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Original Study

Human Immunodeficiency Virus Prevalence Is Increasing Among Men Who Have Sex With Men in China: Findings From a Review and Meta-Analysis

Chow, Eric Pui Fung MApplSc*; Wilson, David P. PhD*; Zhang, Jun ML; Jing, Jun PhD; Zhang, Lei PhD*

Author Information
doi: 10.1097/OLQ.0b013e31821a4f43

Approximately 760,000 people are currently living with human immunodeficiency virus (HIV) in China.1 Although most global hubs of HIV have passed their peak of infection, HIV epidemics are rapidly expanding in China.1,2 Recently, there has been concern of emerging epidemics among men who have sex with men (MSM).3,4 It is estimated that 2% to 5% of sexually active Chinese males have sex at some time with other men, accounting for 2 to 8 million Chinese males.5,6 In recent years, the proportion of HIV diagnoses in China attributed to male homosexual exposure increased from 12.2% in 2007 to 32.5% in 2009.7 Accompanied with the rapid HIV epidemic growth, high syphilis incidence rates among Chinese MSM were also reported in several cohort studies,8,9 indicating an emerging coinfection epidemic among MSM in China.

Chinese MSM also tend to have sex with women. Due to traditional Chinese cultural and moral values, many MSM in China get married and have children, concealing their homosexuality. Previous studies showed that approximately 25% of MSM in China are currently married,10–13 and 44% have ever been married.14 Bisexual behaviors of MSM pose potential threats of acting as a bridge for HIV transmission to their female partners, spreading the epidemic into general female population.

Numerous individual research studies have been conducted to estimate HIV prevalence among MSM in China; the studies have varied by time period and location and findings from only a minority of studies have been published in English. There are little consistent data for understanding the temporal and geographical levels of HIV prevalence among MSM in China. It is timely to review the current evidence of the extent and patterns of HIV prevalence among MSM across all regions of China and summarize by time and space in a meta-analysis framework. This is highly important for public health surveillance of HIV among this growing and important population group at risk in China. In this study, we report results of both temporal and geographical trends of HIV prevalence among MSM from 2001 to 2009 by collating available data from English and Chinese journal articles, government reports and grey literature, and conducting meta-analyses.

METHODS

Search Strategy

A systematic review of published articles, conference presentations, and reports was conducted by searching PubMed, Medline, Chinese Scientific Journals Fulltext Database (CQVIP), China National Knowledge Infrastructure, and Wanfang Data from 2001 to 2009. Keywords used in the database search included (“HIV” OR “AIDS”) AND (“homosexual” OR “gay” OR “bisexual” OR “Tongzhi” (Chinese term referring to homosexual men) OR “men who have sex with men” OR “MSM”) AND “China” OR the name of major cities of China. Two investigators (E.P.F.C., L.Z.) performed the systematic search according to the agreed inclusion criteria. The results obtained from the independent searches were compared and any differences were resolved by consensus with a third investigator (D.P.W.). We followed the standard guidelines issued by Preferred Reporting Items for Systematic Reviews and Meta-analyses in 2009 for conducting and reporting this review and analysis.

Study Selection

Studies were included if they reported the prevalence of HIV infection among Chinese populations of MSM (including homosexual and bisexual groups) through a peer-reviewed journal or reports from Chinese academic institutions and government-managed departments such as the Chinese Center for Disease Control and Prevention. HIV prevalence estimates were included if they were based on laboratory serologic testing. Testing based on other biologic fluids (urine or oral) was excluded in this review. Studies based on self-reported HIV status were also excluded from this review. Studies with no reported HIV prevalence among MSM, site and sampling size of the study were excluded from further analysis.

To avoid overestimation of the prevalence among MSM, we excluded studies that only reported the estimates of HIV prevalence among money boys, transgender MSM and men who also identified as injecting drug users. Studies were included in this review if small proportions of money boys or men who reported injecting drugs (less than 15% of the total sample) were reported. If the same study data were published in both English and Chinese sources, the articles published in Chinese were excluded from the review.

Data Collection

We extracted information about the study design, population, and HIV prevalence. The studies were categorized by geographical location, according to the 6 traditional Chinese regions of administrative division (East China, Northeast China, North China, South Central China, Northwest China, and Southwest China) as well as Beijing city (see Fig. 1). The studies were further categorized into the following 3 time periods with 3-year intervals in each: 2001–2003, 2004–2006, and 2007–2009 (Table 1).

Figure 1.
Figure 1.:
Seven Chinese geographical regions. The number in each province represents the number of publications reporting HIV prevalence among MSM.
TABLE 1
TABLE 1:
Studies Reporting Prevalence of HIV Infection Among Men Who Have Sex With Men in China
TABLE 1
TABLE 1:
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TABLE 1
TABLE 1:
(Continued)
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(Continued)

Statistical Analysis

Analyses were carried out using the Comprehensive Meta-analysis software (V2.0, Biostat, Englewood, NJ). The effect rates of pooled prevalence estimates, 95% confidence intervals, and relative weight for each study were determined by using random effect models. Findings are presented in the form of forest plots.

The significance of heterogeneity across studies in each time period for each geographical region was measured by the Cochran Q statistics (P < 0.10 generally indicates statistically significant heterogeneity). The extent of heterogeneity in the studies was measured by the I2 statistic (I2 = 25, 50, and 75 generally indicate thresholds of low, medium, and high heterogeneity, respectively). Variations between the time periods in each Chinese region were measured by the chi-squared test. The Begg and Mazumdar rank correlation in each category of studies was used to measure the potential presence of publication bias (P < 0.05 on the Kendall τ indicates statistically significant publication bias).

RESULTS

Study Selection for Meta-Analysis

A total of 177 articles were identified by our initial search strategy, and 86 articles were ultimately excluded (40 did not report HIV prevalence among MSM, 22 did not report new estimates of prevalence, 10 did not report the location of study, 9 were overlapped in the databases, 2 were unrelated to the topic, 2 conducted urine HIV test, and 1 conducted oral fluid HIV test) (Fig. 2). The remaining 91 articles reported HIV prevalence among MSM during the period 2001–2009 and were included in this study. Of the 91 articles, 23 were published in English and the remaining 68 articles were published in Chinese.

Figure 2.
Figure 2.:
Flow chart showing the selection process for studies included in the review and meta-analyses.

Among the 91 selected articles, 4 reported multiple study sites and 15 reported HIV prevalence estimates for more than 1 time period, resulting in a total of