Objectives: Assess behavior change of recently HIV-infected men who have sex with men (MSM).
Methods: From 2002 to 2006, 193 recently HIV-infected MSM in the Southern California Acute Infection and Early Disease Research Program were interviewed every 3 months. Changes in HIV status of partners, recent unprotected anal intercourse (UAI), drug use, use of antiretroviral therapy (ART), detectable viral load, and partnership dynamics over 1 year were used to predict recent UAI in a random effect logistic regression.
Results: Over a year significantly fewer partners in the past 3 months were reported (mean 8.81 to 5.84; P < 0.0001). Percentage of recent UAI with HIV-status unknown last partners decreased from enrollment to 9 months (49%-27%) and rebounded at 12 months to 71%. In multivariable models controlling for ART use, recent UAI was significantly associated with: baseline methamphetamine use [adjusted odds ratio (AOR): 7.65, 95% confidence interval (CI): 1.87 to 31.30], methamphetamine use at follow-up (AOR: 14.4, 95% CI: 2.02 to 103.0), HIV-uninfected partner at follow-up (AOR: 0.14, 95% CI: 0.06 to 0.33), and partners with unknown HIV status at follow-up (AOR: 0.33, 95% CI: 0.11 to 0.94). HIV viral load did not influence rate of UAI.
Conclusions: Transmission behaviors of these recently HIV-infected MSM decreased and serosorting increased after diagnosis; recent UAI with serostatus unknown or negative partners rebounded after 9 months, identifying critical timepoints for interventions targeting recently HIV-infected individuals. There was no evidence in this cohort that the viral load of these recently infected men guided their decisions about protected or unprotected anal intercourse.
From the *Department of Epidemiology, School of Public Health, University of California, Los Angeles, CA; †Department of Biostatistics, School of Public Health, University of California, Los Angeles, CA; ‡Department of Medicine, Centre for Infection Prevention and Management, Imperial College London, London, United Kingdom; §Department of Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA and the David Geffen School of Medicine, University of California, Los Angeles, CA; and ∥Department of Medicine, Antiviral Research Center, University of California, San Diego, CA.
Received for publication May 7, 2010; accepted October 1, 2010.
Supported by the NIH AI43638, AI074621 and UARP (CHRP) ID01-SDSU-056 and RN07-SD-702.
The authors have no conflicts of interest to disclose.
Correspondence to: Pamina M. Gorbach, MHS, Dr.PH, Associate Professor, Department of Epidemiology, Behavioral Epidemiology Research Group, University of California, Los Angeles-CHS 41-295, Box 951772, Los Angeles, CA 90095-1772 (e-mail: firstname.lastname@example.org).
Incident HIV infections among men who have sex with men (MSM) in the United States continue to be high.1,2 Individuals with recent or primary HIV infection often participate in risky activities although having high levels of plasma HIV RNA and therefore are highly infectious to others.3-7 Mathematical models of male-to-male sexual transmission of HIV suggest that between 25% and 47% of new infections may be transmitted from those with primary infection.8,9 The latest report from the US Centers for Disease Control and Prevention indicates a higher incidence of HIV in the United States than previously estimated; with one third of adults newly diagnosed with a recent infection.10 These studies suggest that early detection of HIV infection and then prevention of unprotected sex among those with recent infection is likely to be an important component of efforts to control the MSM HIV epidemic in the United States.
Our previous research on recently HIV-infected MSM revealed a wide variation in the types of partnerships reported after diagnosis and changes in both the number of partner types and risk behaviors practiced with different types of partners.11 These findings were limited to the first 3 months after diagnosis with recent infection. Other research indicates that behavior varies by partner type; more HIV-infected MSM report unprotected anal intercourse (UAI) in stable or main partnerships than in shorter term or less intimate partnerships,12-15 although the evidence is mixed.16 Nevertheless, more than half of transmissions among MSM in the United States were estimated to be between main partners.17 Higher transmission of HIV within main partnerships has also been observed among MSM in Europe18 and more recently among women in Africa.19 However, HIV-infected MSM do seem to adjust their behaviors by the HIV status of their partners; fewer report UAI with serodiscordant than seroconcordant partners reported to be “regular partners”.20 The pattern is less clear for partners referred to as “nonregular partners”.
