Research Article: Prevalence and mapping of hepatitis C infections among men who have sex with men in New York City

Date Published: July 18, 2018

Publisher: Public Library of Science

Author(s): Hong-Van Tieu, Oliver Laeyendecker, Vijay Nandi, Rebecca Rose, Reinaldo Fernandez, Briana Lynch, Donald R. Hoover, Victoria Frye, Beryl A. Koblin, Yury E. Khudyakov.

http://doi.org/10.1371/journal.pone.0200269

Abstract

Emerging sexually transmitted hepatitis C virus (HCV) epidemics among men who have sex with men (MSM) have been reported worldwide, with higher HCV infection rates among those who are HIV-infected. This study aims to determine prevalence of recent and chronic HCV infections among community-recruited MSM in New York City (NYC), map HCV infections by home, social, and sexual neighborhoods, and identify clusters of genetically linked HCV variants using phylogenetic analysis. The NYC M2M study recruited MSM via modified time-space, venue-based sampling and internet/mobile app-based recruitment during 2010–13. Participants completed a Google Earth map on neighborhoods of where they lived, socialized, and had sex in the last 3 months, an ACASI questionnaire, and a sexual network inventory about their sex partners. The men received HIV testing and provided serum samples. Testing on stored serum samples included HCV antibody and RNA viral load, HCV antibody avidity assay (avidity index <30% with positive viral load is considered recently infected), and HCV RNA extraction and amplification to generate a 432 base-pair region of Core/E1 for sequencing and phylogenetic analysis. Historic local controls were included in the phylogenetic analysis. Of 1,028 MSM, 79.7% were HIV-negative and 20.3% HIV-positive. Twenty nine MSM (2.8%) were HCV antibody-positive. MSM who were HCV antibody-positive reported a median of 2 male sex partners in last 3 months, with 6.9% aged 18–24, 17.2% 25–29, 13.8% 30–39, and 62.1% 40 and over. 8.1% of HIV-positive MSM were HCV antibody-positive vs. 1.5% of HIV-negative men (p<0.0001). Of 29 HCV-antibody positive MSM, 12 (41%) were HCV RNA-positive (11 subtype 1a and 1 subtype 1b). Two of 12 HCV RNA-positive participants had low antibody avidity values, suggesting recent HCV infection. HCV antibody seropositivity was significantly associated with older age >40 years, adjusted odds ratio (aOR) 3.56 (95% CI 1.57, 8.08), HIV-positive serostatus, aOR 3.18 (95% CI 1.40, 7.22), any sexually transmitted infection (STI) in the last 3 months, aOR 2.81 (95% CI 1.11, 7.13), and injection drug use (IDU) ever, aOR 4.34 (95% CI 1.69, 11.17). Mapping of HCV infections differed slightly by home, social, and sexual neighborhoods. Based on phylogenetic analysis from 12 HCV RNA-positive samples, no evidence of a clustered HCV epidemic was found. Overall HCV seroprevalence was 2.8% among community-recruited MSM in NYC, with higher prevalence among HIV-positive MSM compared to HIV-negative MSM. Only two participants were found to have recent HCV infection, with no evidence of a clustered HCV epidemic based on phylogenetic analysis. Our results support testing of HCV infection among HIV-negative MSM if they report having a recent STI and IDU in the past rather than universal HCV testing in all HIV-negative MSM.

Partial Text

Although primary transmission of hepatitis C virus (HCV) is through the parenteral route[1], epidemics of sexually transmitted HCV infection among men who have sex with men (MSM) have been reported in Europe, Australia, Asia, and North America, with blood remaining the likely medium for sexual transmission of HCV in these outbreaks[2–14]. These sexually transmitted HCV outbreaks have mostly involved HIV-infected MSM, with lower HCV infection rates in HIV-negative MSM[13, 15–26]. Many studies have also reported strong associations between HCV infection risk and sexual risk behaviors, including high number of sexual partners[10, 27], condomless anal sex[10, 11, 17, 27], recreational drug use during sex[10, 11], and traumatic sexual practices such as fisting[10, 27, 28]. In the Multicenter AIDS Cohort Study (MACS) study of HCV infections among HIV positive and HIV negative MSM in four U.S. metropolitan areas from 1984–2011, 115 cases of incident HCV infection were reported (incidence rate of 2.08/1,000 person-years [PYs]). In multivariate analysis, condomless receptive anal sex with more than one male partner, older age, HIV infection, heavy alcohol use, hepatitis B surface antigen positivity, and syphilis infection were significantly associated with incident HCV infection[17]. High rates of HCV reinfection of up to 15/100 PYs have been reported among HIV-infected MSM who had previously received successful HCV treatment or had spontaneously cleared their HCV infections[29–32].

