the intertwined association between trust in physicians and health care system distrust
cannot be separated. Third, as noted earlier, the wording and classification of time intervals for
the Pap test question does not permit a direct comparison with recommended screening
guidelines. Fourth, this study is cross-sectional, which precludes looking at cause and effect
relationships over time. Fifth, while the balancing weights were constructed accounting for
phone type and sociodemographic features,
43
non-response bias is another possible source of
errors. Finally, the data are self-report and therefore subject to recall bias and other measurement
errors.
44, 45

Several policy implications emerge from this study. As distrust plays an important role in the
utilization of cancer screening tests, rebuilding levels of trust in the health care system among the
American public should be a priority. The values and competence distrust in the health care
system has been a barrier to public health research.
46
Maintaining a high level of service quality
and responsiveness (i.e. reducing medical errors, providing transparency to patients) may reduce
both competence and values distrust
47
and in turn may increase the utilization of cancer
screening tests. This could be an example of how macro-level changes can influence individual
behaviors.
As found in this study, having a regular source of care, regardless of type, may increase the
opportunity for advice and compliance with cancer screening test recommendations. Even
though there is an increased vulnerability to cancer with age, older women are less likely to
receive screening tests. Promoting earlier and regular screening can lead to early detection and
will reduce cancer morbidity and mortality within American women.
This study used a recently developed health care system distrust scale to investigate the effects of
different dimensions of distrust on breast and cervical cancer screening. The results indicate that
competence and values distrust are associated with the likelihood of recommended use of
screening tests, even after controlling for other competing covariates. Health care system distrust
was found to be a barrier in the utilization of preventive health services. In addition to traditional
demographic and socioeconomic determinants, future research should include measures of
distrust so as to better understand patterns and determinants of cancer screening.
Go to:
Contributor Information
Tse-Chuan Yang, The Social Science Research Institute, The Pennsylvania State University, 601
Oswald Tower, University Park, PA 16802, Email: tuy111@psu.edu, Tel: 814-865-5553.
Stephen A. Matthews, The Department of Sociology, The Pennsylvania State University, 601
Oswald Tower, University Park, PA 16802.
Marianne M. Hillemeier, The Department of Health Policy and Administration, The
Pennsylvania State University, 601 Oswald Tower, University Park, PA 16802.
Go to:
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Cancer. 1998]
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Aff (Millwood). 2004]
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use. [Am J Public Health. 2006]
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and white adults. [Am J Public Health. 2009]
Development and testing of the health care system distrust scale. [J Gen Intern Med.
2004]
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Gen Intern Med. 2008]
Development of a revised Health Care System Distrust scale. [J Gen Intern Med. 2008]
Demographic predictors of clinical breast examination, mammography, and Pap test
screening among older women. [J Am Acad Nurse Pract. 1996]
Trust in the health care system and the use of preventive health services by older black
and white adults. [Am J Public Health. 2009]
Review Cancer screening in the United States, 2008: a review of current American
Cancer Society guidelines and cancer screening issues. [CA Cancer J Clin. 2008]
Distrust and poor self-reported health. Canaries in the coal mine? [J Gen Intern Med.
2006]
Distrust of the health care system and self-reported health in the United States. [J Gen
Intern Med. 2006]
ACOG Committee Opinion No. 357: Primary and preventive care: periodic assessments.
[Obstet Gynecol. 2006]
Development of a revised Health Care System Distrust scale. [J Gen Intern Med. 2008]
The role of social and built environments in predicting self-rated stress: A multilevel
analysis in Philadelphia. [Health Place. 2010]
Review Reported drop in mammography : is this cause for concern? [Cancer. 2007]
Distrust and poor self-reported health. Canaries in the coal mine? [J Gen Intern Med.
2006]
Review Cancer screening in the United States, 2009: a review of current American
Cancer Society guidelines and issues in cancer screening. [CA Cancer J Clin. 2009]
Contextual analysis of breast and cervical cancer screening and factors associated with
health care access among United States women, 2002. [Soc Sci Med. 2008]
Trust in the health care system and the use of preventive health services by older black
and white adults. [Am J Public Health. 2009]
Review Cancer screening in the United States, 2008: a review of current American
Cancer Society guidelines and cancer screening issues. [CA Cancer J Clin. 2008]
Demographic predictors of clinical breast examination, mammography, and Pap test
screening among older women. [J Am Acad Nurse Pract. 1996]
National trends in the use of preventive health care by women. [Am J Public Health.
1989]
Breast cancer screening practices among users of county-funded health centers vs women
in the entire community. [Am J Public Health. 1992]
Accuracy of self-report of mammography and Pap smear in a low-income urban
population. [Am J Prev Med. 1998]
Review The accuracy of self-reported health behaviors and risk factors relating to cancer
and cardiovascular disease in the general population: a critical review. [Am J Prev Med.
1999]
Distrust, race, and research. [Arch Intern Med. 2002]
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PMC3060184

CMAJ. 2011 March 22; 183(5): 563568.
doi: 10.1503/cmaj.101156
PMCID: PMC3060184




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CMAJ >
v.183(5); Mar 22, 2011 >
PMC3060184

CMAJ. 2011 March 22; 183(5): 563568.
doi: 10.1503/cmaj.101156
PMCID: PMC3060184
Management of Papanicolaou test results
that lack endocervical cells
Lizette Elumir-Tanner, MD and Meghan Doraty, BHSc, for the Southern Alberta Primary Care Research
Network (SAPCReN)
Author information Copyright and License information
Go to:
The case
Mrs. McTavish is a 25-year old patient whose Papanicolaou (Pap) test results have come back
from the laboratory. The smear is described as satisfactory for evaluation; however, it is noted
that an inadequate number of endocervical cells were present in the sample. The results of the
patients past Pap tests have been satisfactory for evaluation and negative for abnormality. She is
otherwise well. Her physical examination, including pelvic examination, showed nothing
unusual.
Rates of cervical cancer have been declining in Canada since the implementation of the
Papanicolaou (Pap) smear, with reduction in both incidence (from 11.1 per 100 000 in 1970
1972 to 5.2 per 100 000 in 19941996) and mortality (7.9 per 100 000 in 19531955 to 1.9 per
100 000 in 19951997).
1
Further improvements will depend on the continuance of screening for
cervical cancer and the effectiveness of screening tools. The Bethesda System the
conventional system for reporting cervical cytologic diagnoses provides feedback about
specimen adequacy using the categories satisfactory or unsatisfactory.
2
Primary health care
providers may receive Pap test results that are identified as satisfactory but accompanied by a
note that indicates a sample from the transformation zone is lacking. Some provincial and
national guidelines are unclear about how clinicians should respond to this type of report.
Because of this uncertainty, we sought to review the current evidence on the topic. How should a
care provider proceed with screening when faced with an otherwise satisfactory Pap smear that
lacks sampling from the transformation zone? If physicians continue with regular screening
intervals without special attention to the lack of endocervical cells, are cervical abnormalities
being missed?
Go to:
Literature review
We searched MEDLINE from 1975 to the end of July 2010 using the following combination of
keywords and subject headings: unsatisfactory Pap smear, endocervical component,
endocervical status, endocervical cells and Pap smear, Pap smear and quality and
abnormal Pap smear. Bibliographies from the identified articles were manually searched.
Summary sites such as Towards Optimal Practice (Alberta) and Cancer Care Manitoba were also
reviewed in July 2010. We identified 462 citations, and reviewed 53 full-text articles. Papers
were excluded if they were written in a language other than English, if they did not discuss the
topic of Pap smear quality and presence or absence of endocervical cells, and if there were
insufficient data to draw conclusions. Twenty-four articles were included in our review and are
summarized in Appendix 1 (available at www.cmaj.ca/cgi/content/full/cmaj.101156/DC1).
The level of evidence was determined by the hierarchy developed by the Canadian Task Force
on the Periodic Health Examination,
3
according to which the highest level of evidence (Level I)
derives from at least one randomized controlled trial, and the lowest level derives from the
opinion of experts (Level III). The evidence identified in our search was predominantly Level II,
indicating that the literature contained mainly cohort, cross-sectional and casecontrol studies.
No randomized controlled trials, systematic reviews or meta-analyses were found.
Go to:
What is an adequate sample?
The effectiveness of screening using the Pap smear relies on adequate sampling from the cervix.
1

Although a conclusive definition of adequate sample remains elusive, the retrieval of
endocervical cells from an area of the cervix known as the transformation zone or
squamocolumnar junction, from which most abnormalities arise,
4
has historically been
considered an indication of quality.
5
Some older studies
514
have shown a relationship between
the presence of endocervical cells and the identification of cervical abnormality. Such findings
are consistent with the hypothesis that samples with endocervical cells are more likely to detect
atypia. However, more recent research
1528
has shown that the absence of endocervical cells is
not necessarily associated with a higher risk of cervical abnormality.
Go to:
What do the guidelines recommend?
Not all provinces and territories in Canada have guidelines for screening for cervical cancer or a
screening program (Table 1). Of those that do,
2935
most do not definitively address how to
respond to a Pap smear result when it lacks a sample from the transformation zone. Guidelines in
Nova Scotia
34
and in Manitoba
32
suggest early repeat testing may not be necessary. The recently
revised guidelines in Alberta
29
note that the sample may still be satisfactory if endocervical cells
are missing.

