HIV and HCV prevalence among entrants to methadone maintenance treatment clinics in China: a systematic review and meta-analysis
BMC Infectious Diseases volume 12, Article number: 130 (2012)
Methadone maintenance treatment (MMT) was implemented in China since 2004. It was initiated in 8 pilot clinics and subsequently expanded to 738 clinics by the end of 2011. Numerous individual research studies have been conducted to estimate HIV and HCV prevalence among MMT clients but an overview of the epidemics in relations to MMT remains unclear. The aim of this study is to estimate the magnitude and changing trends of HIV, HCV and HIV-HCV co-infections among entry clients to MMT clinics in China during 2004-2010.
Chinese and English databases of literature were searched for studies reporting HIV, HCV and co-infection prevalence among MMT clients in China from 2004 to 2010. The prevalence estimates were summarized through a systematic review and meta-analysis of published literatures.
Ninety eligible articles were selected in this review (2 in English and 88 in Chinese). Nationally, pooled prevalence of HIV-HCV and HIV-HCV co-infection among MMT clients was 6.0% (95%CI: 4.7%-7.7%), 60.1% (95%CI: 52.8%-67.0%) and 4.6% (95%CI: 2.9%-7.2%), respectively. No significant temporal trend was found in pooled prevalence estimates. Study location is the major contributor of heterogeneities of both HIV and HCV prevalence among drug users in MMT.
There was no significant temporal trend in HIV and HCV prevalence among clients in MMT during 2004–2010. Prevalence of HCV is markedly higher than prevalence of HIV among MMT clients. It is recommended that health educational programs in China promote the earlier initiation and wider coverage of MMT among injecting drug users (IDUs), especially HIV-infected IDUs.
Since the implementation of open-door policies in 1979, illicit drug trade has re-emerged in China. As the most populous country in the world, China has observed a rapid increase in drug use over the past three decades . The number of officially registered drug users increased from 70,000 in 1990 to 1.33 million at the end of 2009 . Moreover, behind each registered drug user, there were estimated 2–4 implicit drug users . Official statistics indicates that 73.2% of drug users in China in 2009 used heroin . Intravenous injection is the most common mean of drug use, with injecting drug users (IDUs) accounting for 59–85% of drug users [4–10].
Drug users (DUs), especially IDUs, represent a high-risk population for spreading HIV infection due to their high frequency of injection, sharing of contaminated needles and other risk behaviours [11–15]. The first domestic Chinese HIV/AIDS cases were found among heroin users in Yunnan Province as early as 1989 . By the end of 2002, HIV cases among drug users were reported in all 31 Chinese provinces, autonomous regions and municipalities . The cumulative number of diagnosed HIV/AIDS cases in China is now well over 200,000, among which over 60% were drug users [6, 17]. IDUs account for over 40% of new HIV infections [6, 17].
In China, HIV prevalence has wide geographic variations. According to the Chinese national surveillance report for 1995–2009 , five provinces (Yunnan, Guizhou, Sichuan, Guangxi and Xinjiang) were classified as high transmission areas (HTAs) for HIV infection among drug users, and the rest of country was considered as low transmission areas (LTAs). HIV prevalence among drug users in Yunnan and Xinjiang were the highest among all Chinese provinces, of approximately 25%-30% in 2007 [18, 19]. Similarly, HCV prevalence among DUs in China is high, but estimates vary substantially from 15.6% to 98.7% [20–23].
Harm reduction programs for drug users began in 2003 in China and it is believed that they have contributed to reductions in the spread of HIV [24–26]. A major component of this program is methadone maintenance treatment (MMT), which was initiated as a pilot program in 8 clinics serving 1,029 drug users in 2004 and subsequently expanded to 738 clinics serving 344,254 drug users by the end of 2011, which accounts for approximately 30% of registered IDUs in China (personal communication with China CDC). Initially, strict enrolment criteria were imposed to enroll only registered drug users . In July 2006, new implementation protocol of the community-based MMT program has been announced by the Chinese Ministry of Health to cover a wider group of drug users . The new protocol recommended MMT clinics also offer ancillary services including counseling and psychosocial support, testing for HIV and infections, referrals for antiretroviral treatment and other social supports .
There have been numerous independent studies documenting the prevalence of HIV or HCV among MMT clients at baseline of their treatment. Across these studies, large variations in HIV and HCV prevalence estimates were commonly observed, reflecting the complex geographical and chronological overlapping of the two epidemics. Numerous individual research studies have been conducted to estimate HIV and HCV prevalence among MMT clients in China. The studies vary in time and geographical locations, and do not provide a complete overview of HIV and HCV epidemics in relations to MMT in China. This study aims to investigate the geographical and the temporal patterns of HIV and HCV epidemics in China and their likely interaction. We do this through a systematic review and meta-analysis and we also discuss implications for future MMT implementation and health policies for HIV prevention among IDUs in China.
Two independent investigators conducted a systematic review of published peer-reviewed research articles by searching the following databases: PubMed, Chinese Scientific Journals Fulltext Database (CQVIP), China National Knowledge Infrastructure (CNKI) and Wanfang Data from 2004–2010. Keywords used in the database search included (“Methadone” OR “Methadone Maintenance Treatment” OR “Methadone Maintenance Therapy” OR “Methadone Maintenance”) AND (“HIV” OR “AIDS” OR “HCV” OR “hepatitis C virus” OR “co-infection”) AND (“China” OR “China Mainland”). We also performed a manual search of the reference lists of published articles. This review was conducted and reported according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) Statement issued in 2009 .
Studies were eligible for inclusion in this systematic review if they met the following criteria: (1) study published in Chinese or English language; (2) study reported HIV or HCV prevalence estimates among clients in MMT at baseline of treatment in China; (3) HIV and HCV infection must be diagnosed from laboratory serologic testing; (4) study design such as study site, time period and sample size must be reported. Intervention studies among MMT clients were also included. Exclusion criteria were: (1) review papers; (2) non peer–reviewed local/government reports; (3) conference abstracts and presentations; (4) self-reported HIV or HCV infections; (5) dissertations. If the same study data were published in both English and Chinese sources, the articles published in Chinese language were excluded from this study.
