HIV sexual risk behaviors among injection drug users in Shanghai

Available online at www.sciencedirect.com SCII:NCE ~___~DIRECT* DRUG ALCO DEPENDENCE Drug and Alcohol Dependence 82 Suppl. 1 (2006) $43 $47 ELSEV1ER www.elsevier.com/locate/dmgalcdep Short communication HIV sexual risk behaviors among injection drug users in Shanghai M i n Z h a o a' *, J i a n g D u a, G u a n g H. Lu a, Qiu Y. W a n g a, H a n X u a, M i n Z h u a, C l y d e B. McCoy b aS~anghai Drug Abuse Treatment Center, 5~anghai Mental Health Center, 600 South Wanping Road, Shanghai 200030, China bDepartment of Epidemiology and Public Health, University of Miami, 1801 NW 9th Avenue, Suite 313, Miami, FL 33136, USA Received 1 May 2005; received in revised form 23 August 2005; accepted 11 October 2005 Abstract Purpose: This study investigated the sexual risk behaviors among injection drug users (IDUs) in order to inform the development of sexual risk reduction interventions for IDUs. Methods': A cross-sectional survey of IDUs (n 141) was conducted in an in-patient detoxification treatment center in Shanghai, China, to collect information on demographics; drug use history; sexual risk behavior; HIV/AIDS knowledge, attitudes, and other psychosocial variables; and HIM HBV, and HCV seroprevalence. Factors associated with HIV sexual risk behaviors and HBV and/or HCV infection were analyzed. Results': Sexual risk behaviors among IDUs were common: the majority (77%) of the participants had not used a condom consistently in the previous 3 months, 25.5% had multiple partners, 48.2% had IDU partners, and 75.9% did not know their partner's HIV status. IDUs who were married (OR 4.83, p < 0.05) or did not intend to use condoms in the future (OR 0.21, p < 0.05) were more likely to have unprotected sex. The prevalence of HBV and HCV infection was 31.9% and 51.8%, respectively, but no one tested positive for HIV. IDUs with an injection history of 3 years or more (OR 5.86, p < 0.05) and with an overdose history (OR 3.21, p < 0.05) were more likely to be infected with HBV and/or HCV. Conclusions: Sexual risk behaviors among IDUs in Shanghai are common, and many IDUs are vulnerable for transmission of disease. Prevention efforts with IDUs should address sexual risk behaviors in addition to needle-sharing behaviors. 9 2006 Elsevier Ireland Ltd. All rights reserved. Keywords." IDUs; HIV; Sexual risk behaviors; Shanghai, China; Hepatitis 1. Introduction In China, drug use and HIV/AIDS are referred to as twin brothers, and problems associated with them have increased dramatically during the past two decades (Wu et al., 2004; Zhao et al., 2004). The number of registered drug addicts in China reached 1.1 million by the end of 2004, and the majority (74%) were injection drug users (IDUs) (Hao et al., 2004). It is estimated that 1 million people are living with HIV in China, and 80 000 of them have developed AIDS (China Ministry of Health and UN Theme Group on HIV/AIDS in China, 2003). IDU remains the predominant mode of HIV transmission in China, although the proportion of IDUs reporting HIV infection dropped to 43% in 2003 (Chinese CDC, 2004). It is expected that high levels of HIV transmission will continue within the IDU population and the virus will spread rapidly from the *Corresponding author. Tel.: +86 21 64901737 2046; fax: +86 21 64900320. E-mail address." drzhaomin@sh163.net(M. Zhao). IDU population to other groups if no interventions are implemented (Wu et al., 2004). IDUs are a unique population for HIV prevention efforts because they have dual risks for transmission: risk associated with injection behaviors and risk associated with sexual behaviors (Kral et al., 2001). Globally, numerous studies and intervention efforts have targeted IDUs. Early studies of IDUs attributed most HIV infections to injection risks (Chaisson et al., 1987). Some studies suggested that sexual risks existed but were overshadowed by injection risks (Van Ameijden et al., 1994). More recently, studies of IDUs firmly established the important role of sexual transmission among IDUs even after accounting for injection risks (Chitwood