JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Prevention
Prevalence and Correlates of HIV and HCV Infection Among Amphetamine-Type Stimulant Users in 6 Provinces in China
Bao, Yan-Ping MD, PhD*; Liu, Zhi-Min MD*; Lian, Zhi MD*; Li, Jian-Hua MD†; Zhang, Rui-Min MD†; Zhang, Cong-Bin MD†; Hao, Wei MD, PhD‡; Wang, Xu-Yi MD, PhD‡; Zhao, Min MD, PhD§; Jiang, Hai-Feng MD§; Yan, Shi-Yan MD, PhD*; Wang, Qing-Liang MD*; Qu, Zhi MD*; Zhang, Hao-Ran MD*; Wu, Ping MD, PhD*; Shi, Jie MD, PhD*; Lu, Lin MD, PhD*
*National Institute on Drug Dependence, Peking University, Beijing, China
†Yunnan Institute for Drug Abuse, Xi Hua Yuan, Kunming, Yunnan, China
‡Mental Health Institute, The Second Xiangya Hospital, Central South University, Hunan, China
§Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
Correspondence to: Prof. Zhi-Min Liu, MD, National Institute on Drug Dependence, Peking University, 38, Xue Yuan Road, Hai Dian District, Beijing 100191, China (e-mail: firstname.lastname@example.org).
Supported by the Eleventh Five-Year Program of the Chinese Ministry of Science and Technology (no. 2008ZX10001-003 and 2012ZX10001001 to L.L.), National Basic Research Program of China (no. 2009CB522007 to L.Z.M.), and National Natural Science Foundation of China (no. 81001265 to B.Y.P).
The authors have no conflicts of interest to disclose.
All authors contributed to and approved the final article.
Received November 11, 2011
Accepted March 19, 2012
Background: China has experienced an epidemic of amphetamine-type stimulant (ATS) use in recent years. The present study explored the status and correlates of HIV and hepatitis C virus (HCV) infection among ATS users in China.
Methods: A multicenter cross-sectional study of HIV and HCV status and associated behaviors among ATS users was conducted in 6 provinces from September 2009 to December 2010. Socioeconomic/behavioral risk factors were measured. Blood samples were collected to test for HIV and HCV antibodies.
Results: Of the 1327 ATS users, the prevalence of HIV and exposure to HCV were 4.5% and 43.5%, respectively, with large geographic variations (0%–20.3% and 8.6%–67.1%, respectively). HIV infection was independently associated with living in Yunnan province [adjusted odds ratio = 15.8; 95% confidence interval (CI): 2.0 to 125.1), polydrug use (adjusted odds ratio = 2.6; 95% CI: 1.3 to 5.4), increased frequency of sexual behavior (adjusted odds ratio = 2.0; 95% CI: 1.1 to 4.1), history of sex with sexually transmitted infection–positive persons (adjusted odds ratio = 11.4; 95% CI: 1.3 to 98.9), and HCV infection (adjusted odds ratio = 2.8; 95% CI: 1.2 to 6.7). HCV was associated with study site, marital status, unemployment (adjusted odds ratio = 1.8; 95% CI: 1.3 to 2.4), a longer duration of ATS use, and history of injection use of ATS (adjusted odds ratio = 13.3; 95% CI: 1.5 to 116.1).
Conclusions: The prevalence of HIV was high among ATS users in Yunnan province but quite rare elsewhere, and the prevalence of exposure to HCV was high in 6 provinces. Risk factors emphasize the need for new prevention strategies toward this population at risk in China.
