1 San Francisco Department of Public Health, San Francisco, CA.
2 Department of Epidemiology and Biostatistics, Division of Biostatistics, University of California, San Francisco, CA.
3 Fred Hutchinson Cancer Research Center, Seattle, WA.
4 Howard Brown Health Center, Chicago, IL.
5 The New York Blood Center, New York, NY.
6 Department of Medicine, Division of Infectious Diseases, University of Washington, Seattle, WA.
7 Department of Epidemiology, University of Washington, Seattle, WA.
8 National Center of Complementary and Alternative Medicine, Bethesda, MD.
9 Fenway Community Health Center, Boston, MA.
10 Abt Associates Inc., Cambridge, MA.
11 Denver Public Health Department, Denver, CO.
12 University of Colorado Health Sciences Center, Denver, CO.
13 National Institute on Alcohol Abuse and Alcoholism, Bethesda, MD.
14 Department of Medicine, Division of Infectious Diseases, David Geffen School of Medicine, University of California, Los Angeles, CA.
Received for publication May 22, 2003; accepted for publication December 19, 2003.
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ABSTRACT |
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alcohol drinking; amphetamine; amyl nitrite; HIV; logistic models; risk factors; risk-taking; sexual behavior
Abbreviations: Abbreviations: HIV, human immunodeficiency virus; MSM, men who have sex with men; SDUA, serodiscordant unprotected anal sex.
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INTRODUCTION |
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The general relation between noninjection substance use and human immunodeficiency virus (HIV) risk behavior has been reviewed previously (7). Many studies have found an association between sexual risk behavior and substance use, including amphetamines, poppers, alcohol, cocaine, and ecstasy (1, 815). Moreover, higher levels of substance use, including amphetamines and poppers, have been associated with increased risk of HIV infection (16).
The causal relations between substance use and sexual risk remain unclear. General associations between substance use and risk may be due to simple contextual effects, such as the effects of age and relationship status on both substance use and risk (2, 17). Personality disposition may also motivate people toward both substance use and risky behaviors (18). Substance use per se may enhance risk, independent of a persons stable characteristics, or interact with personal characteristics such that risk is increased. However, few studies have explicitly examined the effects of both background substance use and episode-specific use on sexual risk. Alcohol use has been examined most systematically in this context, with results generally indicating that global patterns of use are better predictors of sexual risk than are episode-specific measures (1921). In contrast, some data indicate that episode-specific use of certain substances, including poppers, alcohol, and cocaine, relates to sexual risk behavior (15, 2023). However, these analyses did not adjust for participants background tendencies to use substances, potentially confounding the relation between episode-specific substance use and sex. If substance use induces risk because of stable individual differences, we would expect background use to emerge as the strongest predictor of risk. In contrast, if use during sex induces risk, we would expect episode-specific measures to predict risk beyond any effects of background variables.
We examined the relation between substance use and sexual activity by using baseline data from the EXPLORE trial, a randomized behavioral intervention for MSM. Information was gathered on substance use and sexual risk taking during the most recent sexual episode with each of up to three most recent partners as well as frequency of substance use over the past 6 months. The EXPLORE data provided a unique opportunity to determine the independent effects of substance use during specific sexual episodes, after removing the influence of background frequency of substance use.
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MATERIALS AND METHODS |
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Data collection
At the enrollment visit, audio computer-assisted self-interview was used to collect data on alcohol and substance use and on sexual behaviors. The interview assessed sexual behaviors with all HIV-positive, HIV-negative, and unknown-serostatus partners, as well as substance use (alcohol, marijuana, poppers, hallucinogens, sniffed cocaine, amphetamines, crack cocaine, smoked heroin, or any injection drug), in the 6 months prior to enrollment.
More detailed questions were asked about the most recent sexual episode with each of up to three most recent partners, including type of sex (unprotected receptive oral sex with ejaculation, receptive and insertive anal sex, protected and unprotected); quantity of alcohol used within 2 hours before or during sex; other substances used "immediately before or during sex" (marijuana, poppers, hallucinogens, sniffed cocaine, amphetamines, crack cocaine, smoked heroin, or any injection drug); age; and desirability of partner, type of relationship (primary/steady, nonprimary/casual), location of sex, and serostatus of partner. Participants were asked to report partner serostatus based on the following questions: "How many of your male sex partners were HIV positive?" "How many of your male sex partners told you they were HIV negative and you had no reason to doubt it?" and "How many of your male sex partners never told you their HIV status or told you they were negative and you have reason to doubt it?" Following the interviews, participants received HIV pretest counseling, and specimens were collected for HIV testing. Approximately 2 weeks after screening, participants received their test results and posttest counseling. Eligible men were then randomly assigned to either the intervention (10 counseling sessions) or control arm of the trial.