The quality of studies was assessed using a validated quality assessment tool for cross-sectional studies . The following eight items were assessed to calculate a total quality score: (1) clear definition of the target population; (2) representativeness of probability sampling; (3) sample characteristics matching the overall population; (4) adequate response rate; (5) standardized data collection methods; (6) reliable of survey measures/instruments; (7) valid of survey measures/instruments; (8) appropriate statistical methods. Answers were scored 0 and 1 for ‘No’ and ‘Yes’, respectively. The total quality score varied between 0 and 8 for each study.
We extracted the following information from all eligible studies: published year, study site, study period, gender, age, marital status, education, study design, clients recruitment methods, sample size; laboratory test methods for HIV and HCV, prevalence of HIV, HCV and HIV-HCV co-infection among MMT clients at the baseline of the treatment. The studies were then categorized by geographical locations according to their level of HIV transmission, and also into two specific time periods, prior to and after 2006.
Meta-analyses were carried out with the Comprehensive Meta-Analysis software (V2.0, Biostat, Englewood, New Jersey). The effect rates of pooled prevalence estimates and 95% confidence intervals (CI) were determined based on random effect models. Random effect models were applied when heterogeneity across subgroups were found to be significant. Heterogeneity tests were performed using the Cochran Q-test (p < 0.10 represents statistically significant heterogeneity) and I 2 statistic. We investigated the factors that are associated with heterogeneities in the stratified meta-analyses using meta-regression. Meta-regression was performed in STATA 10.0 (StataCrop, Texas, USA) Potential publication bias was measured by the Begg and Mazumdar rank correlation (p < 0.05). Spearmen correlation was used to assess the relationship between HIV prevalence and HCV prevalence among clients in MMT in China.
Trial flow/flow of included studies
A total of 834 studies were identified from four electronic databases (62 in PubMed, 410 in CNKI, 144 in CQVIP, 218 in Wanfang database). Due to duplication and irrelevance, we excluded 478 articles after screening the titles. We screened the abstracts of the remaining 356 articles, following which 216 articles were excluded (147 were not relevant, 25 were dissertations, 22 were non peer-reviewed theses, 10 were conference presentations or abstracts, 7 were reviews or letters and 5 were not carried out in mainland China). Among the remaining 140 articles eligible for full-text screening; we further excluded 50 articles (32 were not conducted among MMT clients, 5 did not report original data, 5 reported results from already identified data sources, 3 did not report study sites, 3 did not report study period, 2 studies covered multiple provinces). We finally included 90 articles (2 in English and 88 in Chinese) for subsequent quantitative synthesis, of which, 72, 71 and 19 articles were eligible for meta-analysis of HIV, HCV and HIV-HCV co-infection prevalence, respectively. The selection process is illustrated in Figure 1 and the quality score of each study is shown in the Additional file 1: Table S1.
The 90 eligible articles were from 19 of the 31 Chinese provinces. The sample size of the selected studies ranged from 38 to 8662 (median: 300; IQR: 175–512). All participants were recruited from MMT clinics. Eighty-one out of 90 studies (90%) were cross-sectional, 5 (6%) were cohort studies, 2 (2%) were randomized controlled trials and 2 (2%) did not report the study design. There were 72, 71 and 19 prevalence estimates on HIV, HCV and HIV-HCV co-infection among MMT clients at baseline of treatment respectively.
Epidemic trends of HIV, HCV infection and HIV-HCV co-infection
The overall national prevalence of HIV, HCV and HIV-HCV co-infection among MMT clients at baseline of treatment in China were 6.0% (95% CI: 4.7-7.7%), 60.1% (95% CI: 52.8-67.0%) and 4.6% (95% CI: 2.9-7.2%) respectively. Prevalence in HTAs were consistently higher than those in LTAs (HIV: 17.5% (95% CI: 14.0-21.6%) vs. 2.4% (95% CI: 1.6-3.5%); HCV: 70.2% (95% CI: 62.6-76.8%) vs. 55.5% (95% CI: 46.4-64.2%); HIV-HCV co-infection: 8.0% (95% CI: 4.8-12.9%) vs. 2.5% (95% CI: 1.4-4.4%)). Large variations in prevalence were also observed geographically. Whereas HIV prevalence among MMT clients varied from 0.1% (Hubei) to 36.0% (Yunnan) (Table 1, Figure 2a), HCV prevalence varied from 10.9% (Henan) to 65.7% (Guangxi) (Table 2, Figure 2b) and HIV-HCV co-infection varied from 0.5% (Henan) to 12.6% (Guangxi) (Table 3, Figure 2c). The forest plots showing the results of meta-analysis of HIV, HCV and HIV-HCV co-infection prevalence among clients in MMT are illustrated in the Additional file 1: Figure S1, S2 and S3. However, no temporal trends of any of these infections were found at the national level, in HTAs or LTAs since the initiation of MMT in 2004.
Our analysis reported high heterogeneities across the collected studies in evaluation of the pooled prevalence of the infections (HIV: I 2 = 97.614, p < 0.001; HCV: I 2 = 99.163, p < 0.001; HIV-HCV: I 2 = 96.671; p < 0.001). For HIV and HCV infections, meta-regression demonstrated that these heterogeneities were mainly contributed by the geographical locations of the studies and contributions from study language, sample size, sampling method and study time period were not significant. In contrast, studies with sampling sizes greater than 500 tended to report higher HIV-HCV co-infection rates than otherwise and the influence of geographical location was marginal (Table 4). No publication bias was found across the 72, 71 and 19 studies reported HIV, HCV and HIV-HCV co-infection (Begg rank correlation analysis p = 0.163, 0.702 and 0.649, respectively). A significantly positive correlation (Spearman, r = 0.456, p < 0.001) was observed between HIV and HCV prevalence among clients in Chinese MMT during 2004–2010 countrywide.
Consistent with findings from national sentinel surveillance , our meta-analyses indicated that HIV and HCV prevalence in MMT is distinctly higher in HTAs. This confirms that the prevalence of these infections remained highly concentrated among provinces along the traditional drug-trafficking routes but are considerably lower in the rest of the country.