et al., 2003; Spittal et al., 2002; Doherty et al., 2000). During the past 10 years, most research on HIV and IDUs in China has focused on collecting epidemiologic data, such as HIV prevalence and incidence and risk factors for HIV infection, in areas such as Yunnan and Guizhou, where HIV prevalence is high (Feng and Des Jarlais, 2002). In other parts of China, little is known about HIV risk 0376-8716/ $ see front matter 9 2006 Elsevier Ireland Ltd. All rights reserved. $44 3/L Zhao et aL /Drug and Alcohol Dependence 82 SuppL 1 (2006) $43~,47 behaviors, attitudes regarding condom use, self-efficacy, and voluntary HIV testing. To expand our knowledge about sexual risk behaviors among IDUs, we conducted a cross-sectional survey in Shanghai to investigate factors associated with sexual risk behaviors and HIV, HBV, and HCV infection status among IDUs. The findings from this investigation will provide important information pertinent to the development of sexual risk reduction interventions for drug users. 2. M e t h o d s 2.1. Setting and participants Study participants were receiving in-patient methadone tapering detoxification in the Shanghai Drug Abuse Treatment Center, a government-supported public health facility in central Shanghai, whose patients are primarily from that city. The only other drug-abuse treatment clinic in Shanghai is privately funded. It was excluded from this study, which focused only on IDUs from Shanghai, because its patient population is drawn primarily from outside the city. IDUs met the inclusion criteria if they were at least 18 years old; met the DSM-IV diagnostic criteria for opiate dependence as assessed by the structured clinical interview for the Diagnostic and Statistical Manual (SCID-IV) (American Psychiatric Association, 1994); and reported being sexually active within the previous 3 months. Subjects were excluded if they had serious physical or mental illnesses or cognitive deficits. 2.2. Data collection At the time of their admission to the in-patient detoxification treatment, participants were assessed for their study eligibility and interest in study participation. A structured questionnaire was used to collect data on demographic characteristics, drug use, injection practices, and sexual behaviors. The variables included (1) sexual behaviors (participants were asked to recall their sexual behaviors during the previous 3 months); (2) HIV/AIDS knowledge (participants' understanding of HIV/AIDS information was assessed using a 40-item scale, with response options of "true", "false", or "I don't know"; scores on the measure reflected the number of items answered correctly, ranging from 0 to 40, with higher scores indicating greater HIV/AIDS knowledge); (3) negative condom attitudes (four items assessed perceptions of discomfort, diminished pleasure, ejaculation difficulty, and unreliability of condoms using a 4-point scale in which scores ranged from 4 to 16, with higher values indicating more negative attitudes toward condom use); and (4) risk reduction self-efficacy (two items used a 3-point scale to assess the participants' confidence to refuse to have unprotected sex and to persuade their partners to use a condom, with scores ranging from 2 to 6 and lower scores indicating greater self-efficacy). Because all of the in-patients at the Shanghai Drug Abuse Treatment Center underwent routine laboratory testing for HIV, HBV, and HCV, infection status was obtained from the participants' medical records. The Shanghai Mental Health Center Institutional Review Board approved the research protocol. 2. 3. Statistical analyses SPSS (Version 11.0) was used for all data analyses. T-tests were used to make comparisons with continuous variables, and Chi-square tests were used with categorical variables. Multivariable logistic analyses were conducted to determine factors associated with unsafe sex and HBV and/or HCV infection after adjusting for known covariates. 