In the first decade of the HIV epidemic, significant declines in high risk sexual behaviors and HIV incidence were documented among homosexual men in the USA and elsewhere [1–4]. In the Multicenter AIDS Cohort Study (MACS), one of the largest studies of homosexual men, HIV incidence decreased dramatically from 4–8 per 100 person years (py) during 1984–1985, and fluctuated between 0.5 and 2.5 per 100 person years in the late 1980s to mid 1990s [2,5].
Beginning in 1996, the advent of highly active antiretroviral therapy (HAART) led to impressive declines in HIV-associated morbidity and mortality [6,7]. More recently, concerns have surrounded the potential for these therapies to contribute to complacency towards HIV/AIDS among the homosexual community, with an unintended consequence being relapse towards unprotected anal sex [8–10].
Some cities in North America have reported increased rates of HIV infection and sexually transmitted diseases (STD) among homosexual/bisexual men [11,12]. Some studies suggested that virologic and clinical improvements due to HAART may influence sexual behaviors among homosexual men [10,13] but few studies have systematically studied this phenomenon. In particular, HIV-infected and uninfected persons may respond differently in the era of HAART.
We investigated attitudinal and health factors associated with unprotected anal sex among HIV-infected and uninfected homosexual men since the introduction of HAART. Our study population, comprised of homosexual men in four large metropolitan areas, provide new findings particularly relevant for developing timely behavioral interventions.
In 1984–1985 and 1987–1991, 5622 homosexual men were enrolled in the MACS at four locations: Baltimore, Maryland; Chicago, Illinois; Los Angeles, California; and Pittsburgh, Pennsylvania. Details on MACS recruitment and data collection have been published elsewhere . Our study sample was restricted to participants who attended the MACS semiannual visit during April–September 1999 and reported engaging in insertive anal sex (IAS) or receptive anal sex (RAS) in the past 6 months.
Participants completed a 20-item survey including personal attitudes towards HAART and risk behaviors, sensation seeking, and safer sex fatigue. Respondents were asked to express disagreement or agreement with each statement on a 5-point Likert scale (1 = strongly disagree to 5 = strongly agree). Responses were categorized as belonging to one of five subscales based on previous validation studies [15–17]. Reduced HIV concern (e.g., ‘Because of combination drug treatments for HIV, I am less concerned about becoming HIV positive or infecting someone'; Cronbach's α, 0.85); substance use sexual expectancies (e.g., ‘When I am high or drunk I find it more difficult to stay within my sexual limits'; Cronbach's α, 0.81); safer sex fatigue (e.g., ‘I feel tired of always having to monitor my sexual behavior'; Cronbach's α, 0.73); viral load/transmission beliefs (e.g., ‘It would be more difficult for an HIV-positive person to infect a partner through unsafe sex if the HIV-positive person was taking combination drug treatments’ Cronbach's α, 0.83); and sexual sensation seeking (e.g., ‘I like wild ‘‘uninhibited’’ sexual encounters'; Cronbach's α, 0.81).
Categorical scores on the attitudinal subscales were compared among men who reported engaging or not engaging in unprotected RAS and IAS, stratified by HIV-serostatus. Logistic regression models were developed to identify correlates of unprotected RAS and unprotected IAS. Multivariate models adjusted for age; among HIV-positive men, we also adjusted for most recent CD4 cell count, HIV-1 viral load, and use of HAART [18,19]. Statistical significance was defined as P < 0.05.
We also determined whether men who experienced a sudden decrease in HIV-1 RNA levels below the standard limit of detection (400 copies/ml) were more likely to engage in unprotected anal sex. This analysis was restricted to 184 men who initiated HAART prior to September 1998, who could have known if they had a subsequent change in HIV RNA detectability.
Of 1156 men attending visit 31, 611 (52.9%) reported having either RAS or IAS in the prior 6 months and were thus eligible for this analysis. Of these, 547 men (89.5%) completed the attitudinal survey (218 HIV-negative and 329 HIV-positive). Compared to the 64 sexually active men who did not complete the attitudinal survey, the 547 men did not differ significantly by HIV serostatus, race, income or reports of RAS and IAS. However, men in the study sample were slightly older (mean, 45.1 versus 43.1 years;P = 0.02) and reported a greater number of male partners in the prior 6 months (median, 4.0 versus 2.5;P = 0.03), respectively. We also compared demographic and behavioral data for the study sample to that of the 938 men (353 HIV negative and 585 HIV positive) completing the attitudinal survey (data not shown). The study sample did not differ significantly from the total who completed the survey by age, race, income, or number of male partners in the prior 6 months. Of the 547 men included in our analyses, 82% were white.
Comparing subgroups of men within the study sample, there were some slight differences by HIV serostatus. HIV-negative men were older than HIV-positive men (mean, 46.6 versus 44.1 years;P < 0.01) and reported more male partners in the past 6 months (median, five versus four partners;P = 0.02). However, there were no significant differences in the proportions that reported unprotected IAS and RAS by HIV serostatus.
Duration of study participation was also similar (mean, 14 years). Clinical characteristics of HIV-positive men engaging in anal sex did not deviate appreciably from all HIV-positive men completing the attitude survey.
