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Penises not required: A systematic review of

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DOI: 10.1071/SH15089

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CSIRO PUBLISHING
Sexual Health
Review
http://dx.doi.org/10.1071/SH15089

Penises not required: a systematic review of the potential

for human papillomavirus horizontal transmission that
is non-sexual or does not include penile penetration

Zhiyue Liu A, Tasnuva Rashid A and Alan G. Nyitray A,B,C

A
Department of Epidemiology, Human Genetics and Environmental Sciences, School of Public Health,
The University of Texas Health Science Center at Houston, 1200 Pressler Street, Houston, TX 77030, USA.
B
Center for Infectious Diseases, The University of Texas Health Science Center at Houston, 1200 Pressler Street,
Houston, TX 77030, USA.
C
Corresponding author. Email: alan.g.nyitray@uth.tmc.edu

Abstract. The primary mode of human papillomavirus (HPV) transmission is through penetrative sex; however, there is
evidence of other modes of transmission. No systematic review was found that focussed on HPV horizontal transmission
that is not penocentric. A systematic review of the literature by searching Medline (Ovid), PubMed (NLM) and Embase
(Ovid) was conducted to retrieve articles published from 1946 to March 2014. Studies that suggested evidence of non-
sexual or non-penetrative sexual transmission of a-HPV genotypes were included. After review of 2061 titles and abstracts,
51 studies were abstracted. Fifteen studies examined HPV fomites from medical settings or public environments, and 36
examined HPV in humans. Human papillomavirus DNA was detected in the genital tract of female virgins, with prevalence
estimates ranging from 0% to 51.1%. HPV transmission from hands to genitals or genitals to hands was reported for both
sexes and heterosexual couples. Other studies commonly found HPV on surfaces in medical settings and public
environments. Further studies on non-sexual and non-penetrative sexual transmission are needed to understand the
complexity of HPV transmission. Health-care policies may need to be reassessed/established to ensure the safety of medical
instruments and to reduce the risk of HPV nosocomial infection.

Additional keywords: environment, fomites, hand, nosocomial, penetrative sex, transmission, virgins.

Received 1 May 2015, accepted 26 July 2015, published online 5 October 2015

Introduction It is assumed that the primary mode of transmission of HPV is

Human papillomavirus (HPV) infection is the most common
sexually transmissible disease worldwide. Over 150 types of
HPV have been identified. High-risk (HR) HPV (e.g. HPV 16,
18, 31, 33, 35, 39, 45, 51, 52) is responsible for 99% of all
cervical cancers and a substantial proportion of vulvar, vaginal,
anal, penile and oropharyngeal cancers.1 Low-risk (LR) HPV
(e.g. HPV 6, 11, 42, 43, 44) is unlikely to cause cancer, but
is associated with genital warts, low-grade squamous
intraepithelial lesions and recurrent respiratory papillomatosis.2
The skin and mucosa of healthy populations harbor a wide
spectrum of HPV genotypes. However, HPV cannot penetrate the
physical barrier of upper skin layers. HPV requires the presence of
epithelial microtraumas that enables HPV to reach basal cells—
the target cells for HPV infection. The infected basal cells divide
and produce daughter cells that are pushed to the epithelial
surface.3 Subsequently, viral particles are released from these
daughter cells, and as the upper layers of skin are sloughed off, the
infected cells are passed on to other skin or mucosal surfaces or
released into the environment.1,3
through penetrative sex; however, a growing number of studies
suggest additional transmission routes that may be relevant for
transmission modelling and HPV vaccine policy. While there
have been several reviews on vertical and oral transmission of
HPV,4,5 no systematic review has focussed on alternative routes
of HPV transmission, like hand carriage, autoinoculation or
transmission during medical procedures. The objective of this
article was to systematically review studies with evidence of
HPV transmission in ways other than vertical transmission and
penile penetrative sex (i.e. penile-vaginal intercourse, penile-
anal intercourse and penile-oral intercourse).
Methods
Eligibility criteria for included studies required that the
authors examined means of HPV transmission other than
penetrative vaginal, anal or oral sex. Potential transmission
means such as medical equipment, sex toys, non-penetrative
sex acts were included. Articles were excluded if they: (1)
lacked HPV content; (2) addressed potential HPV transmission