3. Results 3.1. Participant characteristics Between October 2004 and March 2005, 202 IDUs were admitted to the Shanghai Drug Abuse Treatment Center; 34 patients from outside Shanghai were excluded from the study. Among the 168 IDUs eligible for the study, 141 agreed to participate and provided voluntary informed consent. All 141 participants were Chinese Hans with an average age of 30.1 years (SD=8.1); 102 (72.3%) were male and 61.8% were unmarried. The study participants had, on average, 9.9 years (SD=2.0) of education; 77.3% were unemployed. The mean age of heroin initiation was 23.1 years (SD = 6.4), and the mean years of heroin use reported was 5.7 years (SD = 3.7). The participants reported having injected heroin on a daily basis for a mean of 2.4 years (SD = 2.3). The mean quantity of heroin consumed was 0.93mg/day (SD=0.6), and the mean number of injections per day was 2.4 (SD =2.3). The majority (60%) of participants reported a history of detoxification treatment, and 36% reported having been in a detention center during the previous 3 years. 3.2. Unsafe injection behaviors Unsafe injection behaviors were common, with 125 participants (88.7%) reporting at least one unsafe injection behavior and 61 (48.8%) of those 125 participants reporting two or three unsafe injection behaviors. Unsafe injection behaviors included reusing syringes and needles (n = 105, 74.5%); not sterilizing injection works (n=54, 38.3%); not using sterile solvents (n=70, 49.6%); and sharing needles and syringes (n =37, 26.2%), cotton (n =48, 34%), or solvent (n=52, 36.9%) with other IDUs within the previous 3 months. Needles were most frequently shared with friends (81%), and 67.6% of those reporting syringe sharing did not use a cleaning procedure. 3/L Zhao et al./Drug and Alcohol Dependence 82 Suppl. 1 (2006) $43~,47 $45 Table 1 Factors important for consistent condom use among IDUs Variable Gender Male (n 102) Female (n 39) Age (years) Unmarried (n 96) Education (years) Age at first drag use (years) Years of drug injection Frequency of daily injection Self-efficacy Number of injection overdoses HIV/AIDS knowledge Negative condom attitude Equipment sharing (n 37) Failure to clean shared equipment (n 25) One sexual partner (n 105) Unsafe injection (n 125) Intended condom use in future (n 85) HBV infection (n 45) HCV infection (n 73) Positive attitude to HIV test (n 110) p-value n (%) or Mean (SD) Protected-sex g r o u p (n = 32) Unprotected-sexgroup (n = 109) 20 (62.5) 12 (37.5) 20.8 (6.5) 28 (87.5%) 10.0 (1.9) 23.3 (5.9) 2.7 (2.3) 4.0 (1.7) 3.7 (0.8) 1.2 (1.6) 25 (4.1) 8.4 (2.2) 7 (21.9%) 3 (9.4%) 24 (7.5%) 26 (81.3%) 26 (81.3%) 12 (37.5%) 15 (46.9%) 30 (93.8%) 82 (75.2) 27 (24.8) 23.3 (5.9) 68 (62.4%) 9.9 (1.9) 20.8 (4.1) 2.4 (2.4) 4.5 (2.9) 4.0 (1.2) 1.8 (1.9) 24.5 (4.0) 9.8 (1.7) 30 (27.5%) 22 (20.2%) 81 (7.4%) 99 (90.8%) 59 (54.3%) 33 (30.3%) 58 (53.2%) 80 (73.4%) 3.3. Sexual risk behavior and prevalence o f HIV, HBV, and H C V infection The mean age of first vaginal intercourse was 18.4 years (SD = 2.6, range 10-30); 105 participants (74.5%) reported only one sexual partner and 36 (25.5%) had multiple sexual partners within the previous 3 months. Almost half (48.2%) of the participants reported having IDU partners, but only 18 participants (12.8%) reported trading sex for drugs. Almost all of the participants (98.6%) were heterosexual, and the primary sexual activity within the previous 3 months was vaginal intercourse. Only 32 (23.0%) of the 139 participants who reported having had vaginal intercourse used condoms consistently. Neither of the two subjects reporting oral or anal sex reported using condoms consistently. The reasons for not using condoms included the following: do not want to use (41.5%); believe partner is healthy (17%); condom was not available (15.1%); feel uncomfortable (13.2%); forget to use (9.4%); and other unspecified reasons (3.8%). Most participants (82.9%) had never been tested for HIV, and three-quarters (75.9%) did not know their partners' HIV status. Almost all of the participants (91.5%) had never participated in an HIV prevention program. The majority (75.2%) believed that it was impossible for them to be infected with HIV, and most (78.0%) reported that they would take a voluntary HIV test if it were available. ns >0.05 <0.01 >0.05 <0.01 >0.05 >0.05 >0.05 <0.01 >0.05 <0.05 >0.05 <0.05 >0.05 >0.05 <0.01 >0.05 >0.05 <0.05 The laboratory test results showed that there were 45 HBVpositive participants, 73 (51.8%) HCV-positive participants, and no HIV-positive participants. 