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Journal of Adolescent Health 43 (2008) S5–S25

Review article

Age-Specific Prevalence of Infection with Human Papillomavirus in


Females: A Global Review
Jennifer S. Smith, Ph.D.a,*, Amy Melendy, D.V.M., M.P.H.a,
Rashida K. Rana, M.S.b, and Jeanne M. Pimenta, Ph.D., B.Sc.b
a
University of North Carolina, Chapel Hill, North Carolina
b
GlaxoSmithKline Research and Development, Greenford, United Kingdom
Manuscript received April 12, 2008, manuscript accepted July 3, 2008

Abstract Purpose: Global data on age-specific prevalence of human papillomavirus (HPV) infection overall,
and for high-risk HPV types 16 and 18, are essential for the future implementation of HPV prophylac-
tic vaccines for cervical cancer prevention.
Methods: A systematic review of peer-reviewed publications was conducted to summarize world-
wide data on genital HPV-DNA prevalence in women. Studies with clear descriptions of polymerase
chain reaction or hybrid capture detection assays were included.
Results: A total of 346,160 women were included in 375 studies. Of 134 studies with age-stratified
HPV prevalence data (116 low sexual risk populations, 18 high sexual risk populations), over 50%
were from Europe and the Middle East (38%) and North America (19%), with smaller proportions
from Asia and Australia (21%), Central and South America (11%), and Africa (10%). Across all geo-
graphical regions, data on HPV prevalence were generally limited to women over 18 years of age. Con-
sistently across studies, HPV infection prevalence decreased with increasing age from a peak
prevalence in younger women (25 years of age). In middle-aged women (35–50 years), maximum
HPV prevalence differed across geographical regions: Africa (~20%), Asia/Australia (~15%), Central
and South America (~20%), North America (~20%), Southern Europe/Middle East (~15%), and
Northern Europe (~15%). Inconsistent trends in HPV prevalence by age were noted in older women,
with a decrease or plateau of HPV prevalence in older ages in most studies, whereas others showed an
increase of HPV prevalence in older ages. Similar trends of HPV 16 and/or 18 prevalence by age were
noted among 12 populations with available data.
Discussion: Genital HPV infection in women is predominantly acquired in adolescence, and peak
prevalence in middle-aged women appears to differ across geographical regions. Worldwide variations
in HPV prevalence across age appear to largely reflect differences in sexual behavior across geograph-
ical regions. Further studies of HPV prevalence in adolescents are needed for all geographic regions.
Ó 2008 Society for Adolescent Medicine. All rights reserved.
Key words: Human papillomavirus; Cervical cancer; Epidemiology

Highly effective prophylactic vaccines against human pap- 80%) of ICC cases worldwide. ICC is the second most com-
illomavirus (HPV) types 16 and 18 [1,2] (the most common mon cancer in women worldwide, with most (83%) of the
types in invasive cervical cancer [ICC]) [3,4]) are uniquely ef- 493,000 estimated global cases occurring in less-developed
fective for the prevention of the majority (approximately 70%– countries [5]. Vulvar, vaginal, oropharygeal, and anal cancers
in women are also manifestations of HPV infection [6,7].
HPV is one of the most common sexually transmitted in-
This study was funded by Worldwide Epidemiology, GlaxoSmithKline fections (STIs) worldwide [8] and in the United States (US),
(GSK).
*Address correspondence to: Jennifer S. Smith, Ph.D., Department of
where it is estimated that 24.9 million women aged 14 to 59
Epidemiology, University of North Carolina, Chapel, Hill, NC 27599 years are infected [9]. Although the estimated risk of HPV is
E-mail address: jennifers@unc.edu notably high over a woman’s lifetime (~80%) [10], most
1054-139X/08/$ – see front matter Ó 2008 Society for Adolescent Medicine. All rights reserved.
doi:10.1016/j.jadohealth.2008.07.009
S6 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

women who acquire HPV infection do not develop more se- of study; dates of sample collection; HPV detection method-
rious high-grade cervical neoplasia or invasive cancer, as ology (i.e., PCR primers or HCII); anatomical site and
most infections are transient [11]. methods of sample collection; population description (i.e.,
Among cross-sectional population-based samples in dif- national survey, antenatal, or commercial sex worker
ferent geographical areas, a broader range of HPV prevalence [CSW]); mean or median age of sample, with range when
and type-distribution has been detected in women with nor- available; sample size; and prevalence of HPV in the total
mal cytology than in women with ICC [12]. The prevalence population sample (overall, high risk, low risk, HPV 16,
of HPV infection, overall and by age, varies by country, re- and HPV 18). Populations were stratified into ‘‘high risk’’
gion within country, and population subgroup. To compare and ‘‘low risk.’’ Populations classified as ‘‘high risk’’ were
HPV prevalence between geographic areas or countries, those at greater risk of having genital HPV infection, such
data on age-specific or age-adjusted prevalence using sensi- as HIV-positive women, CSWs, and women with other
tive HPV detection methods are needed. Age-specific data STIs; all others were classified as ‘‘low-risk’’ populations
on HPV prevalence among female adolescents would also [13]. When published results were presented only graphi-
be useful (in conjunction with data on age at first intercourse) cally, prevalence was estimated from the graphs. In some
to inform future policies to maximize the potential benefits of cases, age-stratified sample sizes were not available. In these
HPV prophylactic vaccination. cases, overall HPV prevalence was reported, for which a sam-
This review summarizes the available published data on the ple size was available with the mean or median age. For arti-
prevalence of HPV-DNA based on highly sensitive HPV de- cles that presented data on HPV prevalence for both PCR and
tection techniques as well as associated HPV prevalence curves HC, all results were presented in the tables, although only the
by age for different female populations throughout the world. PCR results were presented in the figures. For quality control,
all data were entered twice by two independent data abstrac-
Methods tors, and every numbered reference in the text and tables was
crosschecked with those in the bibliography; any discordant
Material reviewed results were resolved by consensus. For studies that pre-
Source material was extracted from a systematic literature sented data on HPV with the same population in multiple
search from January 1, 1989 through March 1, 2007, result- publications, the largest publication was chosen and refer-
ing in approximately 5000 abstracts generated by MEDLINE ences to all corresponding publications were included in
(via PubMed) and references cited in the selected papers. Key data tables for that particular study. Where HPV data are de-
search words included papillomavirus, human, polymerase fined in the tables for individuals within an age group, the
chain reaction (PCR), hybrid capture I or II (HCI/II [Digene mean of the age range was used as data points on the graphs.
Corporation, Gaithersberg, MD]), and DNA. The literature Within each geographic area, studies were ordered by
search was restricted to peer-reviewed articles that provided country and city/region within the country, and are reported
a clear description of PCR or HC methodology for the detec- in Tables 1 and 2 (refer to appendices at http://jahonline.
tion of HPV infection. Studies citing the use of relatively less org). Studies with overall HPV prevalence data for specific
sensitive detection methods (i.e., in situ hybridization) or the age groups are shown in Figures 1 to 5 for low-risk popula-
detection of HPV serum antibodies were excluded. Studies tions by geographic region. Figure 6 shows age-specific prev-
were limited to those that provided data on age; sample sizes alence for HPV 16 and 18. Trends in HPV prevalence by age
were required to be at least 20 subjects per age group, and age were based on data presented in the smoothed curves shown
groups were combined when necessary. There were no lan- as insets in the upper right-hand corner of their respective fig-
guage restrictions on publications included. Of all publica- ure. The curves were estimated using locally weighted regres-
tions, only approximately 3% were published in a foreign sion of HPV prevalence by age with combined data for each
language. For these, the data were extracted and confirmed region and regression estimations were conducted using the
by a second, independent reviewer fluent in the language. As- least-squared methods [14].
sistance with interpretation was requested when needed. In
Results
addition, studies were only included if baseline cytology
was stated as normal, or if from a screening or population- Age-specific HPV prevalence in low-risk groups
based study and had <30% of women with abnormal cytol-
ogy of low-grade squamous intraepithelial lesions (LSIL) Africa
or greater. Articles were reviewed in full if study abstracts In comparison with other geographical regions, few data
gave an indication of fulfilling these criteria. Conference ab- were available on HPV-DNA prevalence by age in Africa,
stracts and other unpublished manuscripts were excluded. with a total of 15 countries surveyed. Available studies orig-
inated from countries in Northern Africa, Western Africa,
and south of the Sahara Desert (Table 1); no data were avail-
Data extraction and analysis
able from Central Africa. The 13 populations with HPV-
For each study, the following information was extracted: DNA data stratified by age were generally limited to women
first author, publication journal, and date; country and city aged 20 to 65 years (smoothed curve of Figure 1). Overall
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S7

Gambia, Farafenni18 Kenya, Nairobi19

Kenya, Nairobi31 Mozambique, Manhica27

Nigeria, Ibadan20 Senegal, Dakar21

Senegal, Dakar Suburbs32 South Africa, Khayelitsha15, 16

Tanzania, Mwanza23, 24 Tunisia, Sousse25

Tunisia, Sousse26 Uganda, Rakai District22

100 Zimbabwe, Chitungwiza and Greater Harare28-30

90
60

Prevalence (%)
80
70 40
Prevalence (%)

60
20
50
40 0
20 30 40 50 60 70
30 Age
20
10
0
0 20 40 60 80 100
Age (Years)

Figure 1. HPV prevalence by age in Africa among low-risk female populations by country, city, and study.

prevalence ranged from 12% in women without cervical can- prevalence in South America (64%) was reported in a cervical
cer (mean age ¼ 39 years) in South Africa [15,16] to 46% in cancer screening sample of Guarani Indian women (mean age
women attending clinics for antenatal care or general genital 15 years) in Argentina [33,34]. Age-stratified data showed
symptoms in Gabon (mean age ¼ 26 years) [17]. high prevalence rates of 54% and 59% from 14- to 24-year-
Stratified data on HPV prevalence in younger women old females attending a gynecologic clinic in Argentina [35]
were limited. Studies on nine low-risk populations [18–27] and an older group of cytologically normal women in Recife,
included women less than 25 years of age. The highest prev- Brazil (mean age 43 years), respectively [36]. A similar trend
alence was 55% in women aged 14 to 20 years from a rural of high HPV prevalence was observed in the youngest age
community in Manhica, Mozambique [27]. groups of other age-stratified studies in South American
Patterns of HPV prevalence by age appeared to differ females [37–42] (Figure 2). In Central America, the highest
across surveyed countries (Figure 1). Only a few studies, HPV prevalence was reported among clinic-based controls
however, included a relatively wide age-band of reproductive aged 15 to 24 years in Tegucigalpa, Honduras (71%) [43–47].
years (15–49 years). In Tunisia [25,26], Kenya [19], Uganda Within the region, the majority of studies with age-specific
[22], and Zimbabwe [28–30], HPV-DNA prevalence was HPV prevalence data followed a slight U-shaped curve
highest in young women and decreased steadily with age. (smoothed curve of Figure 2). Studies from Honduras [43–
In Nigeria [20], Kenya [31], and Mozambique [27], HPV 47], Mexico [48–50], Colombia [39–41], Costa Rica [51–
positivity also declined with age but generally reached a pla- 60], Chile [42], and Brazil [38] found a high HPV prevalence
teau at approximately 40 years of age. In contrast, HPV pos- in women under 30 years old that steadily decreased thereafter
itivity increased slightly in older aged women in Senegal with an upward trend in older women (Figure 2). The age of the
(over 45 years of age) [32] and in South Africa (over 50 years second increase in HPV prevalence in older women in these
of age) [15,16]. In comparison, women surveyed in Gambia studies appeared to differ by geographical location, being
seemed to have a relatively constant prevalence of HPV in- over 40 years in Honduras [43–47], Chile [42], Port Alegre,
fection among those aged 15 to 54 years [18]. Overall, the Brazil [38], and Mexico [48–50], and over 50 years in Costa
highest prevalence of HPV was 58% in a study of family Rica [51–60] and Colombia [39–41]. In contrast, Sao Paulo,
planning clinic attendees aged 25 to 29 years in Nairobi, Brazil [61], and Concordia, Argentina [37], demonstrated
Kenya [31]. a consistent downward trend of HPV prevalence by age.

Central and South America North America


Studies of 35 low-risk populations were included in the Studies on 50 low-risk populations were conducted in
Central and South America region. The highest HPV North America; approximately 80% of reported studies
S8 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

Argentina, Concordia37 Argentina, Ushuaia35 Brazil, Port Alegre38


42
Brazil, Sao Paulo 61
Chile, Santiago Columbia, Bogota39-41
52-60
Costa Rica, Guanacaste 51
Costa Rica, Guanacaste Honduras, Tegucigalpa43-47
48
Mexico, Mexico City 50 Mexico, Morelos Mexico, Morelos347
49
Mexico, Morelos 347 Mexico, Morelos
100 80

90

Prevalence (%)
60
80
40
70
Prevalence (%)

60 20

50
0
40 20 40 60 80
Age
30
20
10
0
0 20 40 60 80 100
Age (Years)

Figure 2. HPV prevalence by age in Central and South America among low-risk female populations by country, city, and study.

were from the US. A recent report of population-based age- In 10 studies from China, HPV prevalence ranged from
specific HPV prevalence in the US National Health and Nu- 5.5% among women aged 30 to 60 years (no city reported)
trition Examination Survey showed a sharp increase from 14 [100] to 53% among women aged 22 to 36 years in Shenyang
to 19 years of age (24.5%) to peak prevalence at 20 to 24 [97]. In Xiangyan and Yangchen [98], age-specific preva-
years of age (44.8%), after which HPV prevalence declined lence was essentially constant across women aged 30 to 50
to 19.6% in 50- to 59-year-olds [9]. In terms of regional dif- years. In 15 studies from India, age-specific HPV was as
ferences within the US, HPV prevalence was particularly low as 0% in a study of 30 women in Vellore (median age
high (55%-70%) in urban youths aged 13 to 20 years in At- 45 years) [113], and as high as 45% in a study of pregnant
lanta, Georgia [62]. Similarly, HPV prevalence was high (ap- women aged 30 to 39 years from Kolkata [108]. Of 17 studies
proximately 24%–55%) among female college students in in Japan, HPV prevalence was generally low, with 12 studies
Berkeley, California [63,64], Maryland [65], New Jersey reporting a prevalence of less than 15% [115,118,121–
[66,67], and New Mexico [68,69]. 127,129–131]. In Australia, four populations [87–91] re-
Among age-stratified low-risk populations, there was ported prevalences ranging from 6% in women with
a clear peak in prevalence in younger women (approximately a mean age of 19 years (range ¼ 13–44 years) [89] to 41%
20–25 years of age), with a downward trend as age increased in women aged 18 to 20 years [87,88] (Table 1). No data
(smoothed curve of Figure 3) [9,70–82]. HPV prevalence were reported from New Zealand.
varied widely, ranging from 2% in women 50 to 59 years
of age in Douglas, Arizona [83], to 70% in females 16 years Europe and the Middle East
of age in Atlanta, Georgia [62]. Data from 111 low-risk populations were available for
Overall, studies in Canada reflected a slightly lower prev- many European countries [25,139,157–271]. For the Middle
alence of HPV compared with the US. Most studies had East, information was available for Egypt [272], Lebanon
a peak prevalence of approximately 20% to 25% in 20- [273], and Turkey [274].
year-old females and a decline associated with increasing In Northern Europe (smoothed curve of Figure 5A), over-
age [84–86]. all HPV prevalence was generally less than 20% and gener-
ally lower than in North America (smoothed curve of
Asia (including Australia) Figure 3). In one large study of 4000 women in Germany,
Seventy-one studies have been conducted in Australia HPV prevalence peaked at 14% in 18- to 25-year-olds, and
[87–91], China [92–101], India [102–114], Japan [115– steadily decreased to 0% in 61- to 70year-olds [198]. One no-
131], Korea [132–138], the Phillippines [139], Taiwan table exception was a study of 90 women attending cervical
[140–145], Thailand [146–155], and Vietnam [156] (Table cancer screening in a gynecology clinic in Poland [241]. HPV
1). HPV prevalence generally tended to be lower than in other prevalence was 59% in women aged 45 to 55 years, and ap-
areas of the world (smoothed curve of Figure 4), with the ex- proximately 26% in women over age 55 [241].
ception of studies in Japan [120], Australia [87,88,90], China In Southern Europe (smoothed curve of Figure 5B),
[97], and India [108,112] (Figure 4). HPV prevalence was generally comparable to that in
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S9

Canada, Newfoundland84 Canada, Nunavut, Non-Inuit-Unknown352 Canada, Nunavut, Inuit-Baffin352


Canada, Nunavut, Inuit-Keewatin352 Canada, Nunavut, Inuit-Unknown 352
Canada, Nunavut, Non-Inuit-Baffin352
Canada, Ontario353 Canada, Ontario85 Canada, Montreal86
USA, California, Berkeley63, 64 USA, Iowa, Iowa City73 USA, Iowa, Iowa City369, 370
USA, Iowa, Iowa City 371
USA, Maryland, College Park 65
USA, Massachusetts, Boston373
USA, New Jersey, New Brunswick66, 67 USA, New Mexico, Albuquerque74 USA, New Mexico, Albuquerque68
USA, Oregon, Portland75-80, 377 USA, Washington, D.C.81 USA, Washington State82
USA/Mexico 70-72
USA/Mexico 83
USA, Nationwide9

100

90
60
80

Prevalence (%)
70 40
Prevalence (%)

60
20
50

40 0
20 30 40 50 60 70
30
Age
20

10

0
0 20 40 60 80 100
Age (Years)

Figure 3. HPV prevalence by age in North America among low-risk female populations by country, city, and study.

Northern Europe (Figure 5A), and generally showed peak of females aged 14 to 75 years [247,248]. Studies in Italy
prevalences in women in their early 20s. In two studies in revealed differing age-specific prevalence trends. One
Reims, France [190,191], female adolescents from 15 study of women in Genova reported an HPV prevalence
years were sampled, with the peak prevalence observed of 15% in women 44 years of age and younger, and
in those aged 21 to 30 years (24% vs. 28%). In Spain, found the highest prevalence (19%) in women 60 years
HPV prevalence was low—1% to 11% in a large sample of age and older [215]. Another study in Turin, Italy,

Australia87, 88 China, Hong Kong96 China, Hong Kong96


China, Xiangyuan98 China, Yangcheng98 India, Dindigul111
India, Kolkata108 India, Manipur110 India, Sikkim110
India, West Bengal110 Japan, Multiple cities130 Japan, Chiba131
Japan, Hirara125 Japan, Ishikawa and Toyama121 Japan, Ishikawa120
Japan, Naha125 Japan, Okinawa124 Japan, Okinawa123
Japan, Osaka126 Japan, Tokyo127 Japan, Yonashiro125
South Korea, Busan137 South Korea, Busan 136
South Korea, Seoul135
Thailand, Kaoka District151 Thailand, Khon Kaen152 Vietnam, Hanoi156
Vietnam, Ho Chi Minh City156
100
90
Prevalence (%)

80 50
40
70
Prevalence (%)

30
60 20
50 10
0
40
20 40 60 80 100
30 Age

20
10
0
0 20 40 60 80 100
Age (Years)

Figure 4. HPV prevalence by age in Asia/Australia among low-risk female populations by country, city, and study.
S10 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

A Belgium, Antwerp159 Belgium, Brussels160, 161 Belgium, Wilrijk394

Denmark 171
Denmark, Copenhagen1 67170
England, London176, 178

England, Manchester 401


England, Nottingham 179
England, Nottingham180

Finland, Helsinki 182


Finland, Helsinki 182
Greenland171
Norway, Oslo 235
Poland, Poznan 241
Russia, St. Petersburg243, 244
Sweden, Stockholm255 Sweden, Umea256, 257 Sweden, Uppsala262
Switzerland, Multiple cities269 The Netherlands, Amstelveen229 The Netherlands, Amstelveen229
The Netherlands, Amstelveen 229
The Netherlands, Amstelveen 229
The Netherlands, Amsterdam227
228
The Netherlands, Amsterdam 227
The Netherlands, Amsterdam United Kingdom, Multiple cities271
100
90

Prevalence (%)
60
80
70 40
Prevalence (%)

60
20
50
40 0
20 40 60 80
30 Age
20
10
0
0 20 40 60 80 100
Age (Years)

B Austria, Vienna157 France, Amiens184 France, Besancon186


France, Poitiers 189
France, Reims190 France, Reims193
203, 204
France, Reims 191
Greece, Northern Region Greece, Thessaloniki207, 208
212 213
Hungary Hungary, Debrecen Italy, Genova215
Italy, Rome216 220
Italy, Turin Lebanon, Beirut273
Spain, Barcelona248
100
90
Prevalence (%)

80 50
70 40
Prevalence (%)

30
60
20
50 10
0
40
20 40 60 80
30 Age
20
10
0
0 20 40 60 80 100
Age (Years)

Figure 5. (A) HPV prevalence by age in Northern Europe among low-risk populations by country, city, and study. (B) HPV prevalence by age in Southern Europe
among low-risk female populations by country, city, and study.

showed a peak prevalence (14%) in women aged 35 to 39 63%) in Senegal [275], South Africa [276], and Tunisia
years that decreased thereafter [220]. [26]. When compared with HIV negative women, overall
HPV prevalence was more than three times higher in
HIV-positive women in Senegal [277] and twice as high
Age-specific HPV prevalence among high-risk groups
in HIV-positive women in rural Zimbabwe [278] (Table
Among the 86 high-risk populations studied, seven 1). The highest reported prevalence in Africa was 75%
were in Africa, nine in Central and South America, 19 in HIV-positive women attending infectious disease clinics
in North America, 14 in Asia and Australia, and 37 in Eu- (mean age ¼ 29 years) in Dakar, Senegal [277], with four
rope/Middle East (Table 2). In Africa, overall HPV preva- of seven studies reporting prevalences greater than 50%
lence was consistently high in female sex workers (39%– (Table 2).
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S11

Columbia, Bogota (HPV 16)39-41 Columbia, Bogota (HPV 18)39-41


England, Nottingham (HPV 16)179 England, Nottingham (HPV 18)179
Italy, Genova (HPV 16)215 Italy, Genova (HPV 18)215
Italy, Rome (HPV 16)216 Italy, Rome (HPV 18)216
Japan, Okinawa (HPV 16)124 Japan, Okinawa (HPV 18)124
Latvia, Riga (HPV 16/18)226 Mexico, Morelos (HPV 16)48
Mexico, Morelos (HPV 18)48 Norway, Oslo (HPV 16)232-235
Poland, Poznan (HPV 16)241 Poland, Poznan (HPV 18)241
Sweden, Uppsala (HPV 16)259-261 Tanzania, Dar es Salaam (HPV 16/18)404
Thailand, Bangkok (HPV 16)304 Thailand, Bangkok (HPV 18)304
The Netherlands, Amsterdam (HPV 16)228 The Netherlands, Amsterdam (HPV 18)228
50

40
Prevalence (%)

30

20

10

0
0 20 40 60 80 100
Age (Years)

Figure 6. HPV 16/18 prevalence by age in women by country, city, and study. HPV 16, solid black or gray lines; HPV 18, black or gray dashed lines; HPV 16/18,
closed gray symbol and solid gray line.

In Central and South America, the highest prevalence of clinic attendees in Sydney, Australia (mean age ¼ 28 years),
HPV was 88% in HIV-positive women in Sao Paulo, Brazil reported an HPV prevalence of greater than 50% [297], de-
(mean age ¼ 32 years) [279]. Four of nine studies, primarily spite the fact that the populations sampled included CSWs,
of HIV-positive women and/or CSWs, reported a prevalence HIV-positive women, and women attending STI clinics.
of greater than 50% [279–282]. Among studies from Central High-risk studies in Europe had findings similar to those
America, three high-risk populations from Mexico [281,283, of North America. The highest prevalence reported was
284] and one from Honduras [285] were described. Peak also 91% in HIV positive women (mean age ¼ 31 years) in
HPV prevalence was observed in the youngest age groups Milan, Italy [217]. Also similar to North America, approxi-
in age-specific studies and generally decreased with increas- mately half of the 36 studies with high-risk populations had
ing age. a prevalence of greater than 50%, which included studies
In North America, 63% (12 of 19) of the high-risk popu- of STI clinic attendees and/or CSWs. A particularly high
lations had a prevalence greater than 40%, and two-thirds of prevalence was observed in STI clinic attendees (85%) under
the studies reported prevalences greater than 50%. The ma- 20 years of age in Greenland [38] and in Spanish CSWs
jority of studies in North America were conducted on STI (75%) of the same age [298]. HIV-positive women in Paris
clinic attendees. The highest HPV prevalence (91%) was re- [299], Germany [196], and Italy [214,300–302] all reported
ported in females aged 11 to 20 years attending STI and uni- an HPV prevalence of 60% or greater.
versity clinics in Baltimore, Maryland [286]. All studies in
North America that included HIV-positive women reported
HPV 16 and 18 prevalence stratified by age
an HPV prevalence of 50% or greater. The highest HPV prev-
alence rates were reported in a multicenter survey of metro- Thirteen studies reported HPV 16 or 18 stratified by age
politan areas (Women’s Interagency HIV Study [WIHS] (Figure 6). Among those sampled in lower sexual risk popu-
cohort) [287-293] and in a study of HIV positive women in lations (n ¼ 11), HPV 16 was generally less than one-quarter
Canada [294,295], both of which had a prevalence of approx- of the overall prevalence (Table 1). Generally, type-specific
imately 63%. prevalence for either HPV 16 or 18 was less than 8% and
Similar to data from low-risk populations, Asia had the overall prevalence of any HPV type was less than 30%. How-
lowest overall HPV prevalence among high-risk populations ever, there were a few notable exceptions, such as family
in comparison with other regions (Table 2). The highest prev- planning clinic attendees in Dalian City, China (mean age
alence reported was 69% in CSWs less than 18 years of age in 29 years), who had a prevalence of 34% for HPV 16 [93].
Bali, Indonesia [296]. Only one other population of STI Relatively higher prevalences for HPV 16 and 18 were
S12 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

observed in Europe, with a few studies in Spain, Denmark, pronounced and occurs at different ages within different geo-
Germany, and Italy reporting type-specific prevalences of graphical regions, these data suggest that the higher preva-
over 25% and 5% for HPV 16 and 18, respectively lence in older age women is largely because of newly
[166,200,215,250]. In Poznan, Poland [241], cervical cancer acquired HPV infections, primarily reflecting differences in
screening patients aged 45 to 78 years with an overall HPV sexual behavior across global regions. Alternatively, the
prevalence of 49% had a generally high prevalence of both U-shaped curves of HPV by age may potentially be explained
HPV 16 and 18; prevalence was the highest for women by reactivation of latent HPV infections in older women.
aged 45 to 49 years, 39% and 27%, respectively, and de- A previous meta-analysis of 157,879 women by de San-
creased to 26% and 17%, respectively, in women aged 56 jose and colleagues [8] summarized the global literature
to 78 years [241]. One study in Khon Kaen, Thailand, also among women with normal cytology. The present review ex-
reported an approximately 11% prevalence for HPV 18 pands upon this previous work by presenting data on women
among women 25 to 60 years of age, with a prevalence of with normal cytology as well as those included in population-
3.8% for HPV 16 [154]. based surveys or routine screening programs to provide
Among the 85 studies conducted on high-risk populations, estimates that more closely represent those of the general
44 had prevalence data for HPV 16 and/or 18. Across all re- population. In the de Sanjose et al [8] review, age data
gions, prevalence of HPV 16 was approximately one-third were grouped into five specific categories, beginning with
to one-half of the overall prevalence reported for the same those aged 25 years or less to women greater than 54 years
studies (Table 2). In some cases, type-specific prevalence of age [8]. In comparison, age ranges were further delineated
rates for HPV 16 and 18 were comparable with overall prev- in the present review (15 years up to 90 years or older), pro-
alence rates. In Europe, sex workers in Copenhagen, Den- viding a clearer understanding of HPV prevalence trends by
mark [303] (mean age ¼ 31 years), had an overall HPV age within and among different geographical regions world-
prevalence of 32% and an HPV 16 prevalence of 31%. HIV wide.
positive women in Ancona, Italy [214], had an overall HPV Given the heterogeneity in laboratory assays employed for
prevalence of 67% and an HPV 16 prevalence of 48%. Sex HPV infection detection, populations surveyed, and the ob-
workers in a brothel (mean age ¼ 19 years) in Bangkok, Thai- served variation in HPV positivity across the different stud-
land [304], had higher HPV prevalence (approximately 26% ies, we have chosen not to present a summary estimate for
and 9% for HPV 16 and 18, respectively) than massage parlor overall HPV prevalence for geographical regions or for
sex workers (mean age ¼ 30 years; approximately 8% and 2% specific age groups [305]. Instead, this review provides
for HPV 16 and 18, respectively) (Table 2). HPV 16 and 18 both age- and country-specific data on HPV infection preva-
prevalence rates were highest in brothel workers 15 to 19 lence to allow for the examination of age-specific trends of
years of age (31% and 13%, respectively) [304]. These studies HPV prevalence within a particular region or a population
suggest that oncogenic HPV types 16 and 18 (included in cer- subgroup of interest. Within specific regions, data trends ap-
vical cancer vaccines) can comprise significant proportions of pear to be generally similar to those presented by de Sanjose
HPV infection in many high-risk populations worldwide. et al [8]. Although for studies in Africa, HPV prevalence was
previously reported to be between 20% and 30% [8], whereas
we observed prevalences that ranged from approximately 7%
Discussion
to 60%, with half of the studies showing less than 20% prev-
This review represents, to our knowledge, the largest alence. For Central and South America, the highest HPV
study of HPV prevalence worldwide, including HPV-DNA prevalence was previously shown to be approximately
prevalence data from over 346,000 women from 70 countries 25%, with a nadir at 10% among females aged 35 to 44 years
worldwide. Age-stratified HPV prevalence varied consider- [8]. This data curve was clearly U-shaped, suggesting a com-
ably across geographical regions, and depended upon many parably higher HPV prevalence in older age groups. In com-
factors, including age, country and region, and type of popu- parison, the present review similarly shows a U-shaped
lation surveyed. Across all geographical regions, observed pattern by age in Central and South America, although rela-
HPV prevalence was strongly associated with age, although tively flatter, with HPV prevalence ranging from less than 5%
age curves of HPV infection differed notably across regions. to approximately 70%. For studies in North America, we
The shapes of the curves were declining in older ages, flat show a decline in HPV prevalence with increasing age; this
across age, or characterized by a U shape, with a relatively is in contrast to data obtained by de Sanjose et al [8] for fe-
higher HPV prevalence in younger and older ages. Overall males above 35 years of age. Also, in contrast to an HPV
HPV prevalence in most geographical regions consistently prevalence of less than 25%, we observed prevalence rates
peaked in women aged 25 years of age, with a decrease of 2% to approximately 56%. For studies in Europe, the
in older age groups. In contrast, age curves of HPV preva- data were divided into northern and southern regions. HPV
lence among women in Central and South America and prevalence was generally similar between these two geo-
Africa were characterized by an increased or stable HPV graphical regions (up to 60%), yet prevalence estimates ap-
prevalence among women aged 45 years or older. Given peared to be relatively higher than those observed by de
that a second peak in HPV prevalence appears to be more Sanjose et al [8] for all of Europe (<25%). In the present
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S13