Table 1:
Clinical guidelines for treatment when transformation zone cells are not present in sample
International guidelines vary. Recent guidelines from the United Kingdom
36
recommend testing
every three years for women aged 25 to 49 years, but make no mention of what to do should
results not include endocervical cells. Australian guidelines,
37
which recommend screening every
two years, cite retrospective cohort studies and note that the quality of a smear is not determined
by the presence or absence of endocervical cells. The American Cancer Society
38
recommends
annual repeat screening for women whose Pap smears show no endocervical cells, or earlier
repeat testing for certain women. These guidelines do not clarify which women qualify for early
repeat testing; this ambiguity may cause confusion for physicians about who and when to retest.
Go to:
What is the evidence?
The debate regarding the significance of endocervical cells was sparked when initial research
found that the presence of endocervical cells on a smear was related to an increase in detection of
abnormalities of the cervix.
510,12,13
One study
8
assessing the cytologic histories of 376 women
diagnosed with invasive carcinoma of the cervix found that endocervical cells were seen less
often in smears reported as negative (45.5%) than in those with atypia (84.4%) and those with
cervical intraepithelial neoplasia (97.8%). This difference was significant (p < 0.001), suggesting
that the composition of the smear was related to the detection of abnormalities. To best identify
atypia, the authors argued, a repeat test is necessary.
Further studies verified this finding. Another study
10
reviewed 36 853 Pap smears to investigate
the effect of the presence or absence of endocervical cells on the detection rate of abnormalities,
with the result that cervical intraepithelial neoplasia (CIN) was detected 2.3 times more often in
smears with endocervical cells. Two further studies reviewed false-negative Pap smears from
patients who had a confirmed diagnosis of cervical cancer. Many of these smears (35 of 94
[37%]
12
and 30 of 47 [64%]
13
) were missing endocervical cells. Based on this evidence, it
became standard practice for physicians to sample endocervical cells to improve the chances that
abnormalities were caught and to test repeatedly as deemed necessary when endocervical cells
were not present.
However, recent retrospective studies
15,21,23,24
assessed the effect of the presence or absence of
endocervical cells on the rate of detection of abnormalities by comparing the concordance
between cytology (assessed by Pap smear) and histology (assessed by colposcopic examination).
One study
23
examined 151 instances of histologically diagnosed CIN II and III and retrieved the
Pap tests to determine discordant, or false-negative, cases. Of the 13 Pap tests lacking an
endocervical component, only 3 (23%) were discordant, whereas of the 138 Pap tests with an
endocervical component, 38 (27%) were discordant. There was no significant difference between
these groups (p > 0.5), suggesting that the inclusion of an endocervical component within a
smear does not guarantee that an existing abnormality will be detected. Other casecontrol
studies
17,18,20,25
support this finding. Thus an endocervical component may not be a good
indicator of specimen quality, and its lack may not indicate that early repeat testing is necessary.
The most convincing evidence, however, is found in longitudinal studies in which patients were
prospectively evaluated for the presence of endocervical cells and for subsequent abnormal Pap
smears.
16,22,26,27
Methods of reporting cervical atypia have changed over the years, so among
these studies, the measured outcome varied (i.e., CIN v. low-grade squamous intraepithelial
lesion v. atypia). As well, the length of follow-up differed among studies. However, the essence
of the findings was consistent: women whose Pap smears did not contain endocervical cells were
not at higher risk for subsequent detection of cervical abnormalities than those whose smears did
contain endocervical cells.
Perhaps the most convincing longitudinal study was performed by Mitchell in 2001.
22
Four
cohorts of women who had an initial negative Pap smear and a subsequent Pap smear three years
later were studied. Endocervical cells were present in both entry and exit smears in cohort A (n
=18618); endocervical cells were absent in the entry smear and present in the exit smear in
cohort B (n = 16 632); endocervical cells were present in the entry smear and absent in the exit
smear in cohort C (n = 16 291); and both smears had absent endocervical cells in cohort D (n =
8603). One would expect a higher incidence of disease in cohort B compared with cohort A,
given that cohort B would be more likely to exhibit missed abnormalities in the entry smear
because of the lack of endocervical cells. This was not the case; cohort B had no more histologic
high-grade disease than cohort A (standardized incidence ratio for cohort B compared with
cohort A 0.89, 95% confidence interval [CI] 0.671.12). This result suggests that the absence of
an endocervical component is not linked to increased rates of subsequent abnormality for both
histologic and cytologic outcomes. The author concluded that early repeat testing is unnecessary.
Another key finding in Mitchells study was that cohorts B, C and D showed less disease than
cohort A. This finding raises a new question: Does the presence of endocervical cells actually
indicate a greater risk of cervical abnormality? Mitchell and Medley suggested in an earlier
study
17
that the transformation zone may be more easily sampled when abnormality is present
because of the reduced adhesiveness of cells. A recent blinded, comparative cross-sectional
study
14
showed that cervical smears with a higher number of endocervical cells (> 50 cells) was
significantly associated with the presence of at least 10 squamous atypical cells (odds ratio 2.87,
95% CI 1.545.35). This finding suggests that there is a positive association between the number
of endocervical cells and the number of atypical cells in a smear, and supports the hypothesis
that endocervical cells may be more accessible in cervices with abnormalities. The presence of
these cells may be a marker in women with a greater risk of cervical abnormality, indicating a
higher risk for disease. However, more research is needed to explore this hypothesis.
Although the longitudinal studies described present the strongest evidence available, some
limitations do exist with this type of study. Other explanations for their findings are possible. For
example, in longitudinal studies with cytologic follow-up, Pap smears without endocervical cells
may be less sensitive than those with endocervical cells. Thus, abnormalities may be missed on
subsequent Pap tests that do not include an endocervical component. In longitudinal studies with
histologic data, only positive cytologic results are usually verified. If Pap tests without
endocervical cells are less sensitive, these test results are less likely to be subject to histologic
verification. As a consequence, verification bias may occur, giving the impression that such
women are at low risk for cervical abnormalities when they are actually not. Studies with shorter
follow-up periods are more prone to this bias. More research is required to address these
concerns.
Go to:
Should women whose Pap smears lack endocervical cells be
retested?
Studies using multiple methodologies have attempted to determine the role of endocervical cells
in Pap tests in the detection of cervical cancer, but the conclusions of these studies have often
been contradictory. According to the criteria of the Canadian Task Force on Preventive Health
Care,
39
contradictory evidence receives a C grade, meaning that no recommendation can be
made. However, the majority of recent, rigorous and validated studies support the view that the
presence of endocervical cells is not necessary for a Pap smear result to be valid and may
possibly be a risk factor for cervical abnormality. As such, this body of research represents fair
evidence to recommend avoiding early repeat testing for those women whose Pap smears are
negative and do not contain an endocervical component.
Go to:
Are there differences among Pap smear sampling
techniques?
Efforts have been made to improve the sampling methodology for the collection of adequate Pap
smear samples. Over the years, accepted sampling techniques have changed. Studies included in
our review used a variety of sampling techniques, such as wooden spatula and cotton swab
19,25