Journal compilation  CSIRO 2015 www.publish.csiro.au/journals/sh

B Sexual Health
only through penetrative vaginal, anal or oral sex; (3) addressed
potential HPV transmission only through vertical transmission;
(4) were comments, reviews or overviews; (5) focussed on bench
work with no epidemiological content; or (6) were therapy
assessments. Only articles published in English and Chinese
between the dates of 1946 and March 2014 were included in
the final review. Research articles, letters and conference
proceedings were included, as were case reports, case series,
cross-sectional, case-control, cohort and clinical trial study
designs. Medline (Ovid), PubMed (NLM) and Embase (Ovid)
were searched for concepts relating to human papillomavirus
and condylomata, sexual abstinence, non-penetrative sexual
transmission, virginity and non-sexual or non-penetrative
means of transmission. See Supplementary Material for the
complete search strategies for each database. Additionally,
references in relevant articles were examined for studies not
found through the database searches; relevant articles were
also searched in Scopus (Elsevier) to determine if they were
cited by studies that previous searches had not found; and an alert
service was used for notification of new relevant articles. All
abstracts and full-text articles were reviewed independently by
two authors (Z.L. and T.R.); any inconsistencies were discussed
to reach consensus.
RefWorks (ProQuest) was used to manage all citations.
A custom Excel workbook (Microsoft Corporation, Redmond,
WA, USA) designed for systematic reviews was used to track
search strategies and results.6 Two authors screened all titles and
abstracts using the Excel workbook in which they were blinded
to the study authors and journal.
Authors of the included conference proceedings were
contacted to obtain full-text articles. For all eligible full-text
articles, the following information was abstracted from each
article: author, publication year, country, study design, sample
size, sex of the study population, age range (mean or median),
brief description of study population, anatomic sites sampled/
sampling method/HPV detection method, presence of fomites
(i.e. inanimate objects that may be contaminated), HPV
genotypes involved and results of the study (Tables 1 and 2).
Results
Search results
Of the 2061 unique citations identified, 93 full-text articles were
assessed for eligibility. Fifty-one publications met the inclusion
criteria and were included in this review (Fig. 1).
All 51 articles reviewed were observational studies published
in English, including two case series, three case reports, two
case–control studies, 13 cohort and 31 cross-sectional studies.
Thirty-one studies identified HPV DNA using polymerase chain
reaction (PCR), 10 using hybrid capture II (HCII) or in situ
hybridisation (ISH), while six additional studies detected the
presence of HPV using other techniques, including cell
morphology observations, detection of condyloma and anti-
HPV antibody detection. Fifteen studies examined HPV via
fomites from medical settings or public environments, and 36
examined HPV in humans. Of these 36 studies, six involved
only males, 22 involved only females and eight included both
sexes. Most of the included studies originated in Europe or North
America.
Z. Liu et al.
HPV in female virgins
Several studies have found HPV DNA in the genital tract of
virgins, with prevalence estimates ranging from 0% to
51.1%;7–24 however, some of these studies did not define
female virginity15,20,25 and others differed in their definitions
of female virginity.7–11,13,14,16–19,21–24 Two articles defined a
virgin as a woman who denied any sexual exposure or sexual
intercourse and had an intact hymen confirmed by physical
examination.14,21 Some defined virgins as not experiencing
sexual intercourse,11,16,19 no intimate sexual contact7 or no
history of sexual activity or sexual abuse.9 Others were more
specific by defining virgins as women who had never had
‘penetrative vaginal intercourse’,8,17,18,23,24 (or the more
general ‘penetrative sexual intercourse’),10,13 or vaginal or
anal sex.22 Some articles were explicit that women may have
been sexually active in other ways.8,17
Winer et al.24 reported that of 148 virgins examined at 757
visits, 1.7% (13/757) of cervical and vulvovaginal specimens
were HPV DNA positive, and that finger-vulvar, penile-vulvar
and oral-penile sexual behaviour increased the risk of genital
infection in virgins. Non-penetrative sexual contact among
virgins was also mentioned in a cohort study by Shew
et al.17 The authors reported that 45.5% (10/22) of vaginal
swabs taken from adolescents before their first vaginal
intercourse were HPV DNA positive. Seven of the 10 virgins
in this study reported non-coital sexual behaviours. Similarly,
Rylander et al.16 observed 1.5% (2/130) of specimens were
HPV 6 positive among 130 vaginal and cervical specimens from
virgins. The authors suggested possible routes of transmission of
HPV through tampon use or fingers because one of the virgins
used tampons during her menstruation and the other had
performed digital vaginal sex.
Tay et al.21 observed 51.1% (23/45) of virgins had subclinical
infection, microwarts and condylomata acuminata of the vulva,
perineum or perianal regions after colposcopic inspection. Among
these, two sisters shared clothing and towels with their mother
who had cervical squamous cell carcinoma. Intra-family
transmission of HPV by fomites is one plausible explanation
offered by the authors. Pao et al.14 reported that 14.8% (9/61) of
virgins’ vulvar swabs were HPV DNA positive. Several other
studies8,9,13,22 reported HPV DNA positivity in cervicovaginal
swabs from virgins ranging from 4.2% to 18%.
There is evidence that HPV antibodies and DNA can be
detected in blood and urine samples, respectively, from virgins.
Shin et al.20 reported that 4.9% (5/103) of virgins had anti-virus-
like particle (VLP) antibodies in their blood samples. A Chinese
population-based study observed that among 649 self-reported
virgins, 2.5% of blood samples tested HPV seropositive.11 An
Indian study reported that 9.2% (22/238) of first void midstream
urine samples were HPV DNA positive among putative virgin
college students.25
HPV DNA can also be found among virgins with vestibular
papillomatosis – a subclinical vulvar lesion, characterised by the
presence of multiple papillae that may cover the mucosal surface
of the labia minora.7 One study observed genital warts in 132
virgins with an intact hymen; 88 denied any type of sexual
intercourse and 44 acknowledged sexual intercourse, but no
penile-vaginal or penile-anal penetration.26
 Table 1. Selected data from studies with evidence of non-sexual transmission of human papillomavirus (HPV)
HCII, hybrid capture II; ISH, in situ hybridisation; NA, not applicable; NS, non-specified; PCR, polymerase chain reaction; SCC, squamous cell carcinomas