Southeast Asia is experiencing an epidemic of amphetamine-type stimulant (ATS) use, including methamphetamine (MA), methylenedioxymethamphetamine (MDMA or ecstasy), and their analog substances.1,2 In China, ATS appeared at the end of the 1990s and dramatically spread during the subsequent decade, particularly among adolescents and young adults.3 Data from the China National Narcotic Control Commission showed that 59,500 people used or abused ATS in 2005, accounting for 6.7% of registered drug users. However, the number of ATS users increased dramatically to 0.43 million, accounting for 28% of the 1.54 million registered drug users by the end of 2010.4 Previous survey on ATS use showed that ATSs are mainly used by noninjection administration in China.5 MA is usually used by the smoking route at home or in hotels. Ecstasy and “magu” pills (mixed MA with other drugs) are usually used orally in dance halls or discos.5 The main purpose of ATS use was reported to be the pursuit of euphoria or improving mood,5 which is different from the purpose of increasing energy for work in other countries in Southeast Asia.2,6
ATSs are addictive stimulants that affect the central nervous system, and the use of ATS was associated with susceptibility to HIV infection and transmission through its influence on sexual behavior.7–9 ATSs enhance sexual desire, lengthen sexual episodes, and prolong sexual pleasure, which have been associated with sexual risk behaviors that result in vulnerability to HIV infection among this population.10 ATS users have also been found to engage in more HIV-related sexual risk behavior, including unprotected sex and sex with multiple partners among men who have sex with men and heterosexual adults.9,11–13 Young adults who use ATS frequently may be at risk for experiencing a greater burden of HIV in Southeast Asia.9,14–16 In China, the increase in ATS use may have contributed to the rapid increase in the spread and transmission of HIV by sexual contact. A recent joint assessment of HIV/AIDS in China demonstrated that sexual transmission has become a major mode of the spread of HIV.17,18 In 2009, China estimated that among the 48,000 new cases of HIV infection, 75% were caused by sexual contact.18–20
Hepatitis C virus (HCV) is primarily transmitted by sharing contaminated needles and other injection paraphernalia in injecting drug users (IDUs). Previous studies have investigated the occurrence of HCV and focused on heroin users.21,22 However, some studies have linked HCV infection and noninjection risk behaviors, including unsafe sexual practices.23 More recent evidence indicated that unsafe sexual behavior was associated with HCV infection in MA users.24,25 Fewer studies have investigated HCV transmission among ATS users in China.
With the increasing number of ATS users and increased HIV transmission by sexual contact in China, the risk of HIV and HCV infection associated with ATS use may have increased. However, little is known about the status and associations of HIV and HCV infection among ATS users in China. Such findings would provide information for the development of prevention and intervention strategies for HIV and HCV infection in this population.
MATERIALS AND METHODS
Setting and Participants
A multicenter cross-sectional study of HIV and HCV status and risk behavior among ATS users was conducted in compulsory detoxification centers in Beijing, Shanghai, and Guangdong province and voluntary detoxification centers in Shanghai, Hunan, Hubei, and Yunnan province from September 2009 to December 2010. Eligible participants met the following criteria: (1) at least 18 years old; (2) urine test positive for at least one ATS drug, including MA, magu pills (the main component of which is MA), and MDMA, at the time they entered the detoxification center; and (3) signed informed consent. The participants were excluded if they had serious physical or mental illnesses or cognitive deficits. The Peking University Health Center's Institutional Review Board approved the research protocol. During the period of investigation, the participants were assessed for their study eligibility and interest in study participation by trained health workers in each center at the time of their admission to the center of detoxification. Private information was collected and stored confidentially and was not connected with any official record or management that might have imposed punishment. The HIV and HCV infection results were conveyed by health care workers to the participants and reported to the local Centers for Disease Control and Prevention. Appropriate risk reduction counseling was provided to all the participants, and referrals for appropriate medical, mental health, and social support services were provided as needed. A total of 1357 ATS users were recruited for an interviewer-administered risk behavior survey, and blood samples were collected to test for HIV and HCV antibodies.
