Sexually Transmitted Diseases:
Unprotected Anal Intercourse and Substance Use Before and After HIV Diagnosis Among Recently HIV-Infected Men Who Have Sex With Men
Drumright, Lydia N. PhD*†‡; Strathdee, Steffanie A. PhD†; Little, Susan J. MD*; Araneta, Maria Rosario G. PhD†; Slymen, Donald J. PhD‡; Malcarne, Vanessa L. PhD§; Daar, Eric S. MD‖; Gorbach, Pamina M. DrPH¶
From the *Antiviral Research Center, Department of Medicine and the †Department of Family and Preventive Medicine, University of California, San Diego, California; the ‡Graduate School of Public Health and the §Department of Psychology, San Diego State University, San Diego, California; the ∥Los Angeles Biomedical Research Institute at Harbor-UCLA and the David Geffen School of Medicine, University of California, Los Angeles, California; and the ¶Department of Epidemiology and Division of Infectious Disease, School of Medicine, University of California, Los Angeles, California
The authors acknowledge and thank Tari Gilbert, Jacqui Pitt, Paula Potter, Joanne Santangelo, and the University of California, San Diego Antiviral Research Center staff for their support in data collection; and W. Susan Cheng for her assistance in data collection and management. The authors also thank Dr. Simon Frost for his suggestions and assistance in data analysis and writing this manuscript. Most of all, the authors thank our participants for volunteering for this study.
Funding for this study was provided by the National Institutes of Allergy and Infectious Diseases grant no. AI43638 (The Southern California Primary Infections Program) and the Universitywide AIDS Research Program grant no. ID01-SDSU-056, and grant no. IS02-SD-701, and grant no. D03-SD-400.
Correspondence: Lydia N. Drumright, PhD, University of California, San Diego, School of Medicine, Department of Family and Preventive Medicine, Division of International Health and Cross-Cultural Medicine, 9500 Gilman Drive Mail Code 0622, La Jolla, CA 92093. E-mail: firstname.lastname@example.org.
Received for publication May 24, 2006, and accepted August 26, 2006.
Objective: The objective of this study was to assess associations between unprotected anal intercourse (UAI) and substance use before and after HIV diagnosis among recently HIV-infected MSM.
Study Design: Two hundred seven MSM completed computer-assisted self-interviews regarding type and timing of sexual activity and substance use with their last 3 partners. Date of HIV diagnosis was extracted from medical records. Generalized estimating equations, including interaction terms, were used to assess associations between substance use and UAI before and after HIV diagnosis.
Results: Among partners with whom sexual activity occurred before diagnosis, UAI was associated with methamphetamine use alone (odds ratio = 7.12) and a combination of methamphetamine and other substances (odds ratio = 4.06). However, after HIV diagnosis, UAI was associated with use of substances other than methamphetamine (odds ratio = 3.36), but not methamphetamine alone.
Conclusions: Use of illicit substances may be differentially associated with UAI based on knowledge of HIV status and could have implications for prevention of HIV transmission.
IN RECENT YEARS, THE UNITED STATES Centers for Disease Control and Prevention has called for HIV-1 prevention to shift efforts from HIV-negative individuals only and include both HIV-negative and -positive individuals.1,2 Such efforts are especially needed among men who have sex with men (MSM) who continue to bear a disproportionate burden of HIV infection in the United States and other developed countries.3–8
When compared with their HIV-negative peers, some researchers have found that HIV-infected MSM report fewer partners,9 more condom use,10 and less frequent trading of sex for money or drugs,9 suggesting a deliberate change in risk behavior, possibly to prevent transmission to others.11,12 Changes in risky behavior after HIV diagnosis have also been noted among MSM, including discontinuation of alcohol or substance use,13 increases in condom use,14,15 and reporting no sexual activity or no insertive anal intercourse.15
However, other studies report ongoing high-risk behaviors among HIV-infected MSM, including unprotected anal intercourse (UAI) despite knowledge of HIV infection.16 Additionally, some have reported that HIV-positive MSM who were aware of their status were more likely to report UAI17 or to be infected with syphilis18 than those who were HIV-negative. Some have suggested that use of illicit substances is associated with ongoing high-risk sexual behaviors among HIV-positive MSM. Use of alcohol19 and nitrites19,20 have been associated with UAI among HIV-positive MSM who were aware of their serostatus. Use of crack cocaine after HIV diagnosis has been associated with trading sex for money or illicit substances among MSM.21 Illicit substance use may also modify the sense of shared responsibility for adopting safer sex behaviors.22
The period soon after HIV seroconversion is a critical juncture for prevention as a result of high HIV viral loads that may result in a higher probability of HIV transmission.23–27 Reduction of risk behavior, coupled with early diagnosis, is important for preventing onward HIV transmission. Understanding how risk behaviors are modified after diagnosis is important in designing appropriate behavioral interventions. However, most studies of behavior change have been conducted in HIV-positive MSM who were not recently infected. The current study aims to elucidate the relationship between illicit substance use and UAI before and after HIV diagnosis among newly infected HIV-positive MSM.
