JAIDS Journal of Acquired Immune Deficiency Syndromes:
Brief Report: Epidemiology and Social Science
Elevated Syringe Borrowing Among Men Who Have Sex With Men: A Prospective Study
Marshall, Brandon D.L BSc*†; Wood, Evan PhD*‡; Li, Kathy PhD*; Kerr, Thomas PhD*‡
From the *British Columbia Centre for Excellence in HIV/AIDS, St. Paul's Hospital, Vancouver, BC, Canada; †Department of Health Care and Epidemiology, University of British Columbia, Vancouver, BC, Canada; and the ‡Department of Medicine, University of British Columbia, Vancouver, BC, Canada.
Received for publication March 12, 2007; accepted June 29, 2007.
Supported by grants from the US National Institutes of Health (R01 DA011591-04A1) and Canadian Institutes of Health Research (MOP-67262).
Thomas Kerr is supported by a New Investigator award from the Canadian Institutes of Health Research (CIHR) and a Scholar Award from the Michael Smith Foundation for Health Research (MSFHR). Brandon Marshall is supported by a Canada Graduate Scholarship from CIHR and a Graduate Trainee Award from MSFHR.
Correspondence to: Thomas Kerr, PhD, BC Centre for Excellence in HIV/AIDS, 608-1081 Burrard St., Vancouver, BC, Canada V6Z 1Y6 (e-mail: firstname.lastname@example.org).
Objective: Despite efforts to scale up HIV prevention services for drug users, high rates of HIV risk behavior persist among some subpopulations. Given that few prospective studies have considered the relationship between sexual activity and syringe sharing, we sought to evaluate syringe sharing among male injection drug users (IDUs) who have sex with men (MSM) in Vancouver.
Methods: We performed a longitudinal analysis of factors associated with syringe borrowing among male participants enrolled in the Vancouver Injection Drug Users Study during the years 1996 to 2005 using generalized estimating equations (GEE).
Results: Among the 1019 male participants included in this analysis, 553 (54.3%) reported borrowing syringes during the study period. In multivariate GEE analysis, MSM were at an elevated risk for syringe borrowing (adjusted odds ratio [AOR] = 1.50, 95% confidence interval [CI]: 1.10 to 2.04) after extensive adjustment for other known risk factors.
Conclusions: Among male participants, having sex with men was found to be strongly and independently associated with syringe borrowing. Our findings may aid policy makers in their efforts to identify IDUs who should be targeted with education and prevention efforts, and indicate the need for ongoing development of prevention interventions that address sexual orientation.
Injection drug use continues to fuel HIV epidemics in many settings throughout the world. Syringe sharing, including both the distributive (“lending”) and receptive (“borrowing”) use of contaminated syringes, remains the primary mechanism driving the transmission of HIV among injection drug users (IDUs).1-4 The proportion of HIV infections associated with injection drug use appears to be declining in some settings,5 but recent data indicates that IDUs and male IDUs who have sex with men (MSM IDUs) continue to account for approximately 17% of new HIV diagnoses.6 In response to the high rates of HIV infection among IDUs, needle exchange programs have been implemented in many countries. Although syringe exchange programs have been effective in reducing HIV risk behavior and HIV seroconversion among IDUs,7-9 several studies have documented persistent high-risk syringe sharing among certain subpopulations most at risk for HIV infection, even in the presence of effective needle exchange programs.10,11
MSM IDUs are known to be a unique population at particularly high risk for acquiring HIV infection.12,13 There is a growing body of evidence documenting the specific elevated risks for MSM drug users. For example, MSM IDUs have been observed to have more sexual partners and trade sex for money or drugs more often than non-MSM IDUs.14 Furthermore, several studies have documented strong associations between injection methamphetamine use and engagement in sexual risk behaviors.15,16 There is also evidence that MSM IDUs are more likely to engage in high-risk injection behaviors than their heterosexual counterparts. For example, homosexuality and bisexuality have been found to be positively and independently associated with shooting gallery use.17
Although male-to-male sexual activity has been previously identified as a risk factor for HIV infection among IDUs,18 there is a dearth of prospective studies examining syringe borrowing and sexual practices among community-recruited samples of male IDUs. Therefore, we undertook the present study to evaluate the impact of sex- and drug-related behaviors on syringe borrowing within a prospective cohort of male IDUs in Vancouver during the years 1996 to 2006. It is hoped that this data will serve to inform harm-reduction efforts that target specific populations of IDUs who may disproportionately engage in syringe-sharing behaviors and thus be most at risk for HIV infection.