study, data from Asia and Australia were grouped and ap- population than the collection of cervicovaginal samples.
peared to be in contrast, for Asia only, to results obtained However, urine-based samples have also resulted in a lower
by de Sanjose et al [8]. HPV prevalence was previously re- sensitivity for HPV-DNA detection than sampling from other
ported to be between 5% and 11%, and these present data sites in the cervicovaginal tract [308].
show specific Asian regions with higher positivity in Japan The present systematic review, to our knowledge, repre-
(0%–50%) and Australia (20%–40%). sents the largest to date, with a comprehensive examination
Both this present review and the review by de Sanjose et al of HPV-DNA prevalence in all major geographical regions.
[8] consistently showed that HPV prevalence was highest For quality assurance, data were extracted and double-
among younger women for all major world regions, reflect- checked by two independent abstractors, and a complete list-
ing a higher probability of acquiring new infections at youn- ing of country and age-specific HPV prevalence data are
ger ages. We observed that HPV-DNA prevalence differed presented in appendices located at http://jahonline.org (Ta-
across geographical regions, with peak HPV prevalence bles 1 and 2). Results are further presented for global regions
among older aged women (35–50 years) differing somewhat of the Caribbean, Western Asia, and Australia, for which data
across geographical regions, being approximately 20% in were not previously presented for women with normal cytol-
Africa, North America, and Central and South America, ogy [8]. Given that few data are available in the literature on
and 15% in Asia/Australia, Southern Europe/Middle East, trends in HPV prevalence over time within specific popula-
and Northern Europe. Relative differences in HPV-DNA tions, data provided in this present review may be useful as
prevalence from one geographical region to another, how- baseline, prevaccination HPV prevalence data. This may be
ever, are not as striking as those seen for HSV-2 (herpes sim- most beneficial for future HPV vaccine evaluation efforts if
plex virus-2) seropositivity, which is characteristic of sequential HPV testing is conducted within individual popu-
a notably higher HSV-2 seropositivity in Africa, and lower lations postvaccination.
HSV-2 seropositivity within several geographical regions, Among study limitations, type-specific data for individual
including Asia [306]. These differences are likely attributed carcinogenic HPV types other than 16 and 18 (i.e., HPV 45,
to differences in the ascertainment methods used to quantify 31, 33, 52, 58, etc.) were not included in the present review,
the burden of HSV-2 (serum antibody detection indicative of although these data have been presented for women with nor-
cumulative exposure) and HPV (DNA detection indicative of mal cytology in the de Sanjose et al [8] review. HPV preva-
current, persistent, or reactivated HPV infection). At present, lence estimates presented here are also largely limited to
currently available methods to detect HPV serum antibodies sexually active or married women. Prevalence results for
[307] are not capable of accurately measuring a woman’s cu- low-risk populations may not entirely reflect those of the gen-
mulative exposure to HPV. Reliable data on a woman’s life- eral population. To provide estimates that may be more rep-
time risk (cumulative, ever-exposure) of acquiring an HPV resentative of general female populations, and because
infection would have been useful to assess the potential previous reviews have focused on comparing HPV type-dis-
long-term impact of prophylactic HPV vaccines. tribution in these female populations with women with low-
Comparisons of HPV prevalence by geographical area or and high-grade cervical precancerous lesions, data were not
country are generally hampered by differences among study limited to women with normal cytology [3,309]. Further,
populations surveyed, laboratory methods used, and the var- this review is limited to cross-sectional prevalence rather
iation in HPV types detected (i.e., overall HPV positivity, than the ascertainment of persistent HPV, which has been
high-risk HPV types, low-risk HPV types, or type-specific shown to be highly predictive of a woman’s future risk of
[i.e., HPV 16 or 18] positivity). To reduce the possibility of high-grade cervical neoplasia or cancer [170,310,311].
an underestimation of overall or type-specific prevalence, Few population-based prevalence surveys of HPV infec-
study criteria included the detection of HPV using PCR or tion have been conducted worldwide. This is likely because
HCII detection assays. Although PCR and HCII detection as- of expense as well as the difficulty in collecting physician-
says have been shown to have a relatively higher sensitivity based samples, which are associated with relatively higher
for HPV detection than earlier detection assays (i.e., dot-blot HPV-DNA detection than currently available self-collected
or Southern blot), the sensitivity of HPV-DNA detection for sampling techniques [9,312]. Further, detailed data presented
studies presented here may not have been optimal if there on different types of HPV detection assays focused on the
were differences in the ability of PCR primers to detect spe- type of PCR consensus primers used, rather than on differ-
cific HPV types, or if there was an underdetection of HPV be- ences in typing methods employed for HPV-positive speci-
cause of in-house laboratory testing procedures. Across mens, which may notably differ across testing laboratories.
geographical regions, HPV-DNA was generally detected us- A limited number of studies provided data on dual DNA
ing GP5þ/6þ, MY09/11, HCII, or type-specific PCR primer positivity to HPV types 16 and 18 in exfoliated cell speci-
systems, with the exception of Japan, where a relatively mens. Available data presented here on HPV-DNA preva-
larger proportion of studies used L1 primers. The sensitivity lence for HPV types 16 and 18 worldwide have
of detecting HPV may also vary based on the type of speci- implications for vaccination programs. In a randomized trial
men analyzed. Although not commonly used in this survey, of women in Costa Rica who were HPV-DNA-positive for
urine specimens may allow for easier sampling within the types 16 and 18, prophylactic HPV vaccination had no
S14 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

therapeutic effect against these two types among women with [5] Ferlay J, Bray F, Pisani, Parkin DM. Globocan 2002: Cancer Inci-
these prevalent HPV 16 or 18 infections [313]. L1 virus-like dence, Mortality and Prevalence Worldwide. 2004. Available at:
from: http://www-dep.iarc.fr. Accessed November 27, 2006.
particle-based vaccines are thus not expected to provide max-
[6] Kreimer AR, Clifford GM, Boyle P, et al. Human papillomavirus
imum benefit to women who are currently DNA positive to types in head and neck squamous cell carcinomas worldwide:
HPV vaccine types (Figure 6). It would have been beneficial a systematic review. Cancer Epidemiol Biomarkers Prev 2005;
to determine the proportion of women within different popu- 14(2):467–75.
lation groups who were DNA positive and serological posi- [7] Parkin DM. The global health burden of infection-associated cancers
in the year 2002. Int J Cancer 2006;118(12):3030–44.
tive for HPV vaccine types 16 and/or 18 within specific
[8] de Sanjose S, Diaz M, Castellsague X, et al. Worldwide prevalence
age stratifications. These data would help clarify the potential and genotype distribution of cervical human papillomavirus DNA in
usefulness of vaccination against HPV 16 and 18 in females women with normal cytology: a meta-analysis. Lancet Infect Dis
[314], given that among women previously exposed to infec- 2007;7(7):453–9.
tion with HPV vaccine types (seropositive/DNA negative to [9] Dunne EF, Unger ER, Sternberg M, et al. Prevalence of HPV infection
among females in the United States. JAMA 2007;297(8):8139.
HPV vaccines types), available vaccine efficacy data suggest
[10] Centers for Disease Control and Prevention. Epidemiology and Pre-
a potential protective effect that needs to be confirmed with vention of Vaccine-Preventable Diseases. 10th ed. Washington, DC:
larger sample sizes. Clearly, HPV vaccines are optimally ef- Public Health Foundation, 2007.
ficacious in women who are dually seronegative and DNA [11] Ostor AG. Natural history of cervical intraepithelial neoplasia: a criti-
negative to included HPV vaccine types. cal review. Int J Gynecol Pathol 1993;12(2):186–92.
[12] Clifford G, Franceschi S, Diaz M, et al. Chapter 3: HPV type-distribu-
tion in women with and without cervical neoplastic diseases. Vaccine
Conclusions 2006;24(Supp 3):26–34.
[13] Smith JS, Herrero R, Bosetti C, et al. Herpes simplex virus-2 as a hu-
Age-specific prevalence data on HPV are essential in un- man papillomavirus cofactor in the etiology of invasive cervical can-
derstanding the trends in HPV prevalence in all major world cer. J Natl Cancer Inst 2002;94(21):1604.
[14] Milton M, Harris P, Smith I, et al. Implementation of a generalized
regions. There is a peak in HPV prevalence among younger least-squares method for determining calibration curves from data
females, with a second peak among older individuals in with general uncertainty structures. Metrologia 2006;43:S291–8.
some, but not all, specific geographical regions. Despite dif- [15] Denny L, Kuhn L, Pollack A, et al. Evaluation of alternative methods
ferences in techniques and collection methods, age-stratified of cervical cancer screening for resource-poor settings. Cancer 2000;
data on high-risk HPV types 16 and 18 (included in current 89(4):826–33.
[16] Kuhn L, Denny L, Pollack A, et al. Human papillomavirus DNA test-
generation HPV prophylactic vaccines) show similar age-re- ing for cervical cancer screening in low-resource settings. J Natl Can-
lated trends across major regions. HPV 18 is typically less cer Inst 2000;92(10):818–25.
prevalent than HPV 16, and prevalence differs notably by [17] Si-Mohamed A, Ndjoyi-Mbiguino A, Cuschieri K, et al. High preva-
geographical region. Further data are needed among adoles- lence of high-risk oncogenic human papillomaviruses harboring atyp-
cent populations and among population-based samples, as ical distribution in women of childbearing age living in Libreville.
Gabon. J Med Virol 2005;77(3):430–8.
many countries currently have limited available data. [18] Wall SR, Scherf CF, Morison L, et al. Cervical human papillomavirus
infection and squamous intraepithelial lesions in rural Gambia, West
Acknowledgments Africa: viral sequence analysis and epidemiology. Br J Cancer
2005;93(9):1068–76.
We thank Sarah Landis for her critical review of the data. [19] Temmerman M, Tyndall MW, Kidula N, et al. Risk factors for human
papillomavirus and cervical precancerous lesions, and the role of
We also thank Michael Hudgens for his help with statistical
concurrent HIV-1 infection. Int J Gynaecol Obstet 1999;65
advice, and Jie Ting, Yuli Chang, Marcus Lynch, and (2):171–81.
Tammy Rahim for their valuable assistance in manuscript [20] Thomas JO, Herrero R, Omigbodun AA, et al. Prevalence of papillo-
preparation. mavirus infection in women in Ibadan, Nigeria: a population-based
study. Br J Cancer 2004;90(3):638–45.
[21] Chabaud M, Le Cann P, Mayelo V, et al. Detection by PCR of human
References papillomavirus genotypes in cervical lesions of Senegalese women.
J Med Virol 1996;49(4):259–63.
[1] Paavonen J, Jenkins D, Bosch FX, et al. Efficacy of a prophylactic ad- [22] Serwadda D, Wawer MJ, Shah KV, et al. Use of a hybrid capture assay
juvanted bivalent L1 virus-like-particle vaccine against infection with of self-collected vaginal swabs in rural Uganda for detection of human
human papillomavirus types 16 and 18 in young women: an interim papillomavirus. J Infect Dis 1999;180(4):1316–9.
analysis of a phase III double-blind, randomised controlled trial. Lan- [23] Mayaud P, Gill DK, Weiss HA, et al. The interrelation of HIV, cervi-
cet 2007;369:2161–70. cal human papillomavirus, and neoplasia among antenatal clinic
[2] Quadrivalent vaccine against human papillomavirus to prevent high- attenders in Tanzania. Sex Transm Infect 2001;77(4):248–54.
grade cervical lesions. The Future II Study Group. N Engl J Med [24] Mayaud P, Weiss HA, Lacey CJ, et al. Genital human papillomavirus
2007;356(19):1915–27. genotypes in northwestern Tanzania. J Clin Microbiol 2003;41:
[3] Smith JS, Lindsay L, Hoots B, et al. Human papillomavirus type dis- 4451–3.
tribution in invasive cervical cancer and high-grade cervical lesions: [25] Hassen E, Remadi S, Chouchane L. [Detection and molecular typing
a meta-analysis update. Int J Cancer 2007;121(3):621–32. of human papillomaviruses: prevalence of cervical infection in the Tu-
[4] Munoz N, Bosch FX, de Sanjose S, et al. Epidemiologic classification nisian central region]. Tunis Med 1999;77(10):497–502.
of human papillomavirus types associated with cervical cancer. N [26] Hassen E, Chaieb A, Letaief M, et al. Cervical human papillomavirus
Engl J Med 2003;348(6):518–27. infection in Tunisian women. Infection 2003;31(3):143–8.
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S15

[27] Castellsague X, Menendez C, Loscertales MP, et al. Human papillo- [48] Lazcano-Ponce E, Herrero R, Munoz N, et al. Epidemiology of HPV
mavirus genotypes in rural Mozambique. Lancet 2001;358(9291): infection among Mexican women with normal cervical cytology. Int J
1429–30. Cancer 2001;91(3):412–20.
[28] Womack SD, Chirenje ZM, Blumenthal PD, et al. Evaluation of a hu- [49] Salmeron J, Lazcano-Ponce E, Lorincz A, et al. Comparison of HPV-
man papillomavirus assay in cervical screening in Zimbabwe. BJOG based assays with Papanicolaou smears for cervical cancer screening in
2000;107(1):33–8. Morelos State, Mexico. Cancer Causes Control 2003;14(6):505–12.
[29] Womack SD, Chirenje ZM, Gaffikin L, et al. HPV-based cervical can- [50] Hernandez-Hernandez DM, Ornelas-Bernal L, Guido-Jimenez M,
cer screening in a population at high risk for HIV infection. Int J Can- et al. Association between high-risk human papillomavirus DNA
cer 2000;85(2):206–10. load and precursor lesions of cervical cancer in Mexican women. Gy-
[30] Gravitt PE, Kamath AM, Gaffikin L, et al. Human papillomavirus ge- necol Oncol 2003;90(2):310–7.
notype prevalence in high-grade squamous intraepithelial lesions and [51] Castle PE, Schiffman M, Bratti MC, et al. A population-based study of
colposcopically normal women from Zimbabwe. Int J Cancer 2002; vaginal human papillomavirus infection in hysterectomized women.
100(6):729–32. J Infect Dis 2004;190(3):458–67.
[31] De Vuyst H, Steyaert S, Van Renterghem L, et al. Distribution of hu- [52] Castle PE, Schiffman M, Burk RD, et al. Restricted cross-reactivity of
man papillomavirus in a family planning population in Nairobi, hybrid capture 2 with nononcogenic human papillomavirus types.
Kenya. Sexually Transm Dis 2003;30(2):137–42. Cancer Epidemiol Biomarkers Prev 2002;11(11):1394–9.
[32] Xi LF, Toure P, Critchlow CW, et al. Prevalence of specific types of [53] Herrero R, Schiffman MH, Bratti C, et al. Design and methods of
human papillomavirus and cervical squamous intraepithelial lesions in a population-based natural history study of cervical neoplasia in a rural
consecutive, previously unscreened, West-African women over 35 province of Costa Rica: the Guanacaste Project. Pan Am J Public
years of age. Int J Cancer 2003;103(6):803–9. Health 1997;1(5):362–75.
[33] Tonon SA, Picconi MA, Zinovich JB, et al. Human papillomavirus [54] Peyton CL, Schiffman M, Lorincz AT, et al. Comparison of PCR- and
cervical infection and associated risk factors in a region of Argentina hybrid capture-based human papillomavirus detection systems using
with a high incidence of cervical carcinoma. Infect Dis Obstet Gyne- multiple cervical specimen collection strategies. J Clin Microbiol
col 1999;7(5):237–43. 1998;36(11):3248–54.
[34] Tonon SA, Picconi MA, Zinovich JB, et al. Human papillomavirus [55] Herrero R, Hildesheim A, Bratti C, et al. Population-based study of
cervical infection in Guarani Indians from the rainforest of Misiones, human papillomavirus infection and cervical neoplasia in rural Costa
Argentina. Int J Infect Dis 2004;8(1):13–9. Rica. J Natl Cancer Inst 2000;92(6):464–74.
[35] Sijvarger CC, Gonzalez JV, Prieto A, et al. [Cervical infection epide- [56] Wang SS, Schiffman M, Shields TS, et al. Seroprevalence of human
miology of human papillomavirus in Ushuaia, Argentina]. Rev Argent papillomavirus-16, -18, -31, and -45 in a population-based cohort of
Microbiol 2006;38(1):19–24. 10000 women in Costa Rica. Br J Cancer 2003;89(7):1248.
[36] Lorenzato F, Singer A, Mould T, et al. Cervical cancer detection by [57] Schiffman M, Khan MJ, Solomon D, et al. A study of the impact of
hybrid capture and evaluation of local risk factors. Int J Gynaecol adding HPV types to cervical cancer screening and triage tests.
Obst 2001;73(1):41–6. J Natl Cancer Inst 2005;97(2):147–50.
[37] Matos E, Loria D, Amestoy GM, et al. Prevalence of human papillo- [58] Wang SS, Schiffman M, Herrero R, et al. Determinants of human pap-
mavirus infection among women in Concordia, Argentina: a popula- illomavirus 16 serological conversion and persistence in a population-
tion-based study. Sexually Transm Dis 2003;30(8):593–9. based cohort of 10 000 women in Costa Rica. Br J Cancer 2004;
[38] Nonnenmacher B, Kruger KS, Svare EI, et al. Seroreactivity to 91(7):1269–74.
HPV16 virus-like particles as a marker for cervical cancer risk in [59] Castle PE, Schiffman M, Herrero R, et al. PCR testing of pooled lon-
high-risk populations. Int J Cancer 1996;68(6):704–9. gitudinally collected cervical specimens of women to increase the ef-
[39] Molano M, Posso H, Weiderpass E, et al. Prevalence and determinants ficiency of studying human papillomavirus infection. Cancer
of HPV infection among Colombian women with normal cytology. Br Epidemiol Biomarkers Prev 2005;14(1):256–60.
J Cancer 2002;87(3):324–33. [60] Viscidi RP, Schiffman M, Hildesheim A, et al. Seroreactivity to hu-
[40] Molano M, van den Brule AJ, Posso H, et al. Low grade squamous in- man papillomavirus (HPV) types 16, 18, or 31 and risk of subsequent
tra-epithelial lesions and human papillomavirus infection in Colom- HPV infection: results from a population-based study in Costa Rica.
bian women. Br J Cancer 2002;87(12):1417–21. Cancer Epidemiol Biomarkers Prev 2004;13(2):324–7.
[41] Molano M, Weiderpass E, Posso H, et al. Prevalence and determinants [61] Eluf-Neto J, Booth M, Munoz N, et al. Human papillomavirus and in-
of Chlamydia trachomatis infections in women from Bogota, Colom- vasive cervical cancer in Brazil. Br J Cancer 1994;69(1):114–9.
bia. Sex Transm Infect 2003;79(6):474–8. [62] Tarkowski TA, Koumans EH, Sawyer M, et al. Epidemiology of hu-
[42] Ferreccio C, Prado RB, Luzoro AV, et al. Population-based prevalence man papillomavirus infection and abnormal cytologic test results in an
and age distribution of human papillomavirus among women in San- urban adolescent population. J Infect Dis 2004;189(1):46–50.
tiago, Chile. Cancer Epidemiol Biomarkers Prev 2004;13(12):2271–6. [63] Bauer HM, Ting Y, Greer CE, et al. Genital human papillomavirus in-
[43] Ferrera A, Baay MF, Herbrink P, et al. A sero-epidemiological study fection in female university students as determined by a PCR-based
of the relationship between sexually transmitted agents and cervical method. JAMA 1991;265(4):472–7.
cancer in Honduras. Int J Cancer 1997;73(6):781–5. [64] Ley C, Bauer HM, Reingold A, et al. Determinants of genital human
[44] Ferrera A, Olivo A, Alaez C, et al. HLA DOA1 and DOB1 loci in papillomavirus infection in young women. J Natl Cancer Inst 1991;
Honduran women with cervical dysplasia and invasive cervical carci- 83(14):997–1003.
noma and their relationship to human papillomavirus infection. Hum [65] Kotloff KL, Wasserman SS, Russ K, et al. Detection of genital human
Biol 1999;71(3):367–79. papillomavirus and associated cytological abnormalities among col-
[45] Ferrera A, Velema JP, Figueroa M, et al. Human papillomavirus infec- lege women. Sex Transm Dis 1998;25(5):243–50.
tion, cervical dysplasia and invasive cervical cancer in Honduras: [66] Burk RD, Ho GY, Beardsley L, et al. Sexual behavior and partner char-
a case–control study. Int J Cancer 1999;82(6):799–803. acteristics are the predominant risk factors for genital human papillo-
[46] Ferrera A, Velema JP, Figueroa M, et al. Co-factors related to the mavirus infection in young women. J Infect Dis 1996;174(4):679–89.
causal relationship between human papillomavirus and invasive cervi- [67] Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicova-
cal cancer in Honduras. Int J Epidemiol 2000;29(5):817–25. ginal papillomavirus infection in young women. N Engl J Med 1998;
[47] Velema JP, Ferrera A, Figueroa M, et al. Burning wood in the kitchen 338(7):423–8.
increases the risk of cervical neoplasia in HPV-infected women in [68] Wheeler CM, Parmenter CA, Hunt WC, et al. Determinants of genital
Honduras. Int J Cancer 2002;97(4):536–41. human papillomavirus infection among cytologically normal women
S16 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

attending the University of New Mexico student health center. Sex [88] Fairley CK, Robinson PM, Chen S, et al. The detection of HPV DNA,
Transm Dis 1993;20(5):286. the size of tampon specimens and the menstrual cycle. Genitourin
[69] Wheeler CM, Greer CE, Becker TM, et al. Short-term fluctuations in Med 1994;70(3):171–4.
the detection of cervical human papillomavirus DNA. Obstet Gynecol [89] Fairley CK, Chen S, Tabrizi SN, et al. The absence of genital human
1996;88(2):261–8. papillomavirus DNA in virginal women. Int J STD AIDS 1992;
[70] Giuliano AR, Denman C, Guernsey dZ, et al. Design and results of the 3(6):414–7.
USA-Mexico border human papillomavirus (HPV), cervical dyspla- [90] Fairley CK, Tabrizi SN, Gourlay SG, et al. A cohort study comparing
sia, and Chlamydia trachomatis study. Rev Panam Salud Publica the detection of HPV DNA from women who stop and continue to
2001;9(3):172–81. smoke. Aust N Z J Obstet Gynaecol 1995;35(2):181–5.
[71] Giuliano AR, Papenfuss M, Abrahamsen M, et al. Differences in fac- [91] Ikenberg H, Maass N, Runge M. HPV 18 in cervical specimens from
tors associated with oncogenic and nononcogenic human papillomavi- the Cook Islands. Int J Cancer 1994;57(1):137.
rus infection at the United States-Mexico border. Cancer Epidemiol [92] Peng HQ, Liu SL, Mann V, et al. Human papillomavirus types 16
Biomarkers Prev 2002;11(9):930–4. and 33, herpes simplex virus type 2 and other risk factors for cervi-
[72] Giuliano AR, Papenfuss M, Abrahamsen M, et al. Human papilloma- cal cancer in Sichuan Province, China. Int J Cancer 1991;
virus infection at the United States-Mexico border: implications for 47(5):711–6.
cervical cancer prevention and control. Cancer Epidemiol Biomarkers [93] Li D, Huang T, Zhang Z. [The relationship between herpes simplex
Prev 2001;10(11):1129–36. virus II, human papillomavirus infection and infertility after artificial
[73] Smith EM, Ritchie JM, Yankowitz J, et al. Human papillomavirus abortion]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi
prevalence and types in newborns and parents: concordance and 1998;12(2):155–7.
modes of transmission. Sex Transm Dis 2004;31(1):57–62. [94] Wu Y, Chen Y, Li L, et al. Associations of high-risk HPV types and
[74] Peyton CL, Gravitt PE, Hunt WC, et al. Determinants of genital hu- viral load with cervical cancer in China. J Clin Virol 2006;
man papillomavirus detection in a US population. J Infect Dis 2001; 35(3):264–9.
183(11):1554–64. [95] Chan MK, Lau KM, Tsui Y, et al. Human papillomavirus infection in
[75] Bauer HM, Hildesheim A, Schiffman MH, et al. Determinants of gen- Hong Kong Chinese women with normal and abnormal cervix—
ital human papillomavirus infection in low-risk women in Portland, detection by polymerase chain reaction method on cervical scrapes.
Oregon. Sex Transm Dis 1993;20(5):274–8. Gynecol Oncol 1996;60(2):217–23.
[76] Schiffman MH, Bauer HM, Hoover RN, et al. Epidemiologic ev- [96] Chan PK, Chang AR, Tam WH, et al. Prevalence and genotype distri-
idence showing that human papillomavirus infection causes most bution of cervical human papillomavirus infection: comparison be-
cervical intraepithelial neoplasia. J Natl Cancer Inst 1993; tween pregnant women and non-pregnant controls. J Med Virol
85(12):958–64. 2002;67(4):583–8.
[77] Liaw KL, Glass AG, Manos MM, et al. Detection of human papillo- [97] Xu S, Liu L, Lu S, et al. Clinical observation on vertical transmission
mavirus DNA in cytologically normal women and subsequent cervical of human papillomavirus. Chin Med Sci J 1998;13(1):29–31.
squamous intraepithelial lesions. J Natl Cancer Inst 1999; [98] Shen YH, Chen F, Huang MN, et al. [Population-based study of hu-
91(11):954–60. man papillomavirus infection in high-risk area for cervical cancer in
[78] Liaw KL, Hildesheim A, Burk RD, et al. A prospective study of hu- Shanxi Province, China]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao
man papillomavirus (HPV) type 16 DNA detection by polymerase 2003;25(4):381–5.
chain reaction and its association with acquisition and persistence of [99] Zhang W, Liu Y, Jin Y, et al. Detection of the HPV16 E6 transforming
other HPV types. J Infect Dis 2001;183(1):8. gene by PCR in tissue samples from normal cervix and from cervix
[79] Cope JU, Hildesheim A, Schiffman MH, et al. Comparison of the hy- with precancerous lesions and carcinomas. Chin Med Sci J 1993;
brid capture tube test and PCR for detection of human papillomavirus 8(3):139–42.
DNA in cervical specimens. J Clin Microbiol 1997;35(9):2262–5. [100] Shen CY, Ho MS, Chang SF, et al. High rate of concurrent genital in-
[80] Sherman ME, Lorincz AT, Scott DR, et al. Baseline cytology, human fections with human cytomegalovirus and human papillomaviruses in
papillomavirus testing, and risk for cervical neoplasia: a 10-year co- cervical cancer patients. J Infect Dis 1993;168(2):449–52.
hort analysis. J Natl Cancer Inst 2003;95(1):46–52. [101] Belinson J, Qiao YL, Pretorius R, et al. Shanxi Province Cervical Can-
[81] Hildesheim A, Gravitt P, Schiffman MH, et al. Determinants of genital cer Screening Study: a cross-sectional comparative trial of multiple
human papillomavirus infection in low-income women in Washing- techniques to detect cervical neoplasia. Gynecol Oncol 2001;
ton, D.C. Sex Transm Dis 1993;20(5):279–85. 83(2):439–44.
[82] Kulasingam SL, Hughes JP, Kiviat NB, et al. Evaluation of human [102] Seshadri L, George SS, Vasudevan B, et al. Cervical intraepithelial
papillomavirus testing in primary screening for cervical abnormalities: neoplasia and human papilloma virus infection in renal transplant re-
comparison of sensitivity, specificity, and frequency of referral. cipients. Indian J Cancer 2001;38(2–4):92–5.
JAMA 2002;288(14):1749–57. [103] Das BC, Sharma JK, Gopalkrishna V, et al. A high frequency of hu-
[83] Giuliano AR, Papenfuss MR, Denman CA, et al. Human papillomavi- man papillomavirus DNA sequences in cervical carcinomas of Indian
rus prevalence at the USA–Mexico border among women 40 years of women as revealed by Southern blot hybridization and polymerase
age and older. Int J STD AIDS 2005;16(3):247–51. chain reaction. J Med Virol 1992;36(4):239–45.
[84] Ratnam S, Franco EL, Ferenczy A. Human papillomavirus testing for [104] Gopalkrishna V, Murthy NS, Sharma JK, et al. Increased human pap-
primary screening of cervical cancer precursors. Cancer Epidemiol illomavirus infection with the increasing number of pregnancies in In-
Biomarkers Prev 2000;9(9):945–51. dian women. J Infect Dis 1995;171(1):254–5.
[85] Sellors JW, Mahony JB, Kaczorowski J, et al. Prevalence and predic- [105] Gopalkrishna V, Aggarwal N, Malhotra VL, et al. Chlamydia tracho-
tors of human papillomavirus infection in women in Ontario, Canada. matis and human papillomavirus infection in Indian women with sex-
Survey of HPV in Ontario Women (SHOW) Group. CMAJ 2000; ually transmitted diseases and cervical precancerous and cancerous
163(5):503–8. lesions. Clin Microbiol Infect 2000;6(2):88–93.
[86] Richardson H, Franco E, Pintos J, et al. Determinants of low-risk and [106] Prusty BK, Kumar A, Arora R, et al. Human papillomavirus (HPV)
high-risk cervical human papillomavirus infections in Montreal Uni- DNA detection in self-collected urine. Int J Gynaecol Obstet 2005;
versity students. Sex Transm Dis 2000;27(2):79–86. 90(3):223–7.
[87] Fairley CK, Chen S, Ugoni A, et al. Human papillomavirus infection [107] Franceschi S, Rajkumar T, Vaccarella S, et al. Human papillomavirus
and its relationship to recent and distant sexual partners. Obstet Gyne- and risk factors for cervical cancer in Chennai, India: a case–control
col 1994;84(5):755–9. study. Int J Cancer 2003;107(1):127–33.
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S17