Materials and Methods
Between May 2002 and October 2005, 222 recently HIV-infected individuals who were referred to the Acute Infection and Early Disease Research Program in San Diego and Los Angeles by clinicians and HIV test counselors were asked to complete a computer-assisted self-interview (CASI) regarding HIV risk behaviors. Two hundred eighteen (98%) volunteered to complete the CASI and provided informed consent. Three of the participants were women, 7 were men who reported sexual contact with only women in the previous 12 months, and 208 were men who reported sexual contact with other men in the previous 12 months. The current analyses include 207 MSM who responded to CASI and reported that at least one of their last 3 sexual partners was a man.
All MSM had recent HIV infection as determined by one of the following: 1) presence of HIV RNA in plasma but a negative enzyme immunoassay (EIA); 2) results on detuned and sensitive EIAs that were consistent with early HIV infection; or 3) HIV seroconversion within the previous 12 months (negative EIA followed by positive EIA). Estimated date of infection for all participants was based on last HIV-negative test result and serology as previously described.28 Date of HIV diagnosis was established through reviewing medical records and assigned as the first positive HIV test that was reported to the participant.
Using CASI, participants were asked to provide detailed information about the last 3 people with whom they had had sexual contact. Questions were asked for each partner regarding duration of time between the interview and the first and last time they had sexual intercourse. Additionally, participants were asked about types of sexual activities that occurred, substances used just before or during sexual activity (e.g., methamphetamine, nitrites), partner demographic information, partner HIV status, and partner type (i.e., main, regular, friends, acquaintances, one-time, anonymous, and trade). Although participants were asked about specific substances, data for these analyses were collapsed into no substance use, methamphetamine only, substances other than methamphetamine, or a combination of methamphetamine and other substances. The protocol for this study was approved by the Institutional Review Boards of the University of California, San Diego; University of California, Los Angeles (UCLA); Harbor-UCLA Medical Center, and Cedars-Sinai Medical Center.
Univariate and multivariate associations between UAI and substance among the 603 male partners reported by 207 MSM were conducted using generalized estimating equations (GEE) to correct for variance estimates of repeated measures.29 Female partners were excluded from analysis because only 9 female partners were reported among the last 3 and substance use and unprotected sexual activity may differ between same-sex and opposite sex partnerships.10 Interactions between timing of sexual activity (i.e., before vs. after HIV diagnosis vs. spanning diagnosis) and substance use were included in GEE models to determine if there were significant temporal changes in the associations between UAI and substance use.
To further assess interactions and to describe changes in associations between UAI and the covariates for partners before, after, and spanning (i.e., both before and after) HIV diagnosis, we conducted a subanalysis in which participants’ last 3 sexual partners were stratified into 3 different categories based on timing of sexual activity in relationship to the participant’s medical record HIV diagnosis date. Separate GEE analyses were used to examine associations between UAI and substance use for each of these strata. All GEE models were conducted using a binomial family, a logit link, and an unstructured correlation matrix. Analyses were performed using STATA version 8.2 SE (STATA Corp., College Station, TX).
Participants completed their baseline interviews a mean of 13 weeks (median, 14 weeks) after their estimated date of HIV infection and 5 weeks (median, 3 weeks) after HIV diagnosis. The mean age of MSM was 35 years (range, 18–65 years) and most were white (70.1%); 20.8% were Hispanic, 2.9% were African American/black, 2.4% were Asian, and 3.9% reported other ethnicity (Table 1). Completion of college or higher education was reported by 46.9%. The median number of male partners was 20.0 in the previous 12 months (mean, 38), 4 in the previous 3 months (mean, 9.2), and one in the previous month (mean, 3.6). A total of 5.8% reported sexual contact with both men and women in the previous 12 months.
Of the last 3 partners who were men, the mean reported age was 33 years, and most (62.2%) were white (Table 1). A range of different partner types were reported among the last 3, including 18.4% who were main partners (e.g., boyfriend, life partner). HIV status was unknown for 45.9% of the last 3 partners, 42.2% were believed to be HIV-negative, and 11.9% were believed to be HIV-positive. Sexual activity before diagnosis was reported with 317 (52.6%) of the partners with 144 (23.9%) after diagnosis and with 142 (23.5%) partners with whom sexual activity spanned diagnosis (Table 1). Use of illicit substances at the time of sexual activity was reported with 45.9% of partners. Recreational substances were classified as follows: methamphetamine alone (5.5%), other substances alone (20.4%), and methamphetamine and other substances combined (18.1%) (Table 1).
