The 902 MSM surveyed by TACASI had a median age of 47 years, median CD4 count of 527 cells per cubic millimeter, 95% were prescribed HAART, and 78% (n = 704) reported having sex in the past 6 months. The characteristics of 704 sexually active MSM are detailed in Table 1. Among these 704 MSM, 649 (92%) reported engaging in any unprotected sex in the past 6 months: 54% reported any unprotected anal sex (37% as insertive partner, 42% as receptive partner), 92% reported any unprotected insertive or receptive oral sex, and 1% unprotected insertive vaginal sex (Fig. 2). Substantial fractions of these MSM engaged in unprotected anal sex with male partners who were HIV-negative (21%) or of unknown serostatus (31%): 24% practiced any unprotected anal sex as the insertive partner and 31% any anal sex as the receptive partner (Fig. 2).
In multivariable analyses of sexually active MSM, engaging in any unprotected anal sex with an HIV-negative or unknown-status male partner within the past 6 months was associated with age <50 years [≤29 years adjusted OR (aOR) = 2.1, P = 0.07; 30–39 years aOR = 2.1, P = 0.002; 40–49 years aOR = 1.6, P = 0.018 compared with ≥50 years], injection drug use (IDU) risk (aOR = 4.7, P = 0.020), having >1 sexual partner (2 partners aOR = 2.4, P ≤ 0.001; ≥3 partners aOR = 5.5, P ≤ 0.001) and disclosing HIV status to only some but not all sexual partners (no partners aOR = 0.8, P = 0.34; some partners aOR = 1.6, P = 0.008; Table 2). Viral load level, ARV adherence, race/ethnicity, alcohol and IDU, CD4 count, HIV VL, and ARV experience were not associated with engaging in unprotected anal sex with HIV-negative or unknown-status male partners.
In the analyses for a subset of 604 MSM who engaged in unprotected sex and also had proximally measured HIV VL available, 90 (14.9%) had a plasma HIV VL ≥400 copies per milliliter; only 41 of these men (46%) were receiving ARV therapy at the time of their TACASI. Sexually active MSM with viral loads <400 copies per milliliter did not differ from MSM with viral loads ≥400 copies per milliliter with respect to the frequency of unprotected sex behaviors, except for unprotected insertive oral sex with HIV-negative partners, which was less common among men with viral loads ≥400 copies per milliliter (Table 3).
Previously reported rates of unprotected anal sex among HIV-infected MSM in the United States have varied widely according to the methods and time frame used to capture the events.13,21,26,27 In the HOPS, the majority of HIV-infected MSM responding to an anonymous survey administered during 2007–2010 engaged in unprotected anal or oral sex placing them them and their partners at risk for HIV and STD infection. Indeed, in our cohort, 54% of MSM reported any unprotected anal sex in the past 6 months (35% with a male partner who was HIV-positive, 21% with a male partner who was HIV-negative, and 31% with a male partner of unknown serostatus). Our estimates are somewhat higher than those derived from a previous large meta-analysis among HIV-infected MSM in the United States, where overall 43% of MSM reported unprotected anal sex (in the prior 1–12 month timeframe): 30% with an HIV-positive, 16% with a male partner of unknown serostatus, and 13% with a male partner who was HIV-negative.20
Based on our analyses of a subset of MSM participants for whom risk behavior and viral load data were available, our findings also highlight the HIV transmission potential posed by the 15% of MSM who had unprotected sex and whose most proximal HIV VL was ≥400 copies per milliliter. Reassuringly, we observed no difference in the percentages engaging in high-risk anal sex by HIV VL (<400 vs ≥400 copies per milliliter). More than half of the MSM who practiced unsafe sex and had HIV VL ≥400 copies per milliliter were currently not receiving ARVs (Fig. 1, footnotes b and c), and these men would be potential candidates for initiating or resuming treatment for prevention of HIV transmission to sexual partners under the current US Department of Health and Human Services HIV treatment guidelines.10,27
Our findings are consistent with those from an earlier US meta-analysis that found that HIV-infected persons with undetectable viral loads were not more likely to engage in unprotected sex than HIV-infected persons with detectable viral loads.26 We identified several factors associated with unprotected insertive or receptive anal sex with HIV-negative or unknown-status male partners. HIV-infected MSM under the age of 50 years were more likely to engage in unprotected anal sex with an HIV-negative or unknown-status male partner than MSM who were aged 50 years and older. This difference may reflect a greater likelihood for older individuals to be in stable, monogamous partnerships (57% of MSM age ≥50 years were not sexually active or had a single sexual partner in the past 6 months compared with 47% of MSM age <50 years), a cohort-calendar effect (ie, survivors of the early phase of HIV epidemic in the United States may be more cautious than younger counterparts), or other factors that we did not measure. The trend toward increasingly less unprotected sex among HIV-infected MSM and other HIV-infected older persons has also been reported elsewhere.28,29
