Sexually Transmitted Diseases:
Influence of Partner's Infection Status on Prevalent Human Papillomavirus Among Persons With a New Sex Partner
Burchell, Ann N. PhD*†; Tellier, Pierre-Paul MD‡; Hanley, James PhD†; Coutlée, François MD*§∥; Franco, Eduardo L. DrPH*†
From the Departments of *Oncology, †Epidemiology, Biostatistics and Occupational Health, and ‡Family Medicine, McGill University, Montreal, Quebec, Canada; §Département de Microbiologie et Infectiologie, Centre Hospitalier de l'Université de Montréal, Québec, Canada; and ∥Département de Microbiologie et Immunologie, Université de Montréal, Montreal, Quebec, Canada
The authors thank to the following employees of the HITCH Cohort Study: research nurses Gail Kelsall and Suzanne Dumais for their efficient management of subject participation and specimen collection; Allita Rodrigues for study management; Vicky D'Anjou-Pomerleau, Jessica Sammut, Jennifer Selinger and Johanna Bleecker for study promotion; and Hélène Voyer for LA-HPV testing. We are also grateful to Melanie Drew (Student Health Services Clinic, Concordia University) and the staff of the Student Health Services Clinics at McGill and Concordia Universities for their helpful collaboration with HITCH research nurses.
Supported by the Canadian Institutes for Health Research for The HITCH Cohort Study (operating grant 68893 and team grant 83320). Supplementary and unconditional funding support was provided by Merck-Frosst Canada Ltd. and Merck & Co. Ltd. ANB was supported by a research studentship from the National Cancer Institute of Canada and the Canadian Cancer Society (NCIC/CCS) and by a Richard H. Tomlinson doctoral fellowship to McGill University.
Correspondence: Eduardo L. Franco, DrPH, Division of Cancer Epidemiology, Department of Oncology, McGill University, 546 Pine Avenue West, Montreal, QC, Canada H2W1S6. E-mail: firstname.lastname@example.org.
Received for publication April 9, 2009, and accepted June 14, 2009.
Background: We evaluated the influence of the partner's human papillomavirus (HPV) status and sexual practices on prevalent HPV infection among new couples to study HPV transmission.
Methods: Women attending university or college in Montreal, Canada, and their male partners (N = 263 couples) were enrolled in 2005–2008. HPV typing was done in self-collected vaginal swabs and clinician-collected penis and scrotum swabs. The outcome measures were overall and type-specific HPV prevalence.
Results: HPV was detected in 56% of women and men. Prevalence was higher among persons with infected partners (85%) than in those whose partners were negative (19%). Type-specific detection was substantially higher among women (OR = 55.2, 95% CI: 38.0–80.1) and men (OR = 58.7, 95% CI: 39.8–86.3) if their partner harbored the type under consideration. Prevalence among women and men with 10 or more lifetime partners was 15.4 (95% CI: 5.9–40.2) and 9.5 (95% CI: 4.4–19.8) times higher than among those with 1 partner. Frequent condom use was protective in men, particularly if his partner was HPV-infected (OR = 0.64, 95% CI: 0.50–0.82). This effect was attenuated among women with an infected partner (OR = 0.88, 95% CI: 0.69–1.11).
Conclusions: The current partner's status was the most important risk factor for prevalent HPV infection. Condoms exerted a stronger protective effect among men than among women.
Human papillomavirus (HPV) is the most common sexually transmitted infection (STI). Population-based estimates of prevalence are 27% among US females aged 14 to 59 years, and 45% among women aged 20 to 24.1 HPV is also common in men.2–4 Persistent infections with high-risk HPV types (HR-HPV) are the central causal factor for cervical cancer and are further responsible for a substantial proportion of many other anogenital neoplasms and head and neck cancers.5,6 Infections with HPV types of low oncogenic risk (LR-HPV), such as HPV-6 and HPV-11, are associated with benign anogenital lesions, including condylomata acuminata (genital warts).6
Most HPV studies to date have focused on individuals, although transmission involves contact between 2 people. In individual-based studies, the number of sexual partners is consistently the strongest risk factor for infection in women and men.1,7–12 Women's estimates of their current male partner's number of partners are also predictive of infection.12–14 Naturally, such assessments are imprecise and can only be proxy measures of the underlying true risk factor—the partner's HPV status.