The Vancouver Injection Drug Users Study (VIDUS) is an ongoing prospective cohort study of injection drug-using individuals recruited through self-referral and street outreach from Vancouver's Downtown Eastside (DTES) starting in May 1996. The study has been described in detail previously.19-21 Briefly, persons were eligible if they had injected illicit drugs at least once in the previous month, resided in the greater Vancouver region, and provided written informed consent. At baseline and semiannually, subjects provide blood samples for HIV and hepatitis C serology and complete an interviewer-administered questionnaire. The questionnaire elicits demographic data and information regarding illicit drug use, HIV risk behaviors, addiction treatment experience, and sexual activity. All participants receive a monetary stipend of $20 CDN after each visit. The University of British Columbia's Research Ethics Board has provided ethical approval for the project.
For the purposes of the present study, we hypothesized that male IDUs who report having sex with men would be more likely to report receptive syringe sharing than those do not. All participants enrolled from May 1996 to December 2005 who identified their biological sex at birth as male were included in the analysis. During follow-up, participants were asked to report any syringe borrowing or male-to-male sexual activity that occurred in the 6-month period prior to the interview. Other explanatory variables of interest in this analysis included socio-demographic information: age, Aboriginal ethnicity (yes/no), and unstable housing. Drug use variables that were considered included frequent heroin injection, frequent cocaine injection, and frequent crack cocaine smoking. Other risk characteristics that were considered included unsafe sex, sex trade involvement, recent incarceration, methadone maintenance therapy, requiring help injecting, binge use of drugs, and residence in the Downtown Eastside (ie, Vancouver's epicenter of illicit drug use and HIV). Consistent with our previous work,21-23 we defined “unsafe sex” as not always using condoms during vaginal or anal intercourse with regular sexual partners, casual sexual partners, or sex trade clients; “unstable housing” as living arrangements such as single room occupancy hotels, hostels, recovery houses, or homelessness; “frequent drug use” as daily injection of cocaine or heroin or daily smoking of crack; “binge drug use” as self-reported periods when drugs were injected more frequently than usual; and “incarceration” as being in detention, jail, or prison overnight or longer. All behavioral variables refer to behaviors occurring during the past 6 months.
As a first step, we examined univariate associations between socio-demographic, sex- and drug-related characteristics and syringe borrowing at baseline using the Pearson χ2 test and the Wilcoxon rank sum test. Because analyses of factors potentially associated with syringe borrowing during follow-up included serial measures for each subject, we used generalized estimating equations (GEE) for binary outcomes with logit link for the analysis of correlated data to determine which factors were independently associated with syringe borrowing in the prior 6 months throughout the 85-month follow-up period. GEE models account for the correlation between repeated measures for each subject, and as such, data from every participant follow-up visit was considered in the analysis. Because an individual participant may or may not have engaged in receptive syringe sharing during a 6-month follow-up period, this approach permits the examination of behaviors and characteristics that are correlated with times borrowing or not borrowing syringes within individuals and between individuals. The GEE method is commonly used for studies in which a repeated-measure, binary-dependent variable is analyzed longitudinally. Furthermore, it has been described in our previous work24 and has also been used successfully in previous studies that examined the correlates of unprotected sex and syringe sharing among IDUs.25 Variables potentially associated with syringe borrowing were examined in bivariate GEE analyses. To adjust for potential confounding, we also fit a multivariate logistic GEE model using an a priori defined model-building protocol of adjusting for all variables that were statistically significant at the P < 0.05 level in bivariate analyses. All statistical analyses were performed using SAS software version 8.0 (SAS, Cary, NC). All P values are 2-sided.