[108] Bandyopadhyay S, Sen S, Majumdar L, et al. Human papillomavirus [128] Kubota T, Ishi K, Suzuki M, et al. Usefulness of hybrid capture HPV
infection among Indian mothers and their infants. Asian Pac J Cancer DNA assay as a diagnostic tool for human papillomavirus infection.
Prev 2003;4(3):179–84. Kansenshogaku Zasshi 1998;72(11):1219–24.
[109] Sankaranarayanan R, Nene BM, Dinshaw KA, et al. A cluster ran- [129] Yoshikawa H, Nagata C, Noda K, et al. Human papillomavirus infec-
domized controlled trial of visual, cytology and human papillomavi- tion and other risk factors for cervical intraepithelial neoplasia in
rus screening for cancer of the cervix in rural India. Int J Cancer Japan. Br J Cancer 1999;80(3–4):621–4.
2005;116(4):617–23. [130] Takakuwa K, Mitsui T, Iwashita M, et al. Studies on the prevalence of
[110] Laikangbam P, Sengupta S, Bhattacharya P, et al. A comparative pro- human papillomavirus in pregnant women in Japan. J Perinat Med
file of the prevalence and age distribution of human papillomavirus 2006;34(1):77–9.
type 16/18 infections among three states of India with focus on north- [131] Ishi K, Suzuki F, Yamasaki S, et al. Prevalence of human papilloma-
east India. Int J Gynecol Cancer 2007;17(1):107–17. virus infection and correlation with cervical lesions in Japanese
[111] Franceschi S, Rajkumar R, Snijders PJ, et al. Papillomavirus infection women. J Obstet Gynaecol Res 2004;30(5):380–5.
in rural women in southern India. Br J Cancer 2005;92(3):601–6. [132] Lee SA, Kang D, Seo SS, et al. Multiple HPV infection in cervical
[112] Bhattacharya P, Duttagupta C, Sengupta S. Proline homozygosity in cancer screened by HPVDNAChip. Cancer Lett 2003;
codon 72 of p53: a risk genotype for human papillomavirus related 198(2):187–92.
cervical cancer in Indian women. Cancer letters 2002; [133] Song YS, Kee SH, Kim JW, et al. Major sequence variants in E7 gene
188(1–2):207–11. of human papillomavirus type 16 from cervical cancerous and noncan-
[113] Sathish N, Abraham P, Peedicayil A, et al. HPV DNA in plasma of cerous lesions of Korean women. Gynecol Oncol 1997;66(2):275–81.
patients with cervical carcinoma. J Clin Virol 2004;31(3):204–9. [134] Cho NH, An HJ, Jeong JK, et al. Genotyping of 22 human
[114] Sankaranarayanan R, Chatterji R, Shastri SS, et al. Accuracy of human papillomavirus types by DNA chip in Korean women: comparison
papillomavirus testing in primary screening of cervical neoplasia: re- with cytologic diagnosis. Am J Obstet Gynecol 2003;188
sults from a multicenter study in India. Int J Cancer 2004; (1):56–62.
112(2):341–7. [135] Oh YL, Shin KJ, Han J, et al. Significance of high-risk human papil-
[115] Paez C, Konno R, Yaegashi N, et al. Prevalence of HPV DNA in cer- lomavirus detection by polymerase chain reaction in primary cervical
vical lesions in patients from Ecuador and Japan. Tohoku J Exp Med cancer screening. Cytopathology 2001;12(2):75–83.
1996;180(3):261–72. [136] Shin HR, Lee DH, Herrero R, et al. Prevalence of human papilloma-
[116] Karube A, Sasaki M, Tanaka H, et al. Human papilloma virus type 16 virus infection in women in Busan, South Korea. Int J Cancer 2003;
infection and the early onset of cervical cancer. Biochem Biophys Res 103(3):413–21.
Commun 2004;323(2):621–4. [137] Shin HR, Franceschi S, Vaccarella S, et al. Prevalence and determi-
[117] Tanaka H, Karube A, Kodama H, et al. Mass screening for human pap- nants of genital infection with papillomavirus, in female and male uni-
illomavirus type 16 infection in infertile couples. J Reprod Med 2000; versity students in Busan, South Korea. J Infect Dis 2004;
45(11):907–11. 190(3):468–76.
[118] Sasagawa T, Basha W, Yamazaki H, et al. High-risk and multiple hu- [138] An HJ, Cho NH, Lee SY, et al. Correlation of cervical carcinoma and
man papillomavirus infections associated with cervical abnormalities precancerous lesions with human papillomavirus (HPV) genotypes
in Japanese women. Cancer Epidemiol Biomarkers Prev 2001; detected with the HPV DNA chip microarray method. Cancer 2003;
10(1):45–52. 97(7):1672–80.
[119] Nishikawa A, Fukushima M, Shimada M, et al. Relatively low prev- [139] Ngelangel C, Munoz N, Bosch FX, et al. Causes of cervical cancer in
alence of human papillomavirus 16, 18 and 33 DNA in the normal cer- the Philippines: a case–control study. J Natl Cancer Inst 1998;
vices of Japanese women shown by polymerase chain reaction. Jpn 90(1):43–9.
J Cancer Res 1991;82(5):532–8. [140] Yang YY, Koh LW, Tsai JH, et al. Correlation of viral factors with
[120] Azar KK, Tani M, Yasuda H, et al. Increased secretion patterns of in- cervical cancer in Taiwan. J Microbiol Immunol Infect 2004;
terleukin-10 and tumor necrosis factor-alpha in cervical squamous in- 37(5):282–7.
traepithelial lesions. Hum Pathol 2004;35(11):1376–84. [141] Donmez H, Menevse S, Guner H, et al. Detection and typing of human
[121] Sasagawa T, Dong Y, Saijoh K, et al. Human papillomavirus infection papillomavirus DNAs by restriction endonuclease mapping of the
and risk determinants for squamous intraepithelial lesion and cervical PCR products. Isr J Med Sci 1997;33(12):789–93.
cancer in Japan. Jpn J Cancer Res 1997;88(4):376–84. [142] Tsai HT, Wu CH, Lai HL, et al. Association between quantitative
[122] Saegusa M, Hashimura M, Machida D, et al. Down-regulation of high-risk human papillomavirus DNA load and cervical intraepithelial
CD44 standard and variant isoforms during the development and neoplasm risk. Cancer Epidemiol Biomarkers Prev 2005;14(11 Pt
progression of uterine cervical tumours. J Pathol 1999; 1):2544–9.
187(2):173–83. [143] Chang CC, Tseng CJ, Liu WW, et al. Clinical evaluation of a new
[123] Asato T, Maehama T, Nagai Y, et al. A large case–control study of model of self-obtained method for the assessment of genital human
cervical cancer risk associated with human papillomavirus infection papilloma virus infection in an underserved population. Chang
in Japan, by nucleotide sequencing-based genotyping. J Infect Dis Gung Med J 2002;25(10):664–71.
2004;189(10):1829–32. [144] Chang YL, Lin CY, Tseng CJ, et al. Prevalence of genital human pap-
[124] Maehama T, Asato T, Kanazawa K. Prevalence of HPV infection in illomavirus infections in patients at a sexually transmitted diseases
cervical cytology-normal women in Okinawa, Japan, as determined clinic. Eur J Clin Microbiol Infect Dis 1992;11(5):454–7.
by a polymerase chain reaction. Int J Gynaecol Obstet 2000; [145] Liaw KL, Hsing AW, Chen CJ, et al. Human papillomavirus and cer-
69(2):175–6. vical neoplasia: a case-control study in Taiwan. Int J Cancer 1995;
[125] Maehama T, Asato T, Kanazawa K. Prevalence of human papilloma- 62(5):565–71.
virus in cervical swabs in the Okinawa Islands, Japan. Arch Gynecol [146] Thomas DB, Ray RM, Koetsawang A, et al. Human papillomaviruses
Obstet 2002;267(2):64. and cervical cancer in Bangkok. I. Risk factors for invasive cervical
[126] Saito J, Sumiyoshi M, Nakatani H, et al. Dysplasia and HPV infection carcinomas with human papillomavirus types 16 and 18 DNA. Am
initially detected by DNA analysis in cytomorphologically normal J Epidemiol 2001;153(8):723–31.
cervical smears. Int J Gynaecol Obstet 1995;51(1):43–8. [147] Lertworapreecha M, Bhattarakosol P, Niruthisard S. Detection and
[127] Takubo K, Shimomura-Izumiyama N, Koiwai H, et al. Detection of typing of human papillomavirus in cervical intraepithelial neoplasia
human papillomavirus infection of the cervix in very elderly women grade III in Thai women. Southeast Asian J Trop Med Public Health
using PCR. Clin Cancer Res 2005;11(8):2919–23. 1998;29(3):507–11.
S18 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

[148] Bhattarakosol P, Lertworapreecha M, Kitkumthorn N, et al. Survey of [168] Kjaer SK, van den Brule AJ, Bock JE, et al. Determinants for genital
human papillomavirus infection in cervical intraepithelial neoplasia in human papillomavirus (HPV) infection in 1000 randomly chosen
Thai women. J Med Assoc Thai 2002;85(Suppl 1):S360–5. young Danish women with normal Pap smear: are there different
[149] Siritantikorn S, Laiwejpithaya S, Siripanyaphinyo U, et al. Detection risk profiles for oncogenic and nononcogenic HPV types? Cancer Ep-
and typing of human papilloma virus DNAs in normal cervix, intrae- idemiol Biomarkers Prev 1997;6(10):799–805.
pithelial neoplasia and cervical cancer in Bangkok. Southeast Asian [169] Kruger-Kjaer S, van den Brule AJ, Svare EI, et al. Different risk factor
J Trop Med Public Health 1997;28(4):707–10. patterns for high-grade and low-grade intraepithelial lesions on the
[150] Chichareon S, Herrero R, Munoz N, et al. Risk factors for cervical can- cervix among HPV-positive and HPV-negative young women. Int J
cer in Thailand: a case–control study. J Natl Cancer Inst 1998; Cancer 1998;76(5):613–9.
90(1):50–7. [170] Kjaer SK, van den Brule AJ, Paull G, et al. Type specific persistence of
[151] Sukvirach S, Smith JS, Tunsakul S, et al. Population-based human high risk human papillomavirus (HPV) as indicator of high grade cer-
papillomavirus prevalence in Lampang and Songkla. Thailand. J In- vical squamous intraepithelial lesions in young women: population
fect Dis 2003;187(8):1246–56. based prospective follow up study. BMJ 2002;325(7364):572.
[152] Ekalaksananan T, Pientong C, Kotimanusvanij D, et al. The relation- [171] Svare EI, Kjaer SK, Smits HL, et al. Risk factors for HPV detection in
ship of human papillomavirus (HPV) detection to pap smear classifi- archival Pap smears. A population-based study from Greenland and
cation of cervical-scraped cells in asymptomatic women in northeast Denmark. Eur J Cancer 1998;34(8):1230–4.
Thailand. J Obstet Gynaecol Res 2001;27(3):117–24. [172] Kjaer SK, de Villiers EM, Caglayan H, et al. Human papillomavirus,
[153] Sriamporn S, Snijders PJ, Pientong C, et al. Human papillomavirus herpes simplex virus and other potential risk factors for cervical cancer
and cervical cancer from a prospective study in Khon Kaen, Northeast in a high-risk area (Greenland) and a low-risk area (Denmark)—a sec-
Thailand. Int J Gynecol Cancer 2006;16(1):266–9. ond look. Br J Cancer 1993;67(4):830–7.
[154] Settheetham-Ishida W, Yuenyao P, Tassaneeyakul W, et al. Selected [173] Ogunbiyi OA, Scholefield JH, Raftery AT, et al. Prevalence of anal
risk factors, human papillomavirus infection and the P53 codon 72 human papillomavirus infection and intraepithelial neoplasia in renal
polymorphism in patients with squamous intraepithelial lesions allograft recipients. Br J Surg 1994;81(3):365–7.
in Northeastern Thailand. Asian Pacific J Cancer Prev 2006;7(1):113–8. [174] Woodman CB, Collins S, Winter H, et al. Natural history of cervical
[155] de Sanjose S, Bosch XF, Munoz N, et al. Screening for genital human human papillomavirus infection in young women: a longitudinal co-
papillomavirus: results from an international validation study on hu- hort study. Lancet 2001;357(9271):1831–6.
man papillomavirus sampling techniques. Diagn Mol Pathol 1999; [175] Bavin PJ, Giles JA, Hudson E, et al. Comparison of cervical cytology
8(1):26–31. and the polymerase chain reaction for HPV 16 to identify women with
[156] Pham TH, Nguyen TH, Herrero R, et al. Human papillomavirus infec- cervical disease in a general practice population. J Med Virol 1992;
tion among women in South and North Vietnam. Int J Cancer 2003; 37(1):8–12.
104(2):213–20. [176] Cuzick J, Szarewski A, Terry G, et al. Human papillomavirus testing
[157] Eppel W, Worda C, Frigo P, et al. Human papillomavirus in the cervix in primary cervical screening. Lancet 1995;345(8964):1533–6.
and placenta. Obst Gynecol 2000;96(3):337–41. [177] Cuzick J, Beverley E, Ho L, et al. HPV testing in primary screening of
[158] Baay MF, Tjalma WA, Weyler J, et al. Human papillomavirus infec- older women. Br J Cancer 1999;81(3):554–8.
tion in the female population of Antwerp, Belgium: prevalence in [178] Cuzick J. Human papillomavirus testing for primary cervical cancer
healthy women, women with premalignant lesions and cervical can- screening. JAMA 2000;283(1):108–9.
cer. Eur J Gynaecol Oncol 2001;22(3):204–8. [179] Grainge MJ, Seth R, Coupland C, et al. Human papillomavirus infec-
[159] Baay MF, Smits E, Tjalma WA, et al. Can cervical cancer screening be tion in women who develop high-grade cervical intraepithelial neopla-
stopped at 50? The prevalence of HPV in elderly women. Int J Cancer sia or cervical cancer: a case–control study in the UK. Br J Cancer
2004;108(2):258–61. 2005;92(9):1794–9.
[160] Vandenvelde C, Scheen R, Van Pachterbeke C, et al. Prevalence of [180] Grainge MJ, Seth R, Guo L, et al. Cervical human papillomavirus
high risk genital papillomaviruses in the Belgian female population screening among older women. Emerging infectious diseases 2005
determined by fast multiplex polymerase chain reaction. J Med Virol Nov;11(11):1680–5.
1992;36(4):279–82. [181] Puranen MH, Yliskoski MH, Saarikoski SV, et al. Exposure of an in-
[161] Vandenvelde C, Van Beers D. High-risk genital papillomaviruses and fant to cervical human papillomavirus infection of the mother is com-
degree of dysplastic changes in the cervix: a prospective study by fast mon. Am J Obstet Gynecol 1997;176(5):1039–45.
multiplex polymerase chain reaction in Belgium. J Med Virol 1993; [182] Auvinen E, Niemi M, Malm C, et al. High prevalence of HPV among
39(4):273. female students in Finland. Scand J Infect Dis 2005;37(11–12):873–6.
[162] Depuydt CE, Vereecken AJ, Salembier GM, et al. Thin-layer liquid- [183] Rintala MA, Grenman SE, Puranen MH, et al. Transmission of high-
based cervical cytology and PCR for detecting and typing human pap- risk human papillomavirus (HPV) between parents and infant: a pro-
illomavirus DNA in Flemish women. Br J Cancer 2003;88(4):560–6. spective study of HPV in families in Finland. J Clin Microbiol 2005;
[163] Sahebali S, Depuydt CE, Segers K, et al. Cervical cytological screen- 43(1):376–81.
ing and human papillomavirus DNA testing in Flanders. Acta Clin [184] Boulanger JC, Sevestre H, Bauville E, et al. [Epidemiology of HPV
Belg 2003;58(4):211–9. infection]. Gynecol Obstet Fertil 2004;32(3):218–23.
[164] Ramael M, Segers K, Pannemans N, et al. Detection of human papil- [185] Dalstein V, Riethmuller D, Pretet JL, et al. Persistence and load of
lomavirus in cervical scrapings by in situ hybridization and the poly- high-risk HPV are predictors for development of high-grade cervical
merase chain reaction in relation to cytology. Histochem J 1995; lesions: a longitudinal French cohort study. Int J Cancer 2003;
27(1):54–9. 106(3):396–403.
[165] Tachezy R, Hamsikova E, Hajek T, et al. Human papillomavirus ge- [186] Riethmuller D, Gay C, Bertrand X, et al. Genital human papillo-
notype spectrum in Czech women: correlation of HPV DNA presence mavirus infection among women recruited for routine cervical can-
with antibodies against HPV-16, 18, and 33 virus-like particles. J Med cer screening or for colposcopy determined by Hybrid Capture II
Virol 1999;58(4):378–86. and polymerase chain reaction. Diagn Mol Pathol 1999;
[166] Herbsleb M, Knudsen UB, Orntoft TF, et al. Telomerase activity, 8(3):157–64.
MIB-1, PCNA, HPV 16 and p53 as diagnostic markers for cervical in- [187] Humbey O, Aubin F, Cairey-Remonnay S, et al. TP53 polymorphism
traepithelial neoplasia. APMIS 2001;109(9):607–17. at exon 4 in caucasian women from eastern France: lack of correlation
[167] Kjaer SK. Risk factors for cervical neoplasia in Denmark. APMIS with HPV status and grade of cervical precancerous lesions. Eur J Ob-
1998;116(Suppl. 80):5. stet Gynecol Reprod Biol 2002;103(1):60–4.
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S19

[188] Jullian EH, Dhellemmes C, Saglio O, et al. Improved detection of hu- parison with human papillomavirus testing. Gynecol Oncol 2001;
man papillomavirus types 16 and 18 in cervical scrapes by a multiplex 82(2):355–9.
polymerase chain reaction: a 4% prevalence among 120 French [207] Agorastos T, Bontis J, Lambropoulos AF, et al. Epidemiology of hu-
women with normal cytology. Lab Invest 1993;68(2):242–7. man papillomavirus infection in Greek asymptomatic women. Eur J
[189] Beby-Defaux A, Bourgoin A, Ragot S, et al. Human papillomavirus Cancer Prev 1995;4(2):159–67.
infection of the cervix uteri in women attending a Health Examination [208] Lambropoulos AF, Agorastos T, Frangoulides E, et al. Detection of
Center of the French social security. J Med Virol 200473(2):262–8. human papillomavirus using the polymerase chain reaction and typing
[190] Clavel C, Masure M, Bory JP, et al. Human papillomavirus testing in for HPV16 and 18 in the cervical smears of Greek women. J Med Vi-
primary screening for the detection of high-grade cervical lesions: rol 1994;43(3):228–30.
a study of 7932 women. Br J Cancer 2001;84(12):1616–23. [209] Kornya L, Cseh I, Deak J, et al. The diagnostics and prevalence of
[191] Clavel C, Bory JP, Rihet S, et al. Comparative analysis of human pap- genital human papillomavirus (HPV) infection in Hungary. Eur J Ob-
illomavirus detection by hybrid capture assay and routine cytologic stet Gynecol Reprod Biol 2002;100(2):231–6.
screening to detect high-grade cervical lesions. Int J Cancer 1998; [210] Veress G, Csiky-Meszaros T, Konya J, et al. Follow-up of human pap-
75(4):525–8. illomavirus (HPV) DNA and local anti-HPV antibodies in cytologi-
[192] Bory JP, Cucherousset J, Lorenzato M, et al. Recurrent human papil- cally normal pregnant women. Med Microbiol Immunol (Berl)
lomavirus infection detected with the hybrid capture II assay selects 1996;185(3):139–44.
women with normal cervical smears at risk for developing high grade [211] Czegledy J, Batar I, Evander M, et al. Analysis of transforming gene
cervical lesions: a longitudinal study of 3,091 women. Int J Cancer regions of human papillomavirus type 16 in normal cervical smears.
2002;102(5):519–25. Arch Gynecol Obstet 1991;249(4):185–9.
[193] Levert M, Clavel C, Graesslin O, et al. [Human papillomavirus typing [212] Nyari T, Kalmar L, Nyari C, et al. Human papillomavirus infection
in routine cervical smears. Results from a series of 3778 patients]. Gy- and cervical intraepithelial neoplasia in a cohort of low-risk women.
necol Obstet Fertil 2000;28(10):722–8. Eur J Obstet Gynecol Reprod Biol 2006;126(2):246–9.
[194] Baldauf JJ, Dreyfus M, Monlun E, et al. [Role of herpes virus simplex [213] Veress G, Konya J, Csiky-Meszaros T, et al. Human papillomavirus
and cytomegalovirus as cofactors of papillomavirus in dysplastic and DNA and anti-HPV secretory IgA antibodies in cytologically normal
cancerous lesions of the uterine cervix]. Chirurgie 1992; cervical specimens. J Med Virol 1994;43(2):201–7.
118(10):652–8. [214] Garzetti GG, Ciavattini A, Butini L, et al. Cervical dysplasia in HIV-
[195] de Cremoux P, Coste J, Sastre-Garau X, et al. Efficiency of the hybrid seropositive women: role of human papillomavirus infection and im-
capture 2 HPV DNA test in cervical cancer screening. A study by the mune status. Gynecol Obstet Invest 1995;40(1):52–6.
French Society of Clinical Cytology. Am J Clin Pathol 2003; [215] Centurioni MG, Puppo A, Merlo DF, et al. Prevalence of human pap-
120(4):492–9. illomavirus cervical infection in an Italian asymptomatic population.
[196] Kuhler-Obbarius C, Milde-Langosch K, Helling-Giese G, et al. Poly- BMC Infect Dis 2005;5:77.
merase chain reaction-assisted papillomavirus detection in cervicova- [216] Gradilone A, Vercillo R, Napolitano M, et al. Prevalence of human
ginal smears: stratification by clinical risk and cytology reports. papillomavirus, cytomegalovirus, and Epstein-Barr virus in the cervix
Virchows Arch 1994;425(2):157–63. of healthy women. J Med Virol 1996;50(1):1–4.
[197] Bollmann R, Bankfalvi A, Griefingholt H, et al. Validity of combined [217] Uberti-Foppa C, Origoni M, Maillard M, et al. Evaluation of the de-
cytology and human papillomavirus (HPV) genotyping with adjuvant tection of human papillomavirus genotypes in cervical specimens
DNA-cytometry in routine cervical screening: results from 31031 by hybrid capture as screening for precancerous lesions in HIV-posi-
women from the Bonn-region in West Germany. Oncol Rep 2005; tive women. J Med Virol 1998;56(2):133–7.
13(5):915–22. [218] Torrisi A, Del Mistro A, Onnis GL, et al. Colposcopy, cytology and
[198] Schneider A, Hoyer H, Lotz B, et al. Screening for high-grade cervical HPV-DNA testing in HIV-positive and HIV-negative women. Eur J
intra-epithelial neoplasia and cancer by testing for high-risk HPV, rou- Gynaecol Oncol 2000;21(2):168–72.
tine cytology or colposcopy. Int J Cancer 2000;89(6):529–34. [219] Badaracco G, Venuti A, Di Lonardo A, et al. Concurrent HPV infec-
[199] Petry KU, Menton S, Menton M, et al. Inclusion of HPV testing in tion in oral and genital mucosa. J Oral Pathol Med 1998;27(3):130–4.
routine cervical cancer screening for women above 29 years in Ger- [220] Ronco G, Ghisetti V, Segnan N, et al. Prevalence of human papilloma-
many: results for 8466 patients. Br J Cancer 2003;88(10):1570–7. virus infection in women in Turin, Italy. Eur J Cancer 2005;
[200] Speich N, Schmitt C, Bollmann R, et al. Human papillomavirus 41(2):297–305.
(HPV) study of 2916 cytological samples by PCR and DNA sequenc- [221] Pasetto N, Sesti F, De Santis L, et al. The prevalence of HPV16DNA
ing: genotype spectrum of patients from the west German area. J Med in normal and pathological cervical scrapes using the polymerase
Microbiol 2004;53(Pt 2):125–8. chain reaction. Gynecol Oncol 1992;46(1):33–6.
[201] Zahm DM, Nindl I, Greinke C, et al. Colposcopic appearance of cer- [222] Astori G, Arzese A, Pipan C, et al. Characterization of a putative new
vical intraepithelial neoplasia is age dependent. Am J Obstet Gynecol HPV genomic sequence from a cervical lesion using L1 consensus
1998;179(5):1298–304. primers and restriction fragment length polymorphism. Virus Res
[202] Strehler E, Sterzik K, Malthaner D, et al. Influence of ovarian stimu- 1997;50(1):57–63.
lation on the detection of human papillomavirus DNA in cervical [223] Tenti P, Zappatore R, Migliora P, et al. Latent human papillomavirus
scrapes obtained from patients undergoing assisted reproductive tech- infection in pregnant women at term: a case–control study. J Infect Dis
niques. Fertil Steril 1999;71(5):815–20. 1997;176(1):277–80.
[203] Agorastos T, Dinas K, Lloveras B, et al. Cervical human papillomavi- [224] Venturoli S, Cricca M, Bonvicini F, et al. Human papillomavirus
rus infection in women attending gynaecological outpatient clinics in DNA testing by PCR-ELISA and hybrid capture II from a single cy-
northern Greece. Eur J Cancer Prev 2004;13(2):145–7. tological specimen: concordance and correlation with cytological re-
[204] Agorastos T, Dinas K, Lloveras B, et al. Human papillomavirus test- sults. J Clin Virol 2002;25(2):177.
ing for primary screening in women at low risk of developing cervical [225] Branca M, Garbuglia AR, Benedetto A, et al. Factors predicting the
cancer. The Greek experience. Gynecol Oncol 2005;96(3):714–20. persistence of genital human papillomavirus infections and PAP
[205] Agorastos T, Dinas K, Lloveras B, et al. Self-sampling versus physi- smear abnormality in HIV-positive and HIV-negative women during
cian-sampling for human papillomavirus testing. Int J STD AIDS prospective follow-up. Int J STD AIDS 2003;14(6):417–25.
2005;16(11):727–9. [226] Silins I, Wang X, Tadesse A, et al. A population-based study of cer-
[206] Paraskevaidis E, Malamou-Mitsi V, Koliopoulos G, et al. Expanded vical carcinoma and HPV infection in Latvia. Gynecol Oncol 2004;
cytological referral criteria for colposcopy in cervical screening: com- 93(2):484–92.
S20 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