Couple-based studies have documented the importance of male sexual behavior on women's risk of HPV-related disease.15–17 Couples in these studies were older with relationships of long duration. Because HPV is thought to be highly transmissible,18,19 the transmission event likely occurred years ago, and many infections would have resolved. Ideally, one would recruit newly-forming couples to study HPV infection closer in the time to the transmission event.18,20
When 2 individuals initiate a sexual relationship, 1 or both may be HPV-infected due to previous sexual exposure. This establishes the opportunity for transmission, the likelihood of which will depend on the inherent transmissibility of the virus and susceptibility of the uninfected partner but also on the number and nature of sexual encounters. Frequent condom use may be protective. Evidence is available from some studies 21–24 but findings have been inconsistent.10,25–27 If condom use truly protects, its effect can only be observed upon exposure to an infected partner. Moreover, use of condoms may be a marker for exposure to an infected partner, because they tend to be used with new or casual partners.28,29 When information on partner's HPV status is lacking, the effect of condom use may be obscured.
Having information on the current partner's HPV status permits answering several questions. Does it correlate with prevalent HPV infection as strongly as the number of partners? How would the effect of condom use differ among persons with and without an HPV-infected partner? To answer these questions, we analyzed data from a study of young heterosexual couples in new relationships, and focused on the individual as the unit of analysis. A companion paper on the type-specific concordance of HPV infections at the level of the partnership has been submitted for publication elsewhere.
MATERIALS AND METHODS
The HITCH Study (HPV Infection and Transmission among Couples through Heterosexual activity) is an ongoing longitudinal investigation initiated in May 2005. The study population consists of young (aged: 18–24) women attending a university or junior college in Montreal, Canada and their male partners. Eligible women had a current male sexual partner for which the relationship duration was no more than 6 months; had an intact uterus and no history of cervical lesions/cancer; and were not pregnant or planning to become pregnant in the next 24 months. Eligible male partners were aged 18 and older. Cross-sectional data obtained at enrolment are the object of the present analysis.
A self-selected volunteer sample was recruited through study promotion on campuses and at venues frequented by students. Promotional materials invited interested persons to visit the study website (www.mcgill.ca/hitchcohort) and to contact the research nurses. Of those making initial contact, 37% were eligible and of these, 58% enrolled. Participants attended the student health services clinics of either McGill or Concordia Universities and were compensated CDN $50 per clinic visit. All provided written informed consent. Study procedures and documents were approved by the ethical review committees at McGill University, Concordia University, and Université de Montréal.
Men and women self-completed separate computerized questionnaires, and were assured that information would not be released to their partner. Sexual behavior within the couple (i.e., with their “HITCH partner”) was measured since the start of their relationship, defined as the first encounter involving mutual masturbation, oral sex, and vaginal or anal intercourse. Participants reported condom use frequency, using the following response categories: never (0% of the time), rarely (1%–25%), some of the time (26%–75%), most of the time (76%–99%), and always (100% of the time), coded from 0 to 4. The responses provided by each partner were averaged for use in the primary analysis.
The outcome of interest was the presence of HPV DNA in genital specimens. Women self-collected vaginal swabs; written instructions advised women to gently insert a Dacron swab into the vagina until it could not go any further (at least 5 cm), then to rotate the swab inside the vagina for 3 full rotations. Self-collection methods are validated for research purposes, and are acceptable to women.30–32 Clinician-obtained specimens of epithelial cells from the penis (i.e., the glans up to and including the external opening of the meatus, coronal sulcus, penile shaft, and foreskin in uncircumcised men) and scrotum were collected, using previously described methods.33 Briefly, the skin was first gently abraded using sterilized ultrafine emery paper (3M 600A-grit Wetordry Tri-M-ite), then swabbed with a Dacron applicator moistened with normal saline. Vaginal and male genital swabs were agitated in PreservCyt and then discarded. Emery papers from male specimens were placed in the vials with the PreservCyt solution. Specimens were stored at 4°C before processing.