Our estimated national HIV prevalence of 6.0% (95% CI: 4.7-7.7%) among people in MMT is not significantly different to the estimated HIV prevalence among non-MMT drug users (4.6-7.5%) reported by national sentinel surveillance during 2004–2009 . We noticed that HIV prevalence among people in MMT in Sichuan (7.1%) and Guizhou (20.7%) province is higher than that from sentinel surveillance data [2, 27, 121–123], indicating that methadone clinics in these areas may have recruited more HIV-positive patients among drug users . Additionally, our stratified time analysis of HIV, HCV and HIV-HCV co-infection among MMT clients did not show significant temporal trends in the prevalence of these infections since initiation of MMT in 2004. This suggested that the 2006 national policy to relax the eligibility criteria for MMT enrollment was not sufficient to encourage more HIV-infected drug users to participate in the program. MMT is known to significantly reduce the consumption of heroin and associated risk behaviours of the participants [24, 125–129]. It is therefore in the best interest of the Chinese government to substantially scale-up the proportion of HIV-infected participants in MMT. The consequent reduction in risk behaviours of the infected population may help to confine the transmission sources of HIV infection. In order to achieve this, more comprehensive services, such as referral services, counseling, social supports targeting HIV-infected drug users etc., should be provided. Educational programs to reduce social stigma as well as psychological barriers for treatment adherence especially for HIV-infected drug users should be implemented.
Our analysis indicated a national HCV prevalence of 59.9% (95% CI: 52.7-66.7%) among MMT clients in China. This result is higher than the reported prevalence of 50.4% (95% CI: 42.5-58.4%) in a recent meta-analysis , in which the subjects were selected not only from MMT, but also from detoxification centers and the community. Chinese sentinel surveillance did not start monitoring HCV among drug users until 2009 and there have been no data currently published. Consistent with findings in other settings, HCV prevalence is positively correlated with HIV prevalence among MMT clients in China [89, 130, 131]. The fact that HCV prevalence was found to be 10 times higher than HIV prevalence may be due to a number of reasons. Biologically, transmission efficiency of blood-borne HCV has been estimated to be approximately 10 times greater than that of HIV for needle-stick injuries . Secondly, HCV infection may have entered drug users population much earlier and hence already established a stabilized epidemic in China [131, 133]. With a large number of chronic HCV-infected individuals in the drug user communities, a susceptible person may be more prone to the infection through needle-sharing with other IDUs.
The prevalence of HIV-HCV co-infection and HIV were not markedly different suggesting that a large proportion of HIV-infected MMT clients in China are also infected with HCV. Studies have shown that the co-infection of these diseases interact synergistically and the presence of each infection can substantially reduce the immune clearance of the other [134–136]. HCV co-infection may accelerate the progression to AIDS stage and death , even among people with continuous suppression of HIV replication . It also blunts the CD4+ cell increase in HIV-infected people receiving antiretroviral therapy . It is therefore a high priority to provide necessary healthcare and treatment for co-infected individuals in parallel to the roll-out of MMT in China.
Several limitations in this study should be noted. First, by the end of November 2010, there were 696 MMT clinics in China, covering 27 Chinese provinces , however, out of these, eight provinces did not publish any reports on the prevalence of HIV or HCV. Furthermore, estimates of HIV or HCV prevalence from Beijing, Henan, Hebei, Ningxia and Qinghai provinces were based on only one report. These may likely contribute to bias of the overall regional or national prevalence. Further investigations in more cities are necessary to provide a more accurate description of HIV and HCV epidemics. Second, our study was focused on HIV and HCV infections among the same study cohorts, studies reporting only HIV or HCV prevalence estimates were excluded in this review and hence some significant studies might be missing in the stratified meta-analyses. Third, there are also a potentially large number of governmental documents, community-level reports and other unpublished data that have never been archived in any of the public literature databases. Fourth, we identified that the presence of high heterogeneities may be attributable to demographical differences in HIV and HCV prevalence among MMT clients across different Chinese geographical regions, but not the language of article, sampling method and study time may not explain the variations observed. It is important to note that other unreported factors, such as age, socio-economic status and sexual behaviours, may also be contributable to the heterogeneities.
Our study has several important implications to the future implementation of MMT in China. First, despite a rapid and substantial expansion of MMT program coverage in China [124, 139] the proportion of HIV- and HCV-infected drug users attending MMT remains low. Although MMT is beneficial at an individual-level, it can potentially be an effective population-level intervention strategy. Future expansion of MMT should target the infected population, as only inclusion of a large proportion of these infected individuals may substantially reduce their risk behaviours and maximize the preventive effects of MMT at a population level. Second, MMT should not be viewed as a replacement for other harm reduction programs, such as, needle and syringe exchange programs (NSEPs). A previous study has demonstrated that NSEPs in China are both effective and cost-effective for HIV prevention . MMT should be rolled-out in conjunction with NSEPs to reduce the number of new infections. Third, as a result of high percentage of HCV co-infection among HIV-infected MMT clients at baseline of the treatment, other programs that providing treatment to HIV and HCV infected patients should also be provided to MMT clients. Fourth, the greater risk of IDUs being infected with HIV and HCV and reported relapse to drug usage may be a contributing factor to low retention in MMT [140, 141]. It is therefore important for MMT to ensure sufficient support and care is provided for enrolled IDUs to maintain their behavioural changes. Peer-group support and frequent counseling follow-ups may be beneficial in building motivating environment for abstinence from addictions.
All authors were involved in the study design, including setting up the keywords search and project protocol. XZ and EPFC performed the literature search, quality assessment and data extraction. EPFC performed data analysis. YFW and YXL assisted with data collection, DPW and LZ assisted with data analysis and interpretation. ZX drafted the manuscript. LZ was responsible for the supervision of the project. All authors read and approved the final manuscript.
YanPing B, ZhiMin L: Current situation and trends of drug abuse and HIV/AIDS in China. HIV Therapy. 2009, 3 (3): 237-240. 10.2217/hiv.09.4.
Liu Z, Lian Z, Zhao C: Drug use and HIV/AIDS in China. Drug Alcohol Rev. 2006, 25: 173-175. 10.1080/09595230500538835.
Zhang L, Yap L, Xun Z, Wu Z, Wilson D: Needle and syringe programs in Yunnan, China yield health and financial return. BMC Public Health. 2011, 11 (1): 250-10.1186/1471-2458-11-250.
China Ministry of Health and UN Theme Group on HIV/AIDS in China: A Joint Assessment of HIV/AIDS Prevention, Treatment and Care in China, 2003. 2003
Zhu QY: Analysis of data AIDS sentinel surveillance from 1996 to 2003 in Guangxi province. CHIN J AIDS STD. 2006, 12 (5): 290-432.