Use of substances other than methamphetamine just before sexual activity was reported with a greater proportion of sexual partners after diagnosis (32.4%, P = 0.01) and who spanned diagnosis (26.6%, P = 0.02) than before diagnosis (12.6%) (Fig. 1). In contrast, the proportion of sexual partners with whom methamphetamine use was reported, either alone (6.7% before vs. 2.9% spanning vs. 4.2% after, P >0.05) or in combination with other substances (18.7% vs. 12.2% vs. 21.8%, respectively, P >0.05), did not change significantly based on timing of diagnosis. UAI was reported with a higher proportion of sexual partners before diagnosis (58.4%, P <0.01) and spanning diagnosis (58.3%, P = 0.01) than after (43.7%).
In multivariate GEE models containing independent variables and interaction terms (Table 2), methamphetamine use only (odds ratio [OR] = 7.12, P = 0.01), methamphetamine and other substances (OR = 4.06, P <0.01), and continued sexual contact with a partner spanning diagnosis (OR = 0.43, P = 0.01) were significantly associated with UAI as independent variables. Interactions (Table 2) between sexual activity after diagnosis as compared with before and substance use were observed for methamphetamine only (P = 0.01) and substances other than methamphetamine (P = 0.03), but not methamphetamine and other substances combined (P = 0.37). Interactions between sexual activity spanning diagnosis and a combination of methamphetamine and other substances were observed (P <0.01) but not for methamphetamine alone (P = 0.73) or other substances alone (P = 0.33).
Before diagnosis, those who used methamphetamine with a particular partner were more than 7 times (OR = 7.12; 95% confidence interval [CI] = 1.8–28.6) as likely to report UAI with that partner (Fig. 2) compared with MSM with no substance use. After HIV diagnosis, those who reported methamphetamine use with a partner were no more likely to report UAI than those who reported no substance use (OR = 0.40; 95% CI = 0.1–3.4). This change in association between methamphetamine and UAI was statistically significant (P = 0.01) (Fig. 2). Similarly, there were significant differences in the association between UAI and other substances when considering sexual contact before and after diagnosis through test by interaction (P = 0.03) (Fig. 2). However, the trend for other substances was the opposite of methamphetamine use (P = 0.01). Those who reported other substance use with partners before diagnosis were no more likely than those who reported no substance use to report UAI with that partner (OR = 0.81; 95% CI = 0.4–1.7) (Fig. 2). However, after diagnosis, use of other substances was significantly associated with UAI (OR = 3.36; 95% CI = 1.4–8.3).
To confirm differences in the associations between substance use and UAI relative to timing of HIV diagnosis, we conducted stratified analyses by timing of sexual contact. The results of these models were highly consistent with the results from the interactions within the whole sample. After controlling for partner’s HIV status and partner type, those who reported methamphetamine use only or a combination of use of other substances and methamphetamine were more likely to report UAI than those who did not report substance use (OR = 8.17, P <0.01 and OR = 4.43, P <0.01, respectively) before diagnosis (Table 3). For partners with whom sexual activity began before diagnosis and continued after diagnosis, UAI was more likely to be reported by those who used a combination of methamphetamine and other substances (OR = 7.75, P <0.01) than those who did not report substance use, but neither methamphetamine alone nor other substance use was associated with UAI (Table 3). After diagnosis, UAI was more likely to be reported with partners with whom other substances were used (OR = 3.25, P = 0.01), but not when methamphetamine alone or methamphetamine in combination with other substances was used. UAI was also less likely if the partner was HIV-negative and spanned diagnosis or if the partner was a main partner and either spanned diagnosis or was a partner before diagnosis (Table 3).
In our study of recently HIV-infected MSM, UAI was reported with fewer partners after HIV diagnosis than before diagnosis. Of greater interest was our finding that use of specific illicit drugs had differential effects on UAI depending on whether sexual contact occurred with a partner before or after HIV diagnosis. Specifically, methamphetamine use was associated with higher odds of UAI with partners before HIV diagnosis but was not associated with UAI after diagnosis. In contrast, use of substances other than methamphetamine was not associated with UAI before HIV diagnosis but was associated with a greater likelihood of UAI after diagnosis. These findings have implications about prevention of high-risk sexual behavior and substance use among HIV-positive MSM and suggest that use of specific recreational substances may have differential effects on the risk of UAI based on an individual’s knowledge of his HIV status.
We observed a modest, yet statistically significant reduction in UAI with sexual partners soon after HIV diagnosis as compared with before diagnosis, suggesting a deliberate reduction in transmission behaviors. A reduction in the number of sexual contacts (from an average of 7.9–5.2 3 months later) has previously been observed in a subset of this cohort after HIV diagnosis.30 In the present analyses, participants were significantly less likely to report UAI with HIV-negative partners who spanned HIV diagnosis. Although not statistically significant, there was a trend toward a greater likelihood of reporting UAI with a negative partner before diagnosis and a lesser likelihood of reporting UAI with a negative partner after diagnosis, suggesting that early diagnosis may help to prevent HIV transmission. Because the data in this study were cross-sectional and participants reported behaviors over a short duration of time, it is unclear if sexual transmission risk reduction behavior will continue or if it will rebound with continued substance use.