HPV Testing and Typing
Genital specimens were tested by a polymerase chain reaction protocol based on amplification of a 450 bp segment in the L1 HPV gene, using the Linear Array HPV genotyping assay (LA-HPV) (Roche Molecular Systems).34 Thirty-six mucosal HPV genotypes can be detected with this technique: Types 6, 11, 16, 18, 26, 31, 33, 34, 35, 39, 40, 42, 44, 45, 51, 52, 53, 54, 56, 58, 59, 61, 62, 66, 67, 68, 69, 70, 71, 72, 73, 81, 82, 83, 84, and 89. Coamplification of a β-globin DNA sequence permitted determining whether the specimens were adequate for testing. To date, 99.6% of vaginal specimens and 100% of combined penile and scrotum epithelial specimens were considered adequate.
The analysis was restricted to enrolment visit data from couples recruited between May 2005 and August 2008. Six couples who did not have valid HPV-DNA results for both partners were excluded, resulting in a final sample of 526 participants, or 263 couples in total. Statistical analysis was conducted using SAS, version 9 (SAS Institute, Inc., Cary, NC). All P-values were 2-sided. Statistical significance was based on a P <0.05. Individual-level sociodemographic and sexual history characteristics were based on self-report. Couple-related characteristics (e.g., condom use frequency) were based on the average of both partners' reports.
We calculated overall and type-specific HPV prevalence rates and prevalence rate ratios with 95% confidence intervals (CI) for overall HPV prevalence within categories of risk factors. Three potential risk factors were evaluated: the HITCH partner's infection status, the participant's lifetime number of vaginal sex partners, and the couple's frequency of condom use. To allow for the type-specific comparison of HPV status between partners, we considered each HPV type as its own observation, such that participants could have as many as 36 HPV-type outcomes. We used logistic regression within a generalized estimating equations framework with an exchangeable correlation structure. This approach ensures that statistical inferences are unbiased by adjusting standard errors and CIs for the actual number of participants. We report gender-stratified results as odds ratios (OR) with 95% CI. The linearity assumption for continuous variables was assessed visually, using logit plots. We tested for interaction to assess whether the effects of number of partners and condom use differed according to the HITCH partner's infection status.
Participant characteristics are shown in Table 1. Men were on average 1 year older than their female partner. Both partners were in their first vaginal sex relationship in only 5% (12/260) of couples. Women and men reported a median of 5 vaginal sex partners in their lifetime. Most (89% women, 87% men) considered their HITCH partner to be their dating partner (i.e., boyfriend or girlfriend). A minority (8% women, 10% men) reported that their HITCH partner was their marital or common-law spouse.
At enrolment, couples had been sexually active together for a median of 4.2 months (interquartile range: 2.8–5.6 months), and had engaged in vaginal sex for a median of 3.9 months (interquartile range: 2.7–5.3 months). The mean frequency of vaginal sex was 4.8 times per week (standard deviation = 4.4). Couples' frequency of condom use was 19% always, (49) 18% (47) most of the time, 28% (74) some of the time, 26% (67) rarely, and 9% (23) never. In most couples (64%, 164/258), both partners reported the same frequency of condom use (κ = 0.54, 95% CI: 0.53–0.55). There was no evidence of a gender difference in reporting (median difference of female report minus male report = 0). Among the 94 couples for which partners provided discrepant answers regarding condom use frequency, the absolute value of the difference was 1 unit for 83% (78), 2 units for 13% (12), 3 units for 3% (3), and 4 units for 1% (1).
Overall HPV prevalence and prevalence of the 10 most common and vaccine-preventable types (i.e., HPV-6, HPV-11, HPV-16, and HPV-18) are shown in Figure 1.35 One or more HPV types was detected in 56% of women (147/263) and 56% of men (147/263). Although prevalence rates exactly correspond, couples were not necessarily concordant for the same HPV type(s). Ignoring type, in 48% (125) both partners were HPV positive. In 36% (94) both partners were HPV negative. Among couples for whom at least 1 partner was infected (n = 169), 64% were concordant for 1 or more types, 56% were male-positive/female-negative for 1 or more types, and 51% were male-negative/female-positive for 1 or more types. Among HPV-infected participants, the mean number of types was 2.8 for women (range: 1–10) and 2.8 for men (range: 1–11).