Author Study design Population description Sample site Collection Assay Sample HPV
Year method size n genotypes
Country detected
Rock et al.37 1986 US Case series Children aged 2–8 years Genital tract papillomas Biopsy Southern transfer 5 6, 16
with genital tract hybridisation
papillomas undergoing
treatment
Fleming et al.38 1987 Case report A 5-year old boy with Genital and skin warts Biopsy Biotinylated probes 1 2
UK genital warts and hand for HPV nucleotide
warts sequences
Tay et al.21 1990 Cross-sectional Female patients referred Vulva, perineum and Biopsy Colposcopic diagnosis 45 NA
Singapore by gynaecologist perianal regions
Hallmo and Naess48 Case report A male laser surgeon, aged Larynx Biopsy ISH 1 6, 11
1991 Norway 44 years
Systematic review of non-sexual HPV transmission

Fairley et al.10 1992 Cross-sectional Female virgin patients and Vagina Tampon PCR 55 NA
Australia high school students,
aged 13–41 years
Handley et al.36 1993 Cohort Prepubertal children with Cervix Smears and ISH 42 NA
UK anogenital warts, aged colposcopic
1–12 years biopsy
Pao et al.14 1993 Case-control Female virgins, mean age Vulva Swab PCR 61 6, 11, 16, 18
China 25 years, presenting for
a compulsory pre-
marital examination
Peters and Case-control Female patients visiting Vagina and cervix Smear Microscopic 75 NA
Trimbos15 1994 clinic, aged 15–19 years evaluation
The Netherlands
Rylander et al.16 1994 Cross-sectional Female virgins attending Vagina and cervix Swab PCR 130 6
Sweden adolescent health-care
centers, aged
10–25 years
Sonnex et al.31 1999 Cross-sectional Patients with genital warts Genital lesions, finger tips Cytobrush PCR 22 6, 66, 11, 31,
UK and tips of fingernails and NS
Forslund et al.32 2000 Cohort Women with a history of Cervical/vulvar lesions, Archival samples PCR 57 16
Sweden genital and upper fingers/hands/arms
extremity SCC
Marrazzo et al.12 2001 Cross-sectional Women who have sex Cervix/vagina Swab PCR and dot blot 248 51/52/55/58
US with women, hybridisation and NS
predominantly
Caucasian
Winer et al.24 2003 Cohort Female students, aged Cervical, vulvo-vaginal Swab PCR 148 16 and NS
US 18–20 years and oral regions
Shin et al.20 2003 Cross-sectional Population-based female Blood samples HPV virus-like particle 103 18
Sexual Health

South Korea subjects, aged >15 years enzyme-linked

immunosorbent assay
C

(continued next page)

 D
Table 1. (continued )
Author Study design Population description Sample site Collection Assay Sample HPV
Year method size n genotypes
Country detected
Myhre et al.40 2003 Cross-sectional Children aged 5–6 years Girls: lower half of the Swab PCR 211 6, 16
Sexual Health