Out of 1019 male participants eligible for this analysis, 553 (54%) reported syringe borrowing at some point during the study period. Of 9702 observations, borrowing was reported a total of 1931 (19.9%) times. In the group of 1019 participants, 199 (20%) self-identified as Aboriginal, and the median age at baseline was 34.9 years of age (interquartile range [IQR] 27.4 to 41.2). At baseline, 102 (10%) participants reported ever having sex with men, while 120 (12%) reported having sex with men at some point during the follow-up period. The total number of reports of male-to-male sexual activity in the 6-month period before an interview was 395 (4.1%).
The baseline characteristics of the participants stratified by syringe borrowing are shown in Table 1. As shown, IDUs who reported syringe borrowing at baseline were more likely to be MSM (odds ratio [OR] = 1.96, 95% confidence interval [CI]: 1.30 to 2.96) and require help injecting (OR = 1.74, 95% CI: 1.33 to 2.27). IDUs who were Aboriginal (OR = 0.62, 95% CI: 0.44 to 0.87) and frequent crack smokers (OR = 0.53, 95% CI: 0.30 to 0.95) were significantly less likely to engage in syringe borrowing compared to those who were not.
The results of the bivariate and multivariate GEE analyses are shown in Table 2. All socio-demographic and drug-use variables considered were found to be statistically significant in the bivariate analysis. Factors positively associated with syringe borrowing included MSM (OR = 2.43, 95% CI: 1.88 to 3.15), unsafe sex (OR = 1.33, 95% CI: 1.17 to 1.52), sex trade involvement (OR = 2.49, 95% CI: 1.94 to 3.20), recent incarceration (OR = 1.83, 95% CI: 1.61 to 2.08), DTES residency (OR = 1.22, 95% CI: 1.06 to 1.41), unstable housing (OR = 1.30, 95% CI: 1.16 to 1.46), frequent heroin injection (OR = 1.98, 95% CI: 1.72 to 2.27), frequent cocaine injection (OR = 2.01, 95% CI: 1.76 to 2.30), requiring help injection (OR = 2.62, 95% CI: 2.27 to 3.04), and binge drug use (OR = 2.34, 95% CI: 2.07 to 2.64). Factors negatively associated with syringe borrowing were older age (OR = 0.95, 95% CI: 0.94 to 0.96), Aboriginal ethnicity (OR = 0.60, 95% CI: 0.46 to 0.78), frequent crack smoking (OR = 0.67, 95% CI: 0.57 to 0.79), and methadone therapy use (OR = 0.60, 95% CI: 0.50 to 0.72).
In the multivariate GEE analysis also shown in Table 2, having had sex with men in the past 6 months remained positively and independently associated with syringe borrowing (adjusted odds ratio [AOR] = 1.50, 95% CI: 1.10 to 2.04). Other factors that remained positively associated with syringe borrowing included unsafe sex (AOR = 1.36, 95% CI: 1.18 to 1.56), sex trade involvement (AOR = 1.54, 95% CI: 1.16 to 2.05), recent incarceration (AOR = 1.32, 95% CI: 1.15 to 1.50), unstable housing (AOR = 1.21, 95% CI: 1.07 to 1.37), frequent heroin injection (AOR = 1.46, 95% CI: 1.26 to 1.69), frequent cocaine injection (AOR = 1.48, 95% CI: 1.28 to 1.71), requiring help injecting (AOR = 2.17, 95% CI: 1.85 to 2.55), and binge drug use (AOR = 1.80, 95% CI: 1.59 to 2.05). Factors negatively associated with syringe borrowing in the multivariate analysis included older age (AOR = 0.97, 95% CI: 0.96 to 0.98), Aboriginal ethnicity (AOR = 0.53; 95% CI: 0.40 to 0.70), frequent crack smoking (AOR = 0.62; 95% CI: 0.53 to 0.74), and methadone therapy use (AOR = 0.83, 95% CI: 0.69 to 0.99).
In the present study, we found high rates of syringe borrowing among a community-recruited sample of male IDUs. In total, 54% of study participants had borrowed syringes at some point during the study period. After adjustment for all known risk factors, we found that male IDUs were significantly more likely to report borrowing syringes at a 6-month follow-up if they had also had sex with men during the same period. Although other factors were also found to be independently associated with syringe borrowing, the strong association between MSM activity and this HIV risk behavior is particularly significant owing to it being a novel finding and because of the potential implications for policy decisions and targeted harm-reduction programming.