Among HIV-positive men, reduced HIV concern, substance use-related sexual expectancies, safer sex fatigue, viral load/transmission beliefs and sensation seeking were all significantly associated with unprotected IAS, as was having a known HIV-positive sexual partner. Among HIV-negative men, reduced HIV concern and having a primary partner was significantly associated with unprotected RAS; having a casual partner was inversely associated with RAS (Table 1).
In multivariate logistic regression models, HIV-positive men who had the highest scores (i.e., upper quartile) for reduced HIV concern were six times more likely to engage in unprotected IAS, compared to those in the lower quartile (Table 2). Safer sex fatigue was also independently associated with unprotected IAS. Not surprisingly, HIV-positive men were much more likely to report unprotected IAS if they had a known HIV-infected sexual partner. Independent predictors of unprotected RAS among these HIV-infected men were similar (data not shown). Current or lagged (visit 30) measures for HIV-1 viral load or CD4 cell count were not significantly associated with unprotected IAS or RAS.
Among HIV-negative men, those with moderate or high scores indicating reduced HIV concern were significantly more likely to report engaging in unprotected RAS (Table 1). HIV-negative men were significantly less likely to report unprotected RAS if they reported having more than one casual male sexual partner in the past 6 months. Findings for unprotected IAS were similar (data not shown).
We tested the hypothesis that a favorable change in HIV-1 viral load (i.e., decrease from detectable to undetectable levels) would be associated with unprotected anal sex. Of 184 men, 107 (58.2%) had detectable viral loads prior to HAART which subsequently decreased to undetectable levels. Contrary to expectation, in multivariate models controlling for the variables described in Table 2, men who experienced a decrease in HIV RNA to below the level of detection were somewhat less likely to engage in unprotected IAS or RAS, but not significantly so [adjusted odds ratio (AOR), 0.55; 95% confidence interval (CI), 0.22–1.37; and AOR, 0.84; 95% CI, 0.38–1.85, respectively).
Despite reductions in HIV risk behaviors observed earlier in the epidemic, approximately half of the HIV-negative and HIV-positive homosexual men in the MACS who reported recently having anal sex did not consistently use condoms. Recent increases in the incidence of HIV and STD have also been documented among homosexual men in other settings, suggesting that this may be a widespread phenomenon [10,12,20].
Among HIV-positive men, decreased concern about infecting someone due to availability of HAART was associated with a three- to sixfold higher odds of unprotected IAS. Similarly, decreased concern about becoming HIV infected due to availability of HAART was independently associated with unprotected RAS among HIV-seronegative men. Our findings suggest that the effect of safer sex fatigue or burnout is more pronounced among HIV-seropositive men relative to HIV-seronegative men, among whom it was a key factor associated with sexual risk taking. These data raise considerable public health concerns regarding the potential for increased HIV transmission among homosexual men in countries where HAART is widely used. Although optimal adherence to HAART can significantly reduce plasma HIV-1 levels, a substantial proportion of patients may be infectious or harbor HIV-1 drug-resistant strains .
As an alternative to promoting consistent condom use, some authors have proposed a role for practicing ‘negotiated safety’ (i.e., unprotected sex within the context of a relationship where both partners’ HIV status is concordant) . We found that HIV-positive men were more likely to engage in unprotected IAS if their partner was also HIV-infected, perhaps under the assumption that re-infection is not a health risk. While the health risks due to re-infection with another HIV subtype are speculative, STD transmission risks persist.
One potential form of negotiated safety could take into account the insertive partner's viral load when deciding whether or not to use a condom during anal intercourse. We tested this hypothesized determinant of unprotected sex and were unable to confirm that men who experienced a dramatic decrease in viral load to below detectable levels were more likely to engage in unprotected anal sex. This is consistent with results from a community-based sample of HIV-positive men in Chicago,  but is contrary to a recent report on homosexual men in Amsterdam .
Our results may underestimate the extent to which attitudes about HAART have influenced rates of unprotected anal sex and changing community norms regarding safer sex. Earlier in the epidemic, HIV-positive and HIV-negative men in the MACS had significantly reduced their levels of unprotected anal sex . The finding that at least some of these men are now increasingly engaging in unprotected anal sex raises concerns about trends among the general population of homosexual/bisexual men. However, as we restricted our study sample to men who currently engaged in anal sex, our findings may not extend to men who engage in other sexual activities.
Our findings support the importance of attitudes as determinants of sexual behavior and behavioral change [3,24]. Attitudinal factors that arose in part due to reductions in morbidity and mortality in the era of HAART were significantly associated with sexual risk taking among both HIV-positive and HIV-negative men. It is therefore important to measure such attitudes directly when designing and evaluating behavioral interventions.
The advent of HAART has had a significant impact on the attitudes and behaviors of both HIV-positive and HIV-negative sexually active men participating in the MACS. Our findings are consistent with recent studies from San Francisco that indicate that the beneficial effect of HAART on reducing HIV incidence has been counterbalanced by an increase in high risk behavior [12,20,25,26]. These findings emphasize the need to tailor prevention programs towards men's HIV serostatus, partnerships, and risk-taking propensities.
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