[227] de Roda Husman AM, Walboomers JM, Hopman E, et al. HPV prev- [247] Margall N, Matias-Guiu X, Chillon M, et al. Detection of human pap-
alence in cytomorphologically normal cervical scrapes of pregnant illomavirus 16 and 18 DNA in epithelial lesions of the lower genital
women as determined by PCR: the age-related pattern. J Med Virol tract by in situ hybridization and polymerase chain reaction: cervical
1995;46(2):97–102. scrapes are not substitutes for biopsies. J Clin Microbiol 1993;
[228] Jacobs MV, Walboomers JM, Snijders PJ, et al. Distribution of 37 mu- 31(4):924–30.
cosotropic HPV types in women with cytologically normal cervical [248] de Sanjose S, Almirall R, Lloveras B, et al. Cervical human papilloma-
smears: the age-related patterns for high-risk and low-risk types. Int virus infection in the female population in Barcelona, Spain. Sex
J Cancer 2000;87(2):221–7. Transm Dis 2003;30(10):788–93.
[229] Melkert PW, Hopman E, van den Brule AJ, et al. Prevalence of HPV [249] Mugica-Van Herckenrode C, Malcolm AD, Coleman DV. Prevalence
in cytomorphologically normal cervical smears, as determined by the of human papillomavirus (HPV) infection in Basque Country women
polymerase chain reaction, is age-dependent. Int J Cancer 1993; using slot-blot hybridization: a survey of women at low risk of devel-
53(6):919–23. oping cervical cancer. Int J Cancer 1992;51(4):581–6.
[230] van der Graaf Y, Molijn A, Doornewaard H, et al. Human papilloma- [250] Simons AM, Mugica vH, Rodriguez JA, et al. Demonstration of
virus and the long-term risk of cervical neoplasia. Am J Epidemiol smoking-related DNA damage in cervical epithelium and correlation
2002;156(2):158–64. with human papillomavirus type 16, using exfoliated cervical cells. Br
[231] Zielinski GD, Snijders PJ, Rozendaal L, et al. HPV presence precedes J Cancer 1995;71(2):246–9.
abnormal cytology in women developing cervical cancer and signals [251] Andersson-Ellstrom A, Hagmar BM, Johansson B, et al. Human pap-
false negative smears. Br J Cancer 2001;85(3):398–404. illomavirus deoxyribonucleic acid in cervix only detected in girls after
[232] Gjooen K, Olsen AO, Magnus P, et al. Prevalence of human papillo- coitus. Int J STD AIDS 1996;7(5):333–6.
mavirus in cervical scrapes, as analyzed by PCR, in a population- [252] Dillner L, Fredriksson A, Persson E, et al. Antibodies against papillo-
based sample of women with and without cervical dysplasia. APMIS mavirus antigens in cervical secretions from condyloma patients. J
1996;104(1):68–74. Clin Microbiol 1993;31(2):192–7.
[233] Olsen AO, Dillner J, Gjoen K, et al. Seropositivity against HPV 16 [253] Rylander E, Ruusuvaara L, Almstromer MW, et al. The absence
capsids: a better marker of past sexual behaviour than presence of of vaginal human papillomavirus 16 DNA in women who have
HPV DNA. Genitourin Med 1997;73(2):131–5. not experienced sexual intercourse. Obstet Gynecol 1994;83
[234] Olsen AO, Gjoen K, Sauer T, et al. Human papillomavirus and cervi- (5 Pt 1):735–45.
cal intraepithelial neoplasia grade II-III: a population-based case–con- [254] Wallin KL, Wiklund F, Angstrom T, et al. Type-specific persistence of
trol study. Int J Cancer 1995;61(3):312–5. human papillomavirus DNA before the development of invasive cer-
[235] Olsen AO, Dillner J, Skrondal A, et al. Combined effect of smoking vical cancer. N Engl J Med 1999;341(22):1633–8.
and human papillomavirus type 16 infection in cervical carcinogene- [255] Hagmar B, Kalantari M, Skyldberg B, et al. Human papillomavirus in
sis. Epidemiology 1998;9(3):346. cell samples from Stockholm Gynecologic Health Screening. Acta
[236] Molden T, Kraus I, Karlsen F, et al. Comparison of human papilloma- Cytol 1995;39(4):741–5.
virus messenger RNA and DNA detection: a cross-sectional study of [256] Evander M, Edlund K, Gustafsson A, et al. Human papillomavirus in-
4,136 women >30 years of age with a 2-year follow-up of high-grade fection is transient in young women: a population-based cohort study.
squamous intraepithelial lesion. Cancer Epidemiol Biomarkers Prev J Infect Dis 1995;171(4):1026–30.
2005;14(2):367–72. [257] Karlsson R, Jonsson M, Edlund K, et al. Lifetime number of partners
[237] Lie AK, Isaksen CV, Skarsvag S, et al. Human papillomavirus (HPV) as the only independent risk factor for human papillomavirus infec-
in high-grade cervical intraepithelial neoplasia (CIN) detected by mor- tion: a population-based study. Sex Transm Dis 1995;22(2):119–27.
phology and polymerase chain reaction (PCR)—a cytohistologic cor- [258] Czegledy J, Rylander E, Evander M, et al. Relation between the pres-
relation of 277 cases treated by laser conization. Cytopathology 1999; ence of human papillomavirus type 16 deoxyribonucleic acid in cervi-
10(2):112–21. covaginal cells and general health condition. Am J Obstet Gynecol
[238] Dybikowska A, Licznerski P, Podhajska A. HPV detection in cervical 1993;169(2 Pt 1):386–8.
cancer patients in northern Poland. Oncol Rep 2002;9(4):871–4. [259] Ylitalo N, Josefsson A, Melbye M, et al. A prospective study showing
[239] Biernat I, Szczudrawa A, Tomaszczyk J, et al. [HPV infection in preg- long-term infection with human papillomavirus 16 before the devel-
nant women]. Ginekol Pol 2003;74(10):1066–9. opment of cervical carcinoma in situ. Cancer Res 2000;
[240] Szostek S, Klimek M, Zawilinska B, et al. Detection of human papil- 60(21):6027–32.
lomavirus in cervical cell specimens by hybrid capture and PCR with [260] Ylitalo N, Sorensen P, Josefsson A, et al. Smoking and oral contracep-
different primers. Acta Biochim Pol 2006;53(3):603–7. tives as risk factors for cervical carcinoma in situ. Int J Cancer 1999;
[241] Zietkowiak W, Zimna K, Sroka L, et al. [Frequency of HPV infection 81(3):357–65.
of the uterine cervix among perimenopausal women in Wielkopolska [261] Gustafsson L, Sparen P, Gustafsson M, et al. Efficiency of organised
Region]. Ginekol Pol 2002;73(11):939–44. and opportunistic cytological screening for cancer in situ of the cervix.
[242] Gajewska M, Marianowski L, Wielgos M, et al. The occurrence of Br J Cancer 1995;72(2):498–505.
genital types of human papillomavirus in normal pregnancy and in [262] Stenvall H, Wikstrom I, Wilander E. High prevalence of oncogenic
pregnant women with pregestational insulin dependent diabetes mel- human papilloma virus in women not attending organized cytological
litus. Neuro Endocrinol Lett 2005;26(6):766–70. screening. Acta Derm Venereol 2007;87(3):243–5.
[243] Aleksandrova I, Lyshchev AA, Safronnikova NR, et al. [Papillomavi- [263] Kjellberg L, Wiklund F, Sjoberg I, et al. A population-based study of
rus infection in healthy women from St. Petersburg]. Vopr Onkol human papillomavirus deoxyribonucleic acid testing for predicting
2000;46(2):175–9. cervical intraepithelial neoplasia. Am J Obstet Gynecol 1998;179(6
[244] Alexandrova YN, Lyshchov AA, Safronnikova NR, et al. Features of Pt 1):1497–502.
HPV infection among the healthy attendants of gynecological practice [264] Kjellberg L, Hallmans G, Ahren AM, et al. Smoking, diet, pregnancy
in St. Petersburg, Russia. Cancer Lett 1999;145(1–2):43–8. and oral contraceptive use as risk factors for cervical intra-epithelial
[245] Syrjanen S, Shabalova I, Petrovichev N, et al. Age-specific incidence neoplasia in relation to human papillomavirus infection. Br J Cancer
and clearance of high-risk human papillomavirus infections in women 2000;82(7):1332.
in the former Soviet Union. Int J STD AIDS 2005;16(3):217–23. [265] Andersson-Ellstrom A, Dillner J, Hagmar B, et al. Comparison of de-
[246] Cuschieri KS, Cubie HA, Whitley MW, et al. Multiple high risk HPV velopment of serum antibodies to HPV16 and HPV33 and acquisition
infections are common in cervical neoplasia and young women in of cervical HPV DNA among sexually experienced and virginal young
a cervical screening population. J Clin Pathol 2004;57(1):68–72. girls. A longitudinal cohort study. Sex Transm Dis 1996;23(3):234–8.
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S21

[266] Hansson BG, Forslund O, Bjerre B, et al. Human papilloma virus [286] Jacobson DL, Womack SD, Peralta L, et al. Concordance of human
types in routine cytological screening and at colposcopic examina- papillomavirus in the cervix and urine among inner city adolescents.
tions. Eur J Obstet Gynecol Reprod Biol 1993;52(1):49–55. Pediatr Infect Dis J 2000;19(8):722–8.
[267] Forslund O, Antonsson A, Edlund K, et al. Population-based type-spe- [287] Holly EA, Ralston ML, Darragh TM, et al. Prevalence and risk factors
cific prevalence of high-risk human papillomavirus infection in mid- for anal squamous intraepithelial lesions in women. J Natl Cancer Inst
dle-aged Swedish women. J Med Virol 2002;66(4):535–41. 2001;93(11):843–9.
[268] Hinchliffe SA, van Velzen D, Korporaal H, et al. Transience of cervi- [288] Massad LS, Ahdieh L, Benning L, et al. Evolution of cervical abnor-
cal HPV infection in sexually active, young women with normal cer- malities among women with HIV-1: evidence from surveillance cytol-
vicovaginal cytology. Br J Cancer 1995;72(4):943–5. ogy in the women’s interagency HIV study. J Acquir Immune Defic
[269] Bigras G, de Marval F. The probability for a Pap test to be abnormal is Syndr 2001;27(5):432–42.
directly proportional to HPV viral load: results from a Swiss study [289] Minkoff H, Ahdieh L, Massad LS, et al. The effect of highly active
comparing HPV testing and liquid-based cytology to detect cervical antiretroviral therapy on cervical cytologic changes associated with
cancer precursors in 13,842 women. Br J Cancer 2005;93(5):575–81. oncogenic HPV among HIV-infected women. Aids 2001;
[270] Ludicke F, Stalberg A, Vassilakos P, et al. High- and intermediate-risk 15(16):2157–64.
human papillomavirus infection in sexually active adolescent females. [290] Minkoff H, Feldman JG, Strickler HD, et al. Relationship between
J Pediatr Adolesc Gynecol 2001;14(4):171–4. smoking and human papillomavirus infections in HIV-infected and
[271] Cuzick J, Szarewski A, Cubie H, et al. Management of women who -uninfected women. J Infect Dis 2004;189(10):1821–8.
test positive for high-risk types of human papillomavirus: the [291] Palefsky JM, Holly EA, Ralston ML, et al. Prevalence and risk factors
HART study. Lancet 2003;362(9399):1871–6. for anal human papillomavirus infection in human immunodeficiency
[272] Ahmed MI, Salahy EE, Fayed ST, et al. Human papillomavirus infec- virus (HIV)-positive and high-risk HIV-negative women. J Infect Dis
tion among Egyptian females with cervical carcinoma: relationship to 2001;183(3):383–91.
spontaneous apoptosis and TNF-alpha. Clin Biochem 2001; [292] Palefsky JM, Minkoff H, Kalish LA, et al. Cervicovaginal human pap-
34(6):491–8. illomavirus infection in human immunodeficiency virus-1 (HIV)-pos-
[273] Mroueh AM, Seoud MA, Kaspar HG, et al. Prevalence of genital hu- itive and high-risk HIV-negative women. J Natl Cancer Inst 1999;
man papillomavirus among Lebanese women. Eur J Gynaecol Oncol 91(3):226–36.
2002;23(5):429–32. [293] Strickler HD, Palefsky JM, Shah KV, et al. Human papillomavirus
[274] Guney AI, Ince U, Kullu S, et al. Detection and typing of human pap- type 16 and immune status in human immunodeficiency virus-sero-
illomavirus in cervical specimens of Turkish women. Eur J Gynaecol positive women. J Natl Cancer Inst 2003;95(14):1062–71.
Oncol 1997;18(6):546–50. [294] Coutlee F, Hankins C, Lapointe N. Comparison between vaginal tam-
[275] Langley CL, Benga-De E, Critchlow CW, et al. HIV-1, HIV-2, human pon and cervicovaginal lavage specimen collection for detection of
papillomavirus infection and cervical neoplasia in high-risk African human papillomavirus DNA by the polymerase chain reaction. The
women. AIDS 1996;10(4):413–7. Canadian Women’s HIV Study Group. J Med Virol 1997;51(1):42–7.
[276] Marais DJ, Vardas E, Ramjee G, et al. The impact of human immuno- [295] Hankins C, Coutlee F, Lapointe N, et al. Prevalence of risk factors as-
deficiency virus type 1 status on human papillomavirus (HPV) prev- sociated with human papillomavirus infection in women living with
alence and HPV antibodies in serum and cervical secretions. HIV. Canadian Women’s HIV Study Group. CMAJ 1999;
J Infect Dis 2000;182(4):1239–42. 160(2):185–91.
[277] Seck AC, Faye MA, Critchlow CW, et al. Cervical intraepithelial neo- [296] Ford K, Reed BD, Wirawan DN, et al. The Bali STD/AIDS study: hu-
plasia and human papillomavirus infection among Senegalese women man papillomavirus infection among female sex workers. Int J STD
seropositive for HIV-1 or HIV-2 or seronegative for HIV. Int J STD AIDS 2003;14(10):681–7.
AIDS 1994;5(3):189–93. [297] Morris BJ, Rose BR, Flanagan JL, et al. Automated polymerase chain
[278] Baay MF, Kjetland EF, Ndhlovu PD, et al. Human papillomavirus in reaction for papillomavirus screening of cervicovaginal lavages: com-
a rural community in Zimbabwe: the impact of HIV co-infection on parison with dot-blot hybridization in a sexually transmitted diseases
HPV genotype distribution. J Med Virol 2004;73(3):481–5. clinic population. J Med Virol 1990;32(1):22–30.
[279] Levi JE, Fernandes S, Tateno AF, et al. Presence of multiple human [298] Canadas MP, Bosch FX, Junquera ML, et al. Concordance of preva-
papillomavirus types in cervical samples from HIV-infected women. lence of human papillomavirus DNA in anogenital and oral infections
Gynecol Oncol 2004;92(1):225–31. in a high-risk population. J Clini Microbiology 2004;42(3):1330–2.
[280] Levi JE, Fink MC, Canto CL, et al. Human papillomavirus preva- [299] Walker F, Bedel C, Dauge-Geffroy MC, et al. Improved detection of
lence, viral load and cervical intraepithelial neoplasia in HIV-infected human papillomavirus infection in genital intraepithelial neoplasia in
women. Braz J Infect Dis 2002;6(3):129–35. human immunodeficiency virus positive (HIV þ) women by polymer-
[281] Juarez-Figueroa LA, Wheeler CM, Uribe-Salas FJ, et al. Human pap- ase chain reaction-in situ hybridization. Diagn Mol Pathol 1996;
illomavirus: a highly prevalent sexually transmitted disease agent 5(2):136–46.
among female sex workers from Mexico City. Sex Transm Dis [300] Lillo FB, Ferrari D, Veglia F, et al. Human papillomavirus infection
2001;28(3):125–30. and associated cervical disease in human immunodeficiency virus-in-
[282] Hernandez DE, Cohen A, Fisher D, et al. Antibody levels against ga- fected women: effect of highly active antiretroviral therapy. J Infect
lactosyl (alpha1 –> 3) galactose epitopes in cervical mucus from pa- Dis 2001;184(5):547–51.
tients with human papillomavirus infection. Gynecol Oncology 2002; [301] Ammatuna P, Giovannelli L, Giambelluca D, et al. Presence of human
84(3):374–7. papillomavirus and Epstein-Barr virus in the cervix of women infected
[283] Suarez Rincon AE, Vazquez VE, Ramirez RM, et al. [Squamous intra- with the human immunodeficiency virus. J Med Virol 2000;
epithelial lesions in HIV seropositive females. Their frequency and as- 62(4):410–5.
sociation with cervical neoplasia risk factors]. Ginecol Obstet Mex [302] Spinillo A, Debiaggi M, Zara F, et al. Human immunodeficiency virus
2003;71:32–43. type 1-related nucleic acids and papillomavirus DNA in cervicovagi-
[284] Garcia F, Barker B, Santos C, et al. Cross-sectional study of patient- nal secretions of immunodeficiency virus-infected women. Obstet Gy-
and physician-collected cervical cytology and human papillomavirus. necol 2001;97(6):999–1004.
Obstet Gynecol 2003;102(2):266–72. [303] Kjaer SK, Svare EI, Worm AM, et al. Human papillomavirus infection
[285] Ferrera A, Melchers WJ, Velema JP, et al. Association of infections in Danish female sex workers. Decreasing prevalence with age despite
with human immunodeficiency virus and human papillomavirus in continuously high sexual activity. Sex Transm Dis 2000;
Honduras. Am J Trop Med Hyg 1997;57(2):138–41. 27(8):438–45.
S22 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

[304] Thomas DB, Ray RM, Kuypers J, et al. Human papillomaviruses and [325] Perez LO, Barbisan G, Abba MC, et al. Herpes simplex virus and hu-
cervical cancer in Bangkok. III. The role of husbands and commercial man papillomavirus infection in cervical disease in Argentine women.
sex workers. Am J Epidemiol 2001;153(8):740–8. Int J Gynecol Pathol 2006;25(1):42–7.
[305] Lipsey M, Wilson D. Practical Meta-Analysis. Thousand Oaks, CA: [326] Picconi MA, Gronda J, Alonio LV, et al. [Human Papilloma virus
Sage Publications Inc., 2001. in Quechua women from Jujuy with high frequency of cervical
[306] Smith JS, Robinson NJ. Age-specific prevalence of infection with her- cancer: viral types and HPV-16 variants]. Medicina 2002;
pes simplex virus types 2 and 1: a global review. J Infect Dis 2002; 62(3):209–20.
186(Suppl 1):S3–28. [327] Cervantes J, Lema C, Hurtado L, et al. Prevalence of human papillo-
[307] Ho GY, Studentsov YY, Bierman R, et al. Natural history of human mavirus infection in rural villages of the Bolivian Amazon. Rev Inst
papillomavirus type 16 virus-like particle antibodies in young women. Med Trop Sao Paulo 2003;45(3):131–5.
Cancer Epidemiol Biomarkers Prev 2004;13(1):110. [328] Franco EL, Villa LL, Ruiz A, et al. Transmission of cervical human
[308] Manhart LE, Holmes KK, Koutsky LA, et al. Human papillomavirus papillomavirus infection by sexual activity: differences between low
infection among sexually active young women in the United States: and high oncogenic risk types. J Infect Dis 1995;172(3):756–63.
implications for developing a vaccination strategy. Sex Transm Dis [329] Naud P, Matos J, Hammes L, et al. Factors predicting intermediate
2006;33(8):502–8. endpoints of cervical cancer and exposure to human papillomavirus
[309] Clifford GM, Rana RK, Franceschi S, et al. Human papillomavirus ge- (HPV) infections in young women screened as potential targets for
notype distribution in low-grade cervical lesions: comparison by geo- prophylactic HPV vaccination in south of Brazil. Eur J Obstet Gyne-
graphic region and with cervical cancer. Cancer Epidemiol col Reprod Biol 2006;124(1):110–8.
Biomarkers Prev 2005;14(5):1157–64. [330] Lorenzato FR, Singer A, Ho L, et al. Human papillomavirus detection
[310] Koshiol JE, Lindsay L, Pimenta JM, et al. A systematic review of hu- for cervical cancer prevention with polymerase chain reaction in self-
man papillomavirus persistence and cervical neoplasia. Am J Epide- collected samples. Am J Obstet Gynecol 2002;186(5):962–8.
miol 2008;168(2):123–37. [331] Carvalho MO, Almeida RW, Leite FM, et al. Detection of human pap-
[311] Cuschieri KS, Cubie HA, Whitley MW, et al. Persistent high risk HPV illomavirus DNA by the hybrid capture assay. Braz J Infect Dis 2003;
infection associated with development of cervical neoplasia in a pro- 7(2):121–5.
spective population study. J Clin Pathol 2005;58(9):946–50. [332] Franco EL, Villa LL, Sobrinho JP, et al. Epidemiology of acquisition
[312] Ogilvie GS, Patrick DM, Schulzer M, et al. Diagnostic accuracy of self and clearance of cervical human papillomavirus infection in women
collected vaginal specimens for human papillomavirus compared to from a high-risk area for cervical cancer. J Infect Dis 1999;
clinician collected human papillomavirus specimens: a meta-analysis. 180(5):1415–23.
Sex Transm Infect 2005;81(3):207–12. [333] Schlecht NF, Kulaga S, Robitaille J, et al. Persistent human papilloma-
[313] Hildesheim A, Herrero R, Wacholder S, et al. Effect of human papil- virus infection as a predictor of cervical intraepithelial neoplasia.
lomavirus 16/18 L1 viruslike particle vaccine among young women JAMA 2001;286(24):3106–14.
with preexisting infection: a randomized trial. JAMA 2007; [334] Bosch FX, Munoz N, de Sanjose S, et al. Human papillomavirus and
298(7):743–53. cervical intraepithelial neoplasia grade III/carcinoma in situ: a case–
[314] Wright TC Jr, Huh WK, Monk BJ, et al. Age considerations when vac- control study in Spain and Colombia. Cancer Epidemiol Biomarkers
cinating against Human papillomavirus. Gynecol Oncol 2008; in press. Prev 1993;2(5):415–22.
[315] Hammouda D, Munoz N, Herrero R, et al. Cervical carcinoma in Al- [335] Bosch FX, Munoz N, de Sanjose S, et al. Risk factors for cervical can-
giers, Algeria: human papillomavirus and lifestyle risk factors. Int J cer in Colombia and Spain. International journal of cancer 1992;
Cncer 2005;113(3):483–9. 52(5):750–8.
[316] La Ruche G, Leroy V, Mensah-Ado I, et al. Short-term follow up of [336] Bosch FX, Munoz N, de Sanjose S, et al. Importance of human pap-
cervical squamous intraepithelial lesions associated with HIV and hu- illomavirus endemicity in the incidence of cervical cancer: an exten-
man papillomavirus infections in Africa. Int J STD AIDS sion of the hypothesis on sexual behavior. Cancer Epidemiol
199910(6):363–368. Biomarkers Prev 1994;3(5):375–9.
[317] La Ruche G, You B, Mensah-Ado I, et al. Human papillomavirus and [337] Guerrero E, Daniel RW, Bosch FX, et al. Comparison of ViraPap,
human immunodeficiency virus infections: relation with cervical dys- Southern hybridization, and polymerase chain reaction methods for
plasia-neoplasia in African women. Int J Cancer 1998;76(4):480–6. human papillomavirus identification in an epidemiological investiga-
[318] Dallabetta GA, Miotti PG, Chiphangwi JD, et al. High socioeconomic tion of cervical cancer. J Clin Microbiol 1992;30(11):2951–9.
status is a risk factor for human immunodeficiency virus type 1 (HIV- [338] Munoz N, Bosch FX, de Sanjose S, et al. The causal link between hu-
1) infection but not for sexually transmitted diseases in women in Ma- man papillomavirus and invasive cervical cancer: a population-based
lawi: implications for HIV-1 control. J Infect Dis 1993;167(1):36–42. case–control study in Colombia and Spain. Int J Cancer 1992;
[319] Miotti PG, Dallabetta GA, Daniel RW, et al. Cervical abnormalities, 52(5):743–9.
human papillomavirus, and human immunodeficiency virus infections [339] Munoz N, Bosch FX, de Sanjose S, et al. Risk factors for cervical in-
in women in Malawi. J Infect Dis 1996;173(3):714. traepithelial neoplasia grade III/carcinoma in situ in Spain and Colom-
[320] Chaouki N, Bosch FX, Munoz N, et al. The viral origin of cervical bia. Cancer Epidemiol Biomarkers Prev 1993;2(5):423–31.
cancer in Rabat, Morocco. Int J Cancer 1998;75(4):546–54. [340] Munoz N, Kato I, Bosch FX, et al. Risk factors for HPV DNA detec-
[321] Astori G, Beltrame A, Pipan C, et al. PCR-RFLP-detected human pap- tion in middle-aged women. Sex Transm Dis 1996;23(6):504–10.
illoma virus infection in a group of senegalese women attending an [341] Hamsikova E, Novak J, Hofmannova V, et al. Presence of antibodies
STD clinic and identification of a new HPV-68 subtype. Intervirology to seven human papillomavirus type 16-derived peptides in cervical
1999;42(4):221–7. cancer patients and healthy controls. J Infect Dis 1994;
[322] Wright TC Jr, Denny L, Kuhn L, et al. HPV DNA testing of self-col- 170(6):1424–31.
lected vaginal samples compared with cytologic screening to detect [342] Strickler HD, Viscidi R, Escoffery C, et al. Adeno-associated virus
cervical cancer. JAMA 2000;283(1):81–6. and development of cervical neoplasia. J Med Virol 1999;59(1):60–5.
[323] Abba MC, Villaverde LM, Gomez MA, et al. The p53 codon 72 ge- [343] Berumen J, Miranda EI, Zafra G, et al. [Molecular epidemiology of
notypes in HPV infection and cervical disease. Eur J Obstet Gynecol high-incidence cancers in Mexico]. Gac Med Mex 1997;133(Suppl
Reprod Biol 2003;109(1):63–6. 1):35–41.
[324] Golijow CD, Perez LO, Smith JS, et al. Human papillomavirus DNA [344] Hernandez-Avila M, Lazcano-Ponce EC, Berumen-Campos J, et al.
detection and typing in male urine samples from a high-risk popula- Human papilloma virus 16-18 infection and cervical cancer in Mex-
tion from Argentina. J Virol Methods 2005;124(1–2):217–20. ico: a case–control study. Arch Med Res 1997;28(2):265–71.
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S23