Norway and without sexual vagina/vestibular area

abuse (93% Caucasian) and anus. Boys: anus
Beznos et al.7 2006 Cross-sectional Female adolescents with Vestibular papillomatosis Biopsy PCR 20 NA
Brazil vestibular
papillomatosis, aged
12–18 years
Frega et al.26 2003 Cross-sectional Virgins with genital warts, NS NA NA 132 NA
Italy aged 18–42 years
Partridge et al.27 2007 Cohort Male university students, Glans, penile shaft, Swab Cytobrush PCR 240 16 and NS
US aged 18–20 years at scrotum, and fingernails
enrolment (84.6%
white)
Jin et al.35 2007 Cohort HIV-negative homosexual NS NA NA 1427 NA
Australia men, aged 18–75 years
Shimada et al.19 2007 Cross-sectional Female psychosomatic Cervix Cytopick HCII 251 None
Japan patients, aged
14–66 years
Hernandez et al.30 Cohort Heterosexual and Genital/cervical, anal and Swab PCR 25 couples NA
2008 US monogamous couples, hand swab; oral
aged 18–59 years cytobrush; urine
(52% Caucasian) specimens
Oh et al.13 2008 Korea Cohort Female students, aged Vagina/cervix Swab PCR 197 NA
16–25 years
Doerfler et al.9 2009 Cohort Female outpatients, aged Vagina/cervix Swab HCII 110 NA
Austria 4–15 years
Widdice et al.28 2010 Cohort Women (mean age Female: PCR 25 couples 84, 51, 39, 52
US 22.6 years) who had an Intra-anal canal, vulva Swab
incident HPV infection and vagina
and their partner (mean Cervix Saline wash
age 25.5 years) Male:
Glans, shaft, inner Swab
foreskin, scrotum,
perianal area
Both:
Palmar surface of Swab
the dominant hand
Buccal mucosa and Cytobrush
tongue
Winer et al.23 2010 US Cohort Female university Fingertip and fingernail tip Cytobrush PCR 14 84, 16
students, aged
18–22 years
Bumbuliene et al.8 Cross-sectional Female outpatients, aged Cervix/vagina Swab HCII 95 51, 53
2011 Lithuania 14–22 years
Z. Liu et al.
Hunt et al.33 2011 US Case report Female patient, aged Digital lesions NS NA 1 16
60 years
Hernandez et al.34 Cohort Male university Glans/coronal sulcus, Swab PCR 331 NA
2011 US community and general shaft, inner foreskin and
public, aged scrotum
18–79 years
Ji et al.11 2012 China Cross-sectional Population-based female Blood and cervical cells NA HCII 649 6, 16, 11, 18
subjects, aged
17–54 years
Thilagavathi et al.25 Cross-sectional Female university First voided mid-stream NA PCR 238 11, 16, & NS
2012 India students, aged urine samples
17–25 years
Widdice et al.22 2012 Cross-sectional Female adolescents from Cervix/vagina Swab PCR 69 6, 11, 16, 51,
US primary care clinic, 52, 56, 58,
aged 13–21 years 59, 61, 66, 68,
70, 81, 84
Widdice et al.29 2013 Cohort Women (mean age Female: PCR 25 couples NA
Systematic review of non-sexual HPV transmission

US 22.6 years) who had an Intra-anal canal, vulva Swab

incident HPV infection and vagina
and their partner (mean Cervix Saline wash
age 25.5 years) Male:
Glans, shaft, inner Swab
foreskin, scrotum,
perianal area
Both:
Palmar surface of the Swab
dominant hand
Buccal mucosa and Cytobrush
tongue
Shew et al.17 2013 Cohort Female patients from Vagina Swab PCR 22 66, 39, 51, 16,
US university-affiliated 42, 62, 6
clinics, aged
14–17 years
Klinglmair et al.39 Cross-sectional Male children Prepuces (without HPV- NA ISH 250 High-risk and
2013 Austria (0–10 years), related lesions) after low-risk types
adolescents circumcision
(11–20 years), adults
(>20 years), median age
15 years
18
Tay and Oon 2014 Cross-sectional Female virgins, aged Vagina Lavage PCR 46 None
Singapore 13–57 years
Sexual Health
E
 F

Table 2. Selected data from studies with evidence of human papillomavirus (HPV) on fomites
ISH, in situ hybridisation; PCR, polymerase chain reaction; NA, not applicable; NS, non-specified; RRP, recurrent respiratory papillomatosis

Author Study settings/patients Sample tested Assay Sample collection time Sample size HPV
Year (no. of specimens) genotypes
Sexual Health