Influences on Overall HPV Prevalence
As shown in Table 2, prevalence was 4.5 times higher among those whose partner was positive for any HPV type than among those whose partner was negative for all types. Similarly, prevalence was higher among those with greater numbers of lifetime vaginal sex partners. No HPV infection was detected in the 12 couples for whom both reported no previous vaginal sex partners. Lower rates were observed among couples who used condoms more frequently (Table 2); protection being significant for men (P = 0.02, χ2 test for trend), but not for women (P = 0.11).
Risk Factors for Type-Specific HPV Infection
Because there are many HPV genotypes, we examined whether the presence of a specific type in 1 partner corresponded with detection of the same type in the other. Results of a logistic regression analysis that treated HPV types as individual observations are shown in Table 3. HPV detection increased by 55.2 times (95% CI: 38.0–80.1) in women and 58.7 times (95% CI: 39.8–86.3) in men if their current partner was infected with the type under consideration, even after adjustment for lifetime number of partners and condom use.
The lifetime number of partners was positively associated with HPV type detection, but this relationship was modified by partner's HPV status among women (P <0.0001, Table 3). For women whose HITCH partner was negative for the HPV type being compared, prevalence was 1.09 (95% CI: 1.06–1.12) times higher for each additional male partner in her lifetime. In contrast, there was no effect of a woman's past sexual history if her HITCH partner was positive for the HPV type under consideration (OR = 0.98, 95% CI: 0.94–1.02). Among men, HPV detection was 1.05 (95% CI: 1.03–1.06) times higher for each additional partner, regardless of his HITCH partner's HPV status.
More frequent condom use was associated with lower odds of HPV detection in men (OR = 0.79, 95% CI: 0.70–0.90) but not in women (OR = 1.02, 95% CI: 0.87–1.18) (interaction P = 0.04) when the HPV status of the partner was ignored. The magnitude of protection increased among those whose HITCH partner was infected with the type under consideration but was more pronounced for men (OR = 0.64, 95% CI: 0.50–0.81) than for women (OR = 0.88, 95% CI: 0.69–1.11). The odds ratio estimates were not materially changed by use of the female or male partner's report of condom use frequency, or by additional adjustment for the length of time the couple had engaged in vaginal sex, report of concurrent partners, or the couples' frequency of mutual masturbation, oral sex, and engaging in anal sex (data not shown).
HITCH participants were asked to abstain from any sexual contact in the 24 hours preceding their clinic visit and 95% (250/263) complied. To identify evidence of possible contamination of genital specimens by recent sexual contact, the OR for the association between type-specific HPV detection and partner's status was reexamined, stratified by time since the couple's last vaginal sex encounter. The OR was 118 among the 7 couples who had sex the same day as the clinic visit (noncompliers), and was 38.6 among those who had sex 1 day prior (n = 37), 91.0 two days prior (n = 63), 50.0 three days prior (n = 22), 26.2 four to six days prior (n = 38), and 45.0 seven or more days before the clinic visit (n = 44). There was no statistical evidence of effect modification by time since last intercourse.
Genital HPV infection was very common among persons with a new sex partner. The strongest risk factor was presence of infection in one's current sexual partner, which resulted in an over fifty-fold increase in the prevalence of type-specific infection. This is the first report that this association is of such high magnitude and is considerably greater than that for the lifetime number of partners. Male prevalence was negatively associated with more frequent condom use, but this relationship did not reach statistical significance in women.