State Council AIDS Working Committee Office UN Theme Group on AIDS in China: A Joint Assessment of HIV/AIDS Prevention,Treatment and Care in China,2007. 2007
Chen J, Alberto D, Min TJ, An ZH, An Q, Ambrose DJ, Min J, Muncho NY: Analysis of data AIDS sentinel surveillance in Xinjiang province 2005. Endemic Disease Bulletin. 2007, 22 (02): 55-56.
Li QP, Chen R, Huang L, Teng XY, Yuan K: Analysis of HIV prevalence from 1997 to 2006 in Anshun City. CHIN J AIDS STD. 2008, 14 (3): 270-271.
Yang L, Li J, Zhang Y, Li H, Zhang W, Dai F, Ren Z, Qi G, Cheng W: Societal perception and support for methadone maintenance treatment in a Chinese province with high HIV prevalence. Am J Drug Alcohol Abuse. 2008, 34 (1): 5-16. 10.1080/00952990701653867.
Zhang H: Monitoring results of HIV among drug users in Zhenning coutry of Guizhou province. Modern Preventive Medicine. 2010, 37 (09): 1717-1718.
Qian HZ, Vermund SH, Wang N: Risk of HIV/AIDS in China: subpopulations of special importance. Sex Transm Infect. 2005, 81 (6): 442-447. 10.1136/sti.2004.014258.
Tan Y, Wei QH, Chen LJ, Chan PC, Lai WS, He ML, Kung HF, Lee SS: Molecular epidemiology of HCV monoinfection and HIV/HCV coinfection in injection drug users in Liuzhou, Southern China. PLoS One. 2008, 3 (10): e3608-10.1371/journal.pone.0003608.
Xia X, Lu L, Tee KK, Zhao W, Wu J, Yu J, Li X, Lin Y, Mukhtar MM, Hagedorn CH: The unique HCV genotype distribution and the discovery of a novel subtype 6u among IDUs co-infected with HIV-1 in Yunnan, China. J Med Virol. 2008, 80 (7): 1142-1152. 10.1002/jmv.21204.
Bao YP, Liu ZM: Systematic review of HIV and HCV infection among drug users in China. Int J STD AIDS. 2009, 20 (6): 399-405. 10.1258/ijsa.2008.008362.
Li H, Goggins W, Lee SS: Multilevel analysis of HIV related risk behaviors among heroin users in a low prevalence community. BMC Public Health. 2009, 9: 137-10.1186/1471-2458-9-137.
Zheng X, Tian C, Choi KH, Zhang J, Cheng H, Yang X, Li D, Lin J, Qu S, Sun X: Injecting drug use and HIV infection in southwest China. AIDS. 1994, 8 (8): 1141-1147. 10.1097/00002030-199408000-00017.
Fang YX, Wang YB, Shi J, Liu ZM, Lu L: Recent trends in drug abuse in China. Acta Pharmacol Sin. 2006, 27 (2): 140-144. 10.1111/j.1745-7254.2006.00270.x.
Guo W, Qu SQ, Ding ZW, Yan RX, Li DM, Wang L: Situations and trends of HIV and syphilis infections among drug users in China, 1995–2009. Zhonghua Liu Xing Bing Xue Za Zhi. 2010, 31 (6): 666-669.
Jia M, Luo H, Ma Y, Wang N, Smith K, Mei J, Lu R, Lu J, Fu L, Zhang Q: The HIV epidemic in Yunnan province, China, 1989–2007. JAIDS Journal of Acquired Immune Deficiency Syndromes. 2010, 53: S34-
Wang NC, Qiao XC, Zhang LF: Seroepidemiology of HCV infection among different populations in Shanxi. China Public Health. 2001, 17 (8): 703-
Yang J, Ding JJ, Yang L: Co-infection with HCV and HGV among 107 injection drug users. Chin J Prev Med. 2000, 34: 85-
Deng LP, Gui XE, Zhang YX: A survey of HIV, HBV, HCV, HGV and TTV infections among drug abusers in Hubei Province. Hubei J Prev Med. 2003, 14 (5): 1-2.
Li WJ, Fan ZF, Pan LJ: A survey of HIV and HCV infections and related knowledge and behavioramong drug abusers in Yangjiang City. South China. Prev Med. 2004, 30 (5): 17-19.
Pang L, Hao Y, Mi G, Wang C, Luo W, Rou K, Li J, Wu Z: Effectiveness of first eight methadone maintenance treatment clinics in China. AIDS. 2007, 21: S103-
Wu Z, Luo W, Sullivan SG, Rou K, Lin P, Liu W, Ming Z: Evaluation of a needle social marketing strategy to control HIV among injecting drug users in China. AIDS. 2007, 21: S115-10.1097/01.aids.0000304706.79541.ef.
Lau JTF, Zhang L, Zhang Y, Wang N, Lau M, Tsui HY, Zhang J, Cheng F: Changes in the prevalence of HIV-related behaviors and perceptions among 1832 injecting drug users in Sichuan, China. Sex Transm Dis. 2008, 35 (4): 325-10.1097/OLQ.0b013e3181614364.
Yin W, Hao Y, Sun X, Gong X, Li F, Li J, Rou K, Sullivan SG, Wang C, Cao X: Scaling up the national methadone maintenance treatment program in China: achievements and challenges. Int J Epidemiol. 2010, 39 (Suppl 2): ii29-ii37.
China Ministry of Health, Ministry of Public Security and the State Food and Drug Administration: Opium abusers community-based drug maintenance treatment protocol (trial version). 2006, Beijing
Moher D, Liberati A, Tetzlaff J, Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009, 6 (7): e1000097-10.1371/journal.pmed.1000097.
Boyle MH: Guidelines for evaluating prevalence studies. Evid Based Ment Health. 1998, 1 (2): 37-39. 10.1136/ebmh.1.2.37.
Zhou XP, He CN, Wei XY: Infection of HBV, HVC, HIV and syphilis at methadone maintenance treatment. Strait J Prev Med. 2009, 15 (3): 80-81.
Chang RZ, Yin WY, Huang YM, Yao YM, Pang L, Wu ZY: A survey of HIV,HCV,syphilis and HSV-2 among drug users attending methadone maintenance clinics in Guangxi and Guizhou. CHIN J AIDS STD. 2010, 16 (05): 470-472. +?505
Bai Y, Lai WS, Wei L: Prevalence of HIV, HCV and Syphilis Infection at Methadone Maintenance Treatment Clinic in Liuzhou City. J Prev Med Inf. 2009, 25 (11): 910-912.