The NYC M2M study was approved by the Institutional Review Board (IRB) of the New York Blood Center, and this identity unlinked substudy was also approved by the New York Blood Center IRB. No new samples or behavioral data were acquired for this substudy. All laboratory testing was performed in a research laboratory incapable of releasing results to patients or clinicians. All participants in the NYC M2M study were contacted by study staff upon completion of laboratory analyses with a summary of study findings and referral to various clinics in NYC for clinical HCV testing and medical management as needed.

Of 1,458 men enrolled in the NYC M2M study between 2010 and 2013, 1,030 (71%) consented to serum storage. Excluding two samples with insufficient serum volume for HCV lab analysis, 1,028 men were included. Of these 1,028 men, 79.7% were HIV-negative and 20.3% HIV-positive by testing and self-report (Table 1); 62 (6%) refused HIV testing, of whom 42% (26/62) self-reported being HIV-positive. Of 1,028 men tested, 29/1028 (2.8%) were HCV antibody-positive. Of these 29 who were HCV antibody-positive, 12/29 (41%) were HCV RNA-positive (11 subtype 1a and 1 subtype 1b). Two of 12 HCV RNA-positive participants had low antibody avidity values, suggesting recent HCV infection. Table 1 shows the HCV infection outcomes based on testing, stratified by HIV serostatus by testing and self-report at the NYC M2M study visit.

This study involving a large sample of community-recruited HIV negative and HIV positive MSM in NYC found an overall HCV seroprevalence of 2.8%. The community-recruited sample had a low prevalence of individuals who reported injecting drugs ever in the past of 5.2%, although they did report sexual risk behaviors that would place them at risk for sexual transmission of HCV, with 14.2% of the MSM reporting any condomless insertive anal sex and 16.8% reporting any condomless receptive anal sex with a male partner in the last 3 months. We found a higher HCV prevalence among HIV-positive MSM compared to HIV-negative MSM (8.1% vs. 1.5%, respectively, p = <0.001), consistent with previously published data showing higher rates of HCV infection among HIV-infected compared to uninfected MSM[13, 15–25]. Of the 29 men who were HCV antibody-positive in our study, only 12 or 41% were HCV RNA-positive, indicating chronic hepatitis C infection. Our HCV seroprevalence of 8.1% (17/209) among HIV-infected MSM is lower than what has been reported in the literature for NYC. In one study, the proportion of HCV infections among HIV-infected individuals in NYC who are MSM dramatically increased from 7% in 2000 to 24% in 2010[64]. In another NYC study from 1999–2007, 10.5% of HCV and HIV co-infected individuals were found to be non-IDU MSM; this study had an older sample of individuals with mean age of 50.4 years[65]. These rates are markedly higher than those reported in other U.S. cities, including San Francisco where HCV prevalence among non-IDU HIV-positive MSM decreased from 9% in 2004 to 2% in 2011[66, 67]. In conclusion, in a large community recruited sample of HIV-negative and HIV-positive MSM in NYC with low prevalence of IDU, overall HCV seroprevalence was 2.8%. A higher HCV prevalence was found among HIV-positive MSM compared to HIV-negative MSM. Of the 29 men who were HCV antibody-positive in our study, 12 or 41% were HCV RNA-positive, indicating chronic HCV infection. Only 2 recent HCV infections were detected based on HCV avidity testing, with no clustering of genetically linked HCV infections based on phylogenetic analysis. HCV antibody seropositivity was significantly associated having reported any recent STI, older age, IDU ever history, and HIV-positive serostatus. Our results support testing of HCV infection among HIV-negative MSM if they report having a recent STI and IDU ever in the past rather than universal HCV testing in all HIV-negative MSM.   Source: http://doi.org/10.1371/journal.pone.0200269