By design, all couples who enrolled in the HITCH Cohort Study had recently initiated their sexual relationship. Prevalence is expected to be high in this population because acquisition of a new partner is an important risk factor for incident infection in women9,13,36 and men.37 In our previous study of Montreal female university students, HPV prevalence in cervical specimens was 29%,38 nearly half that observed in HITCH. Prevalence would be expected to be higher in vaginal than in cervical specimens.39 HPV prevalence based on vaginal swabs among US women aged 20 to 24 was 45%.1 Studies of young male adults observed prevalence rates of 41% in Florida,2 51% in a combined Florida-Arizona sample3 and 65% in a predominantly university-based sample in Hawaii.4
HPV infection among persons with a new partner may arise from 3 possible sources. One may have been infected from a previous sexual contact. The strong association between one's lifetime number of partners and prevalent HPV reflects the role of past exposure.1,7–9,11,12,15,26,40,41 Alternatively, one may have been infected from the current partner. The very strong associations between HPV infection status in partners is evidence of recent transmission. This could not be explained by contamination from recent sexual contact. Due to the cross-sectional nature of these data, we cannot determine whether transmission was male-to-female or female-to-male. A third explanation is that HPV was transmitted from a concurrent partner after the relationship began. Nonetheless, we expect transmission from extradyadic partners to be minimal, as only 15% of women and 14% of men reported concurrent partnerships, and this was not associated with HPV detection (data not shown).
A protective effect of condoms on prevalent male infection has been reported by some,22,23 but not all studies (review by Dunne et al25). Of 3 studies of male incidence, one observed a protective effect of condoms24 but 2 others did not.10,26 None of these previous studies had information on infection status of the female partner. Condom use was protective against prevalent HPV infection among male HITCH participants whose current partner was infected. The OR indicated protection among women whose partner was infected, but it did not reach statistical significance. As for men, an effect of condom use has been inconsistently observed in women,27 but recent data suggest protection against incidence in women's first vaginal sex relationships.21 Furthermore, in a longitudinal study of 25 heterosexual couples, there were fewer HPV transmissions in couples who always used condoms.19
We propose 2 hypotheses for our observed gender difference. First, if male-to-female transmission is more efficient than female-to-male, then a protective effect may be overcome by a high transmission probability to women.18,42 Alternatively, the stronger effect observed in men may be due to more rapid HPV clearance if at enrolment more condom-using men had cleared their infection. In a randomized controlled trial among male partners of women with cervical intraepithelial neoplasia, condom users experienced faster regression of HPV-associated penile lesions.43
This analysis focused on the number of lifetime vaginal sex partners and frequency of condom use for vaginal sex within the couple under the assumption that penile-vaginal exposures were most likely to result in transmission to the genitalia. This was corroborated by the finding that HPV infection was not observed in any of the 12 couples for whom both partners were in their first vaginal sex relationship. Nevertheless, HPV transmission through other sexual activities is plausible.13,44 The impact of sexual activities other than vaginal sex on HPV infection in HITCH couples will be the subject of a future paper.
Measurement error is a potential limitation for these findings. Estimates of one's lifetime number of partners may be imprecise.45 Errors in the reporting of condom use frequency were minimized by collecting this information from both partners, and agreement was excellent between partners. We used accepted methods for cell sampling and a highly-sensitive HPV DNA detection method, but particularly for males, these methods are evolving.6
Generalization of these results to other populations requires careful assessment of sample comparability. The challenge of recruiting research volunteers is well known,46 and this is compounded in studies of couples. Women enrolled in HITCH reported similar numbers of lifetime partners but more frequent sex compared to our previous study of women attending university in Montreal.38 New couples who are willing to join an STI study may differ from those who are unwilling. In particular, new couples may be emotionally fragile. They may not yet have sufficient trust between partners to have the sensitive discussion needed to establish willingness of each partner to participate in an STI transmission study. We suspect participants had more liberal sexual attitudes, and would be more comfortable with communication of sexual matters, although this cannot be known with certainty. This should not bias our risk factor estimates, however, among populations with similar age profiles and sexual histories.
Our study is the first to document HPV prevalence in young adult heterosexual couples that are newly-forming. HPV prevalence was high (56%) and more common than in similar populations without a restriction to persons with a new sex partner. The partner's HPV status was the most important risk factor for HPV infection, and condoms exerted a stronger protective effect among men than among women. These findings underscore the very high sexual transmissibility of HPV infection and should assist policymakers in devising strategies to supplement the preventive effect of prophylactic HPV vaccination.