[345] Torroella-Kouri M, Morsberger S, Carrillo A, et al. HPV prevalence [367] Fife KH, Katz BP, Brizendine EJ, et al. Cervical human papillomavi-
among Mexican women with neoplastic and normal cervixes. Gyne- rus deoxyribonucleic acid persists throughout pregnancy and de-
col Oncol 1998;70(1):115–20. creases in the postpartum period. Am J Obstet Gynecol 1999;
[346] Berumen J, Ordonez RM, Lazcano E, et al. Asian–American variants 180(5):1110–4.
of human papillomavirus 16 and risk for cervical cancer: a case–con- [368] Fife KH, Katz BP, Roush J, et al. Cancer-associated human papillo-
trol study. J Natl Cancer Inst 2001;93(17):1325–30. mavirus types are selectively increased in the cervix of women in
[347] Hernandez-Giron C, Smith JS, Lorincz A, et al. High-risk human pap- the first trimester of pregnancy. Am J Obstet Gynecol 1996;
illomavirus detection and related risk factors among pregnant and 174(5):1487–93.
nonpregnant women in Mexico. Sex Transm Dis 2005;32(10):613–8. [369] Smith EM, Johnson SR, Figuerres EJ, et al. The frequency of human
[348] Rolon PA, Smith JS, Munoz N, et al. Human papillomavirus infection papillomavirus detection in postmenopausal women on hormone re-
and invasive cervical cancer in Paraguay. Int J Cancer 2000; placement therapy. Gynecol Oncol 1997;65(3):441–6.
85(4):486–91. [370] Smith EM, Johnson SR, Ritchie JM, et al. Persistent HPV infection in
[349] Klug SJ, Wilmotte R, Santos C, et al. TP53 polymorphism, HPV in- postmenopausal age women. Int J Gynaecol Obstet 2004;
fection, and risk of cervical cancer. Cancer Epidemiol Biomarkers 87(2):131–7.
Prev 2001;10(9):1009–12. [371] Smith EM, Ritchie JM, Levy BT, et al. Prevalence and persistence of
[350] Moreno V, Bosch FX, Munoz N, et al. Effect of oral contraceptives on human papillomavirus in postmenopausal age women. Cancer Detect
risk of cervical cancer in women with human papillomavirus infec- Prev 2003;27(6):472–80.
tion: the IARC multicentric case–control study. Lancet 2002; [372] Palmisano ME, Gaffga AM, Daigle J, et al. Detection of human pap-
359(9312):1085–92. illomavirus DNA in self-administered vaginal swabs as compared to
[351] Santos C, Munoz N, Klug S, et al. HPV types and cofactors causing cervical swabs. Int J STD AIDS 2003;14(8):560–2.
cervical cancer in Peru. Br J Cancer 2001;85(7):966–71. [373] Cibas ES, Hong X, Crum CP, et al. Age-specific detection of high risk
[352] Healey SM, Aronson KJ, Mao Y, et al. Oncogenic human papilloma- HPV DNA in cytologically normal, computer-imaged ThinPrep Pap
virus infection and cervical lesions in aboriginal women of Nunavut, samples. Gynecol Oncol 2007;104(3):702–6.
Canada. Sex Transm Dis 2001;28(12):694–700. [374] Schiff M, Miller J, Masuk M, et al. Contraceptive and reproductive
[353] Sellors JW, Karwalajtys TL, Kaczorowski JA, et al. Prevalence of in- risk factors for cervical intraepithelial neoplasia in American Indian
fection with carcinogenic human papillomavirus among older women. women. Int J Epidemiol 2000;29(6):983–90.
CMAJ 2002;167(8):871–3. [375] Yarkin F, Chauvin S, Konomi N, et al. Detection of HPV DNA in cer-
[354] Richardson H, Kelsall G, Tellier P, et al. The natural history of type- vical specimens collected in cytologic solution by ligation-dependent
specific human papillomavirus infections in female university stu- PCR. Acta Cytol 2003;47(3):450–6.
dents. Cancer Epidemiol Biomarkers Prev 2003;12(6):485–90. [376] Kemp EA, Hakenewerth AM, Laurent SL, et al. Human papillomavi-
[355] Brisson J, Bairati I, Morin C, et al. Determinants of persistent detec- rus prevalence in pregnancy. Obstet Gynecol 1992;79(5 Pt 1):649–56.
tion of human papillomavirus DNA in the uterine cervix. J Infect [377] Wideroff L, Potischman N, Glass AG, et al. A nested case-control
Dis 1996;173(4):794–9. study of dietary factors and the risk of incident cytological abnormal-
[356] Morin C, Bouchard C, Brisson J, et al. Human papillomaviruses and ities of the cervix. Nutr Cancer 1998;30(2):130–6.
vulvar vestibulitis. Obstet Gynecol 2000;95(5):683–7. [378] Khan MJ, Castle PE, Lorincz AT, et al. The elevated 10-year risk
[357] Rohan T, Mann V, McLaughlin J, et al. PCR-detected genital papillo- of cervical precancer and cancer in women with human papilloma-
mavirus infection: prevalence and association with risk factors for cer- virus (HPV) type 16 or 18 and the possible utility of type-specific
vical cancer. Int J Cancer 1991;49(6):856–60. HPV testing in clinical practice. J Natl Cancer Instit 2005;
[358] Koutsky LA, Ault KA, Wheeler CM, et al. A controlled trial of a human 97(14):1072–9.
papillomavirus type 16 vaccine. N Engl J Med 2002;347(21):1645–51. [379] Harper DM, Hildesheim A, Cobb JL, et al. Collection devices for hu-
[359] Harris TG, Burk RD, Palefsky JM, et al. Incidence of cervical squa- man papillomavirus. J Fam Pract 1999;48(7):531–5.
mous intraepithelial lesions associated with HIV serostatus, CD4 [380] Coker AL, Sanders LC, Bond SM, et al. Hormonal and barrier
cell counts, and human papillomavirus test results. JAMA 2005; methods of contraception, oncogenic human papillomaviruses, and
293(12):1471–6. cervical squamous intraepithelial lesion development. J Womens
[360] Giuliano AR, Harris R, Sedjo RL, et al. Incidence, prevalence, and Health Gend Based Med 2001;10(5):441–9.
clearance of type-specific human papillomavirus infections: The [381] Coker AL, Jenkins GR, Busnardo MS, et al. Human papillomaviruses
Young Women’s Health Study. J Infect Dis 2002;186(4):462–9. and cervical neoplasia in South Carolina. Cancer Epidemiol Bio-
[361] Shroyer KR, Lovelace GS, Abarca ML, et al. Detection of human pap- markers Prev 1993;2(3):207–12.
illomavirus DNA by in situ hybridization and polymerase chain reac- [382] Coker AL, Gerasimova T, King MR, et al. High-risk HPVs and risk of
tion in human papillomavirus equivocal and dysplastic cervical cervical neoplasia: a nested case–control study. Exp Mol Pathol 2001;
biopsies. Hum Pathol 1993;24(9):1012–6. 70(2):90–5.
[362] Goodman MT, Kiviat N, McDuffie K, et al. The association of plasma [383] Swan DC, Tucker RA, Tortolero-Luna G, et al. Human papillomavi-
micronutrients with the risk of cervical dysplasia in Hawaii. Cancer rus (HPV) DNA copy number is dependent on grade of cervical dis-
Epidemiol Biomarkers Prev 1998;7(6):537–44. ease and HPV type. J Clin Microbiol 1999;37(4):1030–4.
[363] Hernandez BY, McDuffie K, Franke AA, et al. Reports: plasma and [384] Tortolero-Luna G, Mitchell MF, Swan DC, et al. A case–control study
dietary phytoestrogens and risk of premalignant lesions of the cervix. of human papillomavirus and cervical squamous intraepithelial le-
Nutr Cancer 2004;49(2):109–24. sions (SIL) in Harris County, Texas: differences among racial/ethnic
[364] Hernandez BY, McDuffie K, Zhu X, et al. Anal human papillomavirus groups. Cad Saude Publica 1998;14(Suppl 3):149–59.
infection in women and its relationship with cervical infection. Cancer [385] Lacey JV Jr, Brinton LA, Abbas FM, et al. Oral contraceptives as risk
Epidemiol Biomarkers Prev 2005;14(11 Pt 1):2550–6. factors for cervical adenocarcinomas and squamous cell carcinomas.
[365] Fife KH, Cramer HM, Schroeder JM, et al. Detection of multiple hu- Cancer Epidemiol Biomarkers Prev 1999;8(12):1079–85.
man papillomavirus types in the lower genital tract correlates with cer- [386] Lacey JV Jr, Swanson CA, Brinton LA, et al. Obesity as a potential
vical dysplasia. J Med Virol 2001;64(4):550–9. risk factor for adenocarcinomas and squamous cell carcinomas of
[366] Fife KH, Coplan PM, Jansen KU, et al. Poor sensitivity of poly- the uterine cervix. Cancer 2003;98(4):814–21.
merase chain reaction assays of genital skin swabs and urine to [387] Winer RL, Lee SK, Hughes JP, et al. Genital human papillomavirus
detect HPV 6 and 11 DNA in men. Sex Transm Dis 2003; infection: incidence and risk factors in a cohort of female university
30(3):246–8. students. Am J Epidemiol 2003;157(3):218–26.
S24 J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25

[388] Carter JJ, Koutsky LA, Hughes JP, et al. Comparison of human pap- [407] Ahdieh L, Munoz A, Vlahov D, et al. Cervical neoplasia and repeated
illomavirus types 16, 18, and 6 capsid antibody responses following positivity of human papillomavirus infection in human immunodefi-
incident infection. J Infect Dis 2000;181(6):1911–9. ciency virus-seropositive and -seronegative women. Am J Epidemiol
[389] Carter JJ, Koutsky LA, Wipf GC, et al. The natural history of human 2000;151(12):1148–57.
papillomavirus type 16 capsid antibodies among a cohort of university [408] Jamieson DJ, Duerr A, Burk R, et al. Characterization of genital hu-
women. J Infect Dis 1996;174(5):927–36. man papillomavirus infection in women who have or who are at
[390] Thomas KK, Hughes JP, Kuypers JM, et al. Concurrent and sequential risk of having HIV infection. Am J Obstet Gynecol 2002;186(1):21–7.
acquisition of different genital human papillomavirus types. J Infect [409] Viscidi RP, Snyder B, Cu-Uvin S, et al. Human papillomavirus capsid
Dis 2000;182(4):1097–102. antibody response to natural infection and risk of subsequent HPV
[391] Xi LF, Carter JJ, Galloway DA, et al. Acquisition and natural history infection in HIV-positive and HIV-negative women. Cancer Epide-
of human papillomavirus type 16 variant infection among a cohort of miol Biomarkers Prev 2005;14(1):283–8.
female university students. Cancer Epidemiol Biomarkers Prev 2002; [410] Moscicki AB, Ellenberg JH, Vermund SH, et al. Prevalence of and
11(4):343–51. risks for cervical human papillomavirus infection and squamous
[392] Hagensee ME, Koutsky LA, Lee SK, et al. Detection of cervical anti- intraepithelial lesions in adolescent girls: impact of infection with
bodies to human papillomavirus type 16 (HPV-16) capsid antigens in human immunodeficiency virus. Arch Pediatr Adolesc Med 2000;
relation to detection of HPV-16 DNA and cervical lesions. J Infect Dis 154(2):127–34.
2000;181(4):1234–9. [411] Moscicki AB, Durako SJ, Houser J, et al. Human papillomavirus in-
[393] Hong IS, Marshalleck J, Williams RH, et al. Comparative analysis of fection and abnormal cytology of the anus in HIV-infected and unin-
a liquid-based Pap test and concurrent HPV DNA assay of residual fected adolescents. AIDS 2003;17(3):311–20.
samples. A study of 608 cases. Acta Cytol 2002;46(5):828–34. [412] Brown DR, Legge D, Qadadri B. Distribution of human papillom-
[394] Baay MF, Tjalma WA, Lambrechts HA, et al. Combined Pap and avirus types in cervicovaginal washings from women evaluated in
HPV testing in primary screening for cervical abnormalities: should a sexually transmitted diseases clinic. Sex Transm Dis 2002;29
HPV detection be delayed until age 35? Eur J Cancer 2005; (12):763–8.
41(17):2704–8. [413] Brinkman JA, Jones WE, Gaffga AM, et al. Detection of human pap-
[395] Rintala MA, Grenman SE, Pollanen PP, et al. Detection of high-risk illomavirus DNA in urine specimens from human immunodeficiency
HPV DNA in semen and its association with the quality of semen. virus-positive women. J Clin Microbiol 2002;40(9):3155–61.
Int J STD AIDS 2004;15(11):740–3. [414] Reed BD, Zazove P, Gregoire L, et al. Factors associated with human
[396] van den Brule AJ, Walboomers JM, Du MM, et al. Difference in prev- papillomavirus infection in women encountered in community-based
alence of human papillomavirus genotypes in cytomorphologically offices. Arch Fam Med 1993;2(12):1239–48.
normal cervical smears is associated with a history of cervical intrae- [415] Reed BD, Ruffin MT, Gorenflo DW, et al. The psychosexual impact
pithelial neoplasia. Int J Cancer 1991;48(3):404–8. of human papillomavirus cervical infections. J Fam Pract 1999;
[397] Rozendaal L, Walboomers JM, van der Linden JC, et al. PCR-based 48(2):110.
high-risk HPV test in cervical cancer screening gives objective risk as- [416] Zazove P, Reed BD, Gregoire L, et al. Presence of human papilloma-
sessment of women with cytomorphologically normal cervical virus infection of the uterine cervix as determined by different detec-
smears. Int J Cancer 1996;68(6):766–9. tion methods in a low-risk community-based population. Arch Fam
[398] Rozendaal L, Westerga J, van der Linden JC, et al. PCR based high Med 1993;2(12):1250–8.
risk HPV testing is superior to neural network based screening for pre- [417] Zazove P, Reed BD, Gregoire L, et al. Low false-negative rate of PCR
dicting incident CIN III in women with normal cytology and border- analysis for detecting human papillomavirus-related cervical lesions.
line changes. J Clin Pathol 2000;3(8):606–11. J Clin Microbiol 1998;36(9):2708.
[399] Bulkmans NW, Rozendaal L, Snijders PJ, et al. POBASCAM, a pop- [418] Burk RD, Kelly P, Feldman J, et al. Declining prevalence of cervico-
ulation-based randomized controlled trial for implementation of high- vaginal human papillomavirus infection with age is independent of
risk HPV testing in cervical screening: design, methods and baseline other risk factors. Sex Transm Dis 1996;23(4):333–41.
data of 44,102 women. Int J Cancer 2004;110(1):94–101. [419] Sun XW, Ellerbrock TV, Lungu O, et al. Human papillomavirus infec-
[400] Lundqvist M, Westin C, Lundkvist O, et al. Cytologic screening and tion in human immunodeficiency virus-seropositive women. Obstet
human papilloma virus test in women undergoing artificial fertiliza- Gyneco 1995;85(5 Pt 1):680–6.
tion. Acta Obstet Gynecol Scand 2002;81(10):949–53. [420] Sun XW, Kuhn L, Ellerbrock TV, et al. Human papillomavirus infec-
[401 Peto J, Gilham C, Deacon J, et al. Cervical HPV infection and neopla- tion in women infected with the human immunodeficiency virus.
sia in a large population-based prospective study: the Manchester co- N Engl J Med 1997;337(19):1343–9.
hort. Br J Cancer 2004;91(5):942–53. [421] Wright TC Jr, Ellerbrock TV, Chiasson MA, et al. Cervical intraepi-
[402] Piper MA, Severin ST, Wiktor SZ, et al. Association of human thelial neoplasia in women infected with human immunodeficiency
papillomavirus with HIV and CD4 cell count in women with virus: prevalence, risk factors, and validity of Papanicolaou smears.
high or low numbers of sex partners. Sex Transm Infect 1999; New York Cervical Disease Study. Obstet Gynecol 1994;84(4):
75(4):253–7. 591–7.
[403] Vernon SD, Reeves WC, Clancy KA, et al. A longitudinal study of hu- [422] Morrison EA, Dole P, Sun XW, et al. Low prevalence of human
man papillomavirus DNA detection in human immunodeficiency vi- papillomavirus infection of the cervix in renal transplant recipients.
rus type 1-seropositive and -seronegative women. J Infect Dis 1994; Nephrol Dial Transplant 1996;11(8):1603–6.
169(5):1108–12. [423] Rompalo AM, Gaydos CA, Shah N, et al. Evaluation of use of a single
[404] ter Meulen J, Eberhardt HC, Luande J, et al. Human papillomavirus intravaginal swab to detect multiple sexually transmitted infections in
(HPV) infection, HIV infection and cervical cancer in Tanzania, active-duty military women. Clin Infect Dis 2001;33(9):1455–61.
east Africa. Int J Cancer 1992;51(4):515–21. [424] Baken LA, Koutsky LA, Kuypers J, et al. Genital human papilloma-
[405] Lopes F, Latorre MR, Campos Pignatari AC, et al. [HIV, HPV, and virus infection among male and female sex partners: prevalence and
syphilis prevalence in a women’s penitentiary in the city of Sao Paulo, type-specific concordance. J Infect Dis 1995;171(2):429–32.
1997–1998]. Cad Saude Publica 2001;17(6):1473–80. [425] Watts DH, Koutsky LA, Holmes KK, et al. Low risk of perinatal trans-
[406] Levi JE, Kleter B, Quint WG, et al. High prevalence of human papil- mission of human papillomavirus: results from a prospective cohort
lomavirus (HPV) infections and high frequency of multiple HPV ge- study. Am J Obstet Gynecol 1998;178(2):365–73.
notypes in human immunodeficiency virus-infected women in Brazil. [426] Marrazzo JM, Koutsky LA, Kiviat NB, et al. Papanicolaou test
J Clin Microbiol 2002;40(9):3341–5. screening and prevalence of genital human papillomavirus among
J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25 S25

women who have sex with women. Am J Public Health 2001; tion: an analysis of HPV genotypes. DIANAIDS Collaborative Study
91(6):947–52. Group. Int J Cancer 1997;72(6):982–6.
[427] Fairley CK, Chen S, Tabrizi SN, et al. Prevalence of HPV DNA in cer- [442] Rezza G, Giuliani M, Branca M, et al. Determinants of squamous in-
vical specimens in women with renal transplants: a comparison with traepithelial lesions (SIL) on Pap smear: the role of HPV infection and
dialysis-dependent patients and patients with renal impairment. Neph- of HIV-1-induced immunosuppression. DIANAIDS Collaborative
rol Dial Transplant 1994;9(4):416–20. Study Group. Eur J Epidemiol 1997;13(8):937–43.
[428] Chan PK, Mak KH, Cheung JL, et al. Genotype spectrum of cervical [443] Rezza G, Giuliani M, Serraino D, et al. Risk factors for cervical pres-
human papillomavirus infection among sexually transmitted disease ence of human papillomavirus DNA among women at risk for HIV in-
clinic patients in Hong Kong. J Med Virol 2002;68(2):273–7. fection. DIANAIDS Collaborative Study Group. Epidemiol Infect
[429] Chan PK, Chan MY, Li WW, et al. Association of human beta-herpes- 1998;121(1):173–7.
viruses with the development of cervical cancer: bystanders or cofac- [444] Pisani S, Gallinelli C, Seganti L, et al. Detection of viral and bacterial
tors. J Clin Pathol 2001;54(1):48–53. infections in women with normal and abnormal colposcopy. Eur J Gy-
[430] Arora R, Kumar A, Prusty BK, et al. Prevalence of high-risk human naecol Oncol 1999;20(1):69–73.
papillomavirus (HR-HPV) types 16 and 18 in healthy women with cy- [445] van den Brule AJ, Snijders PJ, Gordijn RL, et al. General primer-
tologically negative Pap smear. Eur J Obstet Gynecol Reprod Biol mediated polymerase chain reaction permits the detection of se-
2005;121(1):104–9. quenced and still unsequenced human papillomavirus genotypes
[431] Kyo S, Inoue M, Koyama M, et al. Detection of high-risk human pap- in cervical scrapes and carcinomas. Int J Cancer 1990;
illomavirus in the cervix and semen of sex partners. J Infect Dis 1994; 45(4):644–9.
170(3):682–5. [446] van Doornum GJ, Prins M, Juffermans LH, et al. Regional distribution
[432] Garland SM, Tabrizi SN, Chen S, et al. Prevalence of sexually trans- and incidence of human papillomavirus infections among heterosex-
mitted infections (Neisseria gonorrhoeae, Chlamydia trachomatis, Tri- ual men and women with multiple sexual partners: a prospective
chomonas vaginalis and human papillomavirus) in female attendees of study. Genitourin Med 1994;70(4):240–6.
a sexually transmitted diseases clinic in Ulaanbaatar, Mongolia. Infect [447] van Doornum GJ, Hooykaas C, Juffermans LH, et al. Prevalence of
Dis Obstet Gynecol 2001;9(3):143–6. human papillomavirus infections among heterosexual men and
[433] Chan R, Khoo L, Ho TH, et al. A comparative study of cervical cytol- women with multiple sexual partners. J MedVirol 1992;37
ogy, colposcopy and PCR for HPV in female sex workers in Singa- (1):13–21.
pore. Int J STD AIDS 2001;12(3):159–63. [448] van Doornum GJ, van den Hoek JA, Van Ameijden EJ, et al. Cervical
[434] Rugpao S, Nagachinta T, Wanapirak C, et al. Gynaecological condi- HPV infection among HIV-infected prostitutes addicted to hard drugs.
tions associated with HIV infection in women who are partners of J Med Virol 1993;41(3):185–90.
HIV-positive Thai blood donors. Int J STD AIDS 1998;9(11):677–82. [449] Jenkins A, Kristiansen E, Ask E, et al. Human papillomavirus infec-
[435] Delmas MC, Larsen C, van Benthem B, et al. Cervical squamous in- tion in cervical biopsies from Norwegian gynecological in-patients.
traepithelial lesions in HIV-infected women: prevalence, incidence Apmis 1996;104(1):30–4.
and regression. European Study Group on Natural History of HIV In- [450] Syrjanen S, Shabalova I, Petrovichev N, et al. Sexual habits and hu-
fection in Women. AIDS 2000;14(12):1775–84. man papillomavirus infection among females in three new indepen-
[436] Melbye M, Smith E, Wohlfahrt J, et al. Anal and cervical abnormality dent states of the former Soviet Union. Sex Transm Dis 2003;
in women—prediction by human papillomavirus tests. Int J Cancer 30(9):680–4.
1996;68(5):559–64. [451] Voog E, Ricksten A, Lowhagen GB. Prevalence of Epstein-Barr virus
[437] Nieminen P, Vuorma S, Viikki M, et al. Comparison of HPV test versus and human papillomavirus in cervical samples from women attending
conventional and automation-assisted Pap screening as potential screen- an STD-clinic. Int J STD AIDS 1995;6(3):208–10.
ing tools for preventing cervical cancer. BJOG 2004;111(8):842–8. [452] Rymark P, Forslund O, Hansson BG, et al. Genital HPV infection not
[438] Six C, Heard I, Bergeron C, et al. Comparative prevalence, incidence a local but a regional infection: experience from a female teenage
and short-term prognosis of cervical squamous intraepithelial lesions group. Genitourin Med 1993;69(1):18–22.
amongst HIV-positive and HIV-negative women. AIDS 1998; [453] Kalantari M, Karlsen F, Johansson B, et al. Human papillomavirus
12(9):1047–56. findings in relation to cervical intraepithelial neoplasia grade: a study
[439] Clavel C, Masure M, Bory JP, et al. Hybrid Capture II-based human on 476 Stockholm women, using PCR for detection and typing of
papillomavirus detection, a sensitive test to detect in routine high- HPV. Hum Pathol 1997;28(8):899–904.
grade cervical lesions: a preliminary study on 1518 women. Br J [454] Strand A, Rylander E, Evander M, et al. Genital human papillomavi-
Ccancer 1999;80(9):1306–11. rus infection among patients attending an STD clinic. Genitourin Med
[440] Bornstein J, Shapiro S, Goldshmid N, et al. Severe vulvar vestibulitis. 1993;69(6):446–9.
Relation to HPV infection. J Reprod Med 1997;42(8):514–8. [455] Strauss S, Jordens JZ, McBride D, et al. Detection and typing of
[441] Cappiello G, Garbuglia AR, Salvi R, et al. HIV infection increases the human papillomavirus DNA in paired urine and cervical scrapes.
risk of squamous intra-epithelial lesions in women with HPV infec- Eur J Epidemiol 1999;15(6):537–43.
Table 1

S25.e1
HPV prevalence estimates in women from low-risk populations by continent, country, and study year.
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Africa
Algeria, Algiers, 1997–9 [315] GP5þ/6þ Ectocervix—spatula Hospital-based controls 52 (30–88) 145 12.4 6.2 0.7
Endocervix—brush
Gabon, Libreville, 2001 [17] MY09/11 Cervicovaginal—lavage Women attending clinics for 26.4 (18–44) 354 46.0 25.4 10.2 4.5 1.1
antenatal check-up or for
general genital symptoms
Gambia, Farafenni, 1999 [18] GP5þ/6þ Cervix—brush Population-based sample in rural 33.0a (15–54) 710 13.4

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


community
15–24 184 14.7
25–34 213 10.3
35–44 191 14.1
45–54 122 15.6
Ivory Coast, Abidjan, 1995–6 MY09/11 Endocervix—brush Community-based clinic controls 28a b (20–50) 391 24.3 1.8 0.3
[316,317]
Kenya, Nairobi, 1994 [19] GP5þ/6þ Endocervix—brush Family planning clients 29.7, 29b (19– 513 17.0 15.8 1.2 4.1 2.3
54)
19–25 118 22.9
26–29 197 17.3
30–54 198 13.1
Kenya, Nairobi, 1998–2000 [31] SPF10 Cervix—brush Family planning clients 35.2 (25–54) 429 44.3 30.6 6.5 6.3 2.6
25–29 76 57.9a 39a
30–34 143 40.0a 28a
35–39 103 50.0a 39a
40–44 65 30.0a 20a
45–54 37 30.0a 15a
Malawi, No city reported, 1991 MY09/11 Cervicovaginal—lavage Annual visit among urban women 24 (13–45) 244 34.0
[318,319] in Malawi
Morocco, Rabat, 1991–3 [320] GP5þ/6þ Cervix—brush Cytologically normal hospital- 40.7 (18–70) 185 20.5 4.3 1.1
based controls
Mozambique, Manhica, 1999 [27] MY09/11 Cervix—smear Population-based sample in rural 14–61 253 40 27 5.5 4.7
community
14–20 51 55 49.0
21–30 61 48 45.9
31–40 53 38 30.1
41–50 47 30 23.4
51 41 22 21.9
Nigeria, Ibadan, 1999–2000 [20] GP5þ/6þ Ecto/endocervix—brush Population-based sample 44.9a 932 24.8 18.2 6.5 3.2 1.9
<25 120 30.8
25–34 189 25.4
35–44 134 26.9
45–54 196 26.0
55–64 172 24.4
65 121 25.6
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Senegal, Dakar, 1990–1 [277] PCR with consensus Cervix—smear HIV- women 30.6 53 20.8
primers
Senegal, Dakar, 1996 [321] MY09/11 Ecto/endocervix—swab Women attending gynecology 37.2a 158 13.9 5.7 1.3
clinic with various
gynecological complaints
Senegal, Dakar, 1996 [21] Type-specific PCR (6, 11, 16, 18, Cervix—spatula Pregnant women 28 (13–71) 72 23.6 16.7 6.9
31, 33, 45, 35, 52, 58, 68)

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


13–25 29 13.8
26–43 43 30.2
Senegal, Dakar suburbs, 1998– Type-specific primers (16, 18, 26, Cervix—brush Community-based (health clinic 42.7 (35) 1639 12.5 4.9 3.1 1.0 0.9
2000 [32] 31, 33, 35, 39, 42, 45, 51–59, attendees)
66, 68, 73, 82, 83, 84, 6, 11, 40)
and
MY09/11
Cytologically normal 35–39 575 11.3 4.3 3.1
40–44 501 14.2 5.6 3.6
45–49 356 9.3 3.4 2.2
50–54 126 15.9 7.1 4.0
55 81 19.8 8.6 2.5
South Africa, Cape Town, 1998–9 HCII Self-collected vaginal swab Outpatient clinic 39b (35–65) 1269 17.1
[322]
HCII Clinician-collected sample Outpatient clinic 39b (35–65) 1269 15.5
South Africa, Khayelitsha, 1996– HCI Cervix—smear Community-based primary 39 (35–65) 2680 12.2
7 [15,16] cervical cancer screening
(cytologically normal)
HCII Cervix—smear Community-based primary 39 (35–65) 243 18.1
cervical cancer screening
(cytologically normal); all
screening sample
35–39 17.0
40–49 14.0
50–59 17.0
60–65 18.0
Tanzania, Mwanza, 1994 [23,24] MY09/11 Endocervix—brush Pregnant women attending 23.4 (15–44) 612 34.2 19.6 6.5
antenatal clinic
15–19 144 34.7
20–29 388 35.6
30–44 80 26.3
Tunisia, Sousse, 1999 [25] MY09/11 and GP5þ/6þ Endocervix— brush Family planning clients 25.5 (18–53) 103 13.6 6.8 3.9 4.9 0.0
18–30 16.1
31–40 13.8a

S25.e2
41–53 10.3
(Continued )
Table 1

S25.e3
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Tunisia, Sousse, 2002 [26] MY09/11, pu-1M/pu-2R, Cervix—brush Family-planning clients 35 (20–45) 96 14.6
and pu-31B/pu-2R
20–30 17.0a
31–40 14.0a
41–45 13.0a
Uganda, Rakai District, 1996–7 HCII Vagina—swab Community-based trial for HIV 31.3a (15–59) 737 16.3
[22] prevention

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


15–19 118 25.4
20–29 277 20.6
30–39 177 12.4
40–59 165 6.7
Zimbabwe, Chitungwiza and HCII Cervix—brush Cervical cancer screening 34.1a (25–55) 2139 42.7
Greater Harare, 1996–7 [28– program
30]
25–34 1343 48.5
35–44 624 34.9
45–55 172 25.6
Zimbabwe, Mupfure, 2004 [278] GP5þ/6þ Cervicovaginal— lavage Population-based rural (15–49) 174 27.0 3.4 3.4
community screening
Central/South America
Argentina, No city reported, 2002 MY09/11 and GP5þ/6þ Ectocervix— scrape Women with normal cytology 32.4 90 37.8
[323]
Argentina, Concordia, 1998 [37] GP5þ/6þ Cervical external os—spatula Population-based sample 38.9a (15) 987 16.8 12.1 2.5 0.5
Endocervix—brush
15–24 151 25.3
25–34 201 22.0a
35–44 207 18.0a
45–54 199 13.0a
55 179 9.5a
15–25 151 20.0a 4.0a
25–34 201 17.0a 5.0a
35–44 207 11.0a 7.0a
45–54 199 7.0a 6.0a
55–64 5.0a 5.0a
65 5.0a 4.0a
Argentina, La Plata, 1998–2000 MY09/11 and GP5þ/6þ Ecto/endocervix—brush Women with normal cytology 34 (15–67) 79 30.4 11.4 19.0 8.9 1.3
[324] or spatula
Argentina, La Platac [325] MY09/11 and GP5þ/6þ Ecto/endocervix—brush Anonymous specimens from 41a (15–67) 79 30.4 10.1 22.8 8.9 1.3
or spatula public hospital data bank
Argentina, Misiones, 2000–2 [33] MY09/11 Cervix—spatula Cervical cancer screening among 32b (17–69) 458 52
indigenous rural and urban
population
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Argentina, Misiones, 2002 [34] MY09/11 and GP5þ/6þ Ecto/endocervix—brush Cervical cancer screening among 15 (12–64) 207 64.3 19.8 6.3
Guarani Indians
Rural 16 (26–40) 214 43
Urban 33 (21–65) 244 60
Argentina, Jujuy, 2001 [326] MY09/11 Cervix—smear Tribal women undergoing 35 (14–64) 108 51.9 14.8 0.9
cervical screening
Argentina, Ushuaia, Province of MY09/11 and GP5þ/6þ Ecto/endocervix—brush Normal women attending 31.6a 87 26 16 5 5.7 1.1

