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Lancet Infectious Diseases | 2013

HIV prevalence in China: integration of surveillance data and a systematic review

Lei Zhang; Eric P. F. Chow; Jun Jing; Xun Zhuang; Xiaoshan Li; Meiqi He; Huamin Sun; Xiaoyan Li; Marelize Gorgens; David Wilson; Lan Wang; Wei Guo; Dongming Li; Yan Cui; Lu Wang; Ning Wang; Zunyou Wu; David P. Wilson

BACKGROUNDnAsian HIV epidemics are concentrated among particular behavioural groups, but large variations exist in epidemic types, timing, and geographical spread between countries and within countries, especially in China. We aimed to understand the complexity of HIV epidemics in China by systematically analysing prevalence trends by data source, region, population group, and time period.nnnMETHODSnWe collected HIV prevalence data from official national sentinel surveillance sites at the provincial level from Jan 1, 1995, to Dec 31, 2010. We also searched PubMed, VIP Chinese Journal Database (VIP), China National Knowledge Infrastructure, and Wanfang Data from Jan 1, 1990, to Dec 31, 2012, for independent studies of HIV prevalence. We integrated both sets of data, and used an intraclass correlation coefficient test to assess the similarity of geographical pattern of HIV disease burden across 31 Chinese provinces in 2010. We investigated prevalence trends (and 95% CIs) to infer corresponding incidence by region, population group, and year.nnnFINDINGSnOf 6850 articles identified by the search strategy, 821 studies (384,583 drug users, 52,356 injecting drug users, 186,288 female sex workers, and 87,834 men who have sex with men) met the inclusion criteria. Official surveillance data and findings from independent studies showed a very similar geographical distribution and magnitude of HIV epidemics across China. We noted that HIV epidemics among injecting drug users are decreasing in all regions outside southwest China and have stabilised at a high level in northwest China. Compared with injecting drug users, HIV prevalence in female sex workers is much lower and has stabilised at low levels in all regions except in the southwest. In 2010, national HIV prevalence was 9·08% (95% CI 8·04-10·52) in injecting drug users and 0·36% (0·12-0·71) in female sex workers, whereas incidence in both populations stabilised at rates of 0·57 (0·43-0·72) and 0·02 (0·01-0·04) per 100 person-years, respectively. By comparison, HIV prevalence in men who have sex with men increased from 1·77% (1·26-2·57) in 2000, to 5·98% (4·43-8·18) in 2010, with a national incidence of 0·98 (0·70-1·25) per 100 person-years in 2010. We recorded strong associations between HIV prevalence among at-risk populations in each province, supporting the existence of overlap in risk behaviours and mixing among these populations.nnnINTERPRETATIONnHIV epidemics in China remain concentrated in injecting drug users, female sex workers, and men who have sex with men. HIV prevalence is especially high in southwest China. Sex between men has clearly become the main route of HIV transmission.


PLOS ONE | 2011

HIV and Syphilis Co-Infection Increasing among Men Who Have Sex with Men in China: A Systematic Review and Meta-Analysis

Eric P. F. Chow; David Wilson; Lei Zhang

Background This study aims to estimate the magnitude and changing trends of HIV, syphilis and HIV-syphilis co-infections among men who have sex with men (MSM) in China during 2003–2008 through a systematic review of published literature. Methodology/Principal Findings Chinese and English literatures were searched for studies reporting HIV and syphilis prevalence among MSM from 2003 to 2008. The prevalence estimates were summarized and analysed by meta-analyses. Meta-regression was used to identify the potential factors that are associated with high heterogeneities in meta-analysis. Seventy-one eligible articles were selected in this review (17 in English and 54 in Chinese). Nationally, HIV prevalence among MSM increased from 1.3% during 2003–2004 to 2.4% during 2005–2006 and to 4.7% during 2007–2008. Syphilis prevalence increased from 6.8% during 2003–2004 to 10.4% during 2005–2006 and to 13.5% during 2007–2008. HIV-syphilis co-infection increased from 1.4% during 2005–2006 to 2.7% during 2007–2008. Study locations and study period are the two major contributors of heterogeneities of both HIV and syphilis prevalence among Chinese MSM. Conclusions/Significance There have been significant increases in HIV and syphilis prevalence among MSM in China. Scale-up of HIV and syphilis screening and implementation of effective public health intervention programs should target MSM to prevent further spread of HIV and syphilis infection.


