Monitoring for Human Papillomavirus Vaccine Impact Among Gay, Bisexual, and Other Men Who Have Sex With Men—United States, 2012–2014

The Journal of Infectious Diseases MAJOR ARTICLE Monitoring for Human Papillomavirus Vaccine Impact Among Gay, Bisexual, and Other Men Who Have Sex With Men—United States, 2012–2014 Elissa Meites,1 Pamina M. Gorbach,4 Beau Gratzer,5 Gitika Panicker,2 Martin Steinau,2 Tom Collins,6 Adam Parrish,6 Cody Randel,5 Mark McGrath,4 Steven Carrasco,4 Janell Moore,4 Akbar Zaidi,3 Jim Braxton,3 Peter R. Kerndt,4 Elizabeth R. Unger,2 Richard A. Crosby,6 and Lauri E. Markowitz1 1 Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, 2Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Diseases, and 3Division of STD Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia; 4Department of Epidemiology, Fielding School of Public Health, University of California–Los Angeles; 5Howard Brown Health, Chicago, Illinois; and 6College of Public Health, University of Kentucky, Lexington Human papillomavirus (HPV) infection is the most common sexually transmitted infection worldwide [1]. Gay, bisexual, and other men who have sex with men (MSM) have high rates of infection with HPV [2, 3]. In 2 recent studies, the incidence of any anal HPV per 100 person-years was 57.1 cases among 200 MSM aged 16–20 years and 46.2 cases among 94 MSM aged 19–23 years [4, 5]. Commonly reported risk factors include high numbers of lifetime sex partners and concomitant human immunodeficiency virus (HIV) infection [6–9]. Diseases associated with persistent HPV infections include anogenital warts and various types of cancers, including >90% of anal cancers in the United States [10]. In a meta-analysis of data from 9 studies, the pooled incidence rate of anal cancer among MSM was 5.1 cases per 100 000 person-years among Received 16 February 2016; accepted 26 May 2016; published online 13 June 2016. Presented in part: 30th International Papillomavirus Conference, Lisbon, Portugal, September 2015. Abstract HPV15-0175. Correspondence: E. Meites, Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, MS A34, Atlanta, GA 30329-4027 (). The Journal of Infectious Diseases® 2016;214:689–96 Published by Oxford University Press for the Infectious Diseases Society of America 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US. DOI: 10.1093/infdis/jiw232 HIV-negative MSM and 45.9 cases per 100 000 person-years among MSM infected with HIV [11, 12]. These rates are higher than that for all US males, which is estimated to be 1.6 cases per 100 000 persons [13]. In addition, the incidence of HPVassociated oropharyngeal cancer is rising in the United States, although the relative risk among MSM is not well established [14]. HPV type 16 is responsible for the majority of HPVassociated cancers in men [10]. In the United States, 2 prophylactic HPV vaccines are licensed for use in males. Quadrivalent HPV vaccine (4vHPV; Gardasil; Merck) protects against 4 HPV types (6, 11, 16, and 18) and was licensed in 2009 for use for males aged 9–26 years [15]. HPV vaccination was already routinely recommended for girls; the Advisory Committee on Immunization Practices (ACIP) stated that boys could be vaccinated but did not include HPV vaccination in the routine immunization schedule for boys at the time [16]. In 2011, the ACIP recommended routine vaccination for all males at ages 11–12 years, through age 21 years for men not previously fully vaccinated, and through age 26 years for MSM and immunocompromised men, including those infected with HIV [16]. The pivotal 4vHPV efficacy trial in males included heterosexual men and MSM who had 1–5 lifetime sex partners [17, 18]. HPV Vaccine Impact Among MSM • JID 2016:214 (1 September) • 689 Background. Gay, bisexual, and other men who have sex with men (MSM) are at high risk for human papillomavirus (HPV) infection; vaccination is recommended for US males, including MSM through age 26 years. We assessed evidence of HPV among vaccine-eligible MSM and transgender women to monitor vaccine impact. Methods. During 2012–2014, MSM aged 18–26 years at select clinics completed a computer-assisted self-interview regarding sexual behavior, human immunodeficiency virus (HIV) status, and vaccinations. Self-collected anal swab and oral rinse specimens were tested for HPV DNA (37 types) by L1 consensus polymerase chain reaction; serum was tested for HPV antibodies (4 types) by a multiplexed virus-like particle–based immunoglobulin G direct enzyme-linked immunosorbent assay. Results. Among 922 vaccine-eligible participants, the mean age was 23 years, and the mean number of lifetime sex partners was 37. Among 834 without HIV infection, any anal HPV was detected in 69.4% and any oral HPV in 8.4%, yet only 8.5% had evidence of exposure to all quadrivalent vaccine types. In multivariate analysis, HPV prevalence varied significantly (P < .05) by HIV status, sexual orientation, and lifetime number of sex partners, but not by race/ethnicity. Discussions. Most young MSM lacked evidence of current or past infection with all vaccine-type HPV types, suggesting that they could benefit from vaccination. The impact of vaccination among MSM may be assessed by monitoring HPV prevalence, including in self-collected specimens. Keywords. epidemiological monitoring; homosexuality, male; papillomavirus infections; papillomavirus vaccines. METHODS Study Design and Procedures The cross-sectional Young Men’s HPV study (YMHPV study) enrolled consenting gay, bisexual, and other MSM, including transgender women, aged 18–26 years. Enrollment occurred at 3 clinical facilities focused on providing sexual health services to lesbian, gay, bisexual, and transgender populations in 2 US cities (Chicago, Illinois, and Los Angeles, California) during July 2012–August 2014. These cities were selected from among 12 included in the US National HIV/AIDS Strategy operational plan, and sites were identified on the basis of available technical capacity and potential study population size [22]. The study protocol was reviewed and approved by institutional review boards at the participating institutions. Participants were eligible if they provided written informed consent and met the following criteria at the time of enrollment: (1) age 18–26 years, to allow for consent requirements and vaccine eligibility; (2) assigned male sex at birth; and (3) eligible for 690 • JID 2016:214 (1 September) • Meites et al HPV vaccine, based on sexual orientation (ie, identification as gay, homosexual, or bisexual, regardless of past sexual behavior) and/or sexual behavior (ie, ever having engaged in oral or anal sex with a male partner). Each received a gift card incentive of nominal value. Most were enrolled and completed all study elements on the day of a clinic (...truncated)