Driving HIV transmission among MSM in the United States is the interplay between drug use and sexual behavior. Before sex, drug use can diminish the correlation between intimacy and risk behavior within couples, suggesting that drug use affects relationship dynamics.21 Drug intoxication affects individual's abilities to negotiate and correctly use condoms. In fact, some MSM report using drugs in sexual settings specifically to be able to disregard concerns about HIV transmission.22 Among MSM, reported use of stimulants have been associated with incident HIV infection23 and those who report using stimulants during sex are more likely to report high-risk behaviors such as UAI.24-26 Although fewer methamphetamine-using HIV-infected men have reported UAI with HIV-uninfected partners, more reported UAI if the HIV-uninfected or status unknown partners were anonymous partners.27
In Southern California, in particular, use of methamphetamine has been demonstrated to be a significant factor driving continuing transmission of HIV among MSM.28 Our earlier work demonstrated the association between methamphetamine use, high-risk behavior and the acquisition of HIV in this cohort.29,30 Although it is known how drug use influences HIV acquisition, the role drug use plays in behavior of HIV-infected men who know their status and the status of their partners is less clear.
There has been limited research examining the sexual behaviors and drug use of individuals recently infected with HIV.18,19,30-32 We analyzed sexual behaviors and partnering patterns in a cohort of MSM with recent HIV infection during their first year after diagnosis to determine the effects of partner type, partnership stability, partner charactersitics, including serostatus, and drug use on the reported practice of transmission-associated behaviors such as UAI.
The Southern California Acute Infection and Early Disease Research Program recruited, enrolled, and collected biological data on a cohort of recently HIV-infected individuals (infection within the past 12 months). Between 2002 and 2006, 225 HIV-infected MSM completed baseline questionnaires to assess HIV risk behavior by computer-assisted self-interview as previously described.11 The men were offered interviews every 3 months in their first year enrolled in the Acute Infection and Early Disease Research Program cohort. As previously reported, in this cohort, date of infection was estimated from last HIV-negative test result and serology and was a mean of 13weeks (median, 14 weeks) before the baseline study questionnaire was completed; date of HIV diagnosis was established through review of medical records and assigned as the first positive HIV test that was reported to the participant and was a mean of 5 weeks (median, 3 weeks) before the baseline questionnaire was completed.30 The results reported in this analysis reflect behavior changes from the date of enrollment, when detailed behavioral data were collected in the baseline questionnaire.
Detailed questions were asked at baseline about last 3 sexual partners and at follow-up interviews only on the last partner. At all timepoints, men were asked to also report in detail about a main partner (if they had one), if he was not reported as a last partner (follow-up), or one of the last 3 partners (baseline). Information included partner characteristics, types of sexual activity, types of substances used just before and during sexual activity at last sex, and types of substances ever used with that partner for baseline, in the last 3 months and at all follow-up interviews. “Persistent partners” were those partners reported on in a previous interview ascertained in response to a direct question about each reported partner “is this a partner you told us about before” and collection of initials for each partner.
A scale that summarizes the intimacy level of partnerships specific to MSM called the “Partnerships Assessment Scale” (PAS) was included and found to be highly reliable with a Cronbach's Alpha of >0.94 for each partner type at baseline and during follow-up. PAS is generated by adding 27 binary variables resulting in a minimum score of 0 and maximum of 27. The questions ask about amount and type of contact, knowledge about partner's life, and social activities conducted with each partner and are assigned a value for each activity with the final score representing a sum of these items. The PAS was analyzed as a continuous variable for associations with risk behavior. We also assessed changes over time in types of partners reported, numbers of partners, and drug use.
Follow-up behavioral data was available for analysis on 193 men and their reports on 1011 partners during the year after enrollment in the study. Not all data is available for all 1011 reported partners due to participants skipping questions (ie, refuse to answer); missing data was not imputed. We compared those who completed only a baseline interview (n = 225 provided complete data) to those who completed at least 1 follow-up interview (n = 193) and found the only statistically significant differences were there were more men of “other” ethnicity who reported UAI at baseline and dropped out than who continued. There were no differences within the 193 men by demographic characteristics or risk behaviors including practice of UAI, use of methamphetamines, and numbers of partners between those who stayed in the study for 12 months (n = 55) and those who remained for less than 12 months (n = 135). Among those completing a baseline and at least 1 follow-up interview, 597 baseline partners were reported and 414 partners were reported at 3 months or more postdiagnosis; more than 98% of reported partners were male. At each follow-up, there were fewer respondents and they provided complete information on fewer partners (Table 1). A total of 562 interviews were collected from a median of 2 follow-up visits. The participants' viral load and use of antiretroviral therapy (ART) at each visit was acquired from the clinical record of the visit on the date of the behavioral interview (or the most recent prior clinical visit) and was available for 187 of the 193 individuals at baseline and for 554 visits.