Measures and Test
In a separate room, face-to-face interviews were conducted by trained interviewers using a structured questionnaire that included demographic characteristics, drug use history, and sexual behaviors. The demographic variables included sex, age, ethnicity, education, marital status, and employment. Questions about drug use history investigated the types of ATS ever used and used during the past month, frequency of ATS use, duration of ATS use, and history of injection of ATS. Sexual behaviors included changes in sexual desire after using ATS assessed by the visual analog scale (VAS), duration of each sexual episode after using ATS, number of sexual partners after using ATS during the past year, homosexual sex after using ATS, history of sex with an HIV-positive person, and history of sex with sexually transmitted infection (STI)–positive persons. The VAS is a psychometric response scale that measures subjective characteristics or attitudes that cannot be measured directly. A blood sample was collected from each participant to test for HIV and HCV antibodies. HIV and HCV antibodies were tested using an enzyme-linked immunosorbent assay. Positive test results for HIV were further confirmed by Western blot, and positive results on both tests indicated HIV infection.
The data were double entered, and the consistency of both databases was compared using Epi Data software (Epi Data Association, Odense, Denmark). The estimations of the means and proportions were calculated to describe the demographic characteristics, drug use history, and sexual behaviors. Pearson χ2 test and bivariate logistic regression were used for the bivariate analysis of demographic characteristics, drug use history, and sexual history with different HIV and HCV infection status. A multivariate logistic regression model was constructed using a stepwise backward sequence. All significant variables in the bivariate analysis were introduced into the multivariate model. All analyses were performed using SAS software, version 9.1 (SAS Institute, Cary, NC). Statistically significant findings were determined using a 2-tailed P value of 0.05.
General Description of Participants
Of the 1357 participants enrolled in this study, 30 (2.2%) were excluded from the analysis because of missing HIV or HCV results. The remaining 1327 eligible participants (97.8%) were included in the study. Among the 1327 participants, 687 (51.8%) were recruited from compulsory detoxification centers and 640 (48.2%) were recruited from voluntary detoxification centers (Table 1). The ages of the participants ranged from 18 to 65 years (mean, 33.4 years). The majority (95.5%) belonged to the Han ethnic group. Eight hundred fifty-five (66.3%) were male, 869 (66.2%) completed primary school or junior high school, 619 (47.1%) were unmarried, and 596 (46.0%) were unemployed.
History of Drug Use
MA was ever used by 1104 participants, accounting for 84.7%, followed by magu pills (35.2%) and MDMA (21.2%; Table 1). During the past month, 82.1%, 24.8%, and 3.4% used MA, magu pills, and MDMA, respectively. MA was the main drug used in Beijing, Shanghai, Guangdong, and Yunnan provinces and municipalities, and magu pills were mainly used in Hubei and Hunan province. A total of 585 (44.1%) had a history of polydrug use, indicating the use of 2 or more ATS or other drugs. The mean duration of ATS use was 25.2 months (SD = 26.6 months; range, 0.1–200 months), and 19 participants (1.5%) had a history of injection use of ATS.
Half of the ATS users (665; 54.3%) reported enhanced sexual desire on the VAS, and 571 (87.3%) reported a prolonged sexual episode after using ATS. Among the participants who reported sexual behavior after using ATS, 513 (76.5%) had 2 or more different sexual partners during the past year, 258 (38.2%) never used condoms during sex after ATS use, and 13 had a history of male homosexual sex.
TABLE 2-b Risk Facto...Image Tools
Prevalence of HIV Infection and Exposure to HCV
Among the 1327 participants, HIV infection was detected in 4.5% [95% confidence interval (CI): 3.4% to 5.6%] and 577 (43.5%) were exposed to HCV (95% CI: 40.8% to 46.2%). Coinfection with HIV and HCV was found in 48 cases (3.6%; 95% CI: 2.6% to 4.6%). A large geographical variation was observed for HIV prevalence (range by site, 0%–20.3%) and prevalence of exposure to HCV (range by site: 8.6-67.1%) among ATS users in the above areas. The HIV prevalence was the highest (20.3%) in Yunnan province, followed by Beijing (0.7%) and Hubei province (0.4%). No HIV-positive cases were found among the participants from Shanghai, Guangdong, and Hunan provinces. The prevalence of exposure to HCV was highest in Yunnan (67.1%), followed by Guangdong (64.1%), Shanghai (39.0%), Hubei (30.6%), Beijing (17.8%), and Hunan (8.6%).