Country
McCance et al.41 1986 Women with premalignant
UK disease of the cervix
(cervical intraepithelial
neoplasia grades I to III)
Garden et al.49 1988 Patients with plantar or
US mosaic warts
Ferenczy et al.45 1989 Patients with anogenital
US warts
Andre et al.51 1990 Patients with large genital
France warts
Kashima et al.47 1991 7 patients with adult-onset
US RRP, 12 with juvenile-
onset RRP, 2 laryngitis
Bergbrant et al.50 1994 Medical personnel
Sweden operating on patients
with genital warts
Hughes and Hughes53 Patients with clinically
1998 US typical verrucae
vulgares of the
extremities
Strauss et al.54 2002 Genitourinary medicine
UK clinics
Strauss et al.55 2003 Genitourinary medicine
UK clinics
Kac et al.42 2010 Radiology wards
France
detected
Specula ISH After colposcopic 29 16
examination
Biopsy specimens and Hybridisation During treatment 7 2
laser vapour specimens
Surgical nylon gloves, Dot blot hybridisation Before and after use and 16 gloves, 62 forceps, 6/11, 16/18
biopsy forceps, after sterilisation 22 cryoprobe tips
cryoprobe tips swab
Biopsy specimens and Blot hybridisation Biopsy specimens before 3 biopsy specimens and 6
vapour plume treatment; Vapour 3 vapour plume
specimens plumes during specimens
treatment
Vapour specimens PCR At the time of operation 30 6, 11
Nostrils and conjunctiva PCR Before and after CO2-laser CO2-laser treatment: NS
swabs, nasolabial and electrocoagulation 11 from nasolabial
cytobrush treatment sessions fold, 11 nostril,
6 conjunctiva;
Electrocoagulation
treatment: 19 from
nasolabial fold,
19 nostril, 13
conjunctiva
Erbium: yttrium PCR During the ablation 5 None
aluminium garnet laser process
plume swab
Treatment rooms, toilets PCR During working day NA 6, 11, 16
swab
Treatment rooms, toilets PCR During working day 20 6, 11, 16
swab
Transrectal or transvaginal PCR 1. probe cover was tested 336 NA
ultrasound probe swab before its removal 2.
ultrasound probe was
tested after cover
removal 3. probe was
tested after disinfection
Z. Liu et al.
Systematic review of non-sexual HPV transmission Sexual Health G

54, 84, 70, 6

53, 16, 58, 31,
Some studies fail to find evidence to support non-sexual

6, 61, 84, 11
transmission. Fairley et al.10 observed that none of the 55
tampon specimens from virgins were HPV positive. Peters and
Trimbos15 found that 0 of 75 virgins had HPV infection, while

NA
NA

NA
13% of sexually active women had HPV infection based
on cytological diagnosis (i.e. the presence of koilocytosis,
laser plume masks = 20) parakeratosis and multinucleinisation). Another study reported

handle = 9);Vibrator 2
(shaft = 9, handle = 9)
After disinfection: 198.

surgical gloves = 20,

120 (oral mucosa = 70,

Part 1: 120. Part 2: 78

that cervical samples from all 251 psychosomatic patients without

Vibrator 1 (shaft = 9,
previous sexual experience were HPV DNA negative.19 Lastly,
Before use: 216

Tay and Oon.18 found that all 46 virgins were negative for HPV
infection in their vaginal lavage.

101
Evidence of hand-to-genital or genital-to-hand
transmission of HPV
Several studies have published evidence of hand-to-genital
the probe was used on a

cleaning and 24 h after

Part 1.When TVS probe
Oral mucosa before and
1. after endovaginal use

disinfection 2. before

and after disinfection

after each procedure;

procedure but before

Before use, after use

or genital-to-hand transmission of HPV either through

Immediately after use,
Surgical gloves and

not in use. Part 2.

immediately after
autoinoculation or from person-to-person. A cohort study
masks after each

among men reported that of 147 type-specific incident HPV

and standard

new patient

disinfection

infections detected in fingernails from 78 men, ~two-thirds were

cleaning

also detected at a genital site during the same visit or different

visits. Of eight subjects who had HPV 16 detected at both genital
NA

and fingernail sites, 87.5% (7/8) of them had the same HPV 16
variant detected at both sites.27 A cohort study among women
found that 20.1% (58/288) of type-specific HPV detected on the
genitals was also detected on the fingertips. Conversely, 60.4%
(58/96) of HPV types found on the fingertips were also detected
at the genitals.23
Studies of heterosexual couples include evidence suggesting
HPV can be transmitted between couples through hand carriage.
Widdice et al.28,29 found that the same HPV genotypes were
PCR

PCR

PCR

PCR

PCR

detected on one partner’s hand and the other partner’s anogenital

area among 44% (11/25) of couples. The authors suggested
that hands may provide a means for HPV to move between
Vaginal and probe swab
of health-care personnel
gloves and face masks

partners during sexual activity. Hernandez et al.30 observed the

during the treatment
Endocavity ultrasound

probe swab. Part 2.