1. Dunne E, Unger E, Sternberg M, et al. Prevalence of HPV infection among females in the United States. JAMA 2007; 297:813–819.
2. Giuliano A, Lazcano-Ponce E, Villa L, et al. The Human Papillomavirus Infection in Men Study: Human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States. Cancer Epidemiol Biomarkers Prev 2008; 17:2036–2043.
3. Nielson C, Flores R, Harris R, et al. Human papillomavirus prevalence and type distribution in male anogenital sites and semen. Cancer Epidemiol Biomarkers Prev 2007; 16:1107–1114.
4. Hernandez B, Wilkens L, Zhu X, et al. Circumcision and human papillomavirus infection in men: A site-specific comparison. J Infect Dis 2008; 197:787–794.
5. Human Papillomaviruses. Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 90. Lyon, France: International Agency for Research on Cancer (IARC), 2007.
6. Giuliano A, Tortolero-Luna G, Ferrer E, et al. Epidemiology of human papillomavirus infection in men, cancers other than cervical and benign conditions. Vaccine 2008; 26:K17–K28.
7. Herrero R, Castle P, Schiffman M, et al. Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis 2005; 191:1796–1807.
8. Munoz N, Méndez F, Posso H, et al. Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of Colombian women with normal cytological results. J Infect Dis 2004; 190:2077–2087.
9. Moscicki A, Hills N, Shiboski S, et al. Risks for incidence human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 2001; 285:2995–3002.
10. Lu B, Wu Y, Nielson CM, et al. Factors associated with acquisition and clearance of human papillomavirus infection in a cohort of US men: A prospective study. J Infect Dis 2009; 199:362–371.
11. Nielson C, Harris R, Dunne E, et al. Risk factors for anogenital human papillomavirus infection in men. J Infect Dis 2007; 196:1137–1145.
12. Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998; 338:423–428.
13. Winer RL, Lee SK, Hughes JP, et al. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol 2003; 157:218–226.
14. Winer R, Feng Q, Hughes J, et al. Risk of female human papillomavirus acquisition associated with first male sex partner. J Infect Dis 2008; 197:279–282
15. Castellsagué X, Ghaffari A, Daniel R, et al. Prevalence of penile human papillomavirus DNA in husbands of women with and without cervical neoplasia: a study in Spain and Columbia. J Infect Dis 1997; 176:353–361.
16. Castellsagué X, Bosch F, Munoz N, et al. Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med 2002; 346:1105–1112.
17. Thomas D, Ray R, Kuypers J, et al. Human papillomaviruses and cervical cancer in Bangkok. III. The role of husbands and commercial sex workers. Am J Epidemiol 2001; 153:740–748.
18. Burchell A, Richardson H, Mahmud S, et al. Modeling the sexual transmissibility of human papillomavirus infection using stochastic computer simulation and empirical data from a cohort study of young women in Montreal, Canada. Am J Epidemiol 2006; 163:534–543.
19. Hernandez B, Wilkens L, Zhu X, et al. Transmission of human papillomavirus in heterosexual couples. Emerg Infect Dis 2008; 14:888–894.
20. Rowhani-Rahbar A, Hughes JP, Koutsky LA. Difficulties in estimating the male-to-female sexual transmissibility of human papillomavirus infection. Sex Transm Dis 2009; 36:261–263.
21. Winer R, Hughes J, Feng Q, et al. Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med 2006; 354:2645–2654.
22. Baldwin S, Wallace D, Papenfuss M, et al. Condom use and other factors affecting penile human papillomavirus detection in men attending a sexually transmitted disease clinic. Sex Transm Dis 2004; 31:601–607.
23. Vaccarella S, Lazcano-Ponce E, Castro-Garduno J, et al. Prevalence and determinants of human papillomavirus infection in men attending vasectomy clinics in Mexico. Int J Cancer 2006; 119:1934–1939.
24. Kjaer S, Munk C, Winther J, et al. Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 2005; 14:1528–1533.
25. Dunne E, Nielson C, Stone K, et al. Prevalence of HPV infection among men: A systematic review of the literature. J Infect Dis 2006; 194:1044–1057.