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Tierra del Fuego, a gynecology clinic
2002–3 [35]
14–24 39 54.0
25–34 45 38.0
35–54 45 33.1a
Bolivia, Amazonc [327] PCR with L1 primers Cervix—swab Population-based random sample 36.3a (16–71) 135 5.9
San Ramon 36.5 (16–71) 63 3.2
Caranavi 34.9 (16–65) 51 7.8
Palos Blancos 38 (23–67) 9 0.0
Rurrenabaque 40.1 (20–70) 12 16.7
Brazil, Joao Pessoa and Paraiba, MY09/11 Ecto/endocervix—brush Population-based attendees of 41.2, 40b 525 18.3 11.6 9.7 5.3 2.1
1988–90 [328] cervical cancer screening
Brazil, Porto Alegre, 2002 [38] MY09/11 Cervix—brush Attendees of cervical cancer 15–70 975 16.0
screening
15–25 27.9
25–34 17.0
35–49 12.6
50–70 14.4
Brazil, Porto Alegrec [329] LIPA Cervix—brush and spatula Population recruited from 20.3 (15–25) 394 39.8
multicenter prophylactic
vaccine trial
Brazil, Recife, 2000 [36] HCI Ecto/endocervix—swab Cytologically normal women 43 (35–60) 70 58.6
from screening program
Brazil, Recife, 2001 [330] MY09/11 Ectocervix—spatula Randomly selected screening 38 (16–88) 253 28.9 13.0 0.8
Endocervix— brush sample
Tampon (self-sampled) 22.9 8.3 0.4
Brazil, Rio de Janeiro, 2000 [331] HCII Cervix—brush Women undergoing routine 31.5 1055 48.3 42.7 22.8
gynecological exam
Brazil, Sao Paulo, 1990–1 [61] GP5þ/6þ and type-specific PCR Ectocervix—spatula Hospital-based controls 52.4 (25–79) 190 16.8 5.3 1.1
(6, 11, 16, 18, 31, 33) Endocervix—brush
25–44 49 20.4
45–54 58 20.7
55–64 52 11.5
65–79 31 12.9

S25.e4
(Continued )
Table 1

S25.e5
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Brazil, Sao Paulo, 1993–7 MY09/11 Ecto/endocervix—smear Population-based cohort 33.3, 33 (18–60) 1425 13.8 2.7 0.8
[332,333]
18–34 17.1
35–60 9.8

Chile, Santiago, 2000–1 [42] GP5þ/6þ Ectocervix—spatula Population-based random sample 41.0a (15–69) 955 12.8 9.1 3.7 2.6 0.5
Endocervix—brush

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


15–24 134 22.4
25–34 185 11.9
35–44 215 8.4
45–54 168 10.1
55–64 157 12.7
65–69 96 15.6
Colombia, Bogota, 1993–5 [39– GP5þ/6þ Cervix—spatula, brush Population-based cervical cancer 32 (13–85) 1845 14.9 11.4 3.2 2.4 0.4
41] screening sample
<20 230 26.1 20.4 5.2
20–24 220 22.7 18.2 4.1
25–29 337 12.8 10.4 1.8
30–34 404 16.6 11.9 4.2
35–39 284 8.1 6.0 2.1
40–44 192 8.3 7.8 0.5
45–54 86 2.3 2.3 0.0
55 106 13.2 5.7 7.6
<25 2.7 0.9
25–34 2.7 0.5
35 1.9 0.0
Colombia, Cali, 1985–8 Type-specific PCR (6, 11, 16, 18, Cervix—scrape Population-based controls 39.2 (19–70) 181 10.5 3.3 0.0
[4,155,334–341] 31, 33, 35)
Costa Rica, Guanacaste, 1993–4 MY09/11 Cervix or vaginal cuff—swab Population-based 54 (27–88) 569 28.6 13.4 17.7
[51] hysterectomized women
27–34 40.0a 9.0a 30.0a
35–44 34.0a 8.0a 29.0a
45–54 27.0a 8.0a 22.0a
55–64 31.0a 13.0a 25.0a
65–74 29.0a 9.0a 24.0a
75–88 25.0a 11.0a 23.0a
Costa Rica, Guanacaste, 1994–5 MY09/11 and HMBO1 Cervix—brush Population-based screening 37 (18–94) 2308 16.0 7.6 6.7 3.3 0.8
[52–60]
18–24 296 21.0a 9.5a 6.0a
25–34 658 14.0a 5.5a 5.0a
35–44 573 6.0a 2.5a 2.0a
45–54 364 6.5a 3.0a 2.0a
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
55–64 212 14.0a 4.0a 4.0a
65–94 205 19.0a 3.5a 11.0a
Ecuador, Quito, 1985–1992 [115] Type-specific PCR (6/11, 16, 18, Cervix—biopsy Cytologically normal women 50.2a 40 20.0 2.5 0.0
33, 52b, 58)
Honduras, Tegucigalpa, 1993–5 MY09/11 Cervix—spatula Clinic-based controls 40.4 (20–65) 438 38.8 11.0 4.1
[43–47]
15–24 21 71.4

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


25–34 122 38.5
35–44 145 33.8
45–54 111 38.7
55–65 39 41.0
Jamaica, Kingston, 1996–7 [342] MY09/11 and GP1/2 Cervix—spatula, brush Women undergoing routine 37 94 14.0
cervical cancer screening
Mexico, No city reported, 1987– Type-specific PCR (6, 11, Biopsy Women with a normal cervix 49.5 (24–89) 117 31.4
92 [343] 16, 18)
Mexico, Mexico City, 1990–2 PCR with E6/E7 primers (16,18) Cervix—smear Population-based random sample, 44.3 (25–75) 204 13.2
[344] controls
Mexico, Mexico City, 1997 [345] MY09/11 and HMBO1 Cervix—spatula Cytologically normal women 39.7 (15–85) 71 16.9 9.9 7.0 2.8 0.0
attending gynecology clinic for
routine check-up or
gynecological complaint
Mexico, Mexico City, 1997–9 MY09/11 Ecto/endocervix—brush Population-based cervical cancer (26–88) 181 11.0
[346] screening sample
Mexico, Mexico City, HCII Endocervix—brush Outpatient clinic-based controls 38 182 19.8
1998–2000 [50] with negative Pap smear
<25 5.0
25–34 14.6
35–44 19.7
45–54 34.5
55–70 42.9
Mexico, Morelos, 1996–9 [48] PCR with LI primers Cervix—brush Population-based random sample 35.6a 1340 14.5 1.7 1.0
<25 276 16.7 16.3 0.4
25–34 280 9.5a 8.0a 1.0a
35–44 269 3.7 3.0a 0.5a
45–54 179 12.3 10.0a 2.4a
55–64 175 16.0a 10.2a 5.8a
65 161 23.0 16.8 6.2
<35 2.2 0.4
35–54 0.7 0.7
55 1.8 0.6
Mexico, Morelos, 1999 [49] HCII Cervix—brush (nurse-sampled) Cervical cancer screening 42.5, 41b (15– 7736 9.4

S25.e6
population 85)
(Continued )
Table 1

S25.e7
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Vagina—swab (self-sampled) 15–24 495 14.0a
25–34 2035 10.0a
35–44 2047 7.0a
45–54 1602 8.5a
55–64 992 11.0a
65–85 565 12.0a
Mexico, Morelos, 1999–2000 HCII Vagina—swab (self-sampled) Cross-sectional screening study of 25.7 (16–39) 274 37.1

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


[347] pregnant women
16–24 122 49.5
25–29 91 27.7
30–39 61 22.8
Nonpregnant women 26.2 (17–39) 1060 14.2
16–24 493 55.6
25–29 333 24.5
30–39 234 19.9
Paraguay, Asuncion, 1988–90 MY09/11 and GP5þ/6þ Ectocervix—spatula Cancer hospital-based controls 45 (18–85) 91 19.8 17.6 1.1 5.5 0.0
[348] Endocervix—brush
Peru, Lima, 1996–7 [349–351] GP5þ/6þ Cervix—swab Hospital-based controls 50.3a (21–84) 127 13.4 1.6 3.1
North America
Canada, Newfoundland, 1996–8 HCI and HCII Ecto/endocervix—brush, spatula Women presenting for routine 30, 35b, (18–69) 2098 10.8
[84] screening
<25 401 16.7
25–34 1098 11.7
35–44 536 5.0
45 59 3.6
Canada, Nunavut, 1999 [352] HCII Ecto/endocervix—broom Population-based screening of 31, 28b, (13–79) 1290 25.8
aboriginal women
Inuit—Baffin 13–20 100 43
21–30 182 34.1
31–40 110 12.7
>40 80 16.3
Inuit—Keewatin 13–20 28 35.7
21–30 74 29.7
31–40 47 6.4
>40 25 12
Inuit—Unknown 13–20 102 42.2
21–30 162 28.4
31–40 116 15.5
>40 75 13.3
Non-Inuit—Baffit 13–30 32 55.75
31–40 34 20.6
>40 40 17.5
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Non-Inuit—Unknown 13–30 23 34.5
>30 30 6.3
Canada, Ontario, No city reported HCII Cervix—brush Cervical cancer screening with 32.6a (15–49) 955 12.7
(6 health-planning regions), family physician
1998–9 [85]
15–19 89 15.7
20–24 125 24.0

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


25–29 159 16.4
30–34 163 12.3
35–39 157 9.6
40–44 144 8.3
45–49 118 3.4
Type-specific PCR (16, 18, 31, Cervix—brush Cervical cancer screening with 32.5a (15–49) 824 13.5
33, 35, 39, 45, 51, 52, 56, 58, family physician
59, 68, 6, 11, 42, 53)
15–19 80 20.0
20–24 108 23.1
25–29 143 14.7
30–34 136 11.8
35–39 136 11.0
40–44 121 3.3
45–49 100 13.0
Canada, Ontario, No city HCII Cervix—brush Women attending routine 56.2a 156 8.3
reported, 1999–2000 [353] cytological screening
50–54 56 8.0a
55–59 47 4.0a
60 53 12.0a
Canada, Montreal, 1992–3 [86] MY09/11 Ectocervix— spatula Routine gynecology visit, 21.4a 375 22.7 11.8 6.2 4.7 0.9
Endocervix— brush university students
<19 64 22.0 14.3 14.3
20–21 123 24.5 13.2 15.6
22–23 92 20.0 8.5 11.8
>24 92 21.1 13.4 12.3
Canada, Montreal, 1996–9 [354] MY09/11 and HMBO1 Ecto/endocervix University students 23, 21b (17–42) 621 29.0 21.8 14.8 7.0 3.1
Canada, Quebec City, 1991–2 MY09/11 Ectocervix—swab Women undergoing routine (18–49) 1493 12.0 2.8 2.0
[355] gynecological screening
Canada, Quebec City, 1995–7 HCI Cervix—swab Women attending gynecology 22.5 369 20.9 14.1 4.9
[356] clinic with various
gynecological complaints
Canada, Toronto, 1990 [357] Type-specific PCR (6/11, 16, 18, Cervix—spatula Cytologically normal university 23 (21–27) 105 18.1 10.5
33) students undergoing routine

S25.e8
exam
(Continued )
Table 1

S25.e9
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
USA, Nationwide, 1998–9[358] MY09/11 (16, L1) Cervicovaginal—avage and swab Population-based sample 20a (16–25) 2392 5.4
USA, Nationwide, 2003–4 [9] MY09/11 Self-collected cervicovaginal Population-based sample— (14–59) 1921 26.8 15.2 17.8 1.5 0.8
sample women from NHANES
14–19 652 24.5 17.0a 14.0a
20–24 189 44.8 29.0a 31.0a
25–29 174 27.4 14.0a 22.0a
30–39 328 27.5 16.0a 17.0a

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


40–49 324 25.2 14.0a 15.0a
50–59 254 19.6 7.0a 16.0a
USA, New York, New York; MY09/11 Cervicovaginal—lavage Healthy women from clinical and 34 (28–40) 343 27 5 22
Illinois, Chicago; California, outreach sources
Los Angeles and San
Francisco; Washington, DC,
1994–5 [359]
USA, Arizona, Southern Arizona, HCII Ectocervix—spatula Women undergoing routine 24.2 (18–35) 1280 26.2
1996–9 [360] Endocervix— brush gynecological care at Planned
Parenthood clinic
USA, Arizona, Douglas; Mexico, MY09/11 Ecto/endocervix—brush Population-based sample 51.2 (40) 304 9.2 5.9 3.3 2.0
Agua Prieta and Sonora, 1999–
2000 [83]
40–49 155 12.3 7.7a 4.5a
50–59 98 2.0 0.0a 2.0a
60–82 51 13.7 11.8a 2.0a
USA, Arizona, Tucson; Mexico, MY09/11 Ecto/endocervix— brush Family planning clinic sample 33.1 (15) 2246 14.4 11.5 2.9
Sonora, 1997–8 [70–72]
15–19 117 20.5 7.0
20–24 348 20.1 4.5
25–34 784 11.6 3.1
35–44 560 7.5 3.4
45–79 279 6.8 1.1
USA, California, Berkeley, 1989 MY09/11 Vulva and cervix— swab University students 22.9 (17–50) 467 46.0 8.8 5.3
[63,64]
17–19 79 48.1
20–21 135 43.7
22–23 93 54.8
24–25 58 51.7
26–29 77 35.1
30–50 25 32.0
USA, Colorado, Boulder, 1989 MY09/11 Cervix—biopsy Normal cervical biopsy samples 32.0 (16–63) 20 10.0
[361]
USA, Georgia, Atlanta, MY09/11 Ecto/endocervix—smear Urban adolescent population 16.1 (12.8–19.9) 312 64.1 49.4 10.3 5.1
1999–2001 [62]
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
<15 110 54.5
15 53 67.9
16 100 70.0
17 49 69.4
USA, Hawaii, Oahu, 1992–6 MY09/11 and type-specific PCR Cervix—smear Hospital-based controls 39.2 (18–84) 191 19 1.6 0.5
[362,363] (6/11, 16, 18, 45,
31/33/35/39)

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


USA, Hawaii, Oahu, 1999–2004 MY09/11 and HMB01 Ecto/endocervix—swab, brush Random multiethnic population 38.3 (18) 1566 26.2
[364] sample
USA, Indiana, No city reported, MY09/11 Cervicovaginal—lavage Cytologically normal; hospital- 31.7 (20–58) 55 54.5 9.1
1999 [365] based obstetrics clinic
(pregnant women, routine
prenatal care), hospital-based
gynecology clinic (routine
care), and patients undergoing
pretransplant evaluation or
transplantation follow-up
USA, Indiana, Indianapolisc HCII Cervicovaginal—lavage Gynecology clinic attendees 29.2 246 18.7 11.4 9.4
[366–368]
Obstetrics clinic attendees 22.8 245 22.8 24.9 12.7
USA, Iowa, Iowa City, Type-specific PCR (6,11, 16, 18, Cervix—swab Postmenopausal women 56.1a (45–64) 105 38.1
1989–91 [369,370] 31, 33, 35, 39, 45, 51, 52)
46–55 46 32.6
56–65 59 42.4
USA, Iowa, Iowa City, 1997–9 MY09/11 and GP5þ/6þ Ecto/endocervix—swab Postmenopausal women attending 58 (42–85) 260 13.8 5.8 10.0 2.3 0.4
[371] routine exam
42–53 74 13.5
54–59 89 15.7
60–85 97 12.4
USA, Iowa, Iowa City, 1998– MY09/11 and GP5þ/6þ Ecto/endocervix and posterior Pregnant women seeking routine 29 (18–45) 574 28.6 17.9 12.5 6.1 2.6
2001 [73] vaginal fornix—swab care
18–24 140 47.1
25–45 434 24.2
USA, Louisiana, New Orleansc MY09/11 (GP5þ/6þ for nested Cervix and vagina —swab Women referred to colposcopy 30.9 111 41.7 34.7 12.5
[372] PCR) clinic with normal Pap smears
USA, Maryland, College Park, MY09/11 Cervix—brush University students attending 22.5 (17–44) 414 35.0 14.3 5.1 7.7 1.9
1992–3 [65] routine gynecological exam
17–19 74 32.0
20–24 260 37
25–29 53 19
30–44 27 26

S25.e10
(Continued )
Table 1

S25.e11
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
USA, Maryland, College Park, MY09/11, GP1/2, and type- Cervix—spatula and brush US students undergoing routine 23 (18–40) 79 29.0
1996–7 [342] specific PCR (15 types from L1 cervical exam
region)
USA, Massachusetts, Boston, HCII Cervix—smear Healthy subjects; normal cytology 38.9 (30–45) 1000 3.9
2005 [373]
30–35 300 6.7
36–40 200 3.0

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


41–45 500 2.6
USA, New Jersey, New MY09/11 and HMBO1 Cervicovaginal—avage University students 20 604 26.0 11.1 3.8 2.0
Brunswick, 1992–4 [66, 67]
20 486 23.7
21–23 71 50.7
>23 47 36.2
USA, New Mexico, No city Type-specific PCR (6, 11, 16, 18, Cervix—swab Cytologically normal controls 28.6 (18–45) 326 30.4
reported, 1994–7 [374] 26, 31, 33, 35, 39, 40, 42, 45,
51, 52, 53, 54, 55, 56, 57, 58,
59, 66, 68, MM4, MM7, MM8,
MM9)
USA, New Mexico, Albuquerque, Type-specific PCR (6/11, 16, 18, Cervix—swab University students attending 23 (18–47) 357 44.3 7.8
1992 [68] 31, 33, 35, 39, 45, 51, 52, 54, clinic for routine gynecological
59, pap88, pap238a, papw13B) exam
18–20 79 43.0
21–25 152 48.7
26–30 57 33.3
31–47 69 44.9
USA, New Mexico, Type-specific PCR (6/11, 16, 18, Cervix—swab and lavage University students 27 (18–35) 72 36.1
Albuquerquec [69] 31, 33, 35, 39, 45, 51, 52, 54,
59, pap88, pap238a, papw13B)
HCII 35 14.3
USA, New Mexico, Albuquerque, MY09/11 Cervix—swab Gynecology clinic attendees 38.5 (18–40) 3863 39.2 7.5 2.3
1996–2000 [74]
18–22 910 50.5 39.1 21.6
23–27 1015 44.8 31.6 18.0
28–32 848 33.0 20.6 8.6
33–40 1090 29.4 16.5 10.5
USA, New York, New York, MY09/11 Cervix—smear Clinic-based 15–51 35 22.9
1998–9 [375]
HCII Clinic-based 15–51 35 14.2
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)

USA, North Carolina, No city Type-specific PCR with L1 Cervix—swab Pregnant and postpartum women 22.5 (12–50) 215 78.1 17.7
reported, 1989 [376] primers (6, 11, 16, 18)
Nonpregnant women 26.4 160 25.6 5.6
USA, Oregon, Portland, 1989–90 Type-specific PCR (6/11, 16, 18, Cervicovaginal—lavage Cytologically normal women 34 (16–81) 453 17.7 7.1 10.6 2.6 0.2
[75–80,377] 26, 31, 33, 35, 39, 40, 42, 45, presenting for routine Pap
51, 52, 53, 54, 55, 57, 59, smear

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


pap88, pap155, pap238a,
pap251, pap291, W13B)
16–24 81 32.1
25–29 84 27.4
30–34 71 11.3
35–39 65 10.8
40–44 61 19.7
45–81 91 4.4

USA, Oregon, Portland, 1989–90 HCII Cervicovaginal—lavage Routine Pap smear 34.0b 16 20514 13.9 2.2 0.8
[79,378]
USA, Pennsylvania, Philadelphia, HCI Women undergoing routine care 25.6 (18–70) 93 34.6
1999 [379] or colposcopy
Cervicovaginal—tampon (self- 46 29.0 17.2 3.2
sampled)
Ecto/endocervix—swab 47 25.8 14.0 3.2
(physician-sampled)
USA, South Carolina, No city HCI Cervix—smear Family planning clinic-based 28.1 (16–45) 427 18.5
reported, 1995–8 [380] normal controls
USA, South Carolina, Trident PCR with E6 primers (6, 11, 16, Cervix—spatula, brush Routine smear at family planning 23.5 223 2.7
Health District, 1991 [381] 18, 33) visit
USA, South Carolina, Trident MY09/11 Cervix—spatula, brush Routine family planning clinic 29.3 1083 32.5 23.4 9.2
Health District, 1991–2 [382] visit
USA,Texas, Harris County, Type-specific PCR with L1 Cervix—brush Family planning and screening 26.9 (18) 270 19.3
1991–4 [383,384] primers (16, 18, 31, 33, 45, 51, attendees
52, 56)
USA, Washington; Pennsylvania; MY09/11 Cervicovaginal—swab Random sample of population- 40.9a (18–69) 285 17.2 12.6 4.6
Connecticut, 1992–6 [385,386] based controls
USA, Washington, No city MY09/11 and HMBO1 Endocervix—swab Planned Parenthood clinic sample 25a (18–50) 4075 18.3 3.9 5.3 1.5
reported, 1997–2000 [82]
18–19 21.0a
20–24 22.0a
25–29 18.0a
30–34 12.0a

S25.e12
35–50 5.0a
(Continued )
Table 1

S25.e13
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
USA, Washington, Seattle, 1990– MY09/11 and HMBO1 Cervix and vulvovaginal—swab University-based random sample 19.2 (18–20) 553 19.7
7 [387]
USA, Washington, Seattle, 1990– MY09/11 (6, 11, 16, 18) Ecto/endocervix and University students (18–20) 588 8.2 4.1
8 [388–391] vulvovaginal—swab
USA, Washington, Seattle, 1994– L1 primers Cervix—brush spatula, swab University students 19.2 305 16.0
6 [392]
USA, Washington, DC. 1984–7 PCR, MY09/11, HMBO1, GH20, Cervicovaginal—lavage Women undergoing routine 26 (16–72) 404 33.7

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


[81] and PC04 screening at gynecology clinic
16–24 110 53.6
25–29 57 31.6
30–39 59 22.0
40 37 27.0
USA, Washington, D.C. Metro, HCI and HCII Cervix—smear Outpatient population, women 44 76 9.2 0.0
1998–2001 [393] attending gynecology clinic,
university health clinic, and
indigent patients (cytology
within normal limits)
Asia/Australia
Australia, No city reportedc [90] MY09/11 Tampon (self-sampled) Women in smoking cessation trial 38 (20–60) 197 28.9
Australia, Cook Islands, 1994 Type-specific PCR (16, 18) Cervix—swab Cytologically normal women 27 (17–49) 21 14.3
[91]
Australia, Melbourne, 1992–3 PCR with L1 consensus primers Tampon (self-sampled) Women attending gynecology 27 (18–35) 298 30.9
[87,88] clinic
18–20 27 40.7
21–25 81 37.0
26–30 108 31.5
31–35 74 24.3
Australia, Melbournec [89] PCR with L1 consensus primers Tampon (self-sampled) Virgins and cytologically normal 19.4 (13–44) 67 6.0
women attending outpatient
clinic
China, No city reported, 1992 Type-specific PCR with L1 Cervix—smear Controls undergoing (30–60) 55 5.5
[100] primers (6, 11, 16, 18, 31, 33, hysterectomy for uterine
45) leiomyoma
China, No city reported, 1992 [99] Type-specific PCR with E6 Cervix—smear Histologically normal cervix 42 30 16.7
primers (16)
China, Sichuan and Chengdu, Type-specific PCR (16, 33) Ectocervix—swab Gynecology clinic-based controls 51.7 146 1.4
1987 [92]
China, Dalian City, 1994–5[93] Type-specific PCR (16) Cervix—smear Family planning clinic attendees 29a (24–41) 99 34.1
China, Guangdong and Jiangxi, HCII Cervix—smear Healthy controls in clinical study 36.5 (29–60) 68 25.0
2000–4 [94] of cervical disease patients
China, Shanxi, 1999 [101] HCII Self-collected vaginal swab Rural population 39.1 (35–45) 1997 17
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
HCII Clinician-collected cervical Rural population 39.1 (35–45) 1997 18
sample
China, Hong Kong, 1991–2 [95] MY09/11 (6, 11, 16, 18, 31, 33) Cervix—spatula General gynecology clinic 41.6 (16–81) 170 4.1
China, Hong Kongc [96] MY09/11 Cervix—brush Pregnant women, routine 28.9 (17–44) 308 10.1 5.8 1.0 2.9 0.0
antenatal visit
17–25 78 14.1
26–35 198 8.6

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


36–44 32 9.4
Population-based cervical cancer 29.1 (19–40) 308 11.4 7.8 2.9 2.6 1.6
screening
19–25 78 7.7
26–35 198 14.1
36–40 32 3.1

China, Shenyang, 1993 [97] Type-specific PCR with L1 Cervical secretions Pregnant women hospitalized for 22–36 30 53.3
primers (6, 11, 16, 18, 31, 33, delivery
35, 38)
China, Xiangyuan and HCII Cervix—smear Population-based study 30–50 9683 27.4
Yangcheng Countyc [98]
Xiangyuan 30–34 148 25.0
35–39 2566 26.4
40–44 1892 26.5
45–50 1491 26.0
Yangcheng 30–34 93 23.7
35–59 1536 28.9
40–44 1028 31.3
45–50 929 29.6
India, No city reported, 2001 HPV 16 with E6 and E2 PCR Cervix—spatula Clinic-based controls (24–45) 31 34.1
[102] primers
India, No city reportedc [112] Type-specific PCR (16, 18) Cervix—scrape Normal controls attending (16–80) 201 41.8
reproductive clinic
India, Chennai, 1998–9 [107] GP5þ/6þ Ectocervix—spatula Cancer institute-based controls 34 (16–81) 184 27.7 21.7 6.0 18.5 2.2
Endocervix— brush
India, Dindigul, 2003 [111] GP5þ/6þ Cervix—broom, brush Population-based controls 33.1a (16–59) 1891 16.9 12.5 6.0 3.8 1.0
<25 334 16.8
25–34 847 16.2
35–44 446 18.4
45–54 228 17.1
55 36 16.7
India, Kolkata, 1999–2001 [108] MY09/11 Endocervix— brush Pregnant women 26.5a (20–39) 135 28.1 9.6 5.2
20–29 106 23.6

S25.e14
30–39 29 44.8
(Continued )
Table 1

S25.e15
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
India, Kolkata, 1999–2003 [114] HCII Ecto/endocervix—broom, brush Population-based controls 25–65 17365 5.8
India, Maharastra, 1999–2003 HCII Cervix—brush Healthy women attending primary 39.3 (30–59) 2841 10.3
[109] village healthcare center
India, Manipur, 2001–6 [110] MY09/11 Ectocervix—spatula Women attending free 41.05 (20–80) 692 7.4 1.4 2.0
Endocervix—brush annual cervical screening
and general health
exam

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


<26 41 4.9
26–30 80 6.3
31–35 99 4.0
36–40 156 7.0
41–45 114 5.3
46–50 80 7.5
>50 102 10.8
India, New Delhic [103] Type-specific PCR (16, 18) Cervix—smear Cytologically normal women (40–60) 22 18.2
attending gynecology
department
India, New Delhic [104] Type-specific PCR (6, 11, 16, 18) Cervix—scrape Healthy pregnant antenatal 29 (25–40) 200 32.5 10.5
clinic attendees and
nonpregnant women
India, New Delhi c [105] Type-specific PCR (16) Cervix—swab Hospital-outpatient 28 (15–44) 30 13.3
sample
India, New Delhic [106] Type-specific PCR with L1 Urine Self-reported virgin university 21.5a (18–25) 100 6.0 4.0 0.0
primers (11, 16, 18) students
Cervix—scrape Healthy age-matched married 26.5a b (18–35) 104 10.6 6.7 0.0
women
India, Sikkim, 2002–5 [110] MY09/11 Ectocervix— spatula Population-based sample 36.36 (19–75) 415 12.5 5.1 0.2
Endocervix— brush
<26 50 8.0
26–30 72 8.3
31–35 74 17.6
36–40 68 8.8
41–45 54 12.9
46–50 27 7.4
>50 14 14.3
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)

India, Vellore, 2001–3 [113] MY09/11 Cervix—biopsy Women undergoing hysterectomy 45.3 (37–62) 30 0.0
not
associated with
HPV
India, West Bengal, MY09/11 Endocervix—brush Women attending gynecology 30.67 (14–80) 1112 13.0 8.5 0.9
1999–2002 [110] Ectocervix—spatula clinics for routine contraception

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


and reproductive healthcare
<26 429 13.5
26–30 216 9.7
31–35 154 11.0
36–40 88 7.9
41–45 51 13.7
46–50 32 15.6
>50 37 5.4
Japan, No city reported, 1995–6 L1C1/L1C2 Cervix—smear Controls with normal cytology 40.7 130 14.6 1.5 3.1 0.8 0.8
[129] undergoing Pap test screening
Japan, Multiple cities, 2000–1 L1C1/L1C2 Cervix—smear Pregnant women—cooperative 30.0a (19–40) 1183 12.5 1.3 0.5
[130] study group
~19–24 124 22.6
25–29 429 12.4
30–34 432 11.6
35–39 173 7.5
~40 25 16.0
Japan, No city reported, 1985–92 Type-specific PCR (6/11, 16, 18, Cervix—biopsy Cytologically normal women with 46.8a 30 10.0 0.0 0.0
[115] 33, 52b, 58) myoma of the uterus
Japan, Akita, 1992–2000 [116] Type-specific PCR with L1 Ectocervix—swab Women with normal cytology 43.5 (20–81) 132 12.1
primers (16) attending gynecology clinic for
routine screening
Japan, Akita, 1995 [117] Type-specific PCR (16) Cervix—swab Cytologically normal women 33.5 (24–42) 192 5.2
undergoing in vitro fertilization

Japan, Chiba, 1998–2003 [131] HCII Cervix—swab Hospital-based population 35 (17–73) 420 12.1 10.2 2.9
<19 15 46.7 33.3 26.7
20–29 115 21.7 19.1 4.3
30–39 101 9.9 7.9 1.9
40–49 108 1.9 1.9 0
50–59 62 11.3 9.7 1.6
60–69 14 0 0 0
>70 5 0 0 0
Japan, Hokuriku, 1995–9 [118] PCR with E7 primers (11, 16, 18, Cervix—smear Routine cervical cancer screening 16–72 1562 9.7