Correlates of HIV Infection and Exposure to HCV
In the multivariate analysis, the factors associated with HIV infection were living in Yunnan province, polydrug use, increased frequency of sexual behavior after using ATS, history of sex with STI-positive persons, and HCV infection (Table 2). The multivariate model showed that the significant factors associated with exposure to HCV included study site, marital status, unemployment, a longer duration of ATS use, and history of injection use of ATS (Table 3).
TABLE 3-b Risk Facto...Image Tools
To our knowledge, this is the first survey that assessed HIV and HCV infection status and associations among ATS users in a multicenter study that included northern, central, and southern China. We demonstrated that HIV prevalence is high in Yunnan province but quite rare elsewhere. We provide additional information about the prevalence of exposure to HCV and correlates for HIV and HCV transmission among these ATS users.
Because of the large geographical variations (eg, range by site for HIV, 0%–20.3%; range by site for HCV, 8.6%–67.1%), the study site was entered into the multivariate model. The present study found that ATS users who lived in Yunnan province had a higher risk for HIV infection. HIV was epidemic (20.3%) among ATS users in Yunnan province, which is adjacent to the Golden Triangle, an area well known for its extensive heroin use and HIV infection.26 Some possible reasons could explain the highest HIV prevalence in Yunnan province. First, Yunnan province has a high burden of heroin use and HIV/AIDS cases,26,27 and the high proportion of heroin use (61%) among ATS users possibly increased the HIV detection rate in Yunnan province. Second, molecular epidemiologic findings have indicated that HIV began to spread from IDUs to other high-risk populations, and sexual transmission increased dramatically in Yunnan province.26,27 A drug use and sexual network study found high sexual risk behaviors among drug users in Yunnan.28 Another study showed that 84.5% of HIV-positive cases were acquired through sexual transmission in Yunnan province.26,27 Historically, Yunnan province has been described as a key HIV epicenter in China, possibly providing insights into how HIV is spread in Chinese settings.29 The high prevalence of HIV infection among ATS users in Yunnan province may be indicative of HIV transmission among this population in China.
Only one HIV case was found among ATS users in Beijing and Hubei, and no HIV case was found among ATS users in Shanghai, Hunan, and Guangdong provinces. One possible reason for this may be that these provinces have a history of low HIV prevalence, and HIV infection among the sexual and drug network of ATS users was low in these areas. Another reason for this result may be the limited sample size and possible sampling bias from compulsory and voluntary detoxification centers.
The present study found that the factors of living in Yunnan province, history of polydrug use, increased frequency of sexual behaviors after using ATS, history of sex with STI-positive persons, and HCV infection were independently associated with HIV infection among ATS users. Polydrug use complicated the drug use history and was related to a greater severity of drug use that was associated with more risk behaviors of HIV. One study showed that heavy polydrug users had significantly more HIV-positive and unknown serostatus sexual partners and more unprotected sex with these partners.12,30 The present study indicated that the stimulant-induced increase in the frequency of sexual behaviors increased the risk of HIV infection. This finding was supported by a similar result that showed that the stimulant-induced increase in sexual desire was a potential contributing factor in HIV transmission.8,10 Sex with STI-positive persons who have more risk of HIV risk behaviors could increase the potential of HIV infection among ATS users. We also demonstrated a correlation between HIV and HCV infection. HIV prevalence was higher among participants with HCV infection than those without infection. A high prevalence of exposure to HCV in other provinces besides Yunnan suggests that ATS users in these provinces are at an increased risk for HIV infection.