Toilet seats cytobrush

Oral mucosa, surgical

following sources of HPV transmission among 25 monogamous,

sonography (TVS)
Part 1. Transvaginal

heterosexual couples: from female anus to male genitals, female

Vibrator samples
probes swab

hands to male genitals and self-inoculations in both sexes.

Among women who only reported sex with other women,
6.1% (3/49) of cervical/vaginal samples were HPV DNA positive.
Almost all of the 49 subjects reported oral-vaginal and digital-
vaginal sex in the past year. This raises the possibility that the
transmission route may be oral-vaginal or digital-vaginal.12
the surgical treatment of
laryngeal papillomas, 5
A ward in a gynaecology

Among patients with genital warts or squamous cell

12 women who have sex
with women and men
undergoing CO2 laser
5 patients scheduled for

treatment for urethral

Emergency department

carcinomas (SCC) of the cervix and fingers, the rate of

Toilet seats in airport

concordance of genital and digital HPV detection may be

higher. Sonnex et al.31 reported that of eight women and 14
department

restrooms

men with genital warts, type-specific HPV DNA was detected on

the fingers in one woman and five men. Forslund et al.32 found
warts

that among 13 patients with SCC of the cervix and fingers, HPV
16 was detected in cervical samples from seven patients. In these
seven patients, HPV 16 was also present in digital tumours from
five patients and a hand/arm sample was HPV 16 positive in one
Ilmarinen et al.46 2012

Anderson et al.57 2014

Smelov et al.56 2013

patient. Hunt et al.33 reported that a 60-year-old woman with a

Casalegno et al.43

Ma et al.44 2013
2012 Portugal

history of vulvar and cervical SCC had digital lesions with HPV
13 countries
Hong Kong

16. It has also been reported that warts on the fingers, arms and
Finland

trunk increased the risk of genital HPV.34 Additionally, insertive

fingering increased the risk of genital warts, whereas insertive
US

fingering and insertive fisting increased the risk of anal warts.35

H Sexual Health Z. Liu et al.

3070 records found through 12 additional records found

database searching through other sources

2061 records after duplicates removed

1963 titles/abstracts excluded:

– lacked HPV content/HPV

2061 titles and abstracts reviewed transmission content (n = 1087)

– was a comment/review/overview
(n = 365)

– was a therapy assessment (n = 267)

– focussed on bench work (n = 192)

98 full-text records to be reviewed
– was statistical modelling study
(n = 38)

– not non-penetrative sexual

transmission (n = 14)

Record unavailable for review (n = 1)

Duplicate records (n = 4)

93 full-text records reviewed 42 full-text articles excluded:

– lacked HPV content/HPV

transmission content (n = 35)

– was a comment/review/overview
(n = 2)
51 publications included
– was statistical modelling study (n = 1)

– not non-penetrative sexual

transmission (n = 4)

Fig. 1. Flowchart of the screening and eligibility evaluation process.

