Sex trade workers represent an extremely marginalised segment of the general population.¹ Nevertheless, the physical dangers and elevated risk for HIV and other sexually transmitted infections (STIs) that are generally associated with sex trade involvement are increasingly becoming a focus of public attention.^2,3 Despite the consistency of previous studies that indicate high frequencies of sex trade involvement and STIs among male injection drug users (IDUs), remarkably few studies have furthered our understanding of the relation between male sex trade involvement, injection drug use, and unprotected sexual intercourse.^{1,4,5,6,7,8,9,10,11}

Male sex trade involvement may in part account for the up to eightfold elevations in HIV seroprevalence and seroincidence among IDU men who have sex with men compared to other men who have sex with men^10,12,13 and compared to other male IDUs.^14–16 However, many IDU men who have sex with men do not self identify as gay and many report little contact with HIV preventive interventions that target male IDUs, so these men may not benefit from current HIV prevention programmes that target either men who have sex with men or male IDUs.^11,16 Furthermore, there does not appear to be any controlled trial of a sexual intervention for male IDUs who have sex with men and only one published multivariate analysis of the relation between illicit substance use and the sexual behaviour of male IDUs who have sex with men.^6,14 We therefore undertook the present analyses to identify factors associated with male sex trade involvement in a long term, prospective cohort study of male IDUs. We alos attempted to identify unmet health service needs of this important subpopulation of IDUs.

METHODS

Beginning in May 1996, people who had injected illicit drugs in the previous month were recruited into the Vancouver Injection Drug User Study (VIDUS), a prospective cohort study that has been described in detail previously.^17–19 Briefly, as of November 2003, 1560 study subjects had been recruited through self referral and street outreach, and data collection for the project is conducted in a storefront office. People were eligible for VIDUS if they had injected illicit drugs at least once in the previous month, resided in the greater Vancouver region, and provided written informed consent. Participants return semiannually to the study site for a follow up questionnaire and to provide a venous blood sample for HIV serology every 6 months. Participants were compensated $20 (€13) for each study visit and blood draw. The study was approved by the University of British Columbia/Providence Health Care research ethics board.

The present analyses were restricted to male participants who were enrolled between May 1996 and November 2003. The primary end point in this analysis was self reported sex trade involvement during the previous 6 months. Sex trade involvement was defined as exchanging sex for money, goods, drugs, shelter, or anything else during the previous 6 months. Sexual behaviours with casual and regular sex partners were assessed separately, and sexual risk was defined as one or more instances of unprotected vaginal or anal intercourse. Regular partners were defined as “someone you have had a sexual relationship with for more than 3 months (not including clients/tricks)” and casual partners were defined as “someone you have had a sexual relationship with for less than 3 months (not including tricks/clients).” As previously,²⁰ unstable housing was defined as living in a single room occupancy hotel, transitional living arrangements, or homelessness. Difficulty accessing substance abuse treatment was assessed with the question, “Over the last 6 months, have you ever tried to access any alcohol or other drug treatment, but were unable to?”

Factors associated with sex trade involvement were identified using crude and adjusted odds ratios (AOR) with 95% confidence intervals that were computed using generalised estimating equations (GEE) with an exchangeable correlation structure.²¹ These methods are analogous to logistic regression methods but adjust standard errors to account for non-independence among repeat observations (study visits) from the same individual.²²

Potential correlates of male sex work evaluated in this analysis included age at enrolment as well as time updated factors, such as HIV infection, and behaviours relating to the previous 6 months, including unprotected vaginal or anal intercourse, unstable housing, incarceration, daily heroin and cocaine injection, daily crack cocaine smoking, borrowing used syringes, lending used syringes, having sought but been unable to access substance abuse treatment, and current enrolment in methadone maintenance treatment.^20,23

Variables potentially associated with sex trade involvement were examined in bivariate analyses. In order to adjust for potential confounding we also fitted a multivariate model using the a priori defined model building approach in which we adjusted for all variables that were statistically significant at the p <0.05 level in the bivariate analyses. Variables were considered if they were associated with infectious disease risk or known modifiers of this risk behaviour, and variables that were p <0.01 in bivariate analyses, but were no longer significant after adjustment were retained in the final model to ensure maximal control of confounding. All statistical analyses were performed using SAS software version 8.0 (SAS, Cary, NC, USA). All p values are two sided.

RESULTS

Among the 995 male participants recruited into the VIDUS cohort between 1996 and 2003, the median age was 35 (interquartile range (IQR) 28–41), 191 (19%) were Aboriginal, 623 (63%) reported residing in unstable housing, 184 (19%) were HIV seropositive, and 108 (11%) reported being involved in the sex trade at enrolment. Table 1 shows baseline characteristics of the participants stratified by sex trade involvement. As shown here, sex trade involved men were more likely to be younger, HIV positive, and have had unprotected intercourse with their casual partners during the previous 6 months than non-sex trade involved men. These groups did not differ with respect to any of the other variables measured.

Overall, the 995 participants were seen a total of 8046 times during the follow up period and sex trade involvement was reported at 447 (5.6%) of these visits. The median number of follow up visits among this group was eight. During the follow up period, 102 (10%) individuals initiated sex trade involvement and 70 (7%) became HIV infected. When we examined the gender of sex trade clients, sex with men was reported at 348 (78%) of the visits and with women at 99 (22%) of the visits.