and Thin-Prep Pap tests.
23
Many of the studies we reviewed did not differentiate among
sampling techniques. However, Mitchell and Medley
16
found that using a combination of
cytobrush and spatulae, compared with just using spatulae, improved the probability of having
endocervical cells reported in the sample. It is not known, however, whether different sampling
techniques affect detection rates of atypia depending on the presence or absence of endocervical
cells. Therefore, we suggest that clinicians continue to use the sampling technique recommended
by guidelines in their area.
There may be other factors that influence the collection of an adequate sample. For instance, the
Alberta guidelines
29
suggest some conditions for optimal collection, including the stipulation that
patients refrain from use of contraceptive creams or jellies, douching, intravaginal medication
and sexual intercourse for 24 hours before the test. However, a review of the evidence
underlying these recommendations is beyond the scope of this paper. To optimize the collection
of a specimen, clinicians should follow the manufacturers directions.
Go to:
Gaps in knowledge
This review is not designed to posit a biological mechanism that might explain the contradictory
claims of the studies examined. Future inquiry may seek to validate the hypothesis of Mitchell
and Medley
17
that when atypia is present, endocervical cells slough off the transformation zone
more readily, which accounts for their frequent presence in positive samples. Testing other
hypotheses that seek to reconcile the contradictory evidence is also important for a full
understanding of the role of endocervical cells in the development of cervical cancer. Various
sampling methods were used in the studies examined by this review, but this paper does not
address the effectiveness of different sampling techniques.
More studies are needed to determine whether there is a higher incidence of invasive cervical
cancer among women whose Pap smears lack endocervical cells. Prospective, longitudinal
studies of longer duration, encompassing the onset of atypia to the development of cervical
cancer, would also benefit this area of study. A close examination of regional guidelines is also
recommended to ensure that the most accurate and up-to-date information from rigorous research
is being relayed to practitioners.
Go to:
The case revisited
Mrs. McTavish returns to review her Pap test results. Her physician assures her that the result is
normal and that there will be no change in the scheduling of her screening Pap tests. She
wonders about the meaning of the phrase inadequate number of endocervical cells present
included in the report. The physician explains that there is a zone in the cervix from which most
abnormalities arise. There has been some suggestion that, when there is a lack of these
endocervical cells on a Pap smear, perhaps this zone was not adequately sampled. However, a
balance of research articles shows that a lack of endocervical cells on a Pap test result does not
lead to an increased risk of abnormality for someone like Mrs. McTavish. Therefore, Mrs.
McTavish can continue with regularly scheduled Pap tests. Local guidelines should be consulted
to determine the timing of the next Pap test.
Go to:
Conclusion
Based on the strongest evidence available, when a physician is confronted with a Pap smear
result lacking endocervical cells, an appropriate course of action would be to schedule the patient
for regular testing unless there is suspicion of abnormality, such as abnormal bleeding or other
clinical indicators of cervical abnormality. The patient would not be required to undergo an
uncomfortable and invasive procedure a second time. Minimizing unnecessary procedures can
save the health system considerable expenditures in the form of physician time, testing supplies,
laboratory analyses and other costs. It would be helpful for clinicians if provincial and national
guidelines were updated to reflect recent research in this area. Local guidelines, however, are an
excellent resource for best practices in Pap smear techniques.
Key points
Some provincial, national and international guidelines are unclear about how to proceed when a
Papanicolaou smear result is reported as lacking a sample from the transformation zone.
Although controversy exists in the literature, the majority of recent rigorous studies do not
support early repeat testing for women whose smears lack a sample from the transformation
zone.
Unless abnormality is suspected or there are risk factors for cervical dysplasia, such patients may
be scheduled for testing at regular screening intervals.
Go to:
Supplementary Material
[Online Appendix]
Click here to view.
Go to:
Acknowledgements
The authors thank Neil Drummond, Tyler Williamson, Behnaz Somji and members of the
Southern Alberta Primary Care Research Network for their help in the development of this
paper.
Go to:
Footnotes
Competing interests: None declared.
This article has been peer reviewed.
Contributors: Both of the authors contributed to the planning and design of the article, the
review of the literature, and the drafting and revision of the manuscript. Both of them approved
the final version of the manuscript submitted for publication.
Go to:
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Oncol Lett >
PMC3406457

Oncol Lett. 2011 July; 2(4): 701706.
Published online 2011 April 6. doi: 10.3892/ol.2011.290
PMCID: PMC3406457
Prevalence of human papillomavirus in
university young women
MARIA T. MONTALVO,
1
ISMELDA LOBATO,
1
HILDA VILLANUEVA,
1
CELIA
BORQUEZ,
1
DANIELA NAVARRETE,
2
JUAN ABARCA,
3
and GLORIA M. CALAF
4,5

Author information Article notes Copyright and License information
Go to:
Abstract
Cervical cancer is the second most prevalent female cancer worldwide. The majority of cases
appear between the age of 30 and 50. Human papillomavirus (HPV) plays a central role in
cervical cancer with 99.7% of HPV DNA identified in invasive cervical carcinomas. The
prevalence of the HPV infection varies substantially among countries and according to age and
lifestyle. HPV is a common sexually transmitted infection among males and females with a 70%
higher incidence in sexually active females. This study aimed to determine the prevalence of
human papillomavirus in young university women by analyzing the correlation between
Papanicolaou (PAP)-stained cervical tests and HPV detection by genotyping, as well as other
risk factors. A total of 200 women aged between 18 and 25 years were enrolled in this study,
which took place between September 2008 and May 2009 at the Universidad de Tarapac, Arica,
Chile. Results of the PAP smears showed that 97.5% of cells had normal characteristics,
although an inflammatory pattern was noted. The prevalence of generic HPV infection was 3.5%
when testing for HPV DNA using the polymerase chain reaction (PCR) method. An analysis of
the genotype of infected female individuals indicated that high-risk HPV types, such as HPV 16
and 31 were present in 42.84 and 14.29% of females, respectively, and low-risk types such as
HPV 6, in 14.29%. Only one sample with differentiated non-HPV (14.29%) was found. A 95%
correlation between PAP-stained cervical tests and the method of testing for HPV was observed.
Using the PCR method, it was found that of the 195 negative PAP smears, 5 were positive for
HPV and two of the samples that were positive for ASC-US were also positive. A significantly
increased (P<0.05) HPV infection risk was observed in the 1821 age group with a higher
prevalence (71.40%) when compared to the 2225 age group (28.6%). A significant (P<0.042)
difference was found between smoking and HPV infection. In conclusion, a significant (P<0.05)
correlation was found between PAP and PCR methods for HPV testing in young university
women. A significant correlation between smoking and HPV was detected, whereas no
difference was noted with other parameters.
Keywords: human papillomavirus, prevalence
Go to:
Introduction
Cervical cancer is the second most prevalent female cancer worldwide with 493,000 new cases
occurring every year and 80% occurring in developing countries (1,2). The majority of cases
appear between the age of 30 and 50. Human papillomavirus (HPV) plays a central role in
cervical cancer with 99.7% of HPV DNA identified in invasive cervical carcinomas (3,4). The
prevalence of HPV infection varies substantially among countries and according to age and
lifestyle. HPV is a common sexually transmitted infection among men and women with a 70%
higher incidence in sexually active females. The majority of HPV infections are asymptomatic
and transient, especially in the young population. Up to 98% of cervical cancers in females are
positive for HPV and more than 90% of new infections appear to induce high-grade cervical
neoplasia (5,6). HPV prevalence is age-dependent with a peak in women below the age of 25 and
a second peak in women over the age of 55 (710). Risk factors include smoking, drinking,
education, number of partners, diet, nutrition, long-term oral contraceptive use,
immunosuppression and age of first coitus. Reduced participation in screening is a probable
cofactor that should be considered in an analysis of HPV in cervical female cancer (1116).
There is an important public health concern for the control of HPV infection and the
development of cervical female cancer in various countries. In the United States, cervical
cytology screening has proven to be successful, since deaths from invasive cervical cancer have
decreased by over 70%. In other countries with screening programs, cervical cytology screening
has significantly reduced both incidence and mortality. Cervical cancer is currently considered to
be completely preventable with universal cervical cytology screening and treatment. However, a
number of limitations to current cervical cancer prevention programs exist such as racial and
ethnic disparities in cervical cancer screening (17).
HPV is a member of the papillomavirus family. It is 5255 nm in size, and is a non-enveloped
virus with circular double-stranded circular DNA and a genome of approximately 7,900 base
pairs with eight overlapping open reading frames. The late genes (L1 and L2) and early genes
(E6, E7, E1, E2, E4 and E5) that are expressed in more than 100 different HPV genotypes have
been identified based on differences in DNA sequence. These HPV types can be classified
according to various criteria such as their tissue tropism, oncogenic potential and phylogenetic
position using molecular biology techniques (18). At least 40 of these HPV genotypes infect the
epithelial lining of the anogenital and aerodigestive tract, since different studies have shown that
infection with high-risk HPV precedes the development of cervical premalignant disease in
women with cervical cancer. Based upon epidemiological studies, HPV viruses are classified as
high-risk (HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56 and 58) and low-risk (6, 11, 13, 40,
42, 43, 44, 54, 59, 61, 70, 72, 81 and CP108). Several HPV types, such as 16, 18 and 59, have
been implicated in cervical female cancer, and other types, such as HPV 6 and 11, are frequently
detected in benign lesions such as condylomata. Female individuals infected with low-risk HPV
types have a minimal possibility of developing cervical cancer. The World Health Organization
has officially designated HPVs 16 and 18 as carcinogenic agents. In Asia, HPV 58 and 52 are the
most common after HPV 16 and 18. However, HPV infection by multiple genotypes has been
reported to occur in 1020% of HPV-positive cases (1922). HPV 16 is the most common
oncogenic type in preinvasive and cervical cancer, detectable in 21% of women with low-grade
squamous intraepithelial lesions (LSIL) and in more than 50% of women with cervical
intraepithelial neoplasia grade 3 (CIN 3). HPV 18 causes 1015% of CIN 3 and also causes more
than 35% of cervical adenocarcinomas, which are difficult to detect by current screening
methods (23).
Traditional screening for HPV infection is crucial, but early detection can be difficult for most
cervical infections since HPV is asymptomatic. Many countries possess a screening program for
HPV, involving the traditional protocol based on the Papanicolaou smear introduced in 1943,
which uses a cytological staining technique. However, the high number of false negatives
(between 1550% for cervical premalignant lesions and cervical cancer) and false positives
(30%) should be considered (24,25). Cytology examinations have limitations with regards to
specificity and low predictive value for high-grade pathology (26,27). However, PAP smears
have been shown to significantly decrease the incidence of cervical cancer in developed
countries. The introduction of cervical screening programs is an important target in cervical
cancer research since it involves improving the detection of precancerous lesions and reducing
equivocal results by employing better collection, preparation, and testing methods (28).
Highly sensitive methods have been developed to detect HPV such as the polymerase chain
reaction (PCR) method, which in in vitro conditions can amplify the DNA sequence present in a
clinical specimen. This method can detect as little as one molecule of HPV DNA in 10
5
cells,
and is considered the most sensitive HPV detection technique worldwide (29). PCR is based on
the use of primers such as the MY09/MY11 primer set (MY-PCR), which is the most frequently
used amplification system for the detection of the virus in clinical samples. This set is
synthesized with several nucleotides in each primer and then mixed with 25 primers including
HMB01M, which amplify a wide spectrum of HPV-types. MY09/MY11 has been used in studies
predominantly in North and South America as well as in Asia (3033). This study aimed to
determine the prevalence of human papillomavirus in young Chilean university women by
analyzing the correlation between PAP-stained cervical tests and PCR for HPV detection by
genotyping and whether other risk factors were involved.
Go to:
Materials and methods
A total of 200 females aged 1825 with a mean age of 21.55 participated in the study between
September 2008 and May 2009 at the Universidad de Tarapac, Arica, Chile. Written informed
consent was obtained from each female patient. Papanicolaou (PAP)-stained cervical tests (PAP)
were included in this transversal study that was complemented with a standardized questionnaire.
The information obtained included socio-demographic data such as age, marital status, use of
contraceptives (condom, oral contraceptive), number of vaginal deliveries and sexual habits.
Cervical cell samples were collected with a cytobrush from the ectocervix and endocervix of
each woman and samples were preserved in SurePath