BMC Infectious Diseases | 2011

What is the potential for bisexual men in China to act as a bridge of HIV transmission to the female population? Behavioural evidence from a systematic review and meta-analysis

Eric P. F. Chow; David Wilson; Lei Zhang

BackgroundHIV prevalence among men who have sex with men (MSM) in China has rapidly increased in recent years. It is suggested that MSM could be a potential bridge of HIV transmission to the general female population. We investigated the bisexual behaviour of MSM in China through systematic review and meta-analysis.MethodsWe conducted a systematic review and meta-analyses on published peer-reviewed Chinese and English literature during 2001-2010 according to the PRISMA guidelines. Marital status and sexual behavioural indicators of MSM were presented graphically using forest plots. The pooled effect rates with 95% confidence intervals were also calculated. Meta-regression analyses were performed to examine the factors associated with high heterogeneities across the studies.ResultsForty-three eligible articles (11 in English and 32 in Chinese) were identified. Our results showed that 17.0% (95% CI: 15.1-19.1%) of MSM in China are currently married to a woman and 26.3% (95% CI: 23.6-29.1%) of MSM had female sexual partners in the last six months. The pooled estimates for condom use rate between MSM and female sex partners was 41.4% (95% CI: 35.5-47.5%) at the last sex act; and 25.6% (95% CI: 23.0-28.4%) in the last six months. The consistent condom use rates with regular, non-commercial, casual and commercial female sex partners in the last six months were 23.3% (95% CI: 11.25-42.1%), 39.0% (95% CI: 28.8-50.3%) and 55.8% (95% CI: 41.4-69.4%), respectively.ConclusionsA substantial proportion of Chinese MSM is currently married or had sexual relations with a female in the past six months. In addition, low condom usage was common between married MSM and their wives, hence posing a higher risk of transmitting HIV. Harm-reduction programs targeting married MSM and their female partners are necessary to curb the further spread of HIV infection to the general female population.


Aids and Behavior | 2012

Patterns of Condom Use Among Men Who Have Sex with Men in China: A Systematic Review and Meta-Analysis

Eric P. F. Chow; David Wilson; Lei Zhang

HIV is rapidly spreading among men who have sex with men (MSM) in China. We estimate and compare rates of condom use among MSM in different regions of China through a systematic literature review. Meta-analyses were conducted over a final set of 66 studies to estimate national and regional condom use rates among MSM with different types of male sex partners. Country-wide, there has been a modest increase in reported condom use at last sex among MSM, from 56.1% (95% CI: 53.4–58.7%) in 2003–2005 to 61.6% (95% CI: 58.4–64.8%) in 2006–2008. Consistent condom use has also increased, from 32.5% (95% CI: 28.6–36.7%) in 2003–2005 to 36.3% (95% CI: 33.7–38.9%) in 2006–2008. Condom use was greatest and increasing among commercial sex partners, from 49.8 to 75.2% at last anal sex. Further condom promotion is still required to reduce the incidence of HIV infection among MSM in China.


PLOS ONE | 2012

HIV and sexually transmissible infections among money boys in China: a data synthesis and meta-analysis.

Eric P. F. Chow; Ka I. Iu; Xiaoxing Fu; David Wilson; Lei Zhang

Background Commercial sex workers within the population of men who have sex with men (MSM) in China, known as ‘money boys’ (MBs), are perceived to be at higher risk for HIV and other sexually-transmissible infections (STIs). Methods We conducted a systematic review and meta-analyses from peer-reviewed literature accessed in two English (PubMed and Embase) and three Chinese databases (CNKI, CQVIP, Wanfang data). A data synthesis exercise was carried out to determine the extent and patterns of behaviours and HIV/STI epidemics. Pooled estimates, with 95% confidence intervals, for each study variable were calculated. Results Thirty-two eligible articles (9 in English and 23 in Chinese) were identified. Our analysis indicated that Chinese MBs are generally young, currently employed, at low literacy levels and highly mobile. The prevalence of HIV, syphilis and co-infection among MBs were estimated to be 6.0% (4.2–8.5%), 12.4% (9.9–15.3%) and 2.2% (1.1–4.1%) over the period of 2004–2011. Level of condom use among MBs is generally higher than the broader MSM population (69.2% at last act, and 48.5% consistently over the past 6 months). One-third of the Chinese MBs identified themselves as bisexual and 8.7% (5.6–13.5%) are currently married to a female. Further, 40.9% (34.5–47.7%) of MBs participated in group sex in the past 12 months and 14.8% (10.6–20.3%) concurrently use illicit drugs. Conclusions HIV/STI epidemics have affected Chinese MBs but the evidence suggests that the extent of infections is not greater than among other MSM in China.