Our outcome, serodiscordant unprotected anal sex (SDUA), was defined as a report of either insertive or receptive anal sex without a condom with either an HIV-positive partner or a partner of unknown serostatus. These behaviors represent significant risk for HIV transmission (25). For each of up to three of the most recent partners the participant reported, this outcome was defined for the most recent episode of sex and was analyzed as a repeated-measures outcome. In two supplementary analyses, we also examined the SDUA outcome by the participants sexual role, focusing in separate analyses on serodiscordant unprotected receptive and serodiscordant unprotected insertive anal sex.
Statistical analysis
We used multipredictor logistic models to identify the independent predictors of SDUA during each of the three most recent sexual episodes reported by each participant. For participant-level predictors, including demographics and substance use over the past 6 months, the generalized estimating equations approach (26, 27) was used to account for correlation between the repeated outcomes for each participant. This approach is appropriate when the focus is on between-participant comparisons in terms of participant-level predictors that are constant across the three episodes. Background substance use was modeled as the average level of substance use over the previous 6 months. Specifically, average frequency of substance use was coded as never, less than once per week on average, or once per week or more on average. Alcohol use was coded as light (3 drinks/day on no more than 12 days/week), moderate (45 drinks/day on no more than 12 days/week, or 15 drinks/day on 36 days/week, or 13 drinks/day on a daily basis), or heavy (daily drinking of
4 drinks, or drinking
6 drinks on any day). Depression was evaluated by using a shortened version of the Center for Epidemiologic Studies Depression/National Institute of Mental Health scale (28).
To examine the independent influence of episode-level predictors, we used conditional logistic regression. This approach is appropriate when the focus is on within-participant comparisons. By making each subject his own control, the conditional approach eliminates the influence of between-participant predictors and accounts for within-subject correlation. Only those participants who report SDUA during one or two but not all of their three recent sexual episodes contribute information to this analysis; as in simpler applications, including McNemars test, "concordant" observations are uninformative. The predictor of primary interest was substance use just before or during the sexual episode.
All analyses were carried out by using SAS software, version 8.2 (SAS Institute, Inc., Cary, North Carolina).
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RESULTS |
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Table 2 shows univariate and multivariate associations of the participant-level variables shown in table 1 with SDUA. Of the 11,715 sexual episodes reported, 1,867 (16 percent) were SDUA. In univariate analyses, we found that most substances were associated with high-risk sexual behavior; however, when adjusted for the other variables shown, only popper, amphetamine, and sniffed cocaine use and heavy alcohol consumption remained associated with SDUA. Older participants and those with less education and lower incomes were also more likely to report SDUA, as were depressed participants. In supplementary analysis, similar results were seen for both serodiscordant unprotected receptive and serodiscordant unprotected insertive anal sex, with the same patterns holding for the substance use associations (data not shown).
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Episode-specific variables, describing substance use and characteristics of sex partners for these participants, are shown in table 3. For more than one third of all episodes, participants reported consuming alcohol just before or during sex, with nearly one in 10 consuming at least six drinks. Thirty-one percent of sexual episodes involved using nonalcoholic substances, with marijuana, poppers, hallucinogens, and sniffed cocaine being the most common. Participants reported that over one third of episodes involved a partner consuming alcohol; nearly one fifth involved a partner using other substances. Most partners were nonsteady, with 46 percent of participants reporting only one sexual experience with the partner and most reporting having had sexual relations with the partner for less than a month.
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DISCUSSION |
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Although we were unable to determine the mechanisms through which substance use increases sexual risk, several possibilities warrant consideration. A key mechanism may be that being intoxicated "disinhibits" a participant to have sexincluding unprotected sexwith an HIV-positive or unknown-serostatus partner. Substance use may also decrease safer-sex skills, such as the ability to use condoms properly. This interpretation is supported by other data showing that alcohol consumption and amphetamine use are associated with condom failure (29). In a corollary perspective, popper use facilitates anal sex by increasing tactile sensitivity and relaxing sphincter tone, which may lead to more unprotected anal sex because of increased partner receptivity. Thus, the immediate effect of alcohol or drugs on risk may be due to pharmacologic effects that simultaneously disrupt basic safety behaviors and facilitate some risky activities.
We should note that the effect on sexual risk of substance use during sexual episodes is not incompatible with a "person"-based perspective on risk. Thus, some participants may intentionally use substances to reduce anxiety about having sex and/or the potential for disease transmission, leading to higher risk behavior than may have occurred in the absence of substance use (30). In this light, there may be stable individual differences in the substance userisk linkage that operate on an episode-by-episode basis. Our data did not measure alcohol/drug expectancies or other attitude constructs, so we were not able to test this hypothesis. Given that expectancies or attitudes may be important "access points" for behavioral interventions, further studies should examine both cognitive variables and episodic use to test or clarify the interaction of these classes of variables.
Clearly, interventions are needed that target the use of substances during sex. These results suggest that such interventions should focus not only on sexual risk but also on substance use itself, given that the simple presence of alcohol or drugs during a sexual episode was associated with SDUA. Studies have reported that sexual risk behavior declines among MSM who seek treatment for substance use, although these data are largely from observational studies (31). Sporadic substance use during sexual activity was a common pattern in this cohort, including use of substances such as amphetamines and cocaine that can lead to dependency. This finding suggests that interventions may need to be developed to prevent sporadic users from becoming chemically dependent.