preservative fluid and methanol. The test


tube was closed and sent to a molecular biology laboratory to be stored at 4C.
Papanicolaou (PAP)-stained cervical tests
PAP smears were obtained from the endocervix and ectocervix by scraping the squamous
columnar cells with a wooden Ayres spatula. Cervical scraping was then performed by using a
cytology brush to spread the samples over designated slides for each patient. The slides were
fixed with ethanol and colored by PAP technique. The samples were examined under a
microscope by a pathologist and classified by the Bethesda system: ASC-US: consisting of
atypical squamous cells of undetermined significance; LSIL: low-grade squamous intraepithelial
lesion (CIN 1) and HSIL: high-grade squamous intraepithelial lesion (CIN 2 and CIN 3).
Polymerase chain reaction for HPV
The primers used in the PCR assay for HPV were: MY09 (5CGT CC (AC) A (AG)(AG) GGA
(AT)AC TGA TC 3) and MY11 (5 GC(AC) CAG GG(AT) CAT AA(CT) AAT GG 3). The
primers used for -globin were: PCO3 (5 ACA CAA ACT GTG TTC ATC AGC 3) and PCO5
(5 GAA ACC CAA GAG TCT TCT CT 3) to detect and genotype HPV DNA. Each primer is
specific to a DNA segment and when the target sequence is present the primers anneal and allow
in vitro replication of nucleotides. Cycles of heat denaturation, annealing and synthesis allow for
the exponential accumulation of the specific target sequence.
Statistical analysis
Categorical data were analyzed for statistical significance by an analysis of all variables that
included a Chi-square test. P<0.05 was considered to be significant, and when appropriate, the
Fishers exact test was included. The coefficient was used to assess the degree of agreement
between the two tests. Odds ratio prevalence and 95% confidence intervals were calculated as
approximations of the relative risk by logistic regression. The dependent variables were the
results of PAP smears and the PCR method. The independent variables were socio-demographic
characteristics, such as marital status.
Go to:
Results
The prevalence of human papillomavirus in young university women was analyzed by
correlation between PAP-stained cervical tests and PCR for HPV detection by genotyping. Other
risk factors were also considered and found to be involved. A total of 200 university women
were enrolled in the study with a mean age of 21.55 years and an age range between 18 and 25
years. The mean age of first coitus was 17.22 years with an age range between 13 and 25 years
and the mean number of sexual partners since the first coitus was 2.62 with a range of between 1
and 15 partners. PAP smears in 97.5% (195/200) of 200 samples were normal. However, the
normal examinations showed an inflammatory pattern, which is a possible etiology agent that
was found in 2.56% (5/195) of Candida sp. and 0.51% (1/195) of Trichomona vaginalis. Of the
positive cases, 2.5% (5/200) showed an inflammatory pattern; 2 cases had atypical squamous of
undetermined significance (ASC-US) and 3 had low-grade squamous intraepithelial lesion
(LSIL), as shown in Table I. The prevalence of generic HPV infection, using the PCR method,
was 3.5% (7/200) for HPV DNA (Table I). Genotyping showed high-risk HPV types; HPV 16
was detected in 42.84% (3/7) of infected women and HPV 31 in 14.29% (1/7). Low-risk HPV
types were also identified, such as HPV 6 in 14.29% (1/7) and HPV type 59 in 14.29% (1/7).
Only one sample with HPV was not differentiated (14.29%). The distribution of HPV-types in
each positive sample using the PCR method is shown in Table I.

Table I
Papanicolaou (PAP) smear and HPV detection in 200 Chilean University women.
The correlation between the PAP smear and PCR methods of detecting HPV DNA was
significantly high (95%) (P<0.05). Using the PCR method it was found that of 195 negative PAP
smears, 5 were positive for HPV and 2 of the samples that were positive for ASC-US were also
positive. Results of the PAP smears showed that 3 samples were positive for LSIL, but these
samples were in fact found to be negative using the PCR method (Table II). To investigate the
relevance of risk factors other than HPV, a statistical analysis was performed by adjusting the
HPV prevalence by PCR using unconditional logistic regression. Table III indicates risk factors
associated with the number of sexual partners. The age group was an important risk factor for
HPV infection (P=0.05) since a significantly increased risk was observed in the 1821 age group
(OR=2.47; 95% CI=1.0213.06) with a higher prevalence (71.40%) when compared to the 22
25 age group (28.6%). No correlation was found with the age of first coitus (P>0.05); even
though the risk factor was important (OR=2.03; 95% CI=0.2719.82) with the first coitus (<18
year old), no statistical difference was observed. A non-significant risk was observed with the
other parameters. Table IV shows the risk factors associated with lifestyle. A significant
(P<0.042) difference was found between smoking and HPV infection. An increased risk was
found in females who reported to be tobacco smokers (OR=6.87; 95% CI=1.9540.57). No
significant correlation was found with other parameters.

Table II
Correlation between Papanicolaou (PAP) smear and HPV detection in 200 Chilean University
women.

Table III
Papanicolaou (PAP) smear HPV detection and risk factors in 200 Chilean University women.

