Secondary HIV transmission from HIV-positive current or former drug users to their sex partners is a major public health problem. Sexual transmission may be facilitated by the disinhibitive effects of drug use, involvement in the sex trade, and coinfection with a sexually transmitted infection (STI). Previous studies among injecting drug users (IDUs) have found a reluctance to use condoms with regular sex partners,1 low levels of condom use with regular partners, and high proportions of IDUs reporting multiple sex partners.2,3
Drug treatment programs such as methadone maintenance treatment (MMT) offer a unique platform for reaching HIV-positive opioid-dependent individuals and reducing secondary HIV transmission through an integrated approach that combines HIV testing, risk reduction counseling, and linkages to HIV treatment. Participation in drug treatment itself has not been associated with reductions in sexual risk behaviors; however, sexual risk reduction interventions delivered within drug treatment programs in the United States have shown early promise,3–6 as have interventions in the United States among HIV-positive drug users to reduce sexual risk behaviors and improve adherence to highly active antiretroviral therapy.7–9
China’s national MMT program was initiated in 2004 and, by 2009, served more than 112,000 drug users daily.10 Fees are capped at 10 RMB (approximately US $1.60) per day, with fee reductions to reward consistent program attendance. Retention in MMT remains suboptimal, however, with less than 50% of the 240,000 clients who have ever enrolled in MMT remaining in the program as of 2009. Nevertheless, China’s MMT program reaches the largest number of drug users of any government program outside the criminal justice system, and it is therefore an important platform for HIV prevention interventions in this population.
We set out to measure the prevalence of sexual risk behaviors among HIV-positive opioid-dependent individuals receiving MMT in clinics across China as part of an ongoing community intervention trial examining the efficacy of a comprehensive package of behavioral and biological interventions designed to reduce HIV/hepatitis C virus incidence and to prevent secondary sexual transmission of HIV from HIV-positive clients to their spouse and sex partners. In addition, we examined predictors of unprotected sex among married participants whose spouses were either HIV negative or of unknown HIV status.
In 2004, the Chinese government instituted a pilot MMT program to combat the dual epidemics of HIV and heroin use. This program has since grown into a national network of 680 clinics across 27 provinces that provide services to more than 242,000 opioid-dependent individuals.10 Our study was nested within a larger randomized controlled trial to reduce HIV incidence among opiate-dependent individuals receiving MMT and to prevent sexual transmission of HIV from HIV-positive patients receiving MMT to their sex partners (Trial Registration: ClinicalTrials.gov NCT01108614).
Sixty clinics were selected across 5 provinces including Yunnan (18 clinics), Sichuan (12 clinics), Guizhou (6 clinics), Guangxi (10 clinics), and Xinjiang (14 clinics). Clinic inclusion criteria included a patient load of 80 or greater and HIV prevalence of 3% or greater among MMT clinic patients. All MMT clinics report routine data through the national Methadone Maintenance Treatment Network Management Data Information System, part of China’s unified, web-based, national HIV/AIDS information system. Those eligible for randomized controlled trial participation were identified from existing MMT clinic data. Inclusion criteria included being at least 20 years of age, being local residents or having lived in study sites for more than 6 months, and being committed to receive MMT for the coming 12 months or more. Patient exclusion criteria included having dropped out of MMT, having been enrolled in MMT for less than 1 month, and having severe mental or physical health problems.
Of 9499 individuals who completed baseline questionnaires and HIV testing, 2756 (29.0%) were HIV positive. Of these 2756 HIV-positive individuals, 2742 (99.5%) were included in our analyses; 14 individuals with missing data on sexual behaviors were excluded.
Between July 2009 and January 2010, study staff conducted face-to-face interviews with participants in private rooms using a structured questionnaire. Data collection included demographic characteristics, HIV/AIDS knowledge, high-risk behaviors, information on MMT, social function recovery, and HIV/STI testing and treatment. In addition, 6 mL of venous blood was collected from each participant for HIV, hepatitis C virus, syphilis, and herpes simplex virus 2 testing. Participants were paid 10 Chinese Yuan (∼US $1.30) as compensation for their time. The study protocol was reviewed and approved by the institutional review board of the National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing.
Behavioral outcomes included unprotected sex (sex without a condom) with spouse/cohabiting partner in the past 30 days, with a regular sexual partner (nonspouse, noncohabiting) in the past 30 days, and with occasional (casual or commercial) sexual partners in the past 6 months. Participants were asked whether or not they had a spouse or regular sexual partners in the past 12 months, the frequency of vaginal sexual intercourse in the past 30 days, and the number of occasional sexual partners during the previous 6 months. For each type of partner, respondents were asked whether they used a condom always, more than half of the time, less than half of the time, or never.
Blood samples were tested for HIV antibodies using an enzyme-linked immunosorbent assay (ELISA-1: Yingkexinchuang Technology Co, Ltd, Xiamen, China; ELISA-2: Shanghai Kehua Bio-engineering Co, Ltd, Shanghai, China), and positive results were confirmed by Western blot (Singapore MP Biological Asia Pacific Ltd, Singapore, Singapore).