3.4. Factors associated with condom use and H B V and~or H C V infection The participants were divided into two groups according to their use of condoms within the previous 3 months: the "protected-sex group" (with consistent condom use) included 32 participants, and the "unprotected-sex group" (without consistent condom use) included 109 participants (Table 1). Bivariate analyses were conducted to identify statistically significant factors associated with unprotected sex among IDUs. IDUs in the "protected-sex group" were more likely to be unmarried and to report that they intended to use condoms and take voluntary HIV tests in the future. IDUs in the "unprotected-sex group" were younger at the onset of drug use, overdosed more frequently, failed to clean shared injection equipment, and exhibited negative attitudes toward condom use. Additional bivariate analyses did not find any significant differences between male and female IDUs. To understand factors related to HCV and/or HBV infection, participants were recoded into two categories: infected or not infected. Bivariate analyses showed that HBV and/or HCV infection was associated with a previous history of detention, a previous history of $46 3/1. Zhao et aL /Drug and Alcohol Dependence 82 SuppL 1 (2006) $ 4 3 ~ 4 7 overdose, and longer duration of drug use. The multivariate regression analysis results indicate that married IDUs were significantly more likely to have had unprotected sex than unmarried IDUs (OR=4.83, p <0.05). IDUs reporting an intention to use condoms in the future were significantly less likely to have had unprotected sex (OR = 0.21, p < 0.05) than those without future intentions to use condoms. IDUs with an injection history of 3 or more years and an overdose history were more likely to be infected with HBV and/or HCV than were IDUs with an injection history of less than 3 years (OR = 5.86, p < 0.05) and without an overdose history (OR=3.21, p < 0.05). 4. Discussion Our findings support conclusions from other studies that sexual risk behaviors are common among IDUs and that these behaviors are associated with demographic and drug use characteristics (Doherty et al., 2000; Patrick et al., 1997). For example, a 22-site study of almost 27 000 NorthAmerican drug users found that 80% of sexually active IDUs reported having had unprotected sex in their last sexual encounter (Rhodes et al., 1999). Thus, it is through sexual relations with non-drug-using partners that IDUs can transmit HIV infection to the general population. The important implication of our findings is the need for HIV prevention interventions to address both the sexual risk behaviors and needle-sharing behaviors of IDUs. The findings, which suggest that unprotected sex is associated with early onset of drug use, greater severity of drug use, higher number of overdoses, and failure to clean shared equipment, are supported by other studies (Somlai et al., 2003; Belanger et al., 2002) that relate sexual risk behaviors to IDU behaviors, severity of drug use, and negative attitudes toward condom use. Together, these findings provide important information for developing sexual risk reduction interventions for IDUs. To improve outcomes, future sexual risk reduction interventions should focus on vulnerable IDUs and acknowledge drug-use severity, condom-use attitudes, self-efficacy, and other factors associated with condom use. Because previous investigations in other areas of China found that the HIV seroincidence ranges from 20% to 90% among IDU populations (Cheng et al., 2000; Zheng et al., 1994), this study's 0% HIV seroincidence among IDUs in Shanghai was unexpected. China has experienced a unique pattern: the epidemic of HIV among IDUs began in rural areas and then spread to urban areas. This circumstance has contributed to considerable variations in HIV prevalence among Chinese