Analyses were conducted using generalized linear random effects models to account for the correlation among reports from the same individual over time. A random effects logistic regression of reported recent UAI with separate, but correlated random effects for baseline and for follow-up was used to assess the association with individual and partner characteristics including PAS, types of partners reported, methamphetamine use, and use of ART. Numbers of partners reported was not significant in bivariate analysis and not included in the final model. As viral load and use of ART are highly correlated, only use of ART was included in the model as it represented the behavioral aspect of medication. Models were fit using SAS Proc Glimmix (SAS Institute, Cary, NC).
The men in this cohort had a mean age of 35 years (range at baseline of 19-64), were mostly white (71%) and Hispanic (21%) and were highly educated (88% had at least some college education). They reported a mean of 8.8 partners in the last 3 months at baseline (range 0-30, median 4). Twenty two percent (n = 42) had a main partner at baseline but did not report a continuing partner in any follow-up interviews; 29% (n = 56) had a main partner at baseline and reported at least 1 continuing partner in at least 1 follow-up interview; 32% (n = 62) had neither a main partner at baseline nor any main partner reported in a follow-up interview; and 17% (n = 33) did not have a main partner at baseline but reported a new main partner in at least 1 follow-up interview. During the year of follow-up, only 3 men reported abstinence in the 3 months before the interview and none reported abstinence at more than 1 visit or for the duration of the study.
Over the year after diagnosis, there was a significant decrease in the numbers of partners reported in the past 3 months from 8.81 to 5.84 mean partners (P < 0.0001) when time since baseline interview was analyzed as a continuous variable. When time since baseline interview was rounded to the nearest 3 months (Fig. 1), the most significant drop in number of sex partners was shown to occur from baseline to 3 months [rate ratio (RR): 0.71, P < 0.0001, 95% confidence interval (CI): 0.65 to 0.78]. Further changes were not significant but showed decreasing trends through month 9: RR: 0.97 (95% CI: 0.86 to 1.10) from months 3 to 6, RR: 0.88 (95% CI: 0.76 to 1.02) from months 6 to 9, and RR: 1.17 (95% CI: 0.98 to 1.39) from months 9 to 12. Overall a significant decrease of 27% (95% CI: 20% to 32%) was detected from baseline to follow-up in the number of partners reported in the last 3 months (P = 0.0005).
Over the year, more men reported their last partner was a main partner than any other partner type, followed by unknown partners (Fig. 2). The percent of men who reported any main partner significantly increased from 20.4% to 47.6% (P < 0.0001); unknown and 1-time partners decreased over time (P = 0.0014 and .0004, respectively). The largest increase in number of MSM reporting main partners occurred between baseline and 3 months (P = 0.0002), the differences between other consecutive visits were not significant, however, the difference from baseline to follow-up was significant [odds ratio (OR): 0.73, 95% CI: 0.68 to 0.80]. Main partners were most frequently the last partner and the proportion of these increased slightly over the year. The percent of last partners who were unknown or anonymous partners decreased slightly over time (Fig. 2).
Over the year of follow-up, participants reported the HIV status of their partners. Among the 252 main partners with HIV status reported, more than half were reported to be HIV uninfected (56%), a third as HIV positive, and the fewest as HIV status unknown (11%). Among the 646 nonmain partners with HIV status reported, about a third were reported as HIV uninfected, almost 20% as HIV positive and almost half reported that they did not know the HIV status of these partners (47%). Overall, the percent reporting the use of methamphetamines during last sex decreased, yet UAI increased among those that did report methamphetamine use (Table 1).
During follow-up interviews, condom use during anal intercourse with last partner was reported for 414 partners. More men reported not using condoms (ie, UAI) with an HIV-infected partner at any time point than reported UAI with either an uninfected or status unknown partner. For those reporting UAI with HIV-uninfected partners, there was more UAI with main versus nonmain HIV-uninfected partners, with a slight trend toward less UAI; 94% at baseline to 90% at 1 year versus 62% at baseline to 55% at 1 year, respectively, For UAI with HIV-uninfected main partners the pattern was the same, 67% at baseline to 64% at 1 year for main partners and 54% to 38% for nonmain partners. For those with partners of unknown HIV status, there were too few reporting main partners to report a trend. UAI with nonmain partners of unknown HIV status decreased until 9 months when it increased, 51% at baseline to 40% at 9 months and then 67% at 12 months.