It is worrisome that in multivariate longitudinal analysis, MSM IDUs in this cohort were 1½ times more likely than non-MSM IDUs to engage in syringe borrowing. The present study is consistent with earlier cross-sectional studies that found elevated rates of syringe sharing among MSM IDUs compared to non-MSM IDUs18,26 and with evidence indicating that MSM IDUs are at significantly heightened risk for HIV infection.12,18,27-29 The association between MSM and syringe borrowing may be partially explained by differences in sexual partnerships between MSM IDUs and non-MSM IDUs. For example, there is some evidence that syringe sharing among MSM may occur in communal settings that involve or act as a precursor to sexual activity; such environments may include circuit parties, bathhouses, and sex clubs.30,31 Further research should be conducted to investigate the environmental and social factors influencing the complex association between syringe sharing and male-to-male sexual activity. An alternate possibility is that MSM IDUs are using health services and needle-exchange programs less frequently than heterosexual IDUs. However, this explanation is not supported by recent evidence from other settings demonstrating a high proportion of MSM IDUs accessing syringe-exchange programs (SEPs).26 Further investigation would be necessary to effectively characterize any potential differences in service access and SEP utilization among MSM and non-MSM IDU populations at the local level.
The results presented in this study have clear implications for HIV prevention and intervention measures, in terms of explicitly acknowledging specific IDU subpopulations that most frequently engage in injection-related risks. Of concern is that MSM IDUs, when compared to MSM who do not inject drugs, have also been found to more frequently engage in unprotected anal sex with casual partners.32 Although in the present study we did not compare sexual risk behaviors among these populations, we did find engagement in unprotected sex to be positively and independently associated with syringe borrowing. These results suggest that sexual and drug-related behaviors may interact to play substantive roles in determining the risk of HIV infection and transmission in male IDU populations. Our results also support previous research18,27 that suggests pertinent interventions sensitive to diverse sexualities and sexual orientations may be required to effectively address both the sexual and injection-related risks unique to this population. In light of these findings, further study of the multifactorial associations between sexual practices and injection behaviors among male IDUs is urgently needed on the local level.
This study has several limitations that should be noted. First, we have identified only the association between MSM and syringe-borrowing behavior over the 6-month period before a follow-up interview; we did not measure event-specific dynamics surrounding syringe sharing and sexual activity. Although many studies have demonstrated a strong correlation between drug use and unsafe sexual behavior among MSM33 and MSM IDUs,27,34 the immediate temporal determinants of such associations remain unknown. However, it is noteworthy that in longitudinal analysis, the association between MSM and syringe borrowing persisted after adjustment for other sexual and drug-related risk factors that may elevate the rate of syringe sharing. A second limitation is that of reporting bias, a tendency that may underestimate socially undesirable HIV risk behaviors among certain populations of IDUs.35 Given that our study relies on self-report and that syringe borrowing and homosexual activity are both stigmatized behaviors, it is possible that they have been underreported. However, we know of no reason to suspect that differential reports of syringe borrowing would occur between MSM IDUs and non-MSM IDUs. Finally, the study population was not a random sample, and therefore it is not known whether these findings will generalize to other IDU populations.
In summary, we found high rates of syringe borrowing among male IDUs, and among these participants, having sex with men was independently associated with syringe borrowing after adjustment for all other known risk factors. This study points to the need for further study of syringe sharing within certain subpopulations of IDUs and in specific sexual settings. In addition, these results should raise public health concern about the high rates of injection-related risk behaviors among those individuals who are also at high risk for sexual transmission of HIV, and they suggest that harm-reduction efforts such as SEPs should continue to take a multifactorial and population-specific approach to HIV prevention that incorporates both distinct sexual and injection-related risks.
We would particularly like to thank the VIDUS participants for their willingness to participate in the study. We also thank Steffanie Strathdee, Deborah Graham, Caitlin Johnston, Carley Taylor, Will Small, Bonnie Devlin, John Charette, Vanessa Volkommer, Steve Kain, Kathy Churchill, Dave Isham, Cristy Power, Sidney Crosby, Nancy Laliberte, Sue Currie, and Peter Vann for their research and administrative assistance.
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