Data were double entered into a password-protected online data collection management platform and analyzed using SPSS software (version 16.0; SPSS Inc, Chicago, IL). Descriptive analyses were performed to describe the demographic characteristics of study participants and the prevalence of risky sexual behaviors. Univariate associations between independent variables and outcomes were assessed using the χ 2 test and Fisher exact test. Multivariate logistic regression models were constructed using stepwise model selection procedures. Independent variables significant at the P < 0.1 level in univariate analyses and independent variables associated with outcomes according to prior knowledge were included in the multivariate models. We limited our multivariate analysis to married participants because we were unable to combine partnership categories because of questionnaire skip patterns.
The median age of our participants was 35 years (range, 19–63 years). Participants were recruited from MMT clinics in Yunnan (43.3%), Sichuan (10.6%), Guizhou (7.4%), Guangxi (16.2%), and Xinjiang (22.5%). Most participants were male (78.3%), had completed junior high school or lower (77.5%), were members of the Han majority ethnic group (62.5%), and were unemployed (68.0%). Nearly one fourth (22.5%) of the participants reported illicit drug use in the past 30 days, and 8.2% had dropped out in the past 6 months. Still, a sizeable proportion (12.1%) was unaware of their own HIV-positive serostatus. Among 782 participants with awareness of own HIV-positive serostatus and with HIV-negative or unknown of HIV serostatus spouse, 23.0% did not notify their HIV-positive serostatus to spouse. Sociodemographic characteristics of participants by province or autonomous region are shown in Table 1.
More than half of our study participants (1471/2742; 53.6%) were married, 6.4% (176/2742) had a regular sex partner, and 3.5% (95/2742) had 1 or more occasional sex partners. Among married participants, 62.5% (920/1471) reported sex in the past 30 days; among them, 36.1% (332/920) reported unprotected sex in the past 30 days. Among participants with a regular sex partner, 55.7% (98/176) reported sex in the past 30 days; among them, 57.1% (56/98) reported unprotected sex in the past 30 days. Among participants with 1 or more occasional sex partners, all reported sex in the past 6 months, and 64.2% (61/95) reported unprotected sex in the past 6 months. No male participants reported sex with another man.
Predictors of Unprotected Sex in the Past 30 Days Among Married Participants
Among married participants, nearly two thirds (64.6%; 950/1471) had a spouse who was HIV negative or of unknown HIV status. Among them, 62.8% (597/950) reported sex in the past 30 days, and 31.0% (185/597) reported unprotected sex in the past 30 days.
Risk factors for unprotected sex that were significant in bivariate analyses were included in a multivariate logistic regression model (Table 2). In bivariate analyses, factors significantly associated with unprotected sex included the following: age, sex, ethnicity, province where receiving MMT, correctly answering all questions on HIV/AIDS, illicit drug use in the past 30 days, having a spouse who is a current or former drug user, awareness of HIV-positive serostatus, having notified spouse of HIV status, average daily dosage of methadone in the past 30 days, feeling dosage of methadone needed to change, having dropped out of MMT in the past 6 months, and having contact with drug-using friends in the past 30 days.
Multivariate logistic regression identified 3 factors associated with an increased risk of reporting unprotected sex: receiving MMT in Guangxi (odds ratio [OR], 3.72 [2.05–6.75]; P < 0.001) or Xinjiang (OR, 2.23 [1.33–3.73], P < 0.01), having a spouse that is a current or former drug user (OR, 1.80 [1.12–2.90]; P < 0.05), and having dropped out of MMT in the past 6 months (OR, 3.05 [1.63–5.71]; P < 0.001). Two factors were associated with a decreased risk of reporting unprotected sex: being male (OR, 0.46 [0.26–0.79], P < 0.01) and being aware of own HIV serostatus (OR, 0.16 [0.10–0.27]; P < 0.001). Having contact with drug-using friend in the past 30 days was marginally associated with an increased risk of unprotected sex (OR, 1.55 [0.96–2.49]; P < 0.1).
We set out to examine the risk of secondary HIV transmission from HIV-positive MMT clinic patients to their sex partners.
We first set out to assess the prevalence of sexual risk behaviors among HIV-seropositive drug users receiving MMT in provinces with a high HIV prevalence across 5 provinces and autonomous regions in China. We found high levels of sexual risk behaviors among our study population of HIV-positive adults receiving MMT. More than half of participants were sexually active, and one third of married participants and those with regular sex partners reported unprotected sex in the past 30 days. These findings are consistent with previous research in drug user populations in North America and Europe.11–15
We then set out to examine risk factors for unprotected sex among married, sexually active participants with an HIV-negative spouse or spouse of unknown HIV status. Risk factors for unprotected sex in the past 30 days included having a spouse that is a current or former drug user, having dropped out of MMT within the past 6 months, and attending clinic in Guangxi or Xinjiang. Having contact with drug-using friends in the past 30 days was marginally associated with an increased risk of unprotected sex (P < 0.1). These findings suggest that participants at highest risk for relapse to drug use are also at highest risk for engaging in unprotected sex. Protective factors included being aware of one’s own HIV-positive serostatus and being male. These findings suggest that those HIV-positive patients on MMT who are tested and aware of their HIV serostatus take the measures required to protect their spouse from acquiring HIV. This is consistent with previous studies that have shown that awareness of HIV status leads to reduced sexual risk taking.16 These findings also suggest that male patients on MMT living with HIV may have an easier time negotiating condom use in their primary relationship compared with female patients on MMT. Previous studies have found that female IDUs are less likely to use condoms with a primary sex partner compared with male IDUs.17,18 It remains unclear why attending clinic in Guangxi or Xinjiang was associated with reporting engaging in unprotected sex.