When UAI with last partner was assessed by HIV status of partner the percent reporting UAI at last sex at baseline or since last interview at follow-up with a partner who was HIV uninfected or unknown decreased from 42% at baseline to 29% at 6 months, 23% at 9 months but then rebounded at 12 months to 50%. Figure 3 shows UAI separately for HIV negative and unknown partners. It should be noted that by month 12, UAI was entirely with HIV status unknown partners and none reported with HIV-uninfected partners.
The PAS was administered to provide a quantitative measure of the amount of intimacy within a partnership for each category of partnership asked about. Overall, the mean PAS was 12.4 and increased from 10.3 at baseline to 15.9 at 1 year (Table 1). The minimum, maximum, and mean for main partners were 0, 27, and 22.3, respectively. PAS was significantly lower for those that use methamphetamine with their partner than for nonusers (mean PAS of 8.1 vs. 13.1; P < 0.001).34 A higher PAS was associated with increased odds of disclosure to the partner of HIV status both at baseline (OR 1.16, 95% CI: 1.13 to 1.20) and follow-up (OR: 1.19, 95% CI: 1.12 to 1.27).
At baseline, almost all participants (98%) had detectable viral load and only 14% had initiated ART. At each timepoint, there was a significant increase in the proportion of those on therapy and without detectable viral load reaching at 12 months 60% remaining with detectable viral load and about half on therapy (Table 1). Over the year, 55% (107 of 193) of individuals never took ART, 13% (26 of 193) were on ART continuously at every visit at any time point, and 99% (192) of individuals had a detectable viral load at any time point. In univariate analysis, there was no significant difference in reports of UAI between those without and with detectable viral load (43.9% of those with no detectable vs. 47.9% of those with a detectable viral load, P value = 0.62). Similarly, there was no difference in those reporting UAI by ART usage (49.6% of those not on ART reported UAI vs. 40.2% of those on ART, P = 0.14).
Based on multivariable analysis (Table 2), over the year after HIV diagnosis, the following were significantly associated with reported UAI (Table 2): baseline methamphetamine use [adjusted odds ratio (AOR): 7.65, 95% CI: 1.87 to 31.30], methamphetamine use at follow-up (AOR: 14.4, 95% CI: 2.02 to 103.0), HIV-uninfected partner at follow-up (AOR: 0.14, 95% CI: 0.06 to 0.33) and partners with unknown HIV status at follow-up (AOR: 0.33, 95% CI: 0.11 to 0.94). PAS score during the year was marginally not significant (AOR: 1.03, 95% CI: 0.98 to 1.09); race/ethnicity and use of ART were not significant.
Our findings demonstrate how sexual behaviors, partnership status, substance use, and partner choices of MSM with recent HIV infection change during the first year after diagnosis. In this cohort, men with recent HIV infection reduced their total number of partners over the first year of infection; with the greatest decrease in the first 6 months and afterwards declines were minimal although significantly less than baseline. We identify a rebound in unprotected sex with serodiscordant or unknown partners at 1 year, suggesting that risk reduction in transmission behaviors is not sustained after a year. This replicates an earlier report of such a rebound in risk behavior among a smaller sample of men who seroconverted to HIV in a 5-city study conducted 1995-1998 as the HIVNET Vaccine Preparedness Study.31 Together, these studies suggest little progress in behavioral risk reduction for men newly diagnosed with HIV. Moreover, although the change in numbers of partners we report was significant, even with the decrease these recently HIV-infected men still had quite a few partners every few months, most of whom were new partners and over half whose HIV status was negative or unknown during that year. Thus, there is the potential for HIV transmission occurring to many different men during the course of that first year.
Our findings highlight the importance of the first 6 months after diagnosis as a time when behavior change occurs. It also suggests a need for programs to support the maintenance of such changes after this window of opportunity and particularly after 9 months of follow-up. The choices made by these potentially highly infectious men about the type of sex they practice and with whom they practice it affects their likelihood of transmitting to others. Although most of our findings reflect the analysis at the partner level to account for individual differences in behavior across different partners, the level of UAI reported at the individual level in Table 1 (46% baseline and 57% at 12 months) is comparable at baseline but higher after a year to that found in a meta-analysis of HIV-positive men in the United States.33 Because our cohort became too small after a year to follow, we cannot tell if this increase in risk is short term or if this reflects recent increases in risk behavior among HIV-positive men since 2000 as noted in the review.