Table IV
Correlation between Papanicolaou (PAP) smear HPV detection and risk factors in 200 Chilean
University women.
Go to:
Discussion
The prevalence of human papillomavirus in 200 young Chilean university women was analyzed
with regards to the correlation between the PAP smear and PCR method of HPV detection by
genotyping. Other risk factors involved were also analyzed. Using the PCR method, it was found
that there was a 3.5% prevalence of HPV infection in students, which is lower than the data
reported in other countries in South America, such as Mexico with 14.5%, Costa Rica with 16%
and Colombia with 14.8% (10,3435). Prevalence of the HPV infection was 26 and 20% in
Nigerian and Taiwanese women, respectively (35). However, the prevalence in the present study
is similar to that found in Spanish and Bolivian studies, at 3 and 5.2%, respectively (36,37). The
lower prevalence found in this study can be explained by differences in the characteristics of the
population, where variability exists between HPV prevalence as described in numerous studies
(38). It can be observed that each study has a different experimental design in different parts of
the world, such as sample collection and different methods are used for HPV detection and
typing. In the United States, 64% of teenagers were found to be infected, a percentage similar to
that found in Korean prostitutes and female individuals with cervical lesions in Brazil (47 and
43%, respectively) (42). In contrast, a prevalence as low as 314% has been found in married
women from Spain and Amazonian women from Bolivia (36,37,3942). In Chile, the incidence
rate was 29 per 100,000 and the prevalence was 14%, which compares to data from studies in
Mexico (14.5%) and Colombia (14.8%), but the prevalence in Chile was higher than in many
other parts of Europe (10,34,43,49).
Results of the present study showed four types of HPV in six out of seven patients who were
positive, diagnosed using the PCR method, the other patient being of unknown type (14.29%).
Four patients (57.13%) were infected with one of the high-risk HPV types; three with type 16
(42.84%) and one with type 31 (14.29%). Only two patients (28.58%) were infected with a low-
risk type; one with type 6 (14.29%) and one with type 59 (14.29%). No mixed-type infections
were detected by the PCR method. The high-risk HPV types found in this study have also been
described in other studies in association with cervical cancer (2,44) with a predominant HPV
type 16 infection. This type of virus has also been considered of high-risk for cervical carcinoma
by other authors (45). The prevalence of HPV, diagnosed using the Papanicolaou method, was
2.5% (5/200). Among these samples, two (2/200) were considered as ASC-US and three (3/200)
as LSIL by the Bethesda system. Five patients (5/195) had Candida sp. and one person (1/195)
had Trichomona vaginalis. The 2.2% prevalence found in our study using the Papanicolaou
method is similar to that found in Mexican women (46).
Clearly the PCR method (3.5%) is more effective than the PAP method (2.5%) in detecting the
HPV infection since PCR assays can detect DNA sequences in the cells, whereas the
Papanicolaou test can only analyze cellular changes. The differences found between the two
methods were similar to those found in the study carried out in Mexico (46) due to the sensitivity
of each method. PCR has a high level of sensitivity and specificity but the Papanicolaou test
takes into consideration many variables such as the sample collection and reading process.
However, a low correlation was found between two methods with a coefficient of 0.31, but the
agreement was 95%. Of the samples, 195 were normal with the Papanicolaou method and 193
were negative for HPV infection using the PCR method. The results showed a significant
coefficient between PCR and PAP test (0.45), which correlates (74%) with another study in
Sweden (47).
The age of the group is an important risk factor for HPV infection. Female individuals of 1822
years old had a higher risk of infection than those of 2225 years old. It is possible that the
mechanism of acquired immunity due to previous exposure affected the minimal chance of HPV
infection in older women (48). The age of the first coitus was also observed and a significant
correlation was noted in female individuals who had been sexually active when under the age of
18. In this study, a 3.5% prevalence of HPV infection was found using the PCR method. This
prevalence is lower than the figure reported in another study of Chilean women in Santiago (49),
where a prevalence of 14% was reported. This is similar to the data in other studies (10,34,35);
however, 26 and 20% HPV infection was identified in Nigerian and in Taiwanese women,
respectively (35). However, when sexual activity commenced after 18 years of age, a 2.03 higher
risk factor was noted as compared with other female individuals younger than 18 years old, as
confirmed by other authors (49). This discrepancy is significant in increasing the risk of HPV
infection. Smoking is an important risk factor. The female patients who smoked were at a
significantly higher risk than those who did not smoke. It appears that smoking affects the
immune mechanism response of the cervical tissue when the virus is in contact with the tissue
(50,51).
In conclusion, a significant (P<0.05) correlation was found between the PAP and PCR methods
of testing for HPV in young university women. A significant correlation was also found between
smoking and HPV infection, whereas no difference was noted with other parameters.
Go to:
Acknowledgements
The contribution to this study from Claudio Medel and Rosa Zerega is greatly appreciated. This
study was supported by grant UTA-Mayor 7710-08 (MTM), from the Universidad de Tarapac,
Arica, Chile.
Go to:
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Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. [J
Pathol. 1999]
Review The natural history of cervical HPV infection: unresolved issues. [Nat Rev
Cancer. 2007]
Epidemiologic evidence showing that human papillomavirus infection causes most
cervical intraepithelial neoplasia. [J Natl Cancer Inst. 1993]
Prevalence and determinants of HPV infection among Colombian women with normal
cytology. [Br J Cancer. 2002]
Socioeconomic deprivation and the incidence of cervical cancer in New Zealand: 1988-
1998. [N Z Med J. 2004]
Prevalence of human papillomavirus in cervical cancer: a worldwide perspective.
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Inst. 1995]
Review A systematic review of the role of human papilloma virus (HPV) testing within a
cervical screening programme: summary and conclusions. [Br J Cancer. 2000]
Reliable high risk HPV DNA testing by polymerase chain reaction: an intermethod and
intramethod comparison. [J Clin Pathol. 1999]
Management of women with mild dyskaryosis. Cytological surveillance avoids
overtreatment. [BMJ. 1994]
Detection rates for abnormal cervical smears: what are we screening for? [Lancet. 1995]
The polymerase chain reaction: a new epidemiological tool for investigating cervical
human papillomavirus infection. [BMJ. 1989]
Persistence of type-specific human papillomavirus infection among cytologically normal
women. [J Infect Dis. 1994]
Determinants of genital human papillomavirus infection among cytologically normal
women attending the University of New Mexico student health center. [Sex Transm Dis.
1993]
Prevalence and determinants of HPV infection among Colombian women with normal
cytology. [Br J Cancer. 2002]
Epidemiology of HPV infection among Mexican women with normal cervical cytology.
[Int J Cancer. 2001]
Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based
study. [Br J Cancer. 2004]
Cervical human papillomavirus infection in the female population in Barcelona, Spain.
[Sex Transm Dis. 2003]
Prevalence of human papillomavirus infection in rural villages of the Bolivian Amazon.
[Rev Inst Med Trop Sao Paulo. 2003]
Human papillomavirus infection: an anonymous prevalence study in South Wales, UK.
[Br J Cancer. 2006]
Review Chapter 1: Human papillomavirus and cervical cancer--burden and assessment of
causality. [J Natl Cancer Inst Monogr. 2003]
Distribution of 37 mucosotropic HPV types in women with cytologically normal cervical
smears: the age-related patterns for high-risk and low-risk types. [Int J Cancer. 2000]
Epidemiologic classification of human papillomavirus types associated with cervical
cancer. [N Engl J Med. 2003]
Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. [Br
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Asian-American variants of human papillomavirus 16 and risk for cervical cancer: a case-
control study. [J Natl Cancer Inst. 2001]
Natural history of cervicovaginal papillomavirus infection in young women. [N Engl J
Med. 1998]
Prevalence and determinants of HPV infection among Colombian women with normal
cytology. [Br J Cancer. 2002]
Epidemiology of HPV infection among Mexican women with normal cervical cytology.
[Int J Cancer. 2001]
Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based
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Smoking, diet, pregnancy and oral contraceptive use as risk factors for cervical intra-
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PMC2748815

Am J Health Behav. Author manuscript; available in PMC 2010 November 1.
Published in final edited form as:
Am J Health Behav. 2009 NovDec; 33(6): 627638.
PMCID: PMC2748815
NIHMSID: NIHMS145108
Faith Moves Mountains: An Appalachian
Cervical Cancer Prevention Program
Nancy E. Schoenberg, PhD, Marion Pearsall Professor, Jennifer Hatcher, RN, PhD, Assistant Professor,
Mark B. Dignan, MPH, PhD, Professor, Brent Shelton, PhD, Professor, Sherry Wright, Project Associate,
and Kaye F. Dollarhide, Project Manager
Author information Copyright and License information
The publisher's final edited version of this article is available at Am J Health Behav
See other articles in PMC that cite the published article.
Go to:
Abstract
Objective
To provide a conceptual description of Faith Moves Mountains (FMM), an intervention designed
to reduce the disproportionate burden of cervical cancer among Appalachian women.
Methods
FMM, a community-based participatory research program designed and implemented in
collaboration with churches in rural, southeastern Kentucky, aims to increase cervical cancer
screening (Pap tests) through a multiphase process of educational programming and lay health
counseling.
Results
We provide a conceptual overview to key elements of the intervention, including programmatic
development, theoretical basis, intervention approach and implementation, and evaluation
procedures.
Conclusions
After numerous modifications, FMM has recruited and retained over 400 women, 30 churches,
and has become a change agent in the community.
Keywords: cervical cancer, rural, interventions, Appalachia
In this article, we present a conceptual description of one of the first faith-placed intervention
trials in Appalachia, a region with well-documented health disparities. The intention of the
article is to provide readers with an in-depth understanding of the contextual, theoretical, and
methodological components of the project, beyond the capacities of a standard data-driven paper.
Conceptual descriptions of interventions have a time-honored tradition within behavioral
science/public health as a means of providing in-depth explanations on the process, conduct, and
progress of complex interventions.
1-3

Over the past decade, approximately 13,000 new cases of invasive cervical cancer have been
diagnosed in the United States each year, with 4600 deaths resulting annually.
4
These numbers
represent a 75% reduction from the previous 5 decades, generally attributable to the proliferation
of Pap smear screening, increased availability of diagnostic testing, and improvements in
treatment.
5
Pap test screening reduces the likelihood of invasive cervical cancer onset by 90% for
up to 3 years.
6
Indeed, 50 to 70% of new cervical cancer cases occur in seldom or never screened
women. The current US Preventive Services Task Force recommends the following regarding
Pap test screening: initiate Pap testing within 3 years of onset of sexual activity or by age 21,
whichever comes first; obtain Pap test every 3 years; discontinue Pap test for women age 65 and
older who have had negative tests and are not otherwise at high risk for cervical cancer and for
women who have had hysterectomies for benign reasons.
7