PLOS ONE | 2013

Methadone Maintenance Treatment Participant Retention and Behavioural Effectiveness in China: A Systematic Review and Meta-Analysis

Lei Zhang; Eric P. F. Chow; Xun Zhuang; Yanxian Liang; Yafei Wang; Caiyun Tang; Li Ling; Joseph D. Tucker; David Wilson

Background Methadone maintenance treatment (MMT) has been scaled up by the Chinese government alongside persistent compulsory drug user detention, but the extent to which detention interferes with MMT is unknown. The study systematically reviews Chinese MMT retention rates, reasons for drop out, and behavioural changes. Method Chinese and English databases of literature are searched for studies reporting retention rates, drug use and sexual behaviours among MMT participants in China between 2004 and 2013. The estimates are summarized through a systematic review and meta-analysis. Results A total of 74 studies representing 43,263 individuals are included in this analysis. About a third of MMT participants drop out during the first three months of treatment (retention rate 69.0% (95% CI 57.7-78.4%)). Police arrest and detention in compulsory rehabilitation was the most common cause of drop out, accounting for 22.2% of all those not retained. Among retained participants, changing unsafe drug use behaviours was more effective than changing unsafe sexual behaviours. At 12 months following MMT initiation, 24.6% (15.7-33.5%) of MMT participants had a positive urine test, 9.3% (4.7-17.8%) injected drugs and only 1.1% (0.4-3.0%) sold sex for drugs. These correspond to 0.002 (<0.001-0.011), 0.045 (0.004-0.114) and 0.209 (0.076-0.580) times lower odds than baseline. However, MMT participants did not have substantial changes in condom use rates. Conclusion MMT is effective in drug users in China but participant retention is poor, substantially related to compulsory detention. Reforming the compulsory drug user detention system may improve MMT retention and effectiveness.


International Journal of Infectious Diseases | 2012

Estimating HIV incidence among female partners of bisexual men in China

Eric P. F. Chow; David Wilson; Lei Zhang

BACKGROUNDnHIV prevalence among men who have sex with men (MSM) in China is rapidly increasing. The majority of Chinese MSM engage in bisexual behaviors and their female partners may be at high risk of HIV infection.nnnMETHODSnThrough a comprehensive literature review and the utilization of a mathematical optimization approach, this study infers quantitative distributions of sexual behavioral practices between Chinese MSM and their female partners over the past decade, and consequently estimates the trends in HIV incidence rates among female partners of Chinese MSM.nnnRESULTSnThe average Chinese MSM had approximately 0.89 (95% confidence interval (CI) 0.68-1.23) female sexual partners, with a mean number of total penetrative acts with the female partners of 0.57 (95% CI 0.52-0.62), in the past 6 months. Condom usage increased slightly from 23.57% (95% CI 14.20-32.93%) in 2002 to 27.33% (95% CI 19.88-34.78%) in 2010. Thus, the substantially increasing HIV prevalence among MSM has led to an increase in HIV incidence among partners of bisexual MSM of approximately 5.3-fold, from 0.18 per 1000 person-years in 2002 to 0.88 per 1000 person-years in 2010.nnnCONCLUSIONSnBisexual Chinese MSM may be a bridge group to the general female population for HIV transmission. There has been a substantial HIV incidence increase among their female partners.


Drug and Alcohol Dependence | 2012

Risk factors associated with HIV/HCV infection among entrants in methadone maintenance treatment clinics in China: A systematic review and meta-analysis

Xun Zhuang; Yafei Wang; Eric P. F. Chow; Yanxian Liang; David Wilson; Lei Zhang

BACKGROUNDnMethadone maintenance treatment (MMT) has rapidly expanded in China, from 8 pilot sites to 696 clinics covering 27 provinces, during 2004-2010. This study evaluates the demographic characteristics and drug use behaviors associated with Human Immunodeficiency Virus (HIV) and Hepatitis C Virus (HCV) infections among MMT entrants through a systematic review and meta-analysis of published literature.nnnMETHODSnThirty-nine eligible articles (1 in English and 38 in Chinese) were selected for this review. We extracted the relevant indicator information from all eligible studies and performed meta-analyses, by stratifying according to sex of the participants, age groups and drug use behaviors. Five provinces (i.e., Yunnan, Guizhou, Sichuan, Guangxi and Xinjiang) with the population size of HIV-infected drug users greater than 10,000 were defined as high transmission areas (HTAs) for HIV infection; whereas the remaining twenty-six Chinese provinces were considered as low transmission areas (LTAs).nnnRESULTSnThe odds of being infected by HIV among male drug users were significantly higher than for females in high transmission areas (OR=1.49, 95% CI: 1.11-1.99, k=9), while the opposite results were observed in low transmission areas (OR=0.46, 0.27-0.79, k=11). In comparison, no significant differences in risk behaviors were found between sexes in HTAs and LTAs. Younger age was not associated with risk of HIV infection, but was associated with higher risk of HCV infection (<30 years OR=1.88; 30-40 years OR=2.21, compared with >40 years, k=17). Risk of HIV infection was higher among injectors than non-injectors (OR=4.29, 2.70-6.79, k=14) and for those who inject, there was greater risk among sharers than non-sharers (OR=2.47, 1.44-4.23, k=4). Similar patterns were also observed in HCV infection (injectors: OR=10.82, 7.60-15.40; sharers: OR=3.41, 2.56-4.54, k=7).nnnCONCLUSIONSnCharacteristics of MMT entrants positive for HIV or HCV in China vary by disease types, geographical region, sex, age, and injecting behavior. These factors need to be considered in targeted interventions for MMT participants, such as age-specific health education and psychological treatment, antiretroviral therapy and needle-syringe exchange programs.