The methamphetamine use reported in this sample is of great concern. At baseline, just over one third of the men reported using methamphetamine with a partner at last sex and continually during the year of follow-up with the percentage remaining remarkably stable. For HIV-infected men, this suggests that they are not accessing adequate treatment for substance use, illustrating the need for better treatment and services for this problem amongst HIV-infected men. It further highlights the continuing failure in secondary prevention efforts due to the nexus of drug use and HIV risk as the association between methamphetamine use and risky sex has been clearly demonstrated.24,25,34-36 These persistently high levels of methamphetamine use are also of particular concern for this population of men with recent HIV infection, as drug use has been shown to be associated with poor adherence to HIV treatment.36 The finding that the percent reporting UAI did not diminish significantly over time among methamphetamine users was not surprising but lends support to the urgent need to develop better access to, higher treatment adoption, and more effective substance use treatment for those with HIV.
Overall, the partnerships of these recently HIV-infected MSM seemed to stabilize and become stronger (ie, more intimate as measured by PAS) over the year after HIV diagnosis. Being in a stable partnership has been shown to enhance adherence to medication37; a potentially important health benefit for men with HIV infection with partnerships. On the other hand, it has previously been shown that those with low intimacy partners are less likely to disclose their HIV status.39 Consistent with this was the significant association between PAS and disclosure we identified both at baseline and follow-up. This suggests that risk reduction interventions for men in nonregular partnerships must address the dynamics of their partnerships to prevent potential transmission. Finally, we also find evidence of serosorting among these newly HIV-infected men, as the percent of men reporting an HIV-infected partner increased over time, from 14% at baseline to 39% at 12 months.
Although presence of a detectable viral load decreased significantly over the year and use of ART increased significantly for the men in this cohort, neither had an effect on the reported transmission behaviors. Evidence is growing that use of ART can greatly reduce HIV infectiousness and transmission risk38 and some HIV-positive men have been reported to increase risk behavior after initiation of ART and establishment of low viral load.41 suggesting they may be “compensating” in risk for their reduced infectiousness. However, a recent review of the literature suggests an overall lack of effect of ART use on behavior33; providing support for our findings.
There are limitations to the generalizability of our findings. The culture and specific characteristics of the Southern Californian HIV epidemic may result in different substance use and partnership patterns among those with recent HIV infection than in other locations in the United States and internationally. The study also was located at large academic research centers and included those willing to participate in a research study; therefore, enrolled individuals may not be entirely representative of those who acquire HIV and are followed in other settings. Additionally, the men in this study were largely white, highly educated, and there were few men less than 30 years of age. If the sample was more diverse, it is possible that we may have observed different changes in partnering patterns. The design of the study questionnaire presented challenges to identifying “the” partnership over time, as we did not collect actual names to protect the partner's identity; instead we collected nicknames or initials and these proved not to be used consistently by respondents. Nevertheless, it was possible to identify which behaviors occur with previously reported partners which were labeled as “persistent partnerships” for the purpose of the analyses. In addition, assumptions about potential transmission to sexual partners is limited by HIV status of partners being based upon participants' reports, and not otherwise validated. Finally, although the loss to follow-up was substantial, there were no significant differences between those who remained on study for 12 months and those who dropped out. It is important to note that the behavioral data were collected as part of an ancillary study to a large clinical study, and there were minimal incentives offered to complete behavioral interviews and no intensive retention efforts for behavioral follow-up. Clearly, future cohorts studies need to invest resources and special effort into retention of people with recent HIV infection. These limitations are offset by the uniqueness of having longitudinal data over 1 year on partnering patterns from a relatively large sample of men with recent HIV infection.
This study contributes unique perspectives about the risk behaviors and sexual partnering patterns of recently HIV-infected MSM. Interventions for such men around the time of diagnosis that address substance use may have great implications for their health status and the course of the HIV epidemic. It is sobering that our findings mirror those of a cohort collected in the past decade,31 showing that progress has not been made in changing the transmission behaviors of men after HIV infection. A significant reduction in the numbers of partners and although a rebound in risk, less unprotected anal intercourse with known serodiscordant partners than at baseline; such changes may have an important impact on HIV transmission rates as noted in a review of HIV prevention interventions.
Finally, our findings point to decreases in risk behavior in the months after a diagnosis, and then a rebound in risk behaviors after 9 months, perhaps defining timepoints for ongoing interventions that target risk reduction for HIV-infected individuals.
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