Sexual Seroadaptation: Lessons for Prevention and Sex Research from a Cohort of HIV-Positive Men Who Have Sex with Men

Introduction

Surveillance data on sexually transmitted infections (STIs) and results from behavioral studies of the risk of seroconversion have frequently been used as surrogate markers of trends in sexual behaviors that spread new HIV infections and signal changing trends in the HIV epidemic. The incidence of rectal gonorrhea among men who have sex with men (MSM) dropped precipitously with the onset of the AIDS epidemic in the 1980s. STIs, such as gonorrhea, usually become symptomatic soon after infection, and testing and treatment were simple and widely available, making STI surveillance an accessible indicator of HIV risk. At the same time, the rates of high-risk sexual behaviors and the incidence of HIV decreased [1]–[4]. Behavioral surveillance focusing on risk of seroconversion is relatively inexpensive and can be implemented with a wide variety of sampling strategies that can lead to findings that can be generalized. The concomitant decreases in the incidence of rectal gonorrhea, rates of high-risk sexual practices, and HIV incidence in the 1980s in San Francisco suggested that the former two measures were good surrogate indicators of potential trends in HIV incidence.

By the mid-1990s, behavioral studies revealed increasing rates of sex unprotected by condoms among MSM, and STIs rose accordingly [5], [6]. For example, from 1993 to 1999 in San Francisco, the proportion of MSM reporting multiple partners and unprotected intercourse increased while those reporting always using condoms dropped, and the rates of rectal gonorrhea rose [7]. However, more direct measures of HIV incidence in San Francisco did not show a concurrent increase [6]–[10]. This apparent discrepancy may have reflected changes in the infectivity of HIV due to widespread treatment [11] or other factors that specifically inhibited new HIV infections independently of other STIs.

However, changes in sexual mixing based on HIV-1 status could also partially explain discrepancies between trends in HIV and other STIs. Sexual behaviors adapted to the risk of HIV developed quickly among MSM in San Francisco, including abstinence, reduction in numbers of partners, avoiding anal sex, and condom use, and was credited with dramatic reductions in HIV incidence density before the end of the 1980s [1], [2].

The HIV epidemic has engendered an unprecedented sexual behavior surveillance infrastructure; a likewise unprecedented and large body of research on specific sexual practices, especially unprotected anal intercourse (UAI) among MSM has resulted. However, research that narrowly trained its sights on practices that could spread the epidemic was poorly suited to measure the role of behavior change in inhibiting the spread of the epidemic [12] ^(p71). Special adaptive strategies might be particularly relevant in communities in which the members correctly perceive themselves to be at risk of acquiring or transmitting infection. Newer trends in behaviors, discussed by French activists and intellectuals under the term “seroadaptation,” might reverse trends toward fewer partners and more condom use without concomitant increases in HIV incidence [13].

Data from a population-based sample of MSM living in California in 2002 led researchers in 2006 to conclude that knowledge of sexual partner’s serostatus was associated with sexual practices frequently indicating an apparent seroadaptive strategy to reduce the risk of transmission without necessarily limiting numbers of partnerships or ruling out UAI. Serosorting, generally understood to refer to the selection of only concordant-serostatus partners, at least for UAI, was only one tactic characteristic of this seroadaptive strategy. While MSM often chose partners of discordant or unknown status those partnerships were less likely to involve anal intercourse or more likely to include condom use [14].

First described as a harm-reduction strategy in an Australian study, “strategic positioning” was another seroadaptive tactic in which an HIV-positive individual assumed the receptive role during UAI with a negative or unknown-status partner [15]. Because the risk of transmission from a receptive to an insertive partner during unprotected anal intercourse is minimal compared to the obverse [16]–[18], strategic positioning was another adaptive behavior that could mediate HIV incidence.

Other evidence of seroadaptation had been documented before the cohort study reported here although not in these terms. Limited serosorting was reported for Austrailian MSM between 1986 and 1991 [19]. In 1991–1992, 9% of a sample of HIV-positive MSM in Los Angeles reported insertive UAI and were more likely to do so with HIV-positive partners (odds ratio, 3.27) [20]. During the same period in the United Kingdom, one study found that in 15% of partnerships the serostatus of both partners was known to the respondent. Among this group, HIV-positive MSM were more likely to have UAI with HIV-positive MSM and less so with HIV-negative MSM (odds ratio, 1.64 vs. 0.24, p<.05) than with unknown-status partners [21]. During the latter half of the 1990s, patterns of serosorting and strategic positioning were evident in HIV-positive MSM in San Francisco and New York, even though the samples excluded the most successful seroadapters—those who reported no unprotected intercourse with negative or unknown-status partners [22]. In 1992, Hoff et al. found UAI much more likely to occur in seropositive concordant rather than discordant relationships (54% vs. 17%) among MSM in Portland, Oregon, and Tucson [23]. These examples are not an exhaustive list.

However, the present study is the first in which the data collection methodologies and analytic frameworks were chosen for the specific purpose of learning the degree to which seroadaptive tactics arose among sexual partnerships defined as at high-risk for HIV-transmission (involving HIV-positive MSM who practice UAI) that eluded both public health-sanctioned messages and empirical detection. It is also a unique effort to assess the potential impact of such tactics on decreasing exposures that might lead to transmission of new HIV infections. Whether this HIV prevention strategy arose from “grassroots” origins and, especially if they are effective, a theoretical question is raised: Do such tactics add up to a community-based prevention strategy? And under what conditions can they appear? Answers to these questions have bearing on the development of HIV prevention policy and programs.

As early as the mid-1980s, epidemiologists were using sexual mixing–based models of the epidemic that drew heavily on the theory and methods of social network research [24]–[29]. Social network studies have three fundamental characteristics: relationships rather than individuals are studied, relationships between individuals can be drawn or graphed in “sociograms” that illustrate social structure, and social structure can therefore be subjected to mathematical analysis and modeling. An advantage of these methods in studies of HIV seroincidence or superinfection is that exposure data are collected partner by partner, and the characteristics of each partner are documented separately. Thus, one can determine if partnership characteristics predict sexual risk and compare different analytic approaches to see how well they represent sexual risk in the sample overall.

Methods