26. Lajous M, Mueller N, Cruz-Valdéz A, et al. Determinants of prevalence, acquisition, and persistence of human papillomavirus in health Mexican military men. Cancer Epidemiol Biomarkers Prev 2005; 14:1710–1716.
27. Manhart LE, Koutsky LA. Do condoms prevent genital HPV infection, external genital warts, or cervical neoplasia? Sex Transm Dis 2002; 29:726–735.
28. Aral SO, Peterman TA. A stratified approach to untangling the behavioral/biomedical outcomes conundrum. Sex Transm Dis 2002; 29:530–532.
29. Warner L, Newman DR, Austin HD, et al. Condom effectiveness for reducing transmission of gonorrhea and chlamydia: The importance of assessing partner infection status. Am J Epidemiol 2004; 159:242–251.
30. Wright T Jr, Denny L, Kuhn L, et al. HPV DNA testing of self-collected vaginal samples compared with cytologic screening to detect cervical cancer. JAMA 2000; 283:81–86.
31. Sellors J, Lorincz A, Mahony J, et al. Comparison of self-collected vaginal, vulvar, and urine samples with physician-collected cervical samples for human papillomavirus testing to detect high-grade squamous intraepithelial lesions. Can Med Assoc J 2000; 163:513–518.
32. Gravitt P, Lacy J Jr, Brinton L, et al. Evaluation of self-collected cervicovaginal cell samples for human papillomavirus testing by polymerase chain reaction. Cancer Epidemiol Biomarkers Prev 2001; 10:95–100.
33. Weaver BA, Feng Q, Holmes KK, et al. Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis 2004; 189:677–685.
34. Coutlée F, Rouleau D, Petignat P, et al. Enhanced detection and typing of human papillomavirus (HPV) DNA in anogenital samples with PGMY primers and the linear array HPV genotyping test. J Clin Microbiol 2006; 44:1998–2006.
35. Muñoz N, Bosch FX, de Sanjosé S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348:518–527.
36. Giuliano A, Harris R, Sedjo R, et al. Incidence, prevalence and clearance of type-specific human papillomavirus infections: The Young Women's Health Study. J Infect Dis 2002; 186:462–469.
37. Partridge J, Hughes J, Feng Q, et al. Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis 2007; 196:1128–1136.
38. Richardson H, Kelsall G, Tellier P, et al. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 2003; 12:485–490.
39. Bauer H, Ting Y, Greer C, et al. Genital human papillomavirus infection in female university students as determined by a PCR-based method. JAMA 1991; 265:472–477.
40. Rousseau M, Franco E, Villa L, et al. A cumulative case-control study of risk factor profiles for oncogenic and nononcogenic cervical human papillomavirus infections. Cancer Epidemiol Biomarkers Prev 2000; 9:469–476.
41. Franceschi S, Castellsagué X, Dal Maso L, et al. Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 2002; 86:705–711.
42. Mann JR, Stine CC, Vessey J. The role of disease-specific infectivity and number of disease exposures on long-term effectiveness of the latex condom. Sex Transm Dis 2002; 29:344.
43. Bleeker M, Hogewoning C, Voorhorst F, et al. Condom use promotes regression of human papillomavirus-associated penile lesions in male sexual partners of women with cervical intraepithelial neoplasia. Int J Cancer 2003; 107:804–810.
44. Sonnex C, Strauss S, Gray J. Detection of human papillomavirus DNA on the fingers of patients with genital warts. Sex Transm Infect 1999; 75:317–319.
45. Schlecht N, Franco E, Rohan T, et al. Repeatability of sexual history in longitudinal studies on HPV infection and cervical neoplasia: determinants of reporting error at follow-up interviews. J Epidemiol Biostat 2001; 6:393–407.
46. Morton L, Cahill J, Hartge P. Reporting participation in epidemiologic studies: A survey of practice. Am J Epidemiol 2006; 163:197–203.
© Copyright 2010 American Sexually Transmitted Diseases Association
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Data is temporarily unavailable. Please try again soon.
Readers Of this Article Also Read