Early Acquisition of Anogenital Human Papillomavirus Among Teenage Men Who Have Sex With Men

MAJOR ARTICLE Early Acquisition of Anogenital Human Papillomavirus Among Teenage Men Who Have Sex With Men Huachun Zou,1 Sepehr N. Tabrizi,2,3,4 Andrew E. Grulich,5 Suzanne M. Garland,2,3,4 Jane S. Hocking,6 Catriona S. Bradshaw,1,7,8 Andrea Morrow,7 Garrett Prestage,5,9 Alyssa M. Cornall,3,4 Christopher K. Fairley,1,7,9,a and Marcus Y. Chen1,7,9,a 1 (See the editorial commentary by Cranston on pages 635–8.) Background. Anogenital human papillomavirus (HPV) is common among men who have sex with men (MSM) and causes anal cancer. This study examined the determinants of initial anogenital HPV infection among teenage MSM. Methods. Two hundred MSM aged 16 to 20 years were recruited via community and other sources. Men were tested for HPV DNA from the anus and penis. Results. The proportion of men with anal HPV of any type increased from 10.0% in men reporting no prior receptive anal sex to 47.3% in men reporting ≥4 receptive anal sex partners (P < .001).A similar pattern was also seen with HPV type 16 (P = .044). The proportion of men with penile HPV increased from 3.7% in men reporting no prior insertive anal sex to 14.8% in men reporting ≥4 insertive anal sex partners (P = .014). Overall, 39.0% (95% confidence interval (CI), 32.2%−46.1%) of men had at least 1 HPV type: 23.0% (95% CI, 17.4%−29.5%) had a vaccine-preventable type (6, 11, 16 or 18). Conclusions. Early and high per partner transmission of HPV occurred between men soon after their first sexual experiences. HPV vaccination needs to commence early for maximal prevention of HPV among MSM. Keywords. human papillomavirus; HPV; men who have sex with men; vaccination; sexually transmitted infections. The human papillomavirus (HPV) is the most prevalent viral sexually transmitted infection (STI) worldwide and is the cause of genital warts and HPV-associated neoplasia [1]. Men who have sex with men (MSM) are a major risk group for STIs including HIV and they have a high prevalence of anogenital HPV infection and HPV- Received 13 September 2013; accepted 2 October 2013; electronically published 21 November 2013. a Joint last authors. Correspondence: Associate Professor Marcus Y. Chen, 580 Swanston Street, Carlton, Victoria, Australia, 3055 (). The Journal of Infectious Diseases 2014;209:642–51 © The Author 2013. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: . DOI: 10.1093/infdis/jit626 642 • JID 2014:209 (1 March) • Zou et al related lesions including anogenital warts, anal intraepithelial neoplasia, and anal cancer [2–4]. Data indicate that the incidence of anal cancer among MSM is high, with the highest rates among HIV-positive MSM [2, 5]. In a metaanalysis of published studies, overall, 63% of HIV-negative and 92% of HIV-positive MSM were infected with anal HPV. The overall prevalence of HPV 16, the HPV type most commonly associated with anal cancer, among HIV-negative and HIV-positive MSM was 12% and 35%, respectively [6]. The quadrivalent HPV vaccine is effective in preventing infection with HPV types 6, 11, 16, and 18; in preventing the development of genital warts in males [7]; and in protecting against anal intraepithelial neoplasia in MSM [8]. Mathematical modeling suggests that HPV vaccination of MSM is likely to be cost effective [9]. School of Population and Global Health, University of Melbourne, Melbourne, Australia; 2Department of Obstetrics and Gynaecology, University of Melbourne; 3Department of Microbiology and Infectious Diseases, Royal Women’s Hospital, Melbourne, Australia; 4Murdoch Children’s Research Institute, Melbourne, Australia; 5Kirby Institute, University of New South Wales, Sydney, Melbourne, Australia; 6Centre for Women’s Health, Gender and Society, University of Melbourne, Melbourne, Australia; 7Melbourne Sexual Health Centre, Alfred Health, Melbourne, Australia; 8Central Clinical School, Monash University, Melbourne, Australia; and 9Australian Research Centre in Sex, Health and Society, La Trobe University, Melbourne, Australia Studies have shown a high incidence of low- and high-risk genital HPV infection associated with new sexual partners among teenage females [10]. Such studies have underscored the need for HPV vaccination prior to the onset of sexual activity. No previous studies have been designed to examine factors associated with HPV infection among teenage MSM when initial infection with HPV would be expected to occur [11]. Such data would help to inform the development of policies that govern HPV vaccination of MSM. In this study, we sought to elucidate the determinants of initial anogenital HPV infection among teenage MSM and the proportion infected with HPV. Men used a single-use paper emery board to gently exfoliate the epidermis over the entire penile shaft and glans penis and, if uncircumcised, the inner and outer aspects of the foreskin. Men then rolled a saline-moistened swab firmly over these areas. Swabs were placed in RNA (Ambion). A physician verified anal or penile warts. Blood for HPV serology was collected in 10-mL serum collection tubes (Greiner Bio One International AG) and centrifuged at 4800 × g for 10 minutes to separate cells from serum. Serum samples were aliquoted and stored at −80°C until testing. Laboratory Methods METHODS Subjects and Recruitment Specimen Collection Specimens were obtained from men for HPV DNA testing in the following order: an oral rinse, an anal canal swab, a perianal swab, and a penile swab. The oral rinse and penile swab were self-collected by men after watching a video that demonstrated how to self-collect these specimens [12]. The study nurse collected the anal and perianal swabs using a technique that prevents cross-contamination of HPV DNA between the 2 sites. For the oral rinse men, rinsed and gargled 10 mL of saline for 20 seconds. The anal swab was obtained using a salinemoistened, flocked swab (Copan Flock Technologies) that was inserted 3 cm into the anal canal and rotated 6 times. The nurse then used a single-use paper emery board to gently exfoliate the epidermis of the perianal area within 5 cm of the anus. A saline-moistened swab was then rolled over the abraded area. HPV Serology Serum samples were tested at PPD Vaccines and Biologics Lab. Antibodies against HPV types 6, 11, 16, and 18 were measured using a Luminex competitive immunoassay as previously described [16]. STI Testing Men were screened for pharyngeal and rectal Neisseria gonorrhoeae using modified Thayer-Martin media. First-void urine and a rectal swab were tested for Chlamydia trachomatis by strand HPV infection among teenage MSM • JID 2014:209 (1 March) • 643 To be eligible for the Human Papillomavirus in Young People Epidemiological Research (HYPER) Study, participants had to be males aged 16 to 20 years who self-identified as being samesex attracted. Men were not required to have engaged in sex with other males. Men were recruited between Oc (...truncated)