The proportion of sexual partners with whom methamphetamine use was reported did not significantly change after HIV diagnosis, although the association between methamphetamine use and UAI changed markedly. Similar results were also seen when methamphetamine use in general (i.e., not separating methamphetamine from methamphetamine used in combination with other substances) was examined. These results suggest that MSM may be able to modify their risk behavior even if they continue to use methamphetamine. Other investigators have suggested that partners’ disclosure of their HIV status, type of venue in which sexual activity occurs, partner type, and perceived risk of sexual act all affect the decision of HIV-positive, methamphetamine-using MSM to disclose their HIV status, which is likely to result in condom use.22 In a subanalysis of this sample, 22.7% of those who used methamphetamine with a partner before diagnosis reported that they met that partner in a bathhouse, but none of the partners spanning diagnosis or after diagnosis was met in a bathhouse. Further studies are needed to directly evaluate changes in transmission risk behavior of methamphetamine-using MSM before and after diagnosis, including longitudinal studies that measure longer periods of time before and after HIV diagnosis to determine if the observed patterns are related to diagnosis or cyclical changes in substance use.
On the other hand, use of substances other than methamphetamine during sexual activity increased after HIV diagnosis. Use of other substances was associated with a greater likelihood of UAI with partners after diagnosis, whereas methamphetamine use alone was not. However, a switch from methamphetamine to other substances was not observed, because use of methamphetamine alone or in combination with other substances before sexual activity did not change from before to after diagnosis. Instead, use of other substances was more commonly reported with partners after diagnosis. This suggests that among recently HIV-infected MSM, use of other substances may become more important in increasing UAI after HIV diagnosis. This may occur as a result of less public awareness of other substances’ effects on UAI or because these other substances are perceived to have fewer personal health consequences than methamphetamine. However, we did not measure such beliefs in this study, but have anecdotal information suggesting that posttest counseling on substance use primarily covered risks associated with methamphetamine use.
Specific substances that comprise the “other” category were measured in the questionnaire and some substances were more commonly reported than others. The most commonly reported substances of use were nitrites, marijuana, and GHB, although GHB was much more common among users of both methamphetamine and another substance. There was considerable overlap in use of many different substances (i.e., polydrug use) with a single partner among our participants. Consequently, we were unable to explore all combinations of overlap or single use of these substances and methamphetamine because data would become too sparse; however, we stress the relevance of such studies in larger samples.
Interestingly, for partners who spanned HIV diagnosis, UAI was only associated with use of methamphetamine and other substances combined. Methamphetamine users who also use other substances may practice riskier behaviors. Previous studies have demonstrated that MSM who are polydrug users tend to report higher rates of UAI31,32 as compared with single drug users, more sexual partners,33 greater likelihood of sexually transmitted infection,34 and more UAI among HIV-positive MSM with serodiscordant partners.35 Polydrug use is also commonly reported in combination with methamphetamine use.32,35–37 In this sample, most (76.8%) methamphetamine users also reported use of other substances.
As expected with all observational studies, there were some limitations. Additional information on the context of risk behaviors that may have helped to explain our results was not collected (e.g., conscious attempts to alter substance use and UAI behavior after HIV diagnosis). We were unable assess the affect of specific attitudes (e.g., sense of responsibility, HIV treatment optimism, and beliefs about viral load) and sexual positioning with regard to transmission to others in relation to substance use, which have been shown to be important in other studies.11,12,38–43 Our sample consisted of volunteers who were predominantly well-educated, white MSM and may not be representative of all MSM who have recently become infected with HIV. Additionally, substance use among MSM may vary by geographic region44,45; therefore, these data may not be generalizable to all MSM.
This study indicates that use of specific recreational substances may have differential effects on UAI before and after HIV diagnosis among MSM, which has several implications for the study of substance use and HIV/sexually transmitted infection prevention. Our data suggest the need for designing studies that can specifically examine particular patterns of substance use with regard to partnership and situational factors. Without examining the interaction between substance use and sexual timing in regard to UAI, we would have observed associations between substance use and UAI but could have missed the change that occurred before and after HIV diagnosis. Additionally, our data highlight the need for qualitative and quantitative studies that contribute to understanding modifiers and motivations for substance use and UAI such as sense of responsibility with regard to prevention of HIV transmission, HIV treatment optimism, safer sex fatigue, and social dynamics. These data also suggest that new interventions designed to reduce HIV transmission among MSM through cessation of substance use should consider different types of substance use, including polydrug use.
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