S25.e16
31, 51, 56, 58, 72, 72)
(Continued )
Table 1

S25.e17
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Japan, Hokkaido, 1990 [119] Type-specific PCR (16, Cervix—swab Cytologically normal obstetrics/ 38.5 (18–73) 83 6.0
18, 33) gynecology department
attendees
Japan, Ishikawa, 1998–2002 Type-specific PCR (16, 18, 31, Ecto/endocervix—brush Cytologically normal women 31 120 44.2
[120] 45) visiting outpatient gynecology
clinic
17–23 29 48

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


24–29 31 45
30–39 40 40
>39 20 45
Japan, Ishikawa and Toyama, pu-1M/pu-2R and pU31BM (6, Cervix—brush Population-based random sample 40.8a (16–82) 901 14.8 6.4 1.3
1995–6 [121] 11, 16, 18, 31, 33, 35, 52, 58)
16–24 113 11.5
25–34 289 12.5
35–44 167 16.2
45–54 177 14.7
55–82 155 20.0
Japan, Kanagawa, 1981–97 [122] Type-specific PCR (16, 18) Cervix—biopsy Cytologically normal cervical 46.3a (23–72) 24 0.0
tissue
Japan, Okinawa, 1993–2000 L1C1/L1C2 Cervix—swab Hospital-based controls and 52.4 (18–85) 3249 10.2 0.5 0.2
[123] population-based cervical
cancer screening
18–29 5.1
30–39 14.2
40–49 20
50–59 25.9
60–69 25.6
70–79 8.9
80–85 0.4
Japan, Okinawa, 1994–7 [124] PCR with L1 primers 6, 11, 16, Cervix—swab Population-based cervical cancer 17–85 4089 10.7 0.3 0.0
18, 31, 33, 52, 58) screening and women
attending the obstetrics/
gynecology department for
various complaints
17–29 286 20.6 1.0 0.0
30–39 564 9.0 0.0 0.0
40–49 802 9.1 0.2 0.0
50–59 1039 10.0 0.2 0.1
60–69 1029 10.9 0.3 0.1
70–85 372 10.2 0.3 0.0
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Japan, Okinawa Islands, 2001 Type-specific PCR with L1 Cervix—scrape Routine cervical cancer screening 30–85 3963 10.0 0.3 0.1
[125] primers (6, 11, 16, 18, 31, 35,
52, 58)
Yonashiro 591 9.3 0.3 0.2
30–39 9a
40–49 10.0a
50–59 9.8a

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


60–69 9.5a
70–85 5.9a
Naha 1225 10.1 0.2 0.0
30–39 11.5a
40–49 9.2a
50–59 9.5a
60–69 10a
70–85 11.8a
Hirara 2147 10.2 0.4 0.0
30–39 8.2a
40–49 9.0a
50–59 11.0a
60–69 11.5a
70–85 11.5a

Japan, Osaka, 1989–92 [126] PCR with E6 primers Cervix—smear Hospital clinic attendees 40.9 (18–72) 800 6.6
(16, 18)
18–29 142 5.6
30–39 182 7.7
40–49 308 7.5
50–59 111 6.3
60–72 57 1.8
Japan, Tokyo, 1997–2002 [127] Type-specific PCR (6, 11, 16, Cervix—smear Autopsy subjects without 82.7 (60–105) 335 2.7 2.1 0.6
18, 31, 33, 35, cervical
52b, 58) cancer
60–69 25 0.0 0.0 0.0
70–79 104 3.8 3.8 0.0
80–89 133 2.3 0.8 1.5
90–105 73 2.7 2.7 0.0
Japan, Urayasu and Ichikawa MY09/11 and GP5þ/6þ Cervix—swab Histologically normal women 41.5 (17–73) 56 32.1
City, 1997–8 [128] with previous abnormal
smear or routine
screening
(Continued )

S25.e18
Table 1

S25.e19
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Philippines, Manila, 1991–3 GP5þ/6þ Cervix—brush Hospital-based controls 46.8 381 9.2 1.3 1.3
[139]
South Korea, Bundang, 2001–2 GP5þ/6þ Cervix—swab Hospital-based population 30–54 1143 35.1 2.4 16.1
[138]
South Korea, Busan, 1999–2000 Type-specific PCR and GP5þ/6þ Ecto/endocervix—brush Population-based random sample 38.1a (15þ) 863 10.4 6.3 4.2 0.8 0.1
[136]
15–34 156 14.1

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


35–44 278 9.0
45–54 235 11.1
55–59 94 13.8
60 100 4.0
South Korea, Busan, 2002 [137] Type-specific PCR of 25 types Cervix—swab (self-sampled) University students 19 (16–29) 672 15.2 12.5 5.7 1.3 1.2
16–17 108 13.0
18–19 355 14.4
20–21 148 14.2
22–29 61 26.2
South Korea, Seoul, 1996 [135] Type-specific PCR (16, 18, 31, Cervix—brush Annual health check-up, health 23–72 1305 4.1 2.5 0.4
33) clinic sample
21–40 278 6.1
41–50 831 3.1
51–60 175 3.4
61–72 21 19.0
South Korea, Seoul, 1992–5 [132] GP5þ/6þ Cervix—swab Hospital-based population of 49.4a 746 7.2
cytologically normal women
South Korea, Seoul, 1996 [133] Type-specific PCR (16, 18, 33) Cervix—scrape Cytologically normal women 46 (25–65) 87 10.3
admitted to gynecology
department
South Korea, Seoul and GP5þ/6þ Cervicovaginal—swab Outpatient clinic sample 45.5 213 32.4 25.4 4.2
Sungnam City, 2000
[134]
Taiwan, No city reported, 1991–2 MY09/11 Cervix—swab Cytologically normal controls 43 (30–64) 260 9.2 0.8 4.2
[145] from community-based
screening
Taiwan, Northern Taiwan, 1997– HCII Community-based population of 51.3 1194
9 [143] handicapped women living in
rural areas, or elderly women
Vagina—swab (self-sampled) 12.1
Cervix—spatula, brush 13.0
(physician-sampled)
Taiwan, Kaohsiung County, HCII and GP5þ/6þ Cervix—brush, swab Population-based age-matched 44.9a 20 175 16.6 10.9 2.9
2003–4 [142] control
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Taiwan, Taichung and Changhua MY09/11 and type-specific PCR Cervix—scrape Women with normal cervical 39 (21–56) 29 0.0
City, 1997–2001 [140] (6, 11, 16, 18, 31, 33, 35, 45, scrapings, controls
58)
Taiwan, Taipeic [144] Type-specific PCR (6, 11, 16, 18, Cervix—smear Cytologically normal family 28.7 22 14.0 9.3 4.7
33) planning clinic attendees
Taiwan, Taipei, 1994–5 [141] Type-specific PCR (16, 18) Cervix—spatula Pregnant women 27.9 301 22.6 17.6 1.3
Thailand, Bangkok, 1991–3[146] MY09/11 Cervix—swab Hospital-based controls 43 291 6.9 2.1 0.0

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Thailand, Bangkok, 1995–6[147] MY09/11 Cervix—biopsy Outpatient clinic attendees with 43.9, 44.5b 50 6.0
chronic cervicitis and normal
histology
Thailand, Bangkok, 1995–8 [148] MY09/11 and type-specific PCR Cervix—biopsy Obstetrics and gynecological 44.1 (20–75) 147 2.7
(6, 11, 16, 18, 33) outpatient clinic
Thailand, Bangkok, 1997 [149] MY09/11 and type-specific PCR Cervicovaginal—lavage Women with normal cytology 32 (16–59) 102 4.9 1.0 1.0
(6, 11, 16, 18, 31, 33, 35) attending cervical cancer
screening
Thailand, Hat-Yai and Songkla, GP5þ/6þ Ectocervix—spatula Hospital-based controls 49.7 261 15.7 4.6 2.7
1990–3 [150] Endocervix—brush
Thailand, Kaoka District, 1997–8 GP5þ/6þ Ectocervix—spatula Population-based random sample 46.2a 1741 6.3 4.4 1.9 0.5 0.4
[151] Endocervix—brush
<25 198 10.6
25–34 293 9.2
35–44 301 5.0
45–54 300 6.0
55–64 335 4.5
65 314 4.5
Thailand, Khon Kaen, 1990–2001 GP5þ/6þ Cervix—spatula Controls within a cohort study of 54.5 (35) 113 10.6 8.0 5.3
[153] diet and lifestyle
Thailand, Khon Kaen, 1994–5 Type-specific PCR (6, 11, 16, 18, Cervix—scrape Asymptomatic women visiting an 34.8a 260 23.1 3.1 3.8
[152] 33) obstetrics and gynecological
outpatient clinic
<30 76 31.6
30–39 115 19.1
40 69 20.3
Thailand, Khon Kaen, 2002–4 RFLP Cervix—smear Clinic-based controls 25–60 105 18.1 3.8 11.4
[154]
Thailand; Philippines; Spain, GP5þ/6þ Ectocervix—scrape Cytologically normal women
1995–6 [155]
Thailand 49 115 12.2
Philippines 48 115 3.5
Spain 49 99 3.0
Vietnam, 1997 [156] GP5þ/6þ Ectocervix—spatula

S25.e20
Endocervix—brush
(Continued )
Table 1

S25.e21
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Ho Chi Minh City Family-planning clinic sample 41 922 11.0 3.3 1.2
<25 157 22.3
25–34 174 10.9
35–44 185 7.6
45–54 154 7.1
55–64 167 8.4
65 85 9.4

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Hanoi Population-based sample 45 994 2.0 0.2 0.2
<25 123 1.6
25–34 182 2.7
35–44 184 3.3
45–54 164 2.4
55–64 213 1.4
65 128 0.0

Europe/Middle East
Austria, Vienna, 1997–8 [157] HCII Cervix—swab Pregnant women undergoing 29.5 (15.3–46.2) 179 24.6 20.7 10.1
chorionic villus sampling
15–25 46 39.1
26–30 59 22.0
31–35 42 16.7
35–46 32 18.8
Belgium, No city reported, 1993 MY09/11 and GP1/2 Cervix—brush Gynecological outpatient 34.2 (19–43) 200 4.0 1.5 0.5
[164] population
Belgium, Antwerp, 2000 [158] GP5þ/6þ and type-specific PCR Cervix—brush Routine cervical cancer screening 39.4 (17–78) 286 10.8 2.8 1.4
(6, 11, 16, 18, 31, 33)
Belgium, Antwerp, 2001–2[159] GP5þ/6þ Cervix—smear Women undergoing routine 58.4a 1907 4.1 1.5 0.5
screening
50–54 701 5a
55–59 492 3.2a
60–64 321 3.5a
65–69 171 4.2a
70 222 4.5a
Belgium, Brusselsc [160,161] PCR (16, 18, 33) Cervix—scrape Routine cervical cancer screening 36 (20–70) 323 14.2 5.0 1.9
20–30 15.0a
31–40 13.0a
41–50 8.5a
51–60 10.0a
61–70 0.8a
Belgium, Flanders, 2000–1[162] MY09/11 Cervix—brush Population-based sample 40.1 (17–85) 287 24.0 4.2 1.7
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Belgium, Flanders, 2000– MY09/11 Cervix—brush Women with normal cytology 39.6 (17–85) 581 26.7 17.9
2[139,163] referred after routine exam or
screening
Belgium, Wilrijk, 2001–3 [394] GP5þ/6þ Cervix—smear Routine cervical cancer screening 35.8 2293 6.9 2.1 0.8
20–24 314 8.9
25–29 396 9.1
30–34 411 9.2

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


35–39 361 4.7
40–44 343 4.7
45–50 468 4.9
Czech Republic, No city reportedc MY09/11 Cervix—brush Cytologically normal gynecology 32.4 (20–77) 165 23.0 10.3 1.2
[165] clinic attendees
Czech Republic, Prague, 1975–83 MY09/11 and GP5þ/6þ Cervix—spatula Healthy controls from 31.3a 208 5.3
[25] observational study
Controls for cervical neoplasia 35 147 4.8
cases
Controls for borderline or normal 34 108 3.7
cases
Denmark, Copenhagen, 1991–3 GP5þ/6þ Ecto/endocervix—brush Population-based cohort 25 (20–29) 956 15.4 11.3 4.6
[167–170]
20–23 288 19.4
24–36 311 14.1
27–29 357 13.1
Denmark, Skejby, 1997–8 [166] Type-specific PCR (16) Cervix—brush Controls presenting for legal 37 (21–64) 61 33.3
abortion, hysterectomy, or
screening for cervical disease
Egypt, Ain Shams, 1997–9[272] Type-specific PCR (16) Cervix—biopsy Controls undergoing 48 (36–72) 20 25.0
hysterectomy for nonmalignant
conditions
Finland, Helsinki, 2001–3 [182] HCII Vaginal swab—self-collected First year university students 22.7 (19–47) 919 33.7 29.5
<19 68 23.5
20–24 671 33.5
25–29 128 41.4
30–34 24 37.5
35–40 28 25.0
Asymptomatic university students 24.8 (19–40) 550 31.8 25.1
<19–24 312 34.3
25–29 217 27.2
30–40 21 42.9
Finland, Kuopio, 1981 [181] MY09/11 Cervix—brush Pregnant women at delivery 29.2 (18.5–40.5) 105 19.0
(Continued )

S25.e22
Table 1

S25.e23
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Finland, Turku, 1998–2000 MY09/11 and GP5þ/6þ Cervix—brush Third trimester pregnant women 25 (18–35) 76 16a
[183,395]
France, No city reported, 1999– HCII Cervix—brush Women attending screening at 34.5 1785 30.1 22.6 3.2
2000 [195] gynecology clinic
France, Amiens, 2000–1 [184] HCII Cervix—brush Women undergoing routine 38.9 (20–62) 3832 14.3
screening
20–24 513 16.6

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


25–29 610 18.9
30–34 570 13.5
35–39 585 15.6
40–44 627 14.0
45–49 611 12.5
50–54 508 13.4
55–59 263 8.2
60–64 94 8.0
France, Besancon, 1997–8 [186] MY09/11 Cervicovaginal—brush Routine cervical cancer screening 35 (16–76) 596 37.8
and 103 patients from
colposcopy clinic
HCII Routine cervical cancer screening 35 (16–76) 466 22.7 17.8
16–24 49 28.6 20.4
25–34 173 25.4 21.9
35–44 159 23.3 17.6
45–76 85 12.9 8.2
France, Besancon, 1997–2002 HCII Endocervix—brush Hospital-based cohort of normal 35.7 (16–76) 781 33.0
[185] women
16–19 22 63.6
20–29 189 51.9
30–39 301 27.9
40–49 192 25.5
50–76 77 16.9
France, Besancon, 1998–9 [187] MY09/11 Endocervix—brush Cytologically normal Caucasian 35 (16–76) 50 24.0 20.0
women visiting department of
obstetrics and gynecology
France, Paris, 1993 [188] Type-specific PCR (16) Cervix—scrape Cytologically normal women 38.45 120 4.2 0.0
France, Poitiers, 2001–4 [189] MY09/11 Cervix—brush Women presenting for routine 44 (17–77) 657 8.2 5.3 2.4 1.8 0.9
health exam
17–24 88 18.2
25–44 262 9.2
45–77 307 2.6
France, Reims, 1996–7 [191] HCII Cervix—scrape, brush, spatula Women undergoing routine 36.1 (14–68) 1028 10.5 8.8 1.8
screening
14–20 50 12.0 12.0 0.0
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
20–29 270 17.8 15.6 2.2
30–39 310 10.3 8.4 1.9
40–49 261 6.5 4.2 2.3
50–59 102 4.9 3.9 1.0
60–68 35 2.9 2.9 0.0
France, Reims, 1997–9 [193] HCII Cervix—brush Women attending for routine 36 (15–85) 2778 20.4 15.6 4.8
cervical cancer screening

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


15–20 218 23.9 20.2 3.7
21–30 958 28.0 23.8 4.2
31–40 1094 19.8 14.7 5.1
41–50 855 16.0 10.9 5.1
51–60 414 14.5 9.4 5.1
61–85 239 15.5 10.9 4.6
France, Reims, 1997–2001 [190] HCII Cervix—brush Women attending routine 34 (15–76) 7932 15.3 15.3
screening clinics
15–20 418 20.1
21–30 1843 23.6
31–40 2076 13.9
41–50 1925 12.2
51–60 1014 10.8
61–76 656 9.3
France, Reims, 1997–2002[192] HCII Cervix—brush Women undergoing routine 39 (17–77) 3091 21.3
screening (cytology within
normal limits)
France, Strasburg, 1992[194] Type-specific PCR (6, 11, 16, 18) Cervix—biopsy Women receiving contraception 27.1 22 9.1
counseling
Germany, No city reported, 1991– MY09/11 Cervix—swab Routine cancer screening 39.5 65 24.6
2 [196] programs
Pregnancy care unit 29.3 36 19.4
Germany, No city reported, 1992– HCI Cervix—smear Routine screening at gynecology 36.2 (15–72) 967 18.5
3 [201] clinic
15–34 444 25.2
35–72 523 12.8
Germany, No city reported, 1998 GP5þ/6þ Cervix—brush Cytologically normal women 32 (22–45) 294 7.8
[202] entering an in vitro fertilzation
program
Germany, Bonn-Region, 2002 MY09/11 and GP5þ/6þ Ecto/endocervix—swab or Routine cervical cancer screening 36b (17–81) 1393 30.0
[197] spatula
Germany, East Thuringia, 1996–8 GP5þ/6þ Ecto/endocervix—swab, brush Routine cervical cancer screening 35 (18–70) 4671 7.8
[198]
18–25 916 14.0a

S25.e24
26–30 697 9.5a
(Continued )
Table 1

S25.e25
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
31–35 881 7.5a
36–40 776 6.0a
41–45 574 6.5a
46–50 350 4.5a
51–55 272 3.0a
56–60 179 2.0a
61–65 80 0.0a

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


66–70 36 0.0a
Germany, Hannover and HCII Cervix—swab Routine cervical cancer screening 42.7 (30) 8083 6.4
Tuebingen, 1998–2000 [199]
Germany, West Rhine, 2004 MY09/11 and GP5þ/6þ Cervix—brush Population-based sample 40.5 (17–83) 2916 32.5 26.2 5.3
[200]
Greece, Northern Region, 2000–1 MY09/11 Cervix—spatula, cytobrush Women attending clinics for 43 (17–67) 1296 2.9
[203,204] yearly gynecological exam
17–29 101 12.9
30–40 459 2.6
41–67 736 1.6
Greece, Northern Region, 2000–1 MY09/11 Endocervix—cytobrush Outpatient gynecology clinic— 44 (17–65) 379 6.0
[205] Vagina—cytobrush routine screening
Greece, Ioannina, 1997–9 [206] MY09/11 Ectocervix—spatula Outpatient obstetrics and 38 (17–79) 1000 23.8 6.7 1.3
Endocervix—brush gynecologic clinic; no history of
cervical disease
Greece, Thessaloniki, 1992 Type-specific PCR (16, 18) Ecto/endocervix—brush Women attending outpatient (20–55) 226 36.3 6.6 1.3
[207,208] gynecology clinic for routine
smear
20–34 45.3
35–50 25.3
50–55 43.3
Greenland; Denmark, 1988 [171] Cpl/CPIIG (16, 18, 31, 33, 58) Endocervix—spatula, brush Population-based sample (20–39)
Greenland 28.9a (20–39) 118 33.1 21.2 2.5
20–24 39 46.2
25–29 34 32.0
30–39 45 22.0
Denmark 30.2a (20–39) 119 22.7 8.4 2.5
20–24 29 31.0
25–29 24 29.2
30–39 66 15.2
Greenland; Denmark, 1993 [172] Type-specific PCR with E6/E7 Cervix—brush, swab Population registry
primers (11, 16, 18, 33)
Greenland 28.0a 129 43.4
Denmark 31.9a 126 38.9
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Hungary, No city reported, 1998– HCII Cervix—smear Outpatient clinic attendees— 31.1b (20–60) 464 4.3 3.0 1.3
2002 [212] healthy women
20–24 104 7.7
25–29 104 4.8
30–34 77 2.6
35–39 43 4.7
40–44 56 1.8

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


45–49 44 2.3
>50 36 2.8
Hungary, Budapest, 1999 [209] HCI Cervix—swab Routine cytology screening 31.9a 1100 17.5
Hungary, Debrecenc [211] PCR with E6 and E7 primers (16) Ecto/endocervix—swab Cytologically normal family 37 102 8.8
planning attendees
Hungary, Debrecenc [213] PCR with L1 primers (6, 11, 16, Ecto/endocervix—brush Cytologically normal women 28.4 (17–51) 163 21.5 3.7 1.8
18, 31, 33, 52, 58) attending gynecology clinic
17–24 66 34.8
25–32 47 14.9
33–51 50 10.0
Hungary, Debrecenc [210] L1 primers (6, 11, 16, 1,8, 31, 33, Ecto/endocervix—brush Cytologically normal first tri- 23.9 (18–37) 39 17.9
52, 58) mester pregnant women
Italy, No city reported, 1990–1 Type-specific PCR with L1 Cervix—scrape Cytologically normal women 19–65 124 8.9
[221] primers (16)
Italy, Multicenter, 1997–9 [225] MY09/11 Cervix—smear, spatula HIV negative women; 32.5 (21–48) 48 27.1 29.2 16.7
Endocervix—brush DIANAIDS project
Italy, No city reported, 2001 [224] MY09/11 Ecto/endocervix—swab Women presenting for routine Pap 39 (22–74) 94 21.3
smear
Italy, Ancona, 1994 [214] PCR with L1 primers Ecto/endocervix Clinic-based controls 32.9a (22–41) 473 7.2
Italy, Genova, 1992–3 [215] MY09/11 Cervix—swab Routine cytological screening 51 (20–81) 503 15.9 9.1 5.8
44 119 15.1 6.7 3.4
45–52 120 17.5 8.3 9.2
53–59 122 11.5 9.0 8.2
60 142 19.0 12.0 7.0
Italy, Milan, 1995–7 [217] MY09/11 Cervicovaginal—swab Primary cervical cancer screening 35 (25–64) 100 48.0
Italy, Padua, 1997–9 [218] MY09/11 Cervix—brush Routine cytology screening 31 (19–74) 106 6.6 8.8 7.1 1.7 2.6
Italy, Pavia, 1997 [223] MY09/11 Cervicovaginal—lavage Pregnant women 30 (16–43) 751 5.5 0.9
Italy, Rome, 1996 [216] Type-specific PCR (16, 18) Cervix—spatula Cytologically normal women 37.7 (17–70) 143 11.9 2.1
attending routine
gynecological exam
17–25 48 22.9 2.1
26–35 30 10.0 3.3
36–50 32 6.3 3.1
51–70 33 3.0 0.0

S25.e26
Italy, Rome, 1998 [219] MY09/11 Cervix—spatula, swab Routine cytology screening 34 (21–48) 24 33.3
(Continued )
Table 1

S25.e27
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Italy, Turin, 2002 [220] GP5þ/6þ Cervix—brush Population-based sample (25–64) 1013 8.8 7.1 1.7 2.6 0.1
25–29 115 13.0 11.5a 1.8a
30–34 110 13.6 12.5a 1.0a
35–39 115 13.9 11.5a 2.8a
40–44 113 11.5 8.0a 3.5a
45–49 114 5.3 3.5a 1.8a
50–54 115 6.1 4.5a 1.8a

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


55–59 114 7.9 6.0a 1.8a
60–64 115 2.6 1.8a 1.0a
65–70 102 4.9 4.9a 0.0a
Italy, Udine, 1994–5 [222] MY09/11 Cervicovaginal—lavage Cytologically normal women 37.7 (18–67)c 197 20.3 5.1
attending clinical department
Latvia, Riga, 1998–2001 [226] Type-specific PCR with L1, E6, Cervix—brush Population-based controls 50.8 (18–89) 236 5.1 3.8
and E7 primers
40 75 17
41–50 42 4.7
51–60 43 2.3
>60 76 3.9
Lebanon, Beirut, 2002 [273] MY09/11 and GP5þ/6þ Ectocervix—spatula Routine gynecological exam 41.2a (18–79) 1026 4.9 3.0
Endocervix—brush, swab
18–29 4.0a
30–39 3.8a
40–49 6.5a
50–59 4.0a
60–69 10.0a
70–79 0.0a
The Netherlands, Amstelveenc GP5þ/6þ and type-specific PCR Cervix—scrape, brush Routine cervical cancer screening 35–55 1346 3.5 0.4 0.5
[396]
The Netherlands, Amstelveen, Type-specific PCR (6, 11, 16, 18, Cervix—brush Cytologically normal 15–34 156 14.1 3.8
1992 [229] 31, 33) and GP5þ/6þ gynecological check-up
15–24 29 25.0a
25–29 66 14.0a
30–34 61 10.0a
Population-based cervical cancer 35–54 1555 4.1 0.9
screening
35–39 536 4.0a
40–44 387 5.0a
45–49 246 6.0a
50–54 386 3.0a
Outpatient clinic attendees for 15–34 2320 13.9 3.3
contraception/ gynecological
complaints
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
15–19 169 17.0a
20–24 486 22.0a
25–29 775 14.0a
30–34 890 11.0a
Outpatient clinic attendees for 35–54 1826 6.6 1.5
contraception/ gynecological
complaints

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


35–39 734 7.0a
40–44 538 8.0a
45–49 356 7.0a
50–54 198 6.0a
The Netherlands, Amsterdam, GP5þ/6þ Cervix—brush Routine cervical cancer screening 42 (34–54) 1622 6.0 4.6 0.7 1.8 0.9
1988–91 [397,398] in a population-based sample
The Netherlands, Amsterdam, Type-specific PCR (6, 11, 16, 18, Cervix—brush Pregnant women 29.3a 709 9.6 3.1
1994 [227] 31, 33) and GP5þ/6þ
15–19 33 18.2
20–24 136 14.0
25–29 188 9.0
30–34 222 6.8
35–39 99 10.1
40–49 31 3.2
Nonpregnant women 33.1a 3948 10.9 2.9
15–19 169 17.2
20–24 486 20.8
25–29 775 13.7
30–34 890 9.7
35–39 734 6.8
40–49 894 6.7
The Netherlands, Amsterdam, GP5þ/6þ Cervix—brush Routine cervical cancer screening 46.1a (15–69) 3305 4.6 3.0 0.7 0.9 0.5
1995–8 [228] program
15–24 26 19.2 12.5a 0.0 7.7 0.0
25–29 46 23.9 15.0a 8.0a 0.0 2.2
30–34 389 13.6 9.0a 0.5a 2.8 1.0
35–39 316 7.0 2.5a 2.4a 1.6 0.3
40–44 679 3.8 2.4a 0.2a 0.1 0.4
45–49 708 6.1 3.0a 1.3a 1.3 0.8
50–54 431 3.7 2.0a 1.0a 0.0 0.0
55–59 488 3.3 1.5a 1.0a 0.0 0.2
60–69 222 3.2 2.2a 0.5a 1.4 0.0
The Netherlands, Amsterdam, GP5þ/6þ Cervix—brush Population-based cervical cancer 42.8 (29–61) 21245 3.6
1999–2002 [399] screening

S25.e28
29–33 246 8.3
(Continued )
Table 1

S25.e29
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
59–61 38 2

The Netherlands, Utrecht, 1976– PCR with L1 primers Cervix—smear Population-based controls 38.6 (35–54) 270 11.5 8.5 3.0 1.1
84 [230]
The Netherlands, Zeeland, 1976– GP5þ/6þ Cervix—smear Population-based cervical cancer 43 (34–54) 104 6.7 1.8 1.8
96 [231] screening

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Norway, Oslo, 1991–2[232–235] PCR (6, 11, 16, 18, 31, 33) Cervix—brush Population-based controls 32.8, 32b (20– 222 17.1 7.7
44)
20–29 77 24.7 11.7
30–34 68 14.7 7.4
35–39 48 10.4 6.3
40–44 29 13.8 0.0
Norway, Oslo, 2001 [236] GP5þ/6þ (16, 18, 31, 33, 45) Cervix—smear, brush Outpatient population-based 48.9 (30–91) 4136 10.4 1.3 0.8
screening study
30–39 1023 15.3
40–49 1211 9.4
50–59 1208 8.2
>60 694 8.7

Norway, Trondheim, 1992 [237] GP5þ/6þ and Cpl/CPIIG Cervix—smear Archived, normal cervical smears 33 (21–67) 48 16.7
Poland, Gdansk, 2001 [238] PCR with L1 primers (6, 11, 16, Cervix—scrape, swab Healthy women undergoing 58a (28–82) 229 1.7 0.4
18, 31, 33) routine gynecological exam
Poland, Krakow, 2001 [239] HCII Cervix—smear Population-based, pregnant 18–37 145 13.1
women
Population-based, nonpregnant 18–37 145 9.7
women—screening for
cervical cancer
Poland, Krakow, 2006 [240] SPF10 Cervix—brush Healthy controls undergoing 28 (23–33) 42 21.4
preventative exam before
planned pregnancy
Poland, Poznan, 2002 [241] Type-specific PCR (2, 5, 6, 8, 11, Cervix—brush Cervical cancer screening (45–78) 90 48.9 33.3 22.2
13, 16, 18, 26, 27, 30, 31, 32, gynecology clinic
33, 35, 39, 40, 41, 42, 43)
45–49 41 58.5 39.0 26.8
50–55 26 53.8 30.8 19.2
56–78 23 26.1 26.1 17.4
Poland, Warsaw, 2000–02 [242] Type-specific PCR (6, 11, 16) Vaginal discharge Pregnant women with and without 28a (18–38) 45 26.7 20.0 11.1
insulin-dependent diabetes
mellitus
Russia, Latvia and Belarus, 1998– HCII Cervix—smear Women attending gynecology 37.5a (15–60) 448 46.7
2002 [245] clinics or STI clinics for
cervical screening
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Russia, St. Petersburg, MY09/11 Cervix—swab Healthy attendants at gynecology 30.2 (15–45) 309 29.1 6.6 1.6
1999[243,244] practice
15–20 29 31.0
21–25 64 37.5
26–30 67 28.4
31–35 59 27.1
36–40 46 26.1