IDUs. Currently, about 80% of China's HIV-positive individuals reside in rural areas such as Yunnan, Guangxi, and Xinjiang provinces (China Ministry of Health, NCAIDS, and Collaboration Group for National HIV Sentinel Surveillance Program, 2000). Although the generalizability of HIV prevalence among IDUs in Shanghai is limited, the available data from 2004 show that Shanghai has a very low HIV prevalence: only 1124 HIV infections (0.066%) were documented (Shanghai CDC, 2004). Our results suggest that Shanghai might be at the beginning of an HIV epidemic. In addition, the prevalences of HBV and HCV (31.9% and 51.8%, respectively) also were lower than those reported for other areas of China (68% and 92%, respectively) (Cheng, 1993; Li et al., 1994). The risk factors for HBV and/or HCV infection found in our study are similar to those of other studies (Zhao et al., 1999): IDUs with more years of drug injection and more severe drug use (including a history of overdose) are more likely to be infected with HBV and/or HCV. Residents of Shanghai, the biggest and most developed city in China, experience an economy, culture, attitude, and lifestyle vastly different from the rural areas of China that report high HIV prevalence, such as Yunnan and Xingjiang provinces. Consequently, the IDUs in Shanghai might face fewer economic pressures to engage in high-risk behaviors, such as trading sex for drugs, which might translate to relatively lower levels of HIV, HBV, HCV, and other bloodborne viral infections. This possibility was supported by our findings regarding a lower prevalence of sharing syringes and needles (26.2%) and trading sex for drugs or money (12.8%) in Shanghai than in other areas of China (Zhang et al., 2002; Zheng et al., 1994). Further studies are needed to understand the reasons for the differences in HIV prevalence and risk behaviors among IDUs throughout China. Several limitations in this study should be acknowledged. First, no HIV-positive participants were recruited, and no analyses can be conducted on the association between HIV infection and sexual risk behaviors among IDUs. Second, there are obvious limitations of self-reported data: because sexual behavior is a sensitive topic in Chinese culture, the sexual risk data might be underreported and prone to social desirability response bias. Third, we cannot draw definitive causal inferences because the data is cross-sectional. Fourth, our sample was drawn from IDUs seeking in-patient detoxification treatment; therefore, the findings are not generalizable to all IDUs in Shanghai. Finally, the small sample size might inhibit detection of other potentially associated factors. Further epidemiologic prospective cohort studies should be conducted to clarify the relationship between different modes of sharing injection equipment, sexual behavior, and HIV and HCV infection among a large sample that includes high HIV prevalence areas throughout China. Despite these limitations, the findings from this study can provide information for developing effective sexual risk reduction interventions for Chinese IDUs. Facing an increasing HIV epidemic among IDUs, China has established more than 10 clinics to provide methadone maintenance treatment for heroin dependency. These new methadone clinics can provide an ideal platform to develop, implement, and evaluate comprehensive, integrated HIV prevention and treatment programs designed to decrease 3/1. Zhao et aL /Drug and Alcohol Dependence 82 SuppL 1 (2006) $ 4 3 ~ 4 7 both drug use and risky sexual behaviors among this highrisk population and thereby address the increasing HIV epidemic in China. Acknowledgments This study was supported by a Shanghai Public Health Fund grant, #00406 (Min Zhao, PI). The authors extend their appreciation to Mary Comerford at the University of Miami for her constructive comments and editing of the paper. References American Psychiatric Association, 1994. Diagnostic and statistical manual of mental disorders, 4th ed. Washington, DC. Belanger, D., Godin, G., Alary, M., Bernard, RM., 2002. 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