Human papillomavirus (HPV) is the most common sexually transmitted infection (STI) in the United States, and the prevalence of HPV in men who have sex with men (MSM) is higher than the general population.1,2 Despite this fact, and the large body of work on other STIs and HIV in South America, few data on HPV are available there.3 Anecdotal reports from Peruvian sexual health clinics suggest a high burden of genital warts among MSM. At Epicentro, a community sexual health clinic with tailored services for MSM and transwomen (TW) in Lima, HPV-related disease accounts for more than 35% of medical consultations. The disease burden of HPV in MSM and TW in Peru is obscured by the lack of knowledge regarding the interactions between HPV and HIV infection and stigma faced by individuals with genital warts.4 This is especially troubling given the strong link between HPV and HIV and that anal warts are a significant risk factor for anal cancer in HIV-infected men.5,6 Studies have found that a recent history of receptive anal intercourse doubled the risk of HPV infection in MSM, and most of new HIV infections in Latin America occur among MSM through anal sex.7,8 In addition, the relationships between many other ulcerative genital STIs are all known to enhance the transmission of HIV, whereas the role of HPV and HPV-related disease is unknown.9–11 This novel study measured the prevalence of anogenital warts (AGWs) in MSM and TW presenting at a community clinic and determined their level of awareness of HPV and the HPV vaccine.
Six-hundred HIV-uninfected MSM and TW were recruited using venue-based sampling at Epicentro and other locations (bars, clubs, discotheques, volley ball courts). Inclusion criteria were age 18 to 40 years, ability to provide informed consent, residency in Lima, being HIV uninfected, and self-reporting anal sex in the past 12 months. Participation was further limited to those who had not participated in a HIV or HPV vaccine clinical trial, did not have a diagnosis with an immunodeficiency disease, and had not taken HIV preexposure prophylaxis. Potential participants were first screened for HIV using the Determine HIV-1/2 Ag/Ab Combo rapid test. HIV-infected participants were referred to the national HIV program for free HIV care and treatment, whereas HIV-negative persons were invited to participate in the study. Presence of AGW was self-reported and confirmed by physician examination. Institutional review boards at the University of California, Los Angeles, and Asociación Civil Impacta Salud y Educación in Lima, Peru, reviewed and approved the study protocol, recruitment materials, and informed consent forms. Full details of the study protocol have been published elsewhere.12 Participants completed a self-administered questionnaire consisting of 84 questions including demographics, history of STIs, sexuality and sexual behavior, and HPV knowledge. Transactional sex was defined as trade of sex for money or goods. Knowledge of HPV was measured by a standard validated survey.13–15 Upon completion of the questionnaire, participants were offered US $3.00 for transportation, a gift worth US $2.00, and condoms and lubricant. Survey data were entered into SurveyMonkey Gold and checked for logic and range. Stata 12.0 (Statacorp LP, College Station, TX) was used for quantitative data analyses. Mean, ranges, SD, and percentages were reported. Pearson χ2 and Fisher exact tests were computed for differences in HPV knowledge by AGW status.