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


41–45 44 22.7

Spain, Alava, Girona, Guipuzcoa, Type-specific PCR (6, 11, 16, 18, Cervix—scrape Population-based controls 36.1 (18–68) 193 4.7 0.5 0.0
Murcia, Navarra, Salamanca, 31, 33, 35)
Sevilla, Vizcaya, Zaragoza,
1985–8 [4,155,334–340]
Spain, Barcelona, 1992 [247] Type-specific PCR (16, 18) Cervicovaginal—spatula Cytologically normal controls 29 (16–40) 64 10.9
Spain, Barcelona, 1998–2000 GP5þ/6þ Random sample (population- 43 (14–75) 973 3.0 2.2 0.5 0.6
[248] based sample)
14–24 174 7.0a
25–34 147 2.8a
35–44 175 3.0a
45–54 177 1.0a
55–64 175 1.8a
54–75 125 2.2a
Spain, Basque Region, 1991 Type-specific PCR (6, 11, 16, 18) Cervix—spatula Cytologically normal women 34 (16–82) 75 11.0
[249] attending family planning
clinic
Spain, Basque Region, 1994[250] Type-specific PCR (16) Cervix—spatula Women undergoing routine smear 32 (18–57) 38 42.1
Sweden, No city reported, 1993 Type-specific PCR (6, 11, 16, 18, Ectocervix—brush Women attending routine (20–29) 230 13.0 6.1 1.7
[266] 31, 33, 35) screening
Sweden; Finland; Holland, 1994 GP5þ/6þ and type-specific PCR Cervix—brush, spatula Cytologically normal women 28 (18–35) 366 10.9
[268] (6, 11, 16, 18, 31, 33) participating in a clinical trial
for a contraceptive device
Sweden, Nationwide, 2001[267] GP5þ/6þ Cervix—brush Population-based cervical 32–38 6123 6.8 2.1 0.6
screening program
Sweden, Karlstad, 1989–90[251] MY09/11 and type-specific PCR Cervix—brush Upper secondary school students 16.3 (15–17) 52 11.5
(6, 11, 16, 18, 31, 33)
Sweden, Malmo, 1992 [252] Type-specific PCR (6, 11, 16, 18, Cervix—brush Controls with normal cytology 25.1 (17–39) 30 10.0 3.3
31, 33) presenting for contraceptive
counseling
Sweden, Stockholm and MY09/11 and Cpl/CPIIG Cervix—smear Population-based cervical cancer 44 (20–74) 118 2.5
Vasterbotten, 1969–95 [254] screening
(Continued )

S25.e30
Table 1

S25.e31
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
Sweden, Stockholm and Uppsala, MY09/11 Cervix—swab Virgins attending adolescent and 18 (10–25) 130 1.5
1994 [253] primary healthcare clinic
Sweden, Stockholm, 1994 [255] MY09/11 and type-specific PCR Cervix—brush Population-based gynecologic 25 478 13.4 3.1 1.5
health screening
30 15.7
31–40 2.2a
41 11.1

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Sweden, Umea, 1989[256,257] MY09/11 Cervix—swab Population-based study 22.5 (19–25) 581 20.3 12.2 3.8
19 55 20.0
21 139 17.3
23 205 19.0
25 127 33.1
Sweden, Umea, 1991 [258] Type-specific PCR (16) Ecto/endocervix and vagina— Women attending outpatient care 40 (17–42) 99 21.2
smear for gynecologic disorder or
regular check-up
Sweden, Uppsala, 1969–95[259– Type-specific PCR (16, 18) Cervix—smear Population-based screening 35 (20–70) 617 5.8
261]
<25 236 6.4
25–29 178 5.6
30 203 5.4
Sweden, Uppsala, 1997–9 [400] GP5þ/6þ (16, 18, 31, 33) Cervix—smear Routine gynecological screening (25–59) 197 9.1

Sweden, Uppsala, 2007 [262] GP5þ/6þ andHCII Self-sampled vaginal smear Healthy women who have not 40.8a (35–50) 369 25.6
been screened in 6 years
35–42 264 31.3
43–50 105 13.5
Sweden, Vasterbotten, 1993–6 MY09/11 and GP5þ/6þ (11, 16, Cervix—brush Population-based cervical cancer 40 (20–63) 315 7.0
[263,264] 18, 33) screening
Sweden, Wuzburg, 1989–90[265] MY09/11 Cervix—brush Adolescents at healthcare 16.1 (15–17) 89 4.9 2.4
program
Switzerland, Multiple cities, 2005 HCII Cervix—brush Women attending gynecology 44.4 (17–93) 13842 8.2
[269] clinics
16–20 21.0a
21–25 18.0a
26–30 15.0a
31–35 10.0a
36–40 9.0a
41–45 7.0a
46–50 8.0a
51–55 6.0a
56–60 7.0a
61–65 6.0a
(Continued )
Table 1
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
66–70 7.0a
71–75 6.0a
76 10.0a
Switzerland, Genevac [270] HCI Ecto/endocervix—brush Outpatient adolescent clinic; 17.5a (14–20) 134 14.2
sexually active
Turkey, Istanbul, 1996 [274] MY09/11 Cervix—brush Pregnant women 17–36 21 9.5
UK, Multiple cities, 1998– HCII Cervix—brush, spatula Women attending screening 42 (30–60) 10358 7.5

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


2001[271] clinics
30–34 2319 14.5
35–39 2157 8.6
40–44 1931 6.0
45–49 1461 4.4
50–54 1343 3.4
55–60 1147 3.8
UK, England, Birmingham, GP5þ/6þ and MY09/11 Cervix—smear Cytologically normal women at 17.5 (15–19) 1725 14.1
1988–92 [174] baseline screening
UK, England, London, 1987[175] Type-specific PCR (16) Cervix—scrape Women attending cervical cancer 38.4 (18–76) 249 18.9
screening
UK, England, London, 1992–4 Type-specific PCR (16, 18, 31, Cervix—spatula, brush Women attending center for 29 (20–45) 1904 4.5 1.6 0.8
[176,178] 33) routine smear
<24 372 10.4a
25–29 644 10.3a
30–34 477 5.0a
35–39 247 6.0a
40–44 132 1.8a
45–49 71 3.0a
50 25 0.0a
UK, England, London, 1999[177] MY09/11 Cervix—spatula Routine cervical cancer screening 46 (35) 2988 6.0 0.7 0.2
34–39 7.8a
40–44 5.5a
45–49 4.5a
50–54 5.3a
55–59 6.5a
60–64 7.5a
UK, England, Manchester, 1988– MY09/11 Cervix—spatula Routine cervical cancer screening 15–69 6128 7.3 5.1
93 [401]
15–19 319 20.1 17.2
20–24 466 19.1 16.1
25–29 586 13.8 10.4
30–34 1191 8.1 4.5
35–39 914 3.9 2.5

S25.e32
40–44 926 2.8 1.6
(Continued )
Table 1

S25.e33
Continued
Prevalence (%)d
Study location, dates, Assay Site of specimen Group tested Mean or median Sample Overall High Low HPV HPV
reference age, size HPV risk risk 16 18
years (range)
45–49 508 3.5 2.2
50–54 1104 2.9 1.6
55–69 114 1.8 0.9

UK, England, Nottingham, 1988– GP5þ/6þ (16, 18) Cervix—smear Clinic-based controls with normal 591 15.4 3.0 2.9
92 [179] smears
<20 100 18 5.0 3.0

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


20–39 269 18.6 3.8 2.3
40 222 10.4 1.4 3.6
UK, England, Nottingham, 1990– GP5þ/6þ Cervix—smear Stored specimens from regional 42.6a (21–51) 656 18.8
2 [180] screening laboratory collected
from general practitioners
21 86 15.1
31 98 15.3
41 100 14.0
51 372 21.8
UK, England, Sheffield, 1992–3 Type-specific PCR (16) Anus Hospital-based controls 43b (22–56) 95 12.4
[173]
UK, Scotland, Edinburgh, 2000 GP5þ/6þ Cervix—smear Women undergoing routine 36.6 (16.5–78) 3089 12.7 8.3 3 3.4 1.4
[246] screening
HC ¼ hybrid capture; HPV ¼ human papillomavirus; PCR ¼ polymerase chain reaction; STI ¼ sexually transmitted infection; NHANES ¼ National Health and Nutrition Examination Survey; DIANAIDS ¼
Diagnosi Iniziale Anomalie Neoplastiche AIDS Collaborative Study Group.
a
Estimate.
b
Median.
c
Date of sample collection was not specified.
d
Merged columns indicate a combined prevalence rate for 16 and 18.
Table 2
HPV prevalence estimates in women from high-risk populations by continent, country, and study year
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
Africa
Ivory Coast, Abidjan, 1994 HCI Cervicovaginal—lavage Maternal group at risk for 29 (18–48) 258 5.8 28.7
[402,403] HIV
HCI Cervicovaginal—lavage Sex workers 29 (15–54) 273 7.0 30.0
Senegal, Dakar, 1990–1 Southern transfer Ecto/endocervix—smear Women attending infectious 31.6a 84 40.5
[277] hybridization (6, 11, 16, disease clinic
18, 31, 33, 35) and PCR
with consensus primers

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


HIV-1þ women 28.7 16 75.0
HIV-2þ women 38.1 15 73.3

Senegal, Dakar, Thies, and Hybridization of genomic Cervix—swab Sex workers 30.9a 681 43.0 10.7 (16, 18, 45)
Mbour, 1990–3 [275] DNA with type-specific
probes
South Africa, Kwazulu, MY09/11 Cervix—smear Commercial sex workers 26 (16–48) 99 62.6 10.5
1998 [276]
Tanzania, Dar es Salaam, GP5þ/6þ Cervix—swab Gynecologic in-patient 30.2 (15–70) 359 58.8 7.8 10.3
1991 [404] population with various
gynecologic complaints
14–24 20.5
25–34 16.5
35–44 14.7
45–70 3.2
Tunisia, Sousse, 2002 [26] MY09/11, pU-1M/pU-2R, Cervix—brush Legal prostitutes 30 (20–45) 51 39.2 23.5 7.8 11.8
and pU-31B/pU-2R
Zimbabwe, Mupfurec [278] GP5þ/6þ Cervix—lavage HIVþ population-based (15–49) 61 54.1 3.3 9.8
rural community
screening
Central and South
America
Brazil, Sao Paulo, 1997–8 HCI Cervix—smear Prison inmates 32.4 209 34 16.3 4.8
[405]
Brazil, Sao Paulo, 1997–9 MY09/11 and PC04/GH20 Cervix—scrape Routine gynecology visit, 32 (18–67) 223 87.5 27.1 13.3
[279] HIVþ women
Brazil, Sao Paulo, 1997–9 SPF10 Cervix—brush Routine gynecology visit, 32.1 (18–67) 22 4.5 9.1
[406] HIVþ women
Brazil, Sao Paulo, 1997–9 HCII Cervicovaginal—brush Routine gynecology visit, 32.4, 32b (18–67) 265 65.3 33.6 7.5
[280] HIVþ women
Honduras, Tegucigalpa, GP5þ/6þ Cervix—spatula HIVþ and HIV prostitutes 32 51 35.3
1994–5 [285]
Mexico, Mexico City, 1998 MY09/11 and HMB01 Cervix and vagina—swab Sex workers 28.6 (18–62) 495 48.9 11.1 3.6
[281]

S25.e34
18–22 107 75.7
(Continued )
Table 2

S25.e35
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
23–27 165 57.6
28–32 97 40.2
33–62 126 21.4
Mexico, Mexico City, 1998– Type-specific PCR (5, 6, 8, Cervix—smear Cytologically normal, HIVþ 37.2 (20–60) 24 41.7
9 [283] 11, 16, 18, 31, 33, 35, 39, women
45, 51, 56, 58)
Mexico, Hermosillo; Peru, MY09/11 Endocervix—brush (self- Cytology normal women 36.9a (18–67) 144 17.4
Lima; USA, Arizona, sampled) attending colposcopy

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


1999–2000 [284] clinics
Endocervix—spatula, brush 18.7
(physician-sampled)
Venezuela, Caracas, 2001 MY09/11 Ecto/endocervix—swab Women attending uterine 26 (18–35) 60 55.0
[282] cervix clinic
North America
Canada, No city reported, MY09/11 Endocervix—brush, spatula HIVþ women and hospital- 32.5 262 62.6 32.1 5.0
1993 [294,295] based sample with no
dysplasia
<30 131 74.8
30–39 177 64.4
40 67 59.7
USA, New York, New York; MY09/11 Cervicovaginal—lavage HIVþ women from clinical 36 (31–41) 855 52 19 33
Chicago, Illinois; and outreach sources
California, Los Angeles
and San Francisco;
Washington, DC, 1994–5
[359]

USA, Baltimore; Rhode PCR with L1 primers Cervicovaginal—lavage HERS cohort: women at risk 35 1157 51.5 15.2 22.8 5.1 4.6
Island, Providence; for HIV
Detroit; New York,
Bronx, 1993–5 [407–409]
USA, New York, Bronx, MY09/11 and HMB01 Cervicovaginal—lavage WIHS cohort: HIVþ women 37 (17–73) 1778 63.4
Manhattan, and Brooklyn;
Chicago; California, Los
Angeles and San
Francisco; Washington,
DC, 1994–5 [287–293]
WIHS cohort: HIV women 35 (17–62) 500 29.8
17–29 512 73.6
30–39 1035 57.2
40–62 718 52.5
(Continued )
Table 2
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
USA (13 cities in the US), MY09/11 and HMB01 Cervicovaginal—lavage REACH cohort: cervical 13–18 188 70.7 47.3 5.3
1996–7 [410] samples from high-risk
adolescent girls
USA (13 cities in the US)c MY09/11 and HMB01 Anus—swab REACH cohort: cervical 16.9a (13–18) 265 26.4 14.7 8.3 4.9 5.3
[411] samples from high-risk
adolescent girls
13–16 94 25.5
17–18 171 26.9

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


USA, Indiana, No city MY09/11 Cervicovaginal—lavage STI clinic attendees 28.1 (18) 295 49.2 42.4 19.7 15.6 2.7
reported, 2001 [412]
USA, Indiana, Indianapolisc HCII Cervicovaginal— lavage STI clinic attendees 28.2 248 17.7 13.3 8.9
[367, 368]
USA, Louisiana, New GP5þ/6þ Cervix—swab HIV outpatient clinic sample 34.1a 53 50.9 41.5
Orleans, 2001 [413]
USA, Maryland, Baltimore, MY09/11 and HMB01 Cervix—swab Adolescents attending an 17.5 (11–20) 80 91.3 40.0 51.3 21.3 8.8
1996–7 [286] STI clinic and university
adolescent clinic
USA, Maryland, Baltimore, MY09/11 and HMB01 Cervicovaginal—lavage, ALIVE cohort: high-risk 36.2 (18) 268 56.0 6.0 5.2
1998 [407] brush, spatula population injection drug
user, HIVþ/

USA, Michigan, Ann Arbor, PCR with E1 primers Cervix—swab Women attending clinic for 31.8 (18–50) 273 21.2 5.5 1.8
1990–2 [414–417] symptoms of vaginitis

USA, New York, Brooklyn, Hybridization with HPV- Cervicovaginal—lavage Attendees of medical/drug 31 (18–50) 221 16.7
1990–1 [418] DNA probes treatment clinics and
community health centers
<30 110 27.3
30–39 74 9.5
40 37 0

USA, New York, New York, PCR with L1 primers (16, Cervicovaginal—lavage STI clinic attendees 34a 669 48.4 6.0 2.8
1991–3 [419–421] 18)

USA, New York, New York, PCR with L1 primers Cervicovaginal—lavage, Cytologically normal renal 43.9 (26–63) 21 4.8
1995 [422] brush transplant patients
USA, North Carolina, Fort MY09/11, HMB01, and Vagina—swab Military women with 24 (18–59) 768 36.5
Bragg, 1997–8 [423] type-specific PCR (6, 11, genitourinary symptoms
16, 18, 26, 31, 33, 35, 39, or STI screening
40, 45, 51–56, 58, 59, 66,
68, 73)
USA, Washington, Seattle, MY09/11 Cervix and perianal area— STI clinic attendees 26.5 50 72.0 20.0

S25.e36
1991–2 [424] swab
(Continued )
Table 2

S25.e37
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
<25 25 84.0
25 25 60.0
USA, Washington, Seattle, MY09/11 Cervix and vulvovaginal Pregnant women from high 22.7a 144 41.0 11.8 3.5
1997 [425] area—swab HPV prevalent
populations attending
obstetrics clinic
USA, Washington, Seattle, MY09/11 and HMB01 Cervix and vagina—broom Women who have sex with 31 (17–56) 248 12.5 9.3 4.8 2.8 0.8
1998 [426] women

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Asia and Australia

Australia, Melbourne, 1991– MY09/11 Cervix—spatula Renal transplant patients 43 69 21.7


2 [427]
Women undergoing dialysis 44 89 20.2
Women with mild renal 47 22 4.5
impairment
Australia, Sydney, 1988 Type-specific PCR (6/11, 16, Cervix—lavage STI clinic attendees 28 (16–48) 109 51.4 11.9 29.4
[297] 18, 33)
China, Hong Kong, 1991–2 MY09/11 and GH20/PC04 Cervix—spatula Women with inflamed or 35.8 (17–76) 105 10.5 5.7 1.0
[95] normal cervixes attending
colposcopy clinic
17–20 0.0
21–30 6.0a
31–40 12.0a
41–50 22.0a
51–60 0.0
61–70 0.0
71–80 0.0
China, Hong Kong, 2000 MY09/11 Cervix—swab STI clinic attendees 34.6 (15–71) 553 30.6 14.8 10.8 5.1 0.9
[428]
15–25 94 37.2 14.9 11.7
26–35 240 28.3 14.2 10.8
36–45 138 27.5 17.4 8.0
46–71 81 34.6 12.3 14.8
China, Hong Kong, 2000 MY09/11 Cervix—scrape Cytologically normal 40.4 (16–88) 201 5.0d 5.0 7.0
[429] women attending
colposcopy clinic
India, New Delhic [105] Type-specific PCR (16) Cervix—swab STI clinic attendees 27.2 (15–44) 50 30 30
India, New Delhic [430] Type-specific PCR (16, 18) Ectocervix—spatula Cytologically normal 35.8 (20–60) 160 10.0 9.4
women with
inflammation attending
gynecology outpatient
clinic
20–39 108 11.1
(Continued )
Table 2
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
40–59 52 7.7
Indonesia, Bali, Denpasar, Type-specific PCR (6, 11, Cervix—swab Sex workers 25.3 541 38.6 6.7
1997–8 [296] 16, 18, 31, 33, 35, 45, 52)
<18 26 69.2
18–24 216 44.9
25–30 199 34.7
>31 97 21.6
Japan, Osaka, 1993 [431] Type-specific PCR (16, 18) Ectocervix—swab Women presenting for 30.2 (20–48) 53 43.3

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


evaluation of infertility
Mongolia, Ulaanbaatarc MY09/11, type-specific Vagina—tampon (self- STI clinic sample—routine 26.7 110 35.5 15.5 6.4 8.2
[432] PCR, and GH20/PC04 sampled) screening or gynecologic
symptoms
Singapore, No city reported, PVCOU/PVCOD (11, 16, Ectocervix—spatula Sex workers 35 (19–71) 187 14.4 2.1 1.1
1995–6 [433] 18) Endocervix—brush
Taiwan, Taipeic [144] Type-specific PCR (6, 11, Cervix—smear STI clinic attendees 26.9 37 37.8 24.3 8.1
16, 18, 33)
Thailand, Bangkok, 1991–3 Type-specific PCR (6, 11, Cervix—swab Sex workers; brothel 19 (15–24) 82 25.6 8.5
[304] 16, 18, 31, 33, 35, 39, 45)
15–19 48 31.3 12.5
20–24 34 17.6 2.9
Sex workers; massage parlor 30 169 8.3 2.4
20–24 40 10.0 2.5
25–29 39 7.7 7.7
30–34 41 7.3 2.4
35 49 8.2 6.1
Thailand, Chiang Mai, HCI Cervicovaginal—lavage Women whose male partners 26 481 9.1 5.2 4.0
1992–6 [434] were HIVþ
Europe and the Middle
East
Multiple countries (12), GP1/GP2 and type-specific Cervix—brush HIVþ women 31 (17–68) 397 53.7
1993–8 [435] PCR (16, 18, 33, 6, 11, 42,
31, 35, 39)
Denmark, Copenhagen and PCR with L1 primers and Cervix—spatula Women attending HIV 27.5 (19–53) 151 54.0
Aarhus, 1991–3 [436] type-specific PCR (6, 11, screening clinics
16, 18, 31, 33, 35, 45, 39,
51, 52, 2)
HCI 25.3
Denmark, Copenhagen, GP5þ/6þ Cervicovaginal—lavage Sex workers 30.9a 182 32.4 30.5
1992–3 [303]
18–24 27 63.0
25–29 47 42.6
30–34 48 18.8

S25.e38
35–39 33 24.2
(Continued )
Table 2

S25.e39
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
40–44 13 23.1
45 14 14.3
Denmark, Copenhagen, GP5þ/6þ Cervix—swab STI clinic attendees 27.2 124 35.8
1993 [38]
<20 56.0a
20–24 44.0a
25–29 41.0a
30–34 7.0a

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


35 32.0a

Finland, Helsinki, 2000–1 HCII Ectocervix/vagina— Women with gynecologic 38.3 (15–86) 1999 23.0
[437] spatulaEndocervix— disorders attending
brush outpatient clinics
France, Paris, 1992 [299] MY09/11 Cervix, vagina, and vulva— HIVþ women 29 (21–40) 30 63.3 13.3 16.7
biopsy
France, Paris; French PCR with L1 and E6 primers Cervix—brush STI clinic attendees 31 320 21.3 5.0
Guyana, 1993–5 [438] and GP1/GP2
MY09/11 and GP5þ/6þ Ectocervix— spatula, brush HIVþ women 32 (19–72) 307 49.5
Endocervix—swab
France, Reims, 1997–8 [439] HCII Cervix—scrape, brush, Women undergoing routine 37 (15–72) 1518 22.3 16.7 5.6
spatula screening, family
planning clinic attendees,
and women at high risk
for STIs
15–20 85 25.9 20.0 5.9
21–30 411 31.1 25.1 6.1
31–40 484 19.6 14.7 4.9
41–50 369 17.6 11.4 6.2
51–60 128 17.2 10.9 6.2
61–72 41 14.6 14.6 0.0

Germany, No city reported, MY09/11 Cervix—swab Women with previous 33.8 550 56.2
1991–2 [196] cervical lesions or
partners of men with HPV
HIVþ women 32.9 61 62.3
Greenland, Nuuk, 1993 [38] GP5þ/6þ Cervix—swab STI clinic attendees 27.4 153 23.5
<20 85.0a
20–24 25.0a
25–29 12.0a
30–34 19.0a
35 19.0a
(Continued )
Table 2
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
Israel, No city reported, 1997 MY09/11 Vagina—biopsy Women undergoing 17–55 86 53.5
[440] perineoplasty for vulvar
vestibulitis
Italy, Multicenter, 1994–5 MY09/11 Endocervix—brush Women at risk for HIV 26.9 236 36.4
[441–443] infection
17–29 116 40.5
30–45 118 32.2

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


Italy, Multicenter, 1997–9 MY09/11 Cervix—smear, spatula HIVþ women; DIANAIDS 33.5 (21–48) 89 38.2 7.9 0.0
[225] Endocervix—brush project
Italy, Ancona, 1994 [214] PCR with L1 primers Ecto/endocervix—smear HIVþ women 29.2 (22–38) 21 66.7 47.6
Italy, Milan, 1995–7 [300] MY09/11 Cervix—brush HIVþ women 33.6 (20–68) 163 16.0 1.2
HCII 65.0
Italy, Milan, 1995–7 [217] MY09/11 Cervix—swab HIVþ women 33.6 (21–62) 168 91.0
Italy, Padua, 1997–9 [218] MY09/11 Cervix—brush HIVþ women 35 (24–76) 104 53.8
Italy, Palermo, 1997–9 [301] MY09/11 and GP5þ/6þ Cervix—spatula HIVþ women 32a (15–44) 110 60.9 25.5 11.8
Italy, Pavia, 1998–9 [302] MY09/11 Cervicovaginal—swab, HIVþ women, cytologically 31.9 124 63.7 2.4 7.3
lavage normal
Italy, Rome, 1998 [444] MY09/11 Cervix—spatula, brush Colposcopy clinic attendees 31 (19–54) 48 54.8
with past/present
inflammation, but
negative colposcopy
findings
The Netherlands, GP5þ/6þ and type-specific Cervix—scrape, brush Gynecologic outpatient 18–80 239 9.2
Amstelveen, 1991 [396] PCR population with various
gynecologic complaints
The Netherlands, GP1/2 and GP5þ/6þ Cervix—scrape, spatula Cytologically normal 16–60 83 25.3 8.4 2.4
Amsterdam, 1989 [445] women attending the
gynecology department
for various gynecologic
complaints
The Netherlands, Type-specific PCR (6/11, 16, Cervix—spatula or swab STI clinic attendees 30 162 15.4
Amsterdam, 1988–90 18, 33)
[446]
The Netherlands, Type-specific PCR (6, 11, Cervix, anus, and rectum— STI clinic attendees 28 (18) 111 13.5 6.3 4.5
Amsterdam, 1989–90 16, 18, 33) swab
[447]
The Netherlands, Class 1989 and type-specific Cervix—spatula or brush Drug-using sex worker 30.2 121 17.4 5.8 1.7
Amsterdam, 1991–2 PCR (6/11, 16, 18, 33)
[448]
(Continued )

S25.e40
Table 2

S25.e41
Continued
Prevalence (%)d
Study location, dates, Assay (PCR consensus Site of specimen Group tested Mean or median age, Sample Overall High risk Low HPV HPV
reference primer or HCI/II) years (range) size HPV risk 16 18
Norway, Porsgrunnc [449] Type-specific PCR (6, 11, Cervix—biopsy Women undergoing 30 (15–54) 100 5.0 0.0 4.0
16, 18, 33) dilatation and curettage
for either termination of
pregnancy or benign
conditions
Russia; Latvia; Belarus, HCII Cervix—smear STI clinic attendees 27.5 706 44.9
2000 [450]
Spain, Oviedo, 2003 [298] MY09/11 Cervix—smear Sex workers attending 187 27.7 10.2 3.7

J.S. Smith et al. / Journal of Adolescent Health 43 (2008) S5–S25


dermatology or STI
clinics
<20 75.0a
21–25 45.0a
26–30 30.0a
31–35 25.0a
36–40 18.0a
>41 0.0a
Sweden, Gothenburg, 1992 MY09/11 (6, 11, 16, 18, 33) Cervix—brush STI clinic attendees 25 (20–58) 91 33.0
[451]
Sweden, Malmo, 1991 [452] Type-specific PCR (6, 11, Cervix—brush Cytologically normal 18.3 (15–21) 25 16.0 8.0 16.0
16, 18, 33) women attending an STI
clinic
Sweden, Stockholm, 1997 MY09/11 and type-specific Cervix—brush Cytologically normal 24.9a (15–74) 171 69.0 13.0 6.0
[453] PCR (6, 16, 18, 31, 33) women with a previous
history of condyloma or
dysplasia
Sweden, Uppsala, 1991–2 MY09/11 and GP5þ/6 þ Cervix, vulva, introitus, STI clinic attendees 24 (17–47) 66 24.2
[454] perineum, and perianal
area
Sweden, Uppsala, 1997–9 GP5þ/6þ (16, 18, 31, 33) Cervix—smear In vitro fertilization sample 32 (20–40) 214 7 2.3 2.8
[400]
Turkey, Ankara, 1997 [141] MY09/11 Cervix—biopsy Sex workers 29 88 2.3 1.1
UK, England, Sheffield, Type-specific PCR (16) Anus Renal allograft patients 47b (23–68) 53 3.8
1992–3 [173]
UK, England, Cambridge, GP5þ/6þ Cervix—scrape Women attending 26 (16–57) 136 77.9 8.6 3.9
1999 [455] genitourinary department
HC ¼ hybrid capture; HPV ¼ human papillomavirus; PCR ¼ polymerase chain reaction; STI ¼ sexually transmitted infection; ALIVE ¼ AIDS Link to Intravenous Experiences; DIANAIDS ¼ Diagnosi Iniziale
Anomalie Neoplastiche AIDS Collaborative Study Group; REACH ¼ Reaching for Excellence in Adolescent Care and Health; WIHS ¼ Women’s Interagency HIV Study.
a
Estimate.
b
Median.
c
Date of sample collection was not specified.
d
Merged columns indicate a combined prevalence rate for 16 and 18.

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