The following bivariate and multivariate analyses were conducted by comparing the 210 men who were sex trade involved at some point during the entire study period with the 785 men who never reported being involved in the sex trade. As shown in table 2, in bivariate GEE analyses, factors associated with sex trade involvement among men included younger age and positive HIV serostatus. Drug related factors occurring during the previous 6 months that were associated with sex trade work included recent incarceration, injecting cocaine daily, smoking crack daily, borrowing syringes, lending syringes, and having sought but been unable to access substance abuse treatment. Both enrolment in methadone maintenance treatment and unprotected intercourse with casual sexual partners were inversely associated with sex trade work.

In multivariate analyses shown in table 3, factors that were independently associated with sex trade work included age and positive HIV serostatus at enrolment. Drug related factors that were independently associated with sex trade work in multivariate analysis included injecting cocaine daily, smoking crack daily, and borrowing syringes. Sex trade involvement was inversely associated with unprotected intercourse with casual (but not regular) sexual partners. Although failing to reach conventional statistical significance, self reported inability to access substance abuse treatment was associated with male sex trade work. Though non-significant at the p <0.1 level, variables adjusted for in the final model included recent incarceration, syringe lending, and current enrolment in methadone maintenance therapy. Lastly, we did test for statistical interactions in the multivariate model for terms defined as HIV status × syringe borrowing and for HIV status × unprotected intercourse and found no significant interactions.

DISCUSSION

Our results indicate that IDU men involved in the sex trade are more likely to be young, HIV seropositive, high intensity cocaine users who engage in risky injection behaviours including syringe borrowing. A particularly disturbing finding is that even after substantial covariate adjustment, sex workers also tended to be more likely to have sought but were unable to access substance abuse treatment, compared to their non-sex trade involved male IDU counterparts.

Our finding that male sex trade workers are more likely to be HIV seropositive than their non-sex trade involved counterparts is consistent with previous studies that have observed a relatively high prevalence of HIV infection among male and female sex trade workers.^14,24,25 In the present study, syringe borrowing was independently associated with sex trade work, even after adjustment for HIV infection. We also observed elevated rates of syringe lending in unadjusted analyses. These findings demonstrate substantial risk for acquisition and perhaps transmission of HIV infection. The context of such syringe sharing requires more investigation, including the possibility that it occurs with sex trade clients who are men who have sex with men with a relatively high prevalence of HIV.²⁶

Interestingly, while we identified elevations in specific injection related risk behaviours among male sex workers, we also found that they were less likely than other male IDUs to report unprotected intercourse with their casual sex partners. Although we were unable to measure condom use directly, this finding may be the result of a greater proportion of male casual partners among the sex trade workers compared to their counterparts not involved in the sex trade. In two previous studies, restricting analyses to condom use with male casual partners only, we found that male sex trade workers were more likely to engage in unprotected anal sex with casual partners, compared to other men who have sex with men.²⁷ Together, these results suggest that the proportion of male sex trade workers who engage in such unprotected encounters is intermediate between the higher proportion of male IDUs and lower proportion of men who have sex with men but who are not engaged in sex trade work. However, a better understanding of this and related issues will only emerge from future studies that employ standardised survey instruments with all three groups of men.⁶

A surprising finding in the present study is that male sex trade workers reported being less able to access substance abuse treatment, although this variable just failed to reach statistical significance. This result could indicate that sex trade workers are more likely to seek substance abuse treatment as a strategy to exit the trade or it may indicate lower acceptance rates into such treatment programmes. The limited provision of substance abuse treatment in our setting has been previously described,^28,29 and this problem may be particularly urgent given the greater likelihood of sex trade workers to report daily use of both injectable and crack cocaine in our study.

There are several limitations to this study. As with many other studies of IDUs, the study population was not a random sample, although the VIDUS cohort is believed to be broadly representative of IDUs in Vancouver’s Downtown Eastside neighbourhood.³⁰ Nevertheless, our study is unlikely to generalise to non-IDU male sex trade workers. In addition, socially desirable reporting is always a possibility in such studies, and stigmatised behaviours such as involvement in sex trade work may have been under-reported.³¹ However, this type of under-reporting would have led to a reduction in the strength of associations in our study. Another limitation of the present study is that sex trade work was broadly defined as receiving money, goods, drugs, shelter, or anything else in exchange for sex, which may have raised the concern of construct validity. All definitions of sex trade behaviours have limitations but it is noteworthy that if misclassification resulted from our broad definition, this too would have attenuated the associations we report.^1,32 Unfortunately, we did not collect a measure of sexual identity of the participants, which precludes our examination of the relation among sexual identity, use of condoms, and HIV infection. For example, it is possible that more male IDUs who self identify as gay or bisexual trade sex, since several studies of male sex trade workers have reported that the majority of their participants used hard drugs and identified themselves as gay or bisexual.^33,34 Therefore, it is probably that the IDUs in our study who self identify as gay or bisexual would be more likely to be involved in the sex trade.

In summary, our study demonstrates that IDU men involved in the sex trade in a Canadian setting are more likely than their non-sex trade male IDU counterparts to report high intensity cocaine use and significantly elevated injection related risk behaviours. In addition, we found that sex trade work among men tended to be associated with unsuccessful efforts to access substance abuse treatment. These findings suggest that HIV prevention interventions, as well as expanded substance abuse treatment targeted towards male sex trade workers, should be implemented to meet the unmet health service needs of this population.