Han XJ, Xu YX, Jiang HM, He J, Tan B, Cao FB: Infection of HIV, HBV, HCV and syphilis in 300 drug abusers in Guiyang City. Chin J Drug Depend. 2010, 19 (2): 116-119.
Li XY, Mou X, Luo JQ: Detection monitoring and analysis of HCV, HBC and HIV at methadone maintenance treatment. Chinese journal of drug abuse prevention and treatment. 2009, 15 (5): 283-284.
Wang J, Yang XJ: Prevalence ofH IV, HCV Infecti on and Syphilis Among Drug Users at Methadone Maintenance Clinics in Anshun. Journal of Occupational Health and Damage. 2010, 25 (3): 145-148.
Hao C, Hu W, Ruan YH, Ma ZE, Yang XG, Zhang L, Yin L, Liu SZ, Chen KL, Qin GM: Impact of community-based methadone maintenance treatment on high risk sexual behaviors among heroin addicts. CHIN J AIDS STD. 2006, 12 (4): 307-310.
Qian HZ, Hao C, Ruan Y, Cassell HM, Chen K, Qin G, Yin L, Schumacher JE, Liang S, Shao Y: Impact of methadone on drug use and risky sex in China. J Subst Abuse Treat. 2008, 34 (4): 391-397. 10.1016/j.jsat.2007.07.002.
Chen B, Luan RS, Jiang HY, Yu G: Investigation on AIDS related KAP among drug users in Yibin. Morden Prevention Medicine. 2009, 36 (03): 502-504. +?508
Liu JK, Li LH, Chen YH, Liu D, Li l, Luo W: Evaluation of methadone maintenance treatment for heroin users in Panzhihua. J Prev Med Inf. 2009, 25 (9): 723-725.
Dong G, Jia H: H IV, HCV and Syphilis Infection Among Drug Users in Luzhou City. J Prev Med Inf. 2009, 25 (1): 55-57.
Wang Y: Data analysis of 715 methadone maintenance treatment in Luzhou City. Prev Med Trib. 2009, 15 (06): 553-554.
Wang DY, Chen YM, Huang QL, Zhou M, Chen HM, Pan L: Infection and risk factors of HIV and HCV among drug users in Zigong City. South China J Prev Med. 2009, 04: 38-40.
Yao W, Jiang ZH, Jia SG, Yang H, Liao KK: Prevalence of HIV, HCV and syphilis infection at methadone maintenance treatment clinic in Mianyang city. J Prev Med Inf. 2008, 24 (7): 498-500.
Liu JB, Dilixiat YAHAP, Li F: Baseline Investigation on Community Methadone Maintenance Treatment of Heroin Addicts in Urumqi. Endemic Disease Bulletin. 2006, 21 (1): 39-43.
Fu LP, Li F, Zhang ZZ, Mo LR: Effective evaluation on parts of community- based methadone maintenance treatment clinics for heroin addicts in Xinjiang. Endemic Disease Bulletin. 2007, 22 (5): 17-19.
Fang HR, Mo LR, Liu JX: Analysis of test results of HIV and HCV in methadone maintenance treatment clinic. Chinese Community Doctors. 2008, 10 (16): 137-
Reziwa NuErLa, Ailikemu YaHePu, Tian Y: Investigation on herion addicts of Han and Uygur nationality with methadone maintenance. Endemic Disease Bulletin. 2009, 05: 8-10.
Shen L, Du XJ, Fang HT: Analysis the reason of the dropout in the process of the 992 cases on methadone maintenance treatment. China Prac Med. 2009, 4 (30): 39-40.
Yuan L, Dai JH, Tian Y: Diliyati·Yahepu: Investigation on community methadone maintenance treatment on 200 herion addicts in Xinjiang. Endemic Disease Bulletin. 2010, 02: 16-19.
Duan YJ, Yin ZL, Xi CD, Li ZC, Gao Y: Effect assessment of methadone maintenance treatment among heroin addicts in Ruili city. CHIN J AIDS STD. 2008, 14 (3): 240-242.
Zhang MJ, Wang GX, Wang WZ, Sun YH, Du JQ, Tang L, Xue SY, Bi AM: Baseline survey analysis of methadone maintenance treatment in Kaiyuan. Soft Science of Health. 2008, 22 (3): 273-274.
Zhuang HY, Xun JP, Li XT, Deng HC, Cao HL, Dai LH, Chen F, Cao LH, Chen QY: Analysis of reusing herion by patients with physical diseases when on methadone maintenance treatment. Chin J Drug Depend. 2008, 17 (5): 377-379.
Xue HM, Duo L, Yang LH, Zhao XZ, Zhong JR, Lei YJ, Ruan Y, He LP, Wang LM: et al : An analysis of impact factors related with needle sharing among MMT clients. CHIN J AIDS STD. 2010, 06: 548-550.
Yang GW, Yin ZL, Li ZL, Peng KJ, Xi CH, Yang YB, Li ZC, Duan YJ: Analysis Of reasons for patients leaving methadone maintenance treatment mobile pilot service vehicles in Ruili City. Chinese journal of drug abuse prevention and treatment. 2010, 16 (2): 83-85.
Yang YC, Duan S, Xiang LF, Ye RH, Gao J, Yang SS, Yang YB: Adherence and related determinants methadone maintenance treatment among heroin addicts in Dehong prefecture, Yunnan province. Chin J Epidemiol. 2011, 32 (2): 125-129.
Du WJ, Xiang YT, Wang ZM, Chi Y, Zheng Y, Luo XN, Cai ZJ, Ungvari GS, Gerevich J: Socio-demographic and clinical characteristics of 3129 heroin users in the first methadone maintenance treatment clinic in China. Drug Alcohol Depend. 2008, 94 (1–3): 158-164.
Tan XL, Luo BS, Zhu LX: Investigation on AIDS related KAP among drug users in Chongqing. Morden Preventive Medicine. 2007, 34 (6): 1152-1153.
Wu GH, Chen H, Meng X, Zhou C: Epidemiological survey on the HCV and HIV infection among drug users in Chongqing City. Morden Preventive Medicine. 2010, 37 (1): 134-136.