The prevalence of exposure to HCV infection was high, with a mean prevalence of 43.5% and large geographic variations (range by site, 8.6%–67.1%). The prevalence was the more than 50%, in Yunnan (67.1%) and Guangdong provinces (64.1%), whereas the prevalence rates in the remaining areas ranged from 8.8% in Hunan to 39.0% in Shanghai. The prevalence in this study was higher than the data from other countries and areas. A systematic review showed that the prevalence of HCV in non-IDUs (ie, those who sniff or smoke drugs, including MA) ranged from 2.3% to 35.3%.25
The present study showed that study site, unemployment, a long duration of ATS use, and history of injection use of ATS were independently associated with HCV infection. Compared with Hunan province, which had the lowest prevalence of exposure to HCV, the ATS users who lived Hubei, Shanghai, Guangdong, and Yunnan had a higher risk of exposure to HCV. The ATS users with longer durations of drug use had more risk of exposure to HCV, possibly explained by the fact that a longer duration of drug use was associated with an increased risk of unsafe sexual behaviors. Although ATSs were mainly used by the noninjection route in this population, the high prevalence of HCV infection among injection users of ATS was understandable and expected in this study because injection drug use was found to be the primary mode of HCV transmission.22 Importantly, the injection use of ATS was associated with HCV but not HIV. This may be attributable to the low prevalence of HIV detection and potentially different routes of drug administration in this study. Unemployed and unmarried ATS users were more likely to be infected with HCV, suggesting that social and family assistance, including the encouragement of employment and support from family members, possibly decreased the risk of exposure to HCV in this population.
The Chinese government has made efforts to scale up intervention programs for illicit drug users, especially IDUs, and comprehensive prevention and intervention strategies have played a positive important role in controlling HIV/AIDS and HCV transmission in the opiate-dependent population in China.19,31 However, the sexual transmission of HIV has increased dramatically in China, but the government has not paid sufficient attention to the epidemic of HIV and HCV among the ATS user population. Appropriate responses are urgently needed, and more intensive intervention programs should be implemented for this population, including peer education, counseling, and testing.
The present study has several limitations. First, our samples were recruited from compulsory and voluntary detoxification centers and should not be considered representative of all ATS users in these areas. Moreover, the ATS users from compulsory centers were restricted and incarcerated, and they may have worried about the information they provided, thus increasing the risk of information bias, although the interviewers tried to reduce their fears as much as possible. Second, the cross-sectional nature of this study prevented the determination of causal associations between the variables of interest. Third, an obvious limitation is the self-reported data because sexual behavior is a sensitive topic in Chinese culture. Therefore, the sexual risk data might be underestimated and prone to social desirability response bias. Fourth, approximately 30% of the participants had a history of heroin use, with presumed administration by injection, and the risk of HIV and HCV transmission by the parenteral route is higher than by the sexual route. However, injection drug use was not measured or controlled in the data analysis. The bias could limit the detection of other potentially associated factors for HIV and HCV. Fifth, the small sample size and limited geographic coverage might limit the detection of HIV and HCV infection and potentially associated risk factors. Furthermore, multicenter epidemiologic studies with larger sample sizes and larger geographic coverage should be conducted to validate the HIV and HCV prevalence rates and explore the extensive risk factors related to HIV and HCV infection using other recruitment methods.
Despite these limitations, the present findings could provide information for developing prevention and intervention strategies for HIV and HCV infection among ATS users. With the increase in the sexual transmission of HIV among ATS users in China, more attention should be paid to this high-risk population to address the increasing HIV and HCV epidemic in China.
High prevalence of HIV infection in Yunnan province, but quite rare elsewhere, and high exposure to HCV in all 6 provinces and municipalities were found among ATS users in this study. The factors including polydrug use, a longer duration of ATS use, unsafe sexual behaviors associated with ATS use, and living in high-risk areas (such as Yunnan province) increased the risk of HIV and HCV infection among this population. Appropriate responses are urgently needed, and more attention should be paid to scale up intervention programs for this population in China.
The authors wish to thank all the interviewers and participants for their cooperation.
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