The high level of efficacy of cervical cancer screening has led the guiding public health
document Healthy People 2010 to set a goal of 97% 3-year screening rate for women age 18+.
8

Although this goal remains elusive, rates of screening have increased over the past several
decades. In 1970, 68% of women indicated that they had a recent (3 years) Pap smear. By 1997,
this percentage had increased to nearly 80%.
9
Unfortunately, these high rates of Pap tests have
not been consistent across all regions of the United States, and several areas, including
Appalachian Kentucky, have persistent patterns of low participation in screening.
Appalachia and Cervical Cancer Disparities
The Appalachian region includes 410 counties in 13 states and has a population of over 22
million people, or 8.3% of the total US population.
10
Appalachia is well known as a region of
beauty, community connectedness, poverty, and substandard health.
11
Although poverty rates
have been cut in half since 1960, significant socioeconomic and health disparities persist.
12
High
poverty levels in conjunction with other contextual challenges strongly contribute to the excess
cervical cancer burden experienced by Appalachian women and their families.
13
As
demonstrated in Figure 1, Surveillance, Epidemiology, and End Results (SEER) data from
Appalachia reveal that invasive cervical cancer incidence rates are 40% higher than the national
average.
14


Figure 1
Cervical Cancer Mortality Rates by US County, 1970-1998 (Source
13
)
To address this cancer burden in Appalachia, Faith Moves Mountains targeted women aged 40-
64, years when many women stop having regular Pap tests just as cervical cancer rates increase,
as shown in Table 1.

Table 1
Kentucky and Within State Comparisons of Pap Smear Screening, 1999-2000
54,55

Determinants of Pap Test Receipt
Comprehensive frameworks that examine the determinants of cancer prevalence and mortality
focus on characteristics of (1) the individual, (2) the health care provider and the medical system,
and (3) the environmental or community context.
15
Several reasons specific to the individual
have been suggested for this elevated rate of cervical cancer and mortality, including the older
age of women in Appalachia and the lack of resources pervasive in the region. Due to a general
trend in population aging and outmigration of younger people, Appalachias population is older
than national figures,
10
a concern because older age is associated with inadequate cervical cancer
screening and higher mortality.
16
Middle-aged and older women may not receive Pap tests due to
a lack of regular reproductive health care, competing demands, and uncertainty about screening
recommendations, factors described by women in our formative research.
17

In addition, Appalachian residents are more likely to experience individual and community
challenges, like poverty, lack of transportation, and low rates of adequate health insurance, that
increase the risk of inadequate screening and cervical cancer.
18
Health care professional
shortages endemic in Appalachia make it more difficult for lower income women to have access
to preventive health services.
11
Recently, attention has been turned to understanding the linkage
between elevated cervical cancer rates and HPV in the Appalachian context although, to our
knowledge, the prevalence of HPV in Appalachia is unknown.
Faith Moves Mountains (FMM) focused on the individual in the context of the community rather
than health care providers (HCP) and the environment for several reasons. First, as extensive
health research has documented, the mere availability of health services, including physicians
recommendations of procedures, does not ensure patient uptake of those services.
19
Uptake of
services is influenced by more than simple availability and also involves norms, beliefs, and
current health practices. Second, FMM focused on the individual in the community context
because many of the HCP and environmental characteristics implicated in inadequate cervical
cancer prevention are not particularly amenable to extensive modification (eg, inadequate
practice time, particularly in rural healthcare shortage areas, difficulty scheduling appointments,
a poor public transportation system, concerns about privacy and quality of care at the local health
department, and a lengthy waiting time at the providers office).
20

Although many of the patient characteristics associated with barriers to cervical cancer
prevention activities, including lower education and income, are also nonmodifiable,
21,22

individuals behaviors and the influence of their communities increasingly are recognized as vital
elements in optimizing health.
23
Thus, rather than perceiving Appalachia solely in terms of its
challenges to health care, FMM has taken an assets approach and integrated strengths that have
supported and sustained communities in Appalachia for centuries.
24
Two such assets in the
Appalachian context are the church and the strong tradition of social networks, particularly
among women.
Community Assets Underlying the Intervention: Appalachian Church/Faith-
Placed Interventions and Social Networks/LHA Interventions
The rural Appalachian Church and faith-placed interventions. Preliminary work in the
Appalachian region has demonstrated the central and sustainable place of the church; such
institutions are viewed as culturally acceptable environments in which to gather and promote
positive health behavior. The vast majority of families in the region maintain a membership in a
church and well over one third of residents indicate that they attend church at least once per
week.
25
Additionally, recent evidence refutes the assumption that religious communities promote
negative constructs like fatalism or lack of self-efficacy.
26
For the past 2 decades, faith
communities have been selected as a primary setting and/or partner for the delivery of health
educational messages and interventions, most especially in African American faith
organizations.
27,28

Despite the successes of many of these programs, there are very few published research articles
on interventions for rural whites within faith communities.
29
This absence of such intervention
activities in predominantly white rural communities represents a lost opportunity for several
reasons. First, many of the disadvantages experienced by African Americans in both rural and
urban settings also exist among rural white communities, especially in the under resourced
Appalachian region. Furthermore, in both rural white and African American communities,
religious institutions have taken center stage as one of the few empowering and self-directed
entities.
30
For many small, poor, rural communities, churches are among the sole locally-owned
infrastructure and play a central role in community life and information sharing. Finally, many
Appalachian middle-aged and older women are actively involved in churches, enhancing the
likelihood of participation in a faith-placed program
Social Networks and LHA Interventions
Older rural women, who may be less integrated into the health care system, often rely on social
networks for information, especially information related to health.
31
For these women, the church
and other social network opportunities may provide trust and familiarity essential in promoting
cervical screenings. These social networks, particularly those operating in faith institutions, have
been shown to enhance health promotion activities.
32
For example, in one cardiovascular
intervention, participants in a faith-placed program reduced their body weight by 2.8%, and 65%
sustained this weight loss after 6 months. When asked which program components were critical
to losing weight, participants mentioned that social support was the most helpful aspect of the
intervention.
33
In the Appalachian context, social networks intersect with faith activities through
community outreach programs, including health and social service outreach, interdenominational
cooperation and organization, and ministerial associations. For many in Appalachian religious
communities, personal ties among church networks are trusted, familiar points of reference (p.
48) that lead naturally to the acceptability of interventions.
29

Developmental work for this project indicated that a lay health advisor (LHA) intervention might
bring together social networks, faith communities, and health promotion. Such interventions
have demonstrated successes in educating women on the need for Pap smears, decreasing distrust
about the health care environment, and providing suggestions on overcoming barriers
experienced.
34
LHA programs have been shown to be especially useful for hard-to-reach
populations because these populations are often excluded from key facilitators of cancer
screening services, including physician referrals, educational enrichment, and positive patient-
physician communication. Additionally, traditionally underserved women have been shown to
draw heavily on the input from their peers, thereby laying the groundwork for the acceptability
of LHA programs.
32
For rural women, LHAs have been particularly helpful in tailoring
information about area resources to specific community barriers.
35-37

Go to:
METHODS
Development and Implementation of Faith Moves Mountains
Early development. Faith Moves Mountains was designed to increase adherence with
recommendations for obtaining Pap tests. The project was developed through an 18-month
process that included ethnographic and survey research in communities in Appalachian
Kentucky. During this phase, the team developed the Faith Moves Mountains project name,
reflecting a local sense of place (residents refer to themselves as being from the mountains rather
than Appalachia). Faith Moves Mountains also highlighted the central role of religion, referred to
a biblical adage, and ensured discretion with the health topic (by not mentioning cervical cancer).
The project team also undertook several distinct activities to inform the intervention, including
interviews with women rarely or never screened for cervical cancer, a survey of church women,
confirmatory focus groups, a community inventory, and interviews with key informants. All
activities, in both development and intervention phases of the research, were approved by the
universitys institutional review board.
During 25 interviews with rarely or never screened women, approximately 70% said that they
were very likely to attend their church at least twice a month. Participants mentioned the
following reasons why churches would be useful intervention sites: (1) frequent attendance by
targeted population group, (2) generally strong feeling of trust and reliability, (3) established
precedent for health discussions, (4) existing health and womens ministries, (5) availability of
child and elder care, (6) trust by male family members, (7) no worries about financial costs or
being taken advantage of, and (8) local control. A survey of 72 Appalachian women from faith
organizations revealed that over 75% of the women were age 50 and older and 38% of those
aged 50 or older reporting not having Pap smears within the past 3 to 5 years. Nearly all (82%)
reported that they would be interested in participating in a cervical cancer education program
through the church if one were offered.
Finally, the team conducted a series of confirmatory focus groups, a community inventory to
identify regional assets and barriers (eg, transportation, telephone, health clinics, etc.), and in-
depth key informant interviews with health care and service providers and ministers. These
activities improved understanding of recruitment and retention; the resources of the local
communities; and methods for working with religious, social, and health service organizations;
these activities also shaped the content of our educational and lay health advisor interventions.
Two published articles emerged from this phase of the project, as well as a refinement of the
protocol.
17,38
Both of these articles update the literature on Appalachian womens perspectives on
determinants of cervical cancer screening.
Theoretical Basis
As shown in Figure 2, Faith Moves Mountains drew on the strengths of several conceptual
frameworks, including the PRECEDE-PROCEED and social cognitive theory (SCT), and
principles of community-based participatory research (CBPR). PRECEDE-PROCEED facilitates
the identification of many different classes of factorspredisposing, enabling, reinforcing, and
needthat influence health and health behaviors, focusing on social, epidemiologic, behavioral
and environmental, and educational and organizational views of a health problem within a
community context.
39-41
The key predisposing factors that FMM focused on include knowledge,
self-efficacy, and attitudes.