Zhou X, Zhang X, Zhou XM: HIV, HCV examination data analysis among drug users treated with oral methadone maintenance in Panzhihua City from 2005 to 2007. Prev Med Trib. 2009, 15 (08): 745-746.
Wu LH, Chen HM: Infection of HBV, HCV. HIV and syphilis at methadone maintenance treatment in Quanzhou city. CHIN J AIDS STD. 2007, 6: 573-
Zheng WX, Chen G: Baseline investigation on methadone maintenance treatment of 334 drug users. Strait J Prev Med. 2009, 15 (3): 34-35.
Gao LF, Yang J, Li SJ: Detection and analysis of HIV, HBV, syphilis and HCV infections of methadone clinic in Jinchang City. Chinese Community Doctors. 2010, 12 (14): 168-
Zhu XH, Xun JP, Gao L, Peng JJ: Monitoring and analysis of clinical blood in 613 MMT clients. Chinese journal of drug abuse prevention and treatment. 2010, 16 (6): 340-342.
Dai LP, Lu J, Jiang T, Jiang LH, Qiu XL: Investigation and analysis of konwledge of HIV among drug users in methadone maintenance treatment. Chin J of PHM. 2009, 01: 83-84.
Liu XY, Wu B: Analysis of 2007 drug abuse monitor reports in Shenzhen. Chinese journal of drug abuse prevention and treatment. 2009, 15 (1): 30-33.
Zhang QL: A baseline investigation on herion addicts in methadone maintenance treatment clinics in Dongguan. Chin J Drug Depend. 2008, 17 (3): 204-207.
Chen W, Zhao LL, Ling L, Chen A, Xia YH, Han L, Lin P, He Q: Effectiveness evaluation on initial methadone maintenance treatment at community in Guangdong province. Chin J Public Health. 2009, 12: 1416-1418.
Chen A, Xia YH, Chen W, Ling L, Tan WK, Zheng RJ: Predictors of retention related factors at the initial methadone maintenance treatment clinics in Guangdong province. Chin J Epidemiol. 2009, 30 (12): 1230-1233.
Dai LP, Lin SX, Jiang YH, Gong CH: Research of 257 herion addicts in community methadone maintenance treatment. Chin J of PHM. 2010, 26 (004): 417-419.
Hu WS, Wang DP, Huang X, Zheng HB, Peng ZT: Analysis of the efficacy of medicine(methadone) maintenance treatment in 125 cases of heroin dependence patients. Chinese journal of drug abuse prevention and treatment. 2010, 16 (2): 86-88.
Li LY, Qiu YM, Guo JH, Xie ZQ: Effect of health education on therapy compliance of methadone maintenance treatment. Int J Nurs. 2009, 28 (6): 837-839.
Li YF, Luo CQ, Ding GP: Investigation of the prevalence of the HIV and HCV infection in methadone maintenance treatment in Dongguan. Morden Hospital. 2009, 9 (3): 155-156.
Wang M, Lin P, Zhao JK, Li Y, Zhang QL: Correlation Analysis of drug Abuse Sexual Behaviours and Other Risk Factors in the Community-Based drug Addicts. Journal of Tropical Medicine. 2009, 9 (11): 1291-1294.
Wang CQ, Liang QS, Xie HL, Su M, Xu TX: Analysis of methadone treatment compliance. IMHGN. 2009, 15 (14): 78-80.
Wu ZL, Huang YL, Guo LZ: Baseline survey analysis on drug users in methadone maintenance treatment clinics from Doumen area of Zhuhai City. Guide of China Medicine. 2010, 08 (16): 84-85.
Xia L, Zhang QS, Deng XL, Li CX, Shen J, Liu T, Cai CL, Liu WH, Chen YQ, Yang M: Prevalence of HIV, HCV and Syphilis among heroin addicts at methadone maintenance treatment clinic in Shenzhen city. Chinese journal of drug abuse prevention and treatment. 2010, 16 (2): 63-65.
Wu SX: Baseline Investigation Analysis of Methadone maintenance treatment in Sanmenxia community. Henan medical research. 2009, 18 (3): 248-250.
Qiu XQ, Zhou B, Xu M, Tao YB, Wen YM, Wen MX: Investigation into the AIDS knowledge, behavior and serological test among the drug users in Xiangfan. Chinese Journal of Disease Contral and Prevention. 2009, 13 (4): 493-495.
Li XL, Ou QY, Tan HZ, Sun ZQ, Zhang H, Chen MS: Investigation on the drug abuser in methadone maintenance treatment clinic in Changsha. Chin J Dis Control Prev. 2008, 12 (1): 27-29.
Li XL, Tan HZ, Sun ZQ, Zhang H, Chen MS, Ou QY: Study on the time of retention and related influencing factors of patients receiving methadone maintenance treatment in Hunan province. Chin J Epidemiol. 2009, 30 (7): 672-675.
Tang XY, Li J, Huang X, Duan KM, He LP: Baseline investigation on herion addicts of methadone maintenance treatment in Chenzhou City. Practical Prevention Medicine. 2007, 14 (4): 1263-1264.
Chen LF: Survey of infectious status of HIV, HBV, syphilis and HCV on 459 drug users. Practical Preventive Medicine. 2009, 16 (5): 1641-1642.
He HX, Bao YG, Chen LF, Li SX, Xiang CQ, Xie X, Zhang DQ: Effect of MMT on reducing the transmission of HIV among IDUs. CHIN J AIDS STD. 2008, 14 (2): 124-126.
Chen C: Analysis of hydrochloric acid Methadone Maintenance Treatment for Heroin Addicts. Chinese Community Doctors. 2010, 12 (33): 142-143.
Feng YH, Han L, Cui R, Chen DQ, Zhu JH, Fang MS, Xu SQ: General information about patients undergoing methadone maintenance treatment in Wuhan. Journal of Nursing Science. 2010, 25 (23): 70-71.
Wang YP, Zhang GP, Wang F: Survey on Infection of HBV, HCV and HIV among Addicts Receiving Methadone Therapy. Occupation and Health. 2009, 25 (24): 2765-2766.
Feng SQ, Zhou JB, Guo YL, Shi TP, Li JH, Xu XG, Chen SL, Hao C: Effective evaluation of community-based methadone maintenance treatment for heroin addicts. Chin J Public Health. 2010, 26 (7): 924-925.