The relatively low frequency of heavy substance use in this cohort suggests that traditional treatment interventions based on addiction/dependent treatment models may be less useful than interventions that more directly address the effect of episodic use on sexual and other risks. Such programs should be designed to reduce directly substance use during sex and should address indirect processes such as degradation of safer sex skills when high.
A notable exception to participants relatively low, intermittent patterns of substance use is alcohol: approximately one out of 10 men was a heavy user. Alcohol was also the most commonly used substance just before or during sex. The role of alcohol in promoting high-risk sexual activity has been controversial, with some but not all studies suggesting that alcohol use is associated with high-risk sexual behavior (3235). Our findings suggest that, at a population level, alcohol use may be contributing to a greater proportion of high-risk sexual behaviors than any other substance, especially among those who have multiple drinks prior to having sex. Targeting HIV prevention to heavy alcohol users, including focusing on reducing the quantity of alcohol used in sexual settings, may be effective in reducing sexual risk.
In our episode-level analysis, we also found a relatively strong association between partner substance use and SDUA. The fact that this association was independent of participants own substance use suggests that prevention strategies addressing substance use should include addressing whether partners are intoxicated during sexual encounters and suggestions for remaining safe in such settings. The association of participants not knowing whether their partners were on drugs during sex with SDUA is most likely a marker for familiarity with the partner or the partners personality, or it may reflect participants hesitation to answer the question definitively unless they specifically asked their partners about their substance use.
Although the focus of this analysis was to examine substance use and sexual risk behavior, we also found that the possibility of high-risk sex increased among participants with less education and lower incomes. These findings suggest that prevention programs should reemphasize the risk of unprotected sex with nonprimary partners and tailor prevention programs for less-educated MSM, especially those with no college education. While some studies have reported that depression is not associated with sexual risk behavior, our finding that depressive symptoms are independently associated with sexual risk, after controlling for substance use, supports directly addressing the mental health of MSM, through either counseling or pharmacologic treatment, as a potentially important HIV prevention strategy (36). Finally, although we found a small, but significant decrease in risk behavior with increasing partner age in the episode-level analysis, risk behavior increased with increasing participant age in the subject-level analysis, reinforcing the need to focus prevention efforts on MSM of all ages.
There are some limitations to our findings. Participants were recruited through a variety of venues but may not be representative of the general population of high-risk, HIV-negative MSM. Although behavioral data were collected by using an audio computer-assisted self-interview, which has been shown to increase reporting of socially undesirable behaviors compared with interviewer-administered questionnaires (37), participants may still have underreported their substance use or sexual risk behavior. In addition, episode-specific data were collected on only the three most recent sexual partners. It is possible that additional detailed data from more sexual episodes may have changed our results to the extent that people more likely to use substances during sex may also be more likely to report more sexual partners. Our effect sizes may therefore represent lower-bound estimates for the relation between substance use and sexual risk. Although our analysis was able to control for or remove the influence of multiple partner and participant characteristics, other unmeasured episode-level variables may confound the relation between substance use and sex. We also did not measure use of some specific club drugs, including ketamine and gamma-hydroxybutyrate, and were therefore unable to measure their associations with risk behavior. Finally, baseline use of sildenafil citrate (Viagra; Pfizer Labs, New York, New York), which has been associated with risk behavior in prior studies (4, 38), was not assessed in this cohort.
HIV and other sexually transmitted diseases are increasing among gay and bisexual men (39, 40). HIV prevention programs need to increase awareness of the sexual risk associated with substance use. Inquiring about substance use during sexual activity should be emphasized as part of primary care delivered to MSM and as part of HIV testing and counseling procedures. MSM who report using substances just before or during sex should be made aware of the risk potential of that behavior, and they should have risk-reduction and treatment programs available for modifying this key risk precursor.
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ACKNOWLEDGMENTS |
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In addition, this work was supported by the HIV Prevention Trials Network and was sponsored by the National Institute of Allergy and Infectious Diseases, the National Institute of Child Health and Human Development, the National Institute on Drug Abuse, the National Institute of Mental Health, and the Office of AIDS Research of the National Institutes of Health, US Department of Health and Human Services through a cooperative agreement (5 U01 AI46749) with Family Health International, with a subsequent subcontract to Abt Associates Inc., with subcontracts to the Howard Brown Health Center and Denver Public Health; cooperative agreement U01 AI48040 with the Fenway Community Health Center; cooperative agreement U01 AI48016 with Columbia University (including a subagreement with the New York Blood Center); cooperative agreement U01 AI47981 with the University of Washington; and cooperative agreement U01 AI47995 with the University of California, San Francisco.
The content of this article does not necessarily reflect the views or policies of the US Department of Health and Human Services nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.
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NOTES |
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REFERENCES |
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