Figure 2
Summary of Factors Based on Theoretical Models Influential in Receipt of Pap Test
Although PRECEDE-PROCEED provided a general framework for intervention development
and implementation, SCT provided direction for the specific elements of intervention.
39
The
focus on LHAs as culturally consistent role models followed years of effective interventions in
traditionally underserved rural populations.
42,43
Educational input from the lay health advisors
addressed the need aspect of our program; LHAs provided extensive input on the screening
recommendations and efficacy of Pap tests. Enabling factors were a major focus of Faith Moves
Mountains, with a tailored newsletter and counseling session that addressed barriers specified by
participants (eg, finding free/low-cost screenings, connecting with the health department,
contacting public transportation services) and reinforcements through continuing contact with the
FMM staff.
As a community-based participatory research project (CBPR), FMM also employed key
principles including ensuring that the focal issue and approach converge with community needs
and priorities, locating project resources within the community, sharing key decisions between
community members and the scientific community, and providing extensive opportunities for
research training.
24

Implementation Plan
This faith-placed lay health advisor intervention has been conducted in 5 stages: recruitment of
the faith institution and eligible women; baseline interview; educational workshop; follow-up 1
interview; lay health advisor face-to-face, tailored home visit; and final follow-up/exit interview.
The delayed-intervention group followed the same process, except the intervention component
was delayed approximately 4 months and an additional assessment was inserted prior to the
intervention. Figure 3 displays the sequence and timing of intervention activities.

Figure 3
Faith Moves Mountains Intervention Sequence
Community networks
An integral part of the development of a LHA program involved drawing on the social resources
and networks of the community, a task that would not be feasible without well-connected and
highly regarded local personnel. After an extensive and time-consuming search for an
experienced, highly respected, and thoughtful local project manager, staffing and tailoring the
protocols became local decisions; the project manager selected her assistants, interviewers, and
lay health advisors and, with consultation with the entire team, molded the conduct of the
educational and tailored home visits to conform to local norms. Similarly, initially, the scientific
team provided training in human subjects, interviewing, and project protocol through formal
sessions, testing, and standardized manuals; however, early in the project these responsibilities
were assumed by the professional community staff.
Consistent with the overall orientation of the project, as many operational decisions as possible
were made on the local level, including personnel (eg, identifying and hiring a computer
technician or graphic designer), selection of appropriate printed educational materials (eg,
highlighting local images and suitable resources), and implementation of the intervention
procedures (eg, opting for face-to-face recruitment rather than via mail or making follow-up
check-in phone calls for greater individual attention). Ensuring that local communities take
primary ownership of the project reaps multiple benefitsenhancement of the knowledge and
expertise of the community, improved development of community infrastructure, provision of
employment and training opportunities, and stronger likelihood of an acceptable program.
44