Hao C, Zhou JB, Li JH, Xu W, Liu SF, Ji XH, Xu XG, Chen XG: Influencing factors associated with behavior characteristics of drug abuse in a community-based methadone maintenance treatment among drug users. Chin J Public Health. 2009, 25 (7): 781-783.
Xu GY: A baseline investigation on newly enrolling drug users and community drug users from Baixia Area methadone clinics of Nanjing City. Jiangsu Health Care. 2008, 10 (6): 6-7.
Zhang MH, Liu XX, Xu KY, Shan L: Epidemiological Investigation on Drug Abusers in Community Methadone Mai ntenance Treatment Clinic in Zhen jiang City. Occup Health. 2010, 26 (20): 2335-2337.
Yuan ZX, Qiu HX, Mei ZF: Analysis on 226 cases of out-patient methadone treatment of viral hepatitis syphilis. HIV infection detection among drug addicts in Yandu District. Prev Med Trib. 2010, 07: 601-602.
Jiang A, Zhao JH, Wang XZ, Han QQ, Chen SG, Hu XL: Effect analysis of the heroin addicts with methadone maintenance treatment in experimental units of Wuzhong in Ningxia. Modern Preventive Medicine. 2009, 15: 2920-2922.
Hao XQ: Survey on infection of HIV and HCV among 277cases of methadone maintenance treatment. Qinghai Medical Journal. 2009, 06: 75-76.
Jia W, Ye ZS, Zhang R, Wang RQ: Analysis of dose-effect relationship and compliance for methadone maintenance treatment. Chinese journal of drug abuse prevention and treatment. 2008, 14 (5): 253-256.
Zhang HF, Deng KW, Zhang YF, Tong HY, Long HY: Efficacy evaluation on methadone maintenance treatment in Hanzhong Shanxi. Chin J Drug Depend. 2009, 18 (1): 43-46.
Liu Y, Zhang YY, Zhang HF: Baseline investigation of OPD attendance among insisting Meishatong users in Putuo district Shanghai. Shanghai Journal of Preventive Medicine. 2009, 21 (9): 429-430.
Li T, Shen WL, Xu XP, Zhou ZR: AIDS High Risk Behaviors Investigation in Patients Visiting Methadone Maintenance Clinic in Xuhui District. Guide of China Medicine. 2010, 8 (5): 29-30.
Cai CP, Zhou ZM, Chen LX, Chen LX: Investigation of AIDS, hepatitis B and C among methadone-treated drug addicts women of childbearing age. Disease Surveillance. 2008, 23 (2): 126-127.
Zhang XH, Sun J: Denographic characteristics and drug abuse of 165 herion dependent patients on methadone maintenance treatment. Chin J Drug Depend. 2008, 17 (2): 144-147.
Su MF: HIV, HCV and TB infection among drug users receiving methadone treatment in Yuhuan country, Zhejiang province. Disease Surveillance. 2010, 04: 302-304.
Wang J, Yang XJ: Survey of infectious status of HCV among drug users of methadone clinic in XIXIU area, ANSHUN CITY, in 2008. J Prev Med Inf. 2010, 26 (6): 504-505.
Deng CK, Dong F, Sun HB, Xie MJ: Analysis of influencing factors and risk factors of liver function damage in herion addicts from MMT clinic in Qingzhen City. Chinese Journal of Abuse Prevention and Treatment. 2009, 15 (5): 267-269.
Zhao XH, Liao KK, Liu DC, Yang HW, Sun HY: Investigation of reasons of patient-loss in methadone maintenance treatment clinic. J Prev Med Inf. 2009, 25 (5): 457-459.
Wang XR, Zhang F, Chen XN: Analysis of anti-HCV among drug users in Bengbu City. JPMT. 2007, 14 (18): 2417-2418.
Zhan SW, Ding YX: Analysis of cucatinve effects of 215 herion addicts with methadone maintenance therapy in Maanshan. Anhui J Prev Med. 2008, 04: 241-242.
He XX, Lv J, Wei HY: Analysis on relevant factors of HCV Screening Result of 1516 Heroin Addicts. Chinese journal of drug abuse prevention and treatment. 2010, 16 (3): 154-157.
Peng JS, Zhou ZD, Pei DE, Zhou Y, Liu MQ, Tang L, Xu J, Wu XW, Huo WZ, Zhou W: Study on the distribution of hepatitis C virus genotypes in patients visiting one methadone maintenance clinic in Wuhan. Chin J Epidemiol. 2007, 28 (12): 1207-1210.
Xia X, Luo J, Dong J, You H, Qian YH, Qian XC, Yu RB: Epidemiological survey on the HCV infection among drug users in some areas of Jiangsu. Modern Preventive Medicine. 2007, 34 (24): 4616-4618,4621.
Xu YP: Detection results of anti-HCV among drug replacement therapy patients in Wuxi city. Shanghai Journal of Preventive Medicine. 2007, 19 (1): 12-
Song HB: Epidemiological survey on the HCV infection among drug users at methadone maintenance treatment in Nantong city. Medical Journal of Chinese People's Health. 2010, 22 (1): 22-23.
Wang WM: Survey of HIV and HCV infection among drug users in Kunshan City. China Tropical Medicine. 2010, 10 (11): 1362-1363.
Liu XP: Analysis of hepatitis C virus infection among 93 herion addicts in Zhongshan City. Chinese Journal of Coal Industry Medicine. 2010, 13 (12): 1777-
Li YC, Jia W, Shen DH, Wang F, Zhang R: Analysis of influencing factors of HCV infection in drug users from methadone maintenance therapy clinic in Xi'an. Chinese journal of drug abuse prevention and treatment. 2009, 15 (4): 207-209.
Zang JF, Li J, Zhang FQ, Zhai XM, Qiao Y, Luo C: Investigation on HCV infection among drug users in Methadone maintenance treatment. Chinese journal of drug abuse prevention and treatment. 2010, 16 (2): 88-90.
Liu HB, Zhe XL: Study on HCV co-infection in Yulin drug users. J Med Pest Control. 2010, 08: 731-732.
Du J, Wang Z, Zhang HH, Dong AZ, Fan CL, Yuan Y, Jiang HF, Zhao M: HCV knowledge and HCV infection among drug users treated in a methadone maintenance treatment clinic. Chin J Drug Depend. 2009, 18 (6): 495-499.
Zhang XH: Analysis of 117 cases on methadone maintenance treatment. Chin J Drug Depend. 2007, 16 (2): 140-142.