Several limitations of our study are worth noting. First, our study population was derived from a convenience sample of patients on MMT across 5 provinces with serious HIV and heroin use epidemics. Although our study population was diverse, the nature of our sampling approach limits the generalizability of our study findings. It is likely that lower-risk IDUs are overrepresented in our study population. Second, sexual risk behaviors were self-reported and may have been subject to social desirability bias. Finally, the survey was cross sectional, and thus, it is not possible to establish causal links between the risk factors we examined and the study outcome of unprotected sex.
Nevertheless, our study findings underscore the importance of addressing sexual risk among HIV-positive drug users attending MMT. Because patients attend MMT on a near daily basis, interventions can be put in place to increase knowledge and awareness of sexual risk, HIV status, and STI status and to decrease sexual risk-taking behaviors. In addition, our study findings underscore the importance of making sure that patients on MMT are aware of their own HIV status. Although most of our participants were aware of their HIV-positive serostatus, more than 1 in 10 of those who were sexually active (11.4%; 167/1471) were not aware of their HIV-positive serostatus.
Substance abuse is an important risk factor associated with unprotected sex among HIV-discordant couples,19 and concomitant illicit drug use is common among patients on MMT.20,21 In our study, we found that nearly 1 (22.6%) in 4 married participants in HIV-serodiscordant relationships reported illicit drug use in the past 30 days and that nearly 1 (25.8%) in 4 had a spouse who is a current or former drug user. Both of these factors were associated with an increased risk of unprotected sex in the past 30 days. This points to the need to address concomitant illicit drug use among patients on MMT through optimized methadone dosing and interventions that address the context in which illicit drug use and sexual risk behaviors occur.
Treatment dropout is a major problem facing China’s MMT program. Overall, the annual retention rate in China’s national MMT program was 65.6% at the end of 2009.22 Married participants who reported having dropped out of MMT in the past 6 months were at a far higher risk for reporting unprotected sex with their HIV-negative spouse or spouse of unknown HIV status (OR, 3.05 [1.63–5.71]). Previous research has shown that maintaining drug users in MMT clinics has a beneficial effect on reducing high-risk sexual behaviors.23 The factors associated with treatment dropout are many, but key factors appear to be clinic accessibility and inadequate methadone dosage.24 Inadequate methadone dosage has increased the likelihood of concomitant illicit drug use and treatment dropout. Providing patients with appropriate methadone dosing is critical to program retention, and this also has ramifications for the prevention of secondary HIV transmission.
A number of unanswered questions remain. First, why is there a sex difference in sexual risk behaviors, and what can be done to help women take measures to avoid HIV transmission or HIV acquisition? We found that HIV-positive male patients on MMT who are in HIV-serodiscordant marriages were less likely to report unprotected sex than female patients. Further research is needed to understand the reasons why women are engaging in higher-risk sexual behaviors and to determine ways to increase condom use in HIV-serodiscordant partnerships in which the woman is HIV positive.
Second, what is behind the observed geographic variations in sexual risk taking, and what can be done to reduce sexual risk behaviors in provinces with higher levels of reported risk? We observed that HIV-positive, married patients on MMT who are in HIV-discordant partnerships in Guangxi and Xinjiang were more likely to report unprotected sex than participants from other provinces. Further research is needed to understand geographic variations in sexual risk behaviors and the individual, family, and structural factors associated with these variations.
Third, what can be done to reduce MMT dropout and concomitant illicit drug use? Illicit drug use is associated with increased sexual risk taking, and further research should focus on how to improve program retention and reduce concomitant illicit drug use. Multilevel interventions will likely be required to address factors such as inadequate methadone dosing, barriers to service access, and the family and social contexts of dropout, relapse, and illicit drug use.
Conclusions and Implications
Although treatment of opioid dependence has not been shown to reduce sexual risk behaviors in itself, MMT programs offer a unique opportunity to provide patients with additional services to help reduce secondary HIV transmission. This is urgently needed because a substantial proportion of HIV-positive patients on MMT continue to engage in high-risk sexual behaviors. However, individuals in serodiscordant marriages who were aware of their own HIV status took active measures to protect their HIV-negative spouse by using condoms. Interventions to increase awareness of HIV status, to increase partner notification, and to reduce sexual risk behaviors are therefore likely to help reduce the secondary transmission of HIV from HIV-positive patients on MMT to their HIV-negative sexual partners. In addition, interventions are needed to address concomitant illicit drug use and program dropout.
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APPENDIX. Further information on the construction of key variables included in our analyses