HPV in children infection during pregnancy or delivery was collected in the

Non-sexual transmission of HPV involving children has been
suggested by several studies. A cohort study among pre-
pubertal children with anogenital warts reported evidence of
autoinoculation of common hand warts to anogenital regions
in 7.1% (3/42) of children, and unspecified non-sexual
transmission in 59.5% (25/42) of children.36 A case series
study found that two children without evidence of sexual
abuse and whose mother had no history of condylomata at
the time of birth had genital tract papillomas and were HPV
6 or16 positive.37 Another case study found that a 5-year-old boy
with genital and skin warts was HPV 2 positive in both genital
and skin samples. The authors speculated that autoinoculation of
HPV from hand to genital was a possible route of transmission.38
In a cross-sectional study, 45.5% HR and 35.0% LR HPV
positivity was seen in prepuce specimens among children
aged 0–10 years.39 Myhre et al.40 reported that 1.2% (2/161)
of anal specimens and 3.0% (5/164) of genital specimens from
girls aged 5–6 years without reported sexual abuse were HPV
DNA positive. However, no information about maternal HPV
study; thus, vertical transmission of HPV is still a possible
explanation.
HPV in medical settings and environments
HPV DNA has been found in and on medical instruments before
and after chemical disinfection. It was detected on the specula
inserted into the vagina of women with premalignant cervical
disease (CIN grades I to III) after disinfection.41 HPV DNA
has also been found not only on the cover (condom/sheath) of
transrectal and transvaginal probes, but also on the surface of
probes after removing the cover but before disinfection.42
Casalegno et al.43 reported that 3.5% (7/198) of endocavity
ultrasound probes were HPV DNA positive after endovaginal
use and standard disinfection, and 2.8% (6/216) were positive
before the probe was used on a new patient. Ma et al.44 observed
that 7.5% (9/120) of samples of unused transvaginal sonography
probes were HPV DNA positive while 3.8% (3/78) of
transvaginal sonography probes after disinfection were still
HPV DNA positive.
Systematic review of non-sexual HPV transmission
HPV can also contaminate surgical gloves after surgical
procedures for genital warts. Ferenczy et al.45 found that
surgical nylon gloves used on patients with anogenital
condylomata acuminata were HPV DNA positive before and
after disinfection. Ilmarinen et al.46 reported that after the
surgical treatment of laryngeal papilloma, the surgeons’
gloves tested HPV positive in one of the five cases, and also
on the surgical nurses’ gloves in three of five cases before
disinfection. After the treatment of genital warts, all gloves of
the operators were HPV positive before disinfection.
HPV DNA has been detected in the plume produced during
CO2 laser vapourisation of respiratory tract papillomata and
laryngitis.47 According to one case study,48 a 44-year-old laser
surgeon tested HPV 6/11 positive in his laryngeal biopsy. After
ruling out sexual transmission of HPV, it was postulated that
the surgeon’s own patients may have been the source of
transmission. Garden et al.49 detected intact HPV 2 DNA in
the laser vapour from two of seven patients with plantar warts.
Bergbrant et al.50 detected HPV DNA in nasolabial folds and
a nostril specimen of a treating physician during both CO2
laser and electrocoagulation treatment. HPV 6 has also been
identified in plumes of laser-treated genital warts.51 Lobraico
et al. reported that direct contact with the HPV lesion, rather than
the laser plume, was responsible for acquiring a lesion.52 In
addition, HPV DNA was not found in laser plumes during
treatment of verruca vulgaris (i.e. warts on hands or fingers)
in five patients.53
Some studies observed HPV on toilet seats. Strauss et al.54
detected HPV DNA in more than 50% of the treatment rooms
and toilet samples in one genitourinary medicine clinic. The
authors suggested that the possible source for the contamination
of the clinic’s toilets were from genitals via hands to the toilet
seats. In the treatment rooms, a possible route was from a doctor’s
gloves. After cleaning with detergent, a 50% reduction in surface
contamination with HPV DNA was observed and the number of
types detected was reduced but not eliminated.55 HPV DNA was
also found on 22.8% of 101 toilet seat samples collected in airport
restrooms from 13 countries.56
HPV DNA has also been identified on sex toys.57 Among
women whose vaginal samples were HPV positive, HPV DNA
was detected in vibrator shaft samples before, immediately after,
and 24 h after cleaning with water and the supplied cleaning
product.
Discussion
This literature review provides the first summary of published
evidence for non-sexual and non-penile penetrative sexual
transmission of HPV among humans. While this body of
evidence is substantial, detection of HPV DNA sequences does
not guarantee transmission, and concern about HPV disease is
dependent not only on HPV in the environment, but also infection
of basal cells. The detection of HPV DNA may only reflect
contamination of HPV particles from the environment or
the partner. HPV has to reach basal cells through epithelial
microtraumas to establish infection.
The prevalence of HPV DNA detection ranged from 0%
to just over 50% in virgins; however, sexual behaviour was
self-reported and virgins were not clearly defined in most of
Sexual Health I
the included studies. The variation in prevalence could also be
explained by different definitions of virgins, study populations
(both clinical and non-clinical), anatomic sites sampled, sample
collection methods (e.g. swab, biopsy, cytobrush) and the assays
used to detect HPV DNA or HPV infection. Detection of HPV
DNA in a single sample may only reflect transient infection.17
Most of the studies did not follow up the virgins to elucidate
whether HPV detection in them represented true infection. Only
two studies followed up virgins with HPV-positive results.17,58
In the study by Winer et al.,58 six of nine HPV-positive genital
samples from virgins were repeatedly positive at 1 follow-up
visit. Similarly, in the study by Shew et al.,17 HPV DNA was