Injection drug users were also more likely to report unsafe sexual behaviors than were noninjection drug users. Injection drug users may have been more likely than nonusers to encounter situations (eg, impaired judgment from drug use, transactional sex) where they are unable to negotiate or assert safer sexual practices. Additionally, HIV-infected MSM with >1 sexual partner in the preceding 6 months and those who disclosed their HIV status to only some and not all of their sexual partners were more likely to engage in unprotected anal sex with an HIV-negative or unknown-status male partner. Although we do not have additional information to explain these results, it is plausible they reflect behaviors of MSM who meet multiple partners via the Internet or in sex venues where conversations regarding HIV serostatus may or may not take place.30–33
Our analysis had a number of limitations. The behavioral survey was collected from a convenience sample of volunteer respondents, which could have introduced 2 forms of bias. First, we may have underestimated or overestimated the percentage of HOPS patients (including MSM) who engaged in risky sexual behavior, as the persons who completed TACASI differed from those who did not complete the survey by a number of demographic characteristics (please see the Results section). Second, although ACASIs are considered to be among the most reliable methods for capturing complete and accurate data on sensitive behaviors, including unprotected sexual intercourse,34–37 underreporting bias of socially undesirable risk behaviors may have occurred, even though we tried to preclude this bias by assuring participants that their responses will not be shared with their treating clinicians. We do not have information about patients' previous sexual partners beyond the total number and therefore are neither able to make distinctions between primary partners or casual partners, nor ascertain if these sexual partners were consecutive or concurrent. Additionally, among survey respondents with multiple partners, we do not know if these persons were encountered anonymously or if they were known individuals within the patients' sexual networks. Due to the composition of the HOPS cohort, which tends to be primarily non-Hispanic white MSM, our findings may be less generalizable to the larger population of HIV-infected persons in the United States, particularly, those persons who are not engaged in routine care and who are persons of color. Finally, because we have so few ARV-naive study participants, we were not able to adequately ascertain if sexual risk behavior was associated with ARV experience.
Despite these limitations, a notable strength of our analysis was the capacity to link and jointly analyze risk behavior data and clinical data. We suggest that an area of fruitful investigation in studies where behavioral and clinical data are linked would be to assess the extent to which patients' awareness of their HIV VL affects sexual behavior or survey responses about sexual behavior.
In summary, among HIV-infected MSM in care, we observed that over half engaged in unprotected anal sex in the preceding 6 months, especially MSM aged <50 years and MSM with multiple sexual partners; however, patients with elevated HIV VL were no more likely to potentially expose sexual partners to HIV than patients with HIV VL <400 copies per milliliter. Targeted interventions in the routine care of HIV-infected individuals can be effective in reducing the risk of secondary HIV transmission.38–40 Our findings support the current recommendations25,38,41 for HIV care providers to offer to their HIV-infected patients risk behavior screening, referrals to more intensive counseling as warranted, and ARV therapy for the prevention of sexual HIV transmission.27
HIV OUTPATIENT STUDY INVESTIGATORS
The HOPS Investigators include the following persons and sites:
John T. Brooks, Kate Buchacz, Marcus D. Durham, Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention (NCHSTP), Centers for Disease Control and Prevention (CDC), Atlanta, GA; Kathleen C. Wood, Rose K. Baker, James T. Richardson, Darlene Hankerson, Rachel Debes, Carl Armon, Bonnie Dean, and Sam Bozzette, Cerner Corporation, Vienna, VA; Frank J. Palella, Joan S. Chmiel, Carolyn Studney, Onyinye Enyia, and Tiffany Murphy, Feinberg School of Medicine, Northwestern University, Chicago, IL; Kenneth A. Lichtenstein and Cheryl Stewart, National Jewish Medical and Research Center Denver, CO; John Hammer, Kenneth S. Greenberg, Barbara Widick, and Joslyn D. Axinn, Rose Medical Center, Denver, CO; Bienvenido G. Yangco and Kalliope Halkias, Infectious Disease Research Institute, Tampa, FL; Doug Ward, Troy Thomas, and Rob Grant, Dupont Circle Physicians Group, Washington, DC; Jack Fuhrer, Linda Ording-Bauer, Rita Kelly, and Jane Esteves, State University of New York (SUNY), Stonybrook, NY; Ellen M. Tedaldi, Ramona A. Christian, Faye Ruley, Dania Beadle and Princess Graham, Temple University School of Medicine, Philadelphia, PA; Richard M. Novak and Andrea Wendrow and Renata Smith, University of Illinois at Chicago, Chicago, IL; Benjamin Young, Barbara Widick, Joslyn Axinn, APEX Family Medicine, Denver, CO.
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