A total of 756 participants were screened for study participation, of which 156 tested HIV positive and were excluded. Nearly half of the 600 participants self-identified as gay (47.9%), whereas 68 (11.5%) were TW (Table 1). The average age of the participants was 25.5 years (median, 24; interquartile range, 21–29). Most (67%) participants were single, had completed a tertiary or university education (53%), and were current smokers (54%). The average (SD) age of participants’ first anal intercourse was 17 (4.58) years. One hundred seventy-four (29%) participants reported engaging in transactional sex, with an average (SD) age of first transactional sex at 18.5 (4.32) years. Three quarters (77%) of participants reported engaging in some form of unprotected anal or oral sex 6 months before the survey. Of those, 63% reported either insertive (32%) or receptive (37%) condomless anal sex in the past 3 months, and 71% reported having condomless oral sex in the same period. Most participants (81%) who received money or favors for sex reported having only male sex partners. Three hundred participants reported current or previous AGW, and 223 (37%) had visible AGW. Most of the visible warts were either anal only (60%) or penile only (28%). Participants with AGW were significantly more likely to be educated than peers without a history of AGW (odds ratio [OR], 2.41; 95% confidence interval [CI], 1.74–3.36) and to assume an active or equally active and passive role during sex (OR, 1.61; 95% CI, 1.15–2.27). They were significantly less likely to have ever smoked (OR, 0.57; 95% CI, 0.38–0.86) or to have exchanged favors for sex 6 months before the survey (OR, 0.36; 95% CI, 0.24–0.52). Finally, participants with AGW were less likely to have used condoms during their last sexual encounter (OR, 0.44; 95% CI, 0.31–0.61). Less than half (48%) of participants had heard of HPV before their participation in the study, and only 19% reported knowing of HPV vaccine. Few (11%) participants knew of a vaccine to prevent anal cancer, and 60% of participants reported that they would use such a vaccine if made available. Participants with a history of AGW were more likely to report that condoms help prevent HPV (OR, 2.12; 95% CI, 1.13–4.01) and that the absence of genital warts does not mean the absence of HPV (OR, 1.64; 95% CI, 1.27–2.13). Those with a history of AGW were also less likely to report the availability of a vaccine to prevent genital warts (OR, 0.3; 95% CI, 0.15–0.62). Participants with present AGW were significantly more likely to know that condoms prevent HPV (P = 0.02). Participants with a tertiary education or beyond (including university) were more likely to correctly identify that condoms help prevent HPV (OR, 1.64; 95% CI, 1.5–2.59) and that the absence of genital warts does not mean the absence of HPV (OR, 9.52; 95% CI, 3.75–24.19). Paradoxically, those with a higher education were less likely to report HPV vaccine knowledge (OR, 2.86; 95% CI, 1.39–5.92). In addition, participants who were having condomless sex and those who did not identify as gay were significantly more likely to answer correctly with regard to the availability of a vaccine that prevents genital warts (P = 0.04 and P = 0.01, respectively). Transwomen participants (34.8%) were 4 times as likely compared with other participants (7.7%) to respond that a lack of genital warts meant that HPV infection had also been resolved.
Study participants had low levels of knowledge of HPV and HPV vaccines but likely high HPV exposure due to frequency of condomless anal sex (Table 2). Of note, participants with a higher education were more likely to have current or a history of AGW and less likely to be knowledgeable about HPV vaccines than those with a lower education. This knowledge gap may be explained, in part, by barriers such as the stigma of sex work, underreporting of STIs, high cost of the vaccine in Peru, and misinformation and fear about the vaccine.13 Compared with female sex workers in Lima, participants in our study were less likely to report that condoms help prevent HPV transmission and less desirous of an HPV vaccine. Registered female sex workers must visit a special clinic to obtain their health card, which serves as a license to conduct sex work.13 Although this does not guarantee sexual health education, it provides an opportunity to seek it, especially when compared with MSM and TW, who are often excluded. There were several limitations in our study. Visual presence of current AGW was confirmed by clinical examination, and no biopsies were done. Most of our questions were closed-ended, and it is possible that open-ended questions may have better gauged HPV knowledge. This limitation is compounded by the fact that our survey relied on participant recall. In addition, our results may not be generalizable to MSM or TW outside Lima because of the convenience and clinic-based sampling method used. Finally, although TW face disproportionate STI burden throughout Latin America, even when compared with MSM,16 they represented only a fraction of respondents (11.5%). Special efforts must be made to be inclusive of TW in population-based STI research. All men and women should have access to HPV vaccines and be targeted for education campaigns to gain HPV-related knowledge and overcome the barriers they would face in vaccine campaigns. Both MSM and TW groups face a disproportionate disease risk and burden because of the social stigma they face, the difficulty in finding culturally competent services, and the cost of relevant treatments. Additional studies on MSM and TW are needed to determine the potential cost-effectiveness of the vaccine in HPV-exposed populations.
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