Recruitment protocol (Faith Communities)
FMM drew on a variety of faith communitieswhite and African American, large and small,
nondenominational and mainline churches and faith-related activities (outreach in Bible studies
or food pantries) to help find and recruit this hard-to-reach population.
Initially, the study was designed to obtain a stratified (by one of 4 counties) simple random
sample of faith-based organizations in the catchment area. Ultimately, identification of
organizations via random sampling and eventual contact either by postcard, phone, or visits from
our project office in eastern Kentucky, proved to be futile as only a handful of churches
randomly selected were able to be contacted and ultimately showed interest. The recruitment
protocol focus was then changed from using a randomly shuffled comprehensive list of
organizations to a protocol that called for taking advantage of established connections to
organizations for which our field staff had personal connections. The initial focus was on
recruiting organizations within the county of residence of our field office. This approach met
with immediate success, and acceptance of the program enabled churches to be recruited in the
same manner in the remaining 3 counties.
Our project staff made a contact with the churchs leaders (minister, lay people, ministers wife)
to describe the project. Discussing the project often took several meetings; however, FMM has
had a 90% success rate in church recruitment, mainly attributable to the local staffs expertise,
excellent reputation in the community, and increasingly positive word of mouth about the
project. In addition to visits with church representatives, FMM staff frequently attended church
services and special events.
Currently, the project has recruited 30 churches with the following denominations: 3 (10%)
mainline protestant (AME, Presbyterian, Methodist, etc); 13 (43%) Baptist and Anabaptist
(Southern Baptist, Freewill Baptists, Old Regular Baptists, Missionary Baptists, etc); 10 (33%)
non-denominational, Evangelical, Pentecostal; and 3 (10%) Holiness or Nazarene. These
denominational representations are nearly identical to the population of congregations in the 4
counties in which Faith Moves Mountains operates. Other groups, including Latter Day Saint,
Catholic, and Jehovahs Witness congregations, compose 3.7% of the religious affiliations in the
projects 4 counties. Thus far, the project has recruited one of these groups (Catholic) into the
project.
Intervention participants
After recruiting congregations, FMM staff focused on eligible participant recruitment.
Collaborating with church personnel, team members arranged a date for an educational
workshop to interested church members prior to which recruitment and the baseline interview
occurred. Although any interested person was invited to attend the presentation, our staff
members specifically requested the participation of eligible women (40-64 years of age, rarely or
never screened for cervical cancer).
Nearing the completion of the project, the FMM team has recruited approximately 420 rarely or
never screened women, with 10 women dropping out prior to completing the protocols. The
average age of the women is 52 years. Reflecting Kentucky Appalachia, most participants are
white (93%) and married (60%). Just under half (43%) have more than a high school education.
Nearly half of the women work outside the home (49%); however, about 25% have annual
family incomes under $10,000, and more than half (53%) selected the subjective assessment
statement I sometimes struggle to make ends meet. At least half of the women describe their
health as either very good or good despite half of them reporting having heart disease or high
blood pressure; 20%, diabetes; and more than 30% report having at least one other chronic
disease. Regarding their last Pap test, approximately one quarter (24.7%) had a Pap test 3 years
ago; half (45.5%) indicated it had been over 3 but under 5 years ago; 29% reported receiving a
Pap test 5 or more years ago; and less than 1% (.7%) had never had a Pap test.
Interview and intervention protocol
For those eligible and willing to participate, informed consent documents and a pilot tested,
baseline questionnaire were administered. Our local team offered to orally administer all
documents throughout the project in order to avoid problems associated with limited literacy. In
addition to current state of Pap receipt and staged readiness to receive the test, baseline and
follow-up interviews include sociodemographic questions, a cervical cancer-specific
instrument,
45
a cervical cancer-specific knowledge questionnaire and barriers assessment,
46
a
measure of decisional balance,
47
and self-efficacy for cervical cancer-related activities and stages
of readiness for Pap test receipt.
48
The project relies on self-report for receipt of Pap test for
several reasons. First, with most studies demonstrating approximately 70% positive and 95%
negative predictive value of recall for Pap tests,
49,50
self-report tends to be acceptably predictive
of Pap receipt. Second, FMM resources are too limited to undertake medical records review.
Third, medical records review likely would undermine trust.
Those in the intervention group receive a culturally tailored educational program about cervical
cancer, Pap tests, and local resources that may facilitate screening. Cultural tailoring, undertaken
primarily by lay health advisors (LHA), has been accomplished in several ways. First, simply by
having LHAs local women selected because they are well integrated into the social and
religious life of the community- the program acknowledged the importance of local traditions
and insider status. In addition, cultural tailoring was put into place as the LHAs and other project
staff guide intervention development and delivery, including reviewing and revising
questionnaires, intervention protocols, and the tailored newsletter for appropriateness and
meaning.
Approximately 5 to 10 weeks after the educational intervention, the participants received a
second interview to assess any changes in stage of readiness, knowledge base, and perceived
barriers to receipt of Pap tests. Two to 3 months after the second interview, participants receive a
home visit from a local, trained LHA, who, prior to the session, reviews the participants specific
barriers to Pap tests and creates a custom-made information packet. Interviewers obtain
responses about these barriers (ie, transportation problems, lack of health insurance coverage,
conflict between clinic hours and employment) during each participants baseline interview. This
packet, consisting of a tailored newsletter and a contract, comprises the basis for the LHA
visit.
The Faith Moves Mountains newsletter is culturally and personally tailored. Culturally, there are
local touches including appropriate local references, photos, and descriptions of facilities and
services unique to the participants community. Personally, the newsletters discuss each
participants specific barriers to Pap tests and suggest resources to overcome these challenges.
This process of LHAs incorporating stated barriers into the newsletter and then reviewing the
newsletter with the participant in a nonthreatening home environment ensures that the
intervention is stage-matched and its language and delivery style are acceptable to community
members.
Two weeks later, the participant receives a telephone follow-up call from her LHA, asking
whether she has experienced any barriers to receiving a pap test and has any questions. Two
months later, the participant has her final or exit interview in which she is asked about whether
she has received a Pap test or plans to, which (if any) portion of the intervention had an influence
on receiving a Pap test, and overall satisfaction with the program. This entire process is repeated
for the delayed-intervention group, with the addition of one assessment immediately prior to the
LHA intervention. During this assessment, FMM staff determine whether the delayed
participant, who is serving the function of a control group member, has received a Pap test (and
when and what precipitated the decision).
Evaluation Plan
Faith Moves Mountains evaluation involves a mixed-method approach. Qualitative and
quantitative analyses of in-person interviews and questionnaires allow a description of the
program experience and satisfaction and detects changes in knowledge of cervical cancer and
receipt of Pap tests. Debriefing qualitative process evaluations involving exit interviews are
being conducted with a randomly selected set of participants, all LHAs, and a subsample of key
informants to determine their experience and satisfaction with the intervention, consistency with
programmatic goals, potential contamination, and costs.
2,51
The quantitative evaluation focuses
on the main outcome measure, receipt of Pap smear, in addition to several moderating factors
such as (1) knowledge of cervical cancer and Pap tests, consistency with recommended intervals
for screening, and perceived efficacy of the screening tests and mediating variables; (2)
decisional balance; and (3) self-efficacy.
Go to:
CONCLUSIONS AND FUTURE DIRECTIONS
This article has described a health education program designed to decrease the burden of cervical
cancer among Appalachian women by increasing Pap test use. Currently, 421 rarely or never
screened women have completed a baseline interview and educational workshops. Most
participants (355) have completed their follow-up 1 interview; 248 have had the lay health
advisor face-to-face, tailored home visit; and 119 have completed the entire protocol, including
their exit interview.
Faith Moves Mountains draws on the assets of local communitiesstrength of social ties,
respect and trust afforded to faith institutions, and the dynamism and commitment of local
citizens to improve the lives of othersin combination with scientific frameworks and
principles. Such frameworks and principles include the SCT, PRECEDE-PROCEDE models as
well as community-based participatory research concepts. From the 4 years working in the
central Appalachian communities of Kentucky, the FMM team has drawn several conclusions.
First, planning for and early administration of the intervention required multiple learning paths.
Prior to the planning of Faith Moves Mountains, many community members did not realize the
disproportionate burden of cervical cancer shouldered by their community, a realization essential
to increase community empowerment and motivate action. Early efforts in enlisting the support
of churches, social service agencies, and key individuals in the community required our team to
demonstrate the health disparities of cervical cancer. Once explained, many community members
embraced the projects goal of early detection. Similarly, the community-based staff worked hard
to educate the scientific staff on the rather extensive modifications to the research design
necessary for community acceptance. For example, the proximity of congregations, the frequent
trips made across county lines, and the strong connections of many in the region required
rethinking of a standard control and experimental group design. Ultimately, FMM adopted an
early- and delayed-intervention approach.
Like most CBPR-based interventions, this project has modified its design and conduct to
conform to community expectations, logistical requirements, and budget reductions. For
example, as described in this article, initial plans for randomized recruitment of faith institutions
yielded to sampling that is more productive and remains representative of the denominational
distribution in central Appalachia. Once staff realized that mailed invitations soliciting
participation in the project were being returned to sender or remaining unopened on already
overcommitted preachers desks, they took a personal, door-knocking approach. Beyond that,
team members attended church and participated in numerous outreach programs. Initial plans to
make data collection more efficient by using laptops in the field took a different direction, as
interviewers preferred to hand-enter data and double-check for quality assurance, placing less
distance between them and the participants and engendering more trust. Finally, although the
project sustained a sizable budget reduction and had to reduce the scope of work, the team has
been able to strategize to operate on lean resources, something well known to residents of eastern
Kentucky. Such tweaks and modifications have resulted in more appropriate and acceptable
practices while remaining true to research design and objectives.
Another conclusion the team has drawn pertains to planning for the next health promotion
project. During the formative research and throughout project implementation, FMM staff has
remained vigilant about health concerns expressed by a wide array of community members,
positioning the project to respond to community input as well as subsequent project initiatives.
Such receptivity aligns closely with principles of CBPR.
24,44
Over the next half year, FMM will
complete our recruitment and finalize their program activities. Although early results look
promising, research activities must draw to a close prior to any definitive conclusions about the
efficacy or effectiveness of Faith Moves Mountains.
Go to:
Acknowledgments
This project is supported by the National Cancer Institute (R01CA108696). The team would like
to express its appreciation to the many community members who have offered extensive support
to this project, most especially the 420+ women who graciously agreed to be a part of it.
Go to:
Contributor Information
Nancy E. Schoenberg, Behavioral Science.
Jennifer Hatcher, College of Nursing.
Mark B. Dignan, Department of Internal Medicine.
Brent Shelton, Department of Internal Medicine, University of Kentucky, Lexington, KY.
Kaye F. Dollarhide, Faith Moves Mountains, Whitesburg, KY.
Go to:
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Med Assoc. 1998]
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cytology and its implication for screening policies. IARC Working Group on evaluation of cervical
cancer screening programmes. [Br Med J (Clin Res Ed). 1986]
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[Am J Public Health. 1995]
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from the 1992 National Health Interview Survey. [Med Care. 1998]
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Gerontol. 1992]
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inadequate screening. [Prev Med. 1990]
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Med. 1995]
Review Cancer education takes on a spiritual focus for the African American faith community. [J
Cancer Educ. 2002]
Illness experiences and health recovery behaviors of patients in southern Appalachia. [West J
Nurs Res. 1996]
Institutionalizing social support through the church and into the community. [Health Educ Q.
1985]
The Fitness Through Churches project: description of a community-based cardiovascular health
promotion intervention. [Hygie. 1986]
"God brought all these churches together": issues in developing religion-health partnerships in
an Appalachian community. [Public Health Nurs. 1999]
Trust, benefit, satisfaction, and burden: a randomized controlled trial to reduce cancer risk
through African-American churches. [J Gen Intern Med. 2003]
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and art" of community health promotion. [Health Soc Work. 1998]
Faith-placed cardiovascular health promotion: a framework for contextual and organizational
factors underlying program success. [Health Educ Res. 2007]
Lose weight and win: a church-based weight loss program for blood pressure control among
black women. [Patient Educ Couns. 1992]
"God brought all these churches together": issues in developing religion-health partnerships in
an Appalachian community. [Public Health Nurs. 1999]
Breast and cervical cancer screening in minority populations: a model for using lay health
educators. [J Cancer Educ. 1992]
Faith-placed cardiovascular health promotion: a framework for contextual and organizational
factors underlying program success. [Health Educ Res. 2007]
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North Carolina. [Health Educ Res. 1998]
Early detection of cervical cancer among Native American women: a qualitative supplement to a
quantitative study. [Health Educ Behav. 1999]
The vicious cycle of inadequate early detection: a complementary study on barriers to cervical
cancer screening among middle-aged and older women. [Prev Chronic Dis. 2007]
Cervical cancer prevention. An individualized approach. [Alaska Med. 1993]
Development of a cervical cancer education program for native American women in North
Carolina. [J Cancer Educ. 1995]
Tailoring and targeting a worksite health promotion program to address multiple health
behaviors among blue-collar women. [Am J Health Promot. 2000]
Self-efficacy and rural women's performance of breast and cervical cancer detection practices. [J
Health Commun. 2001]
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on future screening participation. [Prev Med. 1997]
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women. [J Cancer Educ. 1995]
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J Prev Med. 1998]
Validation of recall of breast and cervical cancer screening by women in an ethnically diverse
population. [Prev Med. 2002]
The Forsyth County Cervical Cancer Prevention Project--I. Cervical cancer screening for black
women. [Health Educ Res. 1994]
Use of process evaluation to guide health education in Forsyth County's project to prevent
cervical cancer. [Public Health Rep. 1991]
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