Fu FY, Qian YP: Detection results of HIV, HCV and syphilis and behavior characteristics among 349 drug users in Hangzhou City. J of Radioimmunology. 2009, 22 (6): 639-640.
Wang DY, Chen YM, Huang QL, Zhou M: Study in HIV/HCV co-infection in Zigong drug users. Modern Preventive Medicine. 2010, 37 (2): 361-362.
GH L: The analysis on HIV surveillance among Guangxi IDUS in 2005–2007. Intern Med. 2008, 3 (3): 325-326.
Liao KK, Zhao XH, Su J, Lui DC, Jia SG, Yang H, Yao W: AIDS surveillance among drug users in Mianyang 2009. J Prev Med Inf. 2011, 27 (02): 94-96.
Zhang Q, Wu T, Huang Y, Tan DY, Xi DR: The analysis of sentinel surveillance among drug users from 2006 to 2010 in Shunqing district of Nanchong City. Parasitoses and Infectious Disease. 2011, 9 (01): 38-40.
Liu EW, Liang T, Shen LM, Zhong H, Wang B, Wu ZY, Detels R: Impact of methadone maintenance treatment on HIV risk behaviors of heroin drug users. Zhonghua Yu Fang Yi Xue Za Zhi. 2010, 44 (11): 981-984.
Joseph H, Stancliff S, Langrod J: Methadone maintenance treatment (MMT): a review of historical and clinical issues. Mt Sinai J Med. 2000, 67 (5–6): 347-364.
Wu JL, Wu ZY: The effectiveness of methadone maintenance treatment and related factors. Chinese Journal of AIDS/STD. 2004, 10 (001): 69-70.
Tang Y, Zhao D, Zhao C, Cubells JF: Opiate addiction in China: current situation and treatments. Addiction. 2006, 101 (5): 657-665. 10.1111/j.1360-0443.2006.01367.x.
Shi J, Zhao LY, Epstein DH, Zhang XL, Lu L: Long-term methadone maintenance reduces protracted symptoms of heroin abstinence and cue-induced craving in Chinese heroin abusers. Pharmacol Biochem Behav. 2007, 87 (1): 141-145. 10.1016/j.pbb.2007.04.010.
Sullivan SG, Wu Z: Rapid scale up of harm reduction in China. Int J Drug Policy. 2007, 18 (2): 118-128. 10.1016/j.drugpo.2006.11.014.
Wang HP, Yang JJ, Deng XZ, Xu K, Wang J, Zhang Y: HIV/HBV/HCV infection among drug users: a meta analysis of data collected in Chinese mainland. Chin J Dis Control Prev. 2010, 14 (04): 300-304.
Xu C, Pang L, Wu ZY: Human immunodeficiency virus and hepatitis C virus infections among drug users in China. Chin J Dis Contr ol Pr ev. 2009, 13 (2): 193-196.
Aceijas C, Rhodes T: Global estimates of prevalence of HCV infection among injecting drug users. Int J Drug Policy. 2007, 18 (5): 352-358. 10.1016/j.drugpo.2007.04.004.
Sulkowski MS, Thomas DL: Hepatitis C in the HIV-infected person. Ann Intern Med. 2003, 138 (3): 197-10.7326/0003-4819-138-3-200302040-00012.
Verucchi G, Calza L, Manfredi R, Chiodo F: Human immunodeficiency virus and hepatitis C virus coinfection: epidemiology, natural history, therapeutic options and clinical management. Infection. 2004, 32 (1): 33-46. 10.1007/s15010-004-3063-7.
Garten RJ, Zhang J, Lai S, Liu W, Chen J, Yu XF: Coinfection with HIV and hepatitis C virus among injection drug users in southern China. Clin Infect Dis. 2005, 41 (Suppl 1): S18-24.
Sulkowski MS, Thomas DL, Mehta SH, Chaisson RE, Moore RD: Hepatotoxicity associated with nevirapine or efavirenz?containing antiretroviral therapy: role of hepatitis C and B infections. Hepatology. 2002, 35 (1): 182-189. 10.1053/jhep.2002.30319.
Choi SY, Cheung YW, Chen K: Gender and HIV risk behavior among intravenous drug users in Sichuan Province, China. Soc Sci Med. 2006, 62 (7): 1672-1684. 10.1016/j.socscimed.2005.08.046.
Ministry of Health: China has established key areas of drug addiction treatment covered by the network. 2010, http://wwwgovcn/jrzg/2010-12/14/content_1765546htm,
Mohamad N, Bakar NH, Musa N, Talib N, Ismail R: Better retention of Malaysian opiate dependents treated with high dose methadone in methadone maintenance therapy. Harm Reduct J. 2010, 7: 30-10.1186/1477-7517-7-30.
Lai WS: Reasons for heroin dependent patients’ dropout from methadone maintenance treatment. Chin J Drug Depend. 2007, 16 (4): 299-301.
Wang B, Zhao J, Qian XC, Pan XW, Gao Q, Ding L: Reasons and influencing factors of patient-loss in methadone maintenance clinics in Wuxi. Chin J Epidemiol. 2010, 31 (2): 238-239.
The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/12/130/prepub
This study was funded from the following sources: Round 8 of the AusAID Australian Leadership Awards (ALA) Fellowships Program; Overseas Scholarship of Jiangsu Government, China; Nantong University, Jiangsu province, China; The University of New South Wales; Australian Research Council (FT0991990); Graduate student science and technology innovative project of Nantong University (YKC12035).
The authors declare that they have no competing interests.
Electronic supplementary material
Additional file 1: Figure S1: Forest Plot showing the results of meta-analysis of HIV prevalence among clients in MMT (N = 72). Figure S2. Forest Plot showing the results of meta-analysis of HCV prevalence among clients in MMT (N = 71). Figure S3. Forest Plot showing the results of meta-analysis of HIV-HCV co-infection prevalence among clients in MMT (N = 19). Table S1. Quality assessment score of all studies [31, 32, 34–53, 55–109, 111, 113–120]. (DOC 564 KB)
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Zhuang, X., Liang, Y., Chow, E.P. et al. HIV and HCV prevalence among entrants to methadone maintenance treatment clinics in China: a systematic review and meta-analysis. BMC Infect Dis 12, 130 (2012). https://doi.org/10.1186/1471-2334-12-130