Molecular Epidemiology of HIV-1 Infection among Men who Have Sex with Men in Taiwan in 2012

RESEARCH ARTICLE Molecular Epidemiology of HIV-1 Infection among Men who Have Sex with Men in Taiwan in 2012 Szu-Wei Huang1,2, Sheng-Fan Wang2,3, Ángel E. Cowó4, Marcelo Chen5,6,7, Yu-Ting Lin2, Chun-Po Hung8, Yi-Hsien Chen2, Jyh-Yuan Yang9, Hung-Jen Tang10,11, Yi-Ming Arthur Chen1,2,12* a11111 OPEN ACCESS Citation: Huang S-W, Wang S-F, Cowó ÁE, Chen M, Lin Y-T, Hung C-P, et al. (2015) Molecular Epidemiology of HIV-1 Infection among Men who Have Sex with Men in Taiwan in 2012. PLoS ONE 10(6): e0128266. doi:10.1371/journal.pone.0128266 Academic Editor: Janaki Amin, UNSW Australia, AUSTRALIA Received: October 7, 2014 Accepted: April 23, 2015 Published: June 3, 2015 Copyright: © 2015 Huang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All sequences are available from the NCBI GenBank database (accession numbers KM668624 - KM668703). Funding: This research was supported by the Centers for Disease Control of Taiwan [grant number DOH101-DC-1001] and partially by Kaohsiung Medical University Aim for the Top Universities Grant [grant number KMU-TP103E01] and Chi-Mei Medical Center and Kaohsiung Medical University Research Foundation [grant number 103CM-KMU-02]. Competing Interests: The authors have declared that no competing interests exist. 1 Institute of Microbiology and Immunology, National Yang Ming University, Taipei 11221, Taiwan, 2 Center for Infectious Disease and Cancer Research, Kaohsiung Medical University, Kaohsiung 80708, Taiwan, 3 Department of Medical Laboratory Science and Biotechnology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan, 4 International Health Program, National Yang Ming University, Taipei 11221, Taiwan, 5 Department of Urology, Mackay Memorial Hospital, Taipei 10449, Taiwan, 6 Department of Cosmetic Applications and Management, Mackay Junior College of Medicine, Nursing and Management, Taipei 25245, Taiwan, 7 School of Medicine, Mackay Medical College, New Taipei City 25245, Taiwan, 8 Rainbow Queer Health and Culture Center, Living with Hope Organization, Taiwan Society of Preventive Medicine, Taipei 10084, Taiwan, 9 Centers for Disease Control, Taipei 10050, Taiwan, 10 Department of Medicine, Chi Mei Medical Center, Tainan 71067, Taiwan, 11 Department of Health and Nutrition, Chia Nan University of Pharmacy and Science, Tainan 71710, Taiwan, 12 Department of Microbiology and Immunology, Institute of Medical Research and Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung 80708, Taiwan * Abstract The number of men who have sex with men (MSM) infected with HIV-1 in Taiwan has increased rapidly in the past few years. The goal of this study was to conduct a molecular epidemiological study of HIV-1 infection among MSM in Taiwan to identify risk factors for intervention. Voluntary counseling program and anonymous testing were provided to patrons at 1 gay bar, 7 night clubs and 3 gay saunas in Taipei and New Taipei Cities in 2012. HIV-1 subtypes were determined using gag subtype-specific PCR and phylogenetic analysis by env sequences. Recent HIV-1 infection was determined using LAg-Avidity EIA. Indepth interviews and questionnaires were used to identify risk factors. The prevalence and incidence of HIV-1 among MSM in Taiwan were 4.38% (53/1,208) and 3.29 per 100 personyears, respectively. Of 49 cases genotyped, 48 (97.9%) were infected with subtype B and 1 with CRF01_AE (2%). Phylogenetic analysis of 46 HIV-1 strains showed that 25 (54.4%) subtype B strains formed 9 clusters with each other or with other local strains. The CRF01_AE case clustered with a reference strain from a Thai blood donor with bootstrap value of 99. Multivariate logistic regression analysis showed that risk factors associated with HIV-1 infection included use of oil-based solution as lubricant (vs. saliva or waterbased lubricants, OR= 4.23; p <0.001); exclusively receptive role (vs. insertive role, OR= 9.69; p <0.001); versatile role (vs. insertive role, OR= 6.45; p= 0.003); oral sex (vs. insertive role, OR= 11.93; p= 0.044); times of sexual contact per week (2-3 vs. zero per week, OR= 3.41; p= 0.021); illegal drug use (OR= 4.12; p <0.001); and history of sexually transmitted PLOS ONE | DOI:10.1371/journal.pone.0128266 June 3, 2015 1 / 22 Risk Factors Associated with HIV-1 Infection among MSM diseases (OR= 3.65; p= 0.002). In conclusion, there was no new HIV-1 subtype or circulating recombinant form responsible for the increase of HIV-1 among MSM in Taiwan in 2012. Misuse of oil-based solution as lubricant is a new risk factor identified among MSM in Taiwan. The Taiwan’s Centers for Disease Control has created a video (www.youtube.com/ watch?v=BinExvvOTMM&feature = iv&src_vid=BW81-PfmY3E&annotation_id = annotation_2436493705) to correct such misconception in its AIDS prevention campaign. Introduction According to the Joint United Nations Program on HIV/AIDS (UNAIDS) report, 35.3 million people worldwide were living with HIV in 2012 [1]. A recent review has shown that the global trend of HIV-1 infection among men who have sex with men (MSM) has continued to increase, especially in East Asia, Africa, and Russia [2]. By the end of 2012, there were 25,081 cases of HIV infection been reported to Taiwan’s Centers for Disease Control (CDC) and Taiwanese nationals accounted for 96.6% of those cases (Taiwan CDC report 2012; http://www. cdc.gov.tw/info.aspx?treeid=1f07e8862ba550cf&nowtreeid=6c5ea6d932836f74&tid= 58114AFB86117F53). Among them, homosexual men accounted for 41.9% of cases, followed by injection drug users (IDUs, 27.6%), heterosexuals (20.3%) and bisexual men (8.3%). There was an explosive outbreak of circulating recombinant form (CRF) _07BC among Taiwanese IDUs from 2004 to 2006 [3–5]. However, the HIV epidemic took a turn in 2007 as HIV-1 infection among IDUs decreased rapidly due to the implementation of harm reduction programs [6] and infection among MSM kept increasing exponentially [7]. Therefore, special attention needs to be given to any new HIV-1 subtype or CRF transmitted to a Taiwanese MSM. However, studies of the HIV-1 subtypes in MSM in Taiwan after 2009 are lacking. Risk factors for HIV infection in MSM include unprotected anal intercourse [8–11], illegal drug use [11–13], a history of other sexually transmitted diseases (STDs) [12], condom use, multiple sex partners and role during anal intercourse [8, 11, 14, 15]. Previous studies have shown an association between high level of substance use, sexual risk behavior and risk of HIV infection in young MSM [16–19]. A study by Hikada et al. reported that 45% of MSM ever used one type of drug and 19.6% ever used more than one type of drugs [20]. According to the San Francisco Young Men’s Study, 43% of the subjects had used multiple illeg (...truncated)