BMC Public Health | 2012

Distributions and trends in sexual behaviors and HIV incidence among men who have sex with men in China

Lei Zhang; Eric P. F. Chow; David Wilson

BackgroundHIV prevalence is increasing at a concerning rate among men who have sex with men (MSM) in China. Numerous studies have reported on levels of behaviors of Chinese MSM for different types of sexual partnerships, such as regular, non-commercial casual and commercial. This study aims to investigate the trends HIV incidence rates in relation to their risk sexual behaviors and partnership types among Chinese MSM.MethodThrough a comprehensive literature research from available English and Chinese literature databases, we collated relevant information of sexual behaviors of Chinese MSM. Further, with the utilization of a mathematical optimization approach, this study reconciles the distributions of sexual behavioral data over the last decade and infers the heterogeneous distributions of behavioral patterns among Chinese MSM. Distributions of high-risk behavioural indicators, including the number of sexual partners, number of sexual acts and condom usage in the past 6u2009months, are calibrated to available empirical data. Based on the resultant temporal trends in these distributions, the trends in HIV incidence rates associated with each type of partnership among MSM in China are also estimated.ResultsA total of 55 qualified articles have been identified. An average MSM has approximately 0.96 (95% CI, 0.59-1.18) regular, 3.75 (1.72-6.25) casual and 1.61 (0.97-2.78) commercial partners over a 6u2009month period and 4.33 (2.81-6.46), 1.42 (0.62-3.08), 1.48 (0.79-3.30) sexual acts per partnership respectively, corresponding to a total of 11.87 (8.87-15.25) acts. Condom usage has increased significantly during 2002–2010, at annual increases of 3.58% (2.98-4.12%), 5.55% (4.55-6.54%), and 5.03% (4.19-5.74%) for regular, casual and commercial partners respectively. These behavioral data implies an increase in HIV incidence of approximately 3.3-fold, from 2.04 (1.96-2.12) to 7.02 (6.71-7.35) per 1000 person-years during the same period. The proportion of new infections attributed to regular partnerships increased from 34% to 40%, whereas infections attributed to commercial partnerships reduced from 29% to 23% during 2002–2010.ConclusionRegular partnerships are the main contributor of new HIV cases among MSM in China, public health intervention strategies are required to increase condom usage and HIV testing rates among regular partners to curb the growing trend HIV incidence.


PLOS ONE | 2013

Sexually transmitted infections among heterosexual male clients of female sex workers in China: a systematic review and meta-analysis.

Megan M. McLaughlin; Eric P. F. Chow; Cheng Wang; Li Gang Yang; Bin Yang; Jennifer Z. Huang; Yanjie Wang; Lei Zhang; Joseph D. Tucker

Background Female sex workers have been the target of numerous sexually transmitted infection (STI) prevention strategies in China, but their male clients have attracted considerably less public health attention and resources. We sought to systematically assess the prevalence of HIV, syphilis, gonorrhea, and chlamydia among heterosexual male clients of female sex workers in China. Methods/Principal Findings Original research manuscripts were identified by searching Chinese and English language databases, and 37 studies analyzing 26,552 male clients were included in the review. Client STI prevalence across studies was heterogeneous. Pooled prevalence estimates and 95% confidence intervals were 0.68% (0.36–1.28%) for HIV, 2.91% (2.17–3.89%) for syphilis, 2.16% (1.46–3.17%) for gonorrhea, and 8.01% (4.94–12.72%) for chlamydia. Conclusions/Significance The pooled prevalence estimates of HIV, syphilis, gonorrhea, and chlamydia among clients in this review exceed the prevalences previously reported among population-representative samples and low-risk groups in China. However, heterogeneity across studies and sampling limitations prevent definitive conclusions about how the prevalence of STIs in this population compares to the general population. These findings suggest a need for greater attention to clients’ sexual risk and disease prevalence in China’s STI research agenda in order to inform effective prevention policies.

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Xiaoxing Fu

Renmin University of China

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Liang Chen

Centers for Disease Control and Prevention

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Liangmin Gao

Centers for Disease Control and Prevention

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