detected in 10 adolescents before their first vaginal intercourse,
and seven of these 10 virgins had the same HPV type detected a
second time, with a median interval of 91 days.
Importantly, information about non-penetrative sexual
contacts (e.g. kissing, masturbation, frottage, cunnilingus) was
rarely collected. Only a few studies10,16,17,22,24,26,30,35 collected
relatively limited information about non-penetrative sexual
behaviour; for example, Fairley et al.10 collected information
on hand-genital contact and genital-genital contact not involving
penetration. Other studies collected information such as non-
penetrative genital contact,22,24,26 hand-genital contact,16,17,35
cunnilingus30 and deep kissing.17,35 Therefore, HPV DNA
detected in vaginal or cervical samples from virgins does not
exclude the possibility of sexual transmission of HPV in those
self-reported virgins. To further investigate HPV transmission
among virgins, more detailed sexual behaviour histories, for
example, using sexual diaries, are needed.
Some studies failed to find evidence to support non-
penetrative sexual transmission in virgins. This could be due
to the lack of HPV in these persons, but it could also be due to a
small sample size,23 low sensitivity of some HPV infection
diagnostics15 and specimen adequacy (e.g. tampon specimens
may be less effective for detecting HPV).10,59
HPV was detected in children without a history of sexual
abuse and whose mother had no history of HPV infection at the
time of birth. This suggests non-sexual transmission of HPV,
likely through skin-to-skin contact.36–38
It has been shown that 31% of infectious units of in vitro-
generated pseudotype HPV 16 remain infectious after 7 days
of desiccation at room temperature.60 The infectivity of HPV 16
can also persist for at least 7 days in a wet environment.61 Even
after disinfection, HPV was detected on medical devices
like vaginal specula,41 endovaginal ultrasound probes,43
transvaginal sonography probes44 and surgical gloves.45,46
Add to that the detection of HPV in the plume produced
during CO2 laser vapourisation,47 and it raises the question of
the adequacy of disinfection procedures and workplace
protection. In these studies, adequate disinfection procedures
may not have been followed or possibly the prescribed
disinfection is inadequate for eliminating HPV. However,
detection of HPV DNA on medical devices and environments
does not necessarily indicate a higher risk of infection upon
exposure. The infectivity of HPV is difficult to determine as
no feasible in vitro or in vivo culture system for HPV exists.44
Given the potential for nosocomial transmission, health-care
providers should follow disinfection procedures strictly to
reduce the hazard of nosocomial transmission of HPV and
J Sexual Health
adopt high-level disinfectants that can destroy non-enveloped
viruses such as HPV.43
This literature search was limited to Medline, PubMed and
Embase databases. Other relevant studies could have been
overlooked if they were not published in these databases.
Most of the included articles were not designed to study non-
sexual transmission of HPV. These studies unintentionally
collected evidence of routes of HPV transmission other than
penetrative sexual transmission. Although penetrative sex is the
main route of HPV transmission, reviewing evidence for non-
sexual transmission of HPV is also worth exploring given the
limited number of studies designed to directly test the question
of non-sexual transmission and given the potential for disease
caused by HPV.
As HPV natural history studies have generally attempted to
explain factors associated with prevalence and incidence of
HPV only within the context of penocentric penetrative sexual
transmission, it is not clear how the lack of inclusion of other
factors (e.g. use of sex toys and masturbation) in multivariable
modelling might alter point estimates. In addition, if non-sexual
transmission of HPV is non-trivial, then the lack of inclusion
of non-sexual transmission routes may bias transmission dynamic
and vaccine modelling studies. HPV transmits remarkably
efficiently in new couples, which is evidence of high
infectivity;62 thus, there is room for concern that a full picture
of the virion’s substantial ability to transmit from human-to-
human may be incomplete without considering non-sexual
transmission. Finally, the distribution of HPV vaccines has
been hindered, in part, by societal discomfort with the role of
HPV in human sexuality. A fuller appreciation of the potential
for non-sexual HPV transmission could help increase vaccine
acceptance.
This article provides a comprehensive review of the
current evidence of non-sexual and/or non-penetrative sexual
transmission of HPV. HPV DNA has been found in female
virgins, women who only have sex with women, and children
with no evidence of sexual abuse. HPV has also been reported to
transmit from hands to genitals or genitals to hands among both
sexes and heterosexual couples. Studies also indicate that HPV
has the potential to be transmitted via contaminated medical
instruments and environments. Future studies may seek to
explore the infectivity of HPV on medical instruments,
common objects (e.g. toilet seats and sex toys) and whether
standard disinfection and cleaning procedures are adequate. In
addition, the non-sexual transmission of HPV may bias point
estimates of the association between penetrative sexual activities
and HPV infection. Future research should provide explicit and
objective definitions of virgins, and collect detailed information
on non-sexual contacts and non-penetrative sexual behaviours.
Finally, policies could be reassessed/established to help ensure
the safety of medical instruments and to reduce the risk of HPV
nosocomial infection.
Conflict of interests
None declared.
Acknowledgements
The authors declare that there is no source of funding. The authors wish to
thank Helena VonVille for her support and advice on search strategies for
Z. Liu et al.
this literature review. The authors would also like to thank Christine
M. Pierce Campbell and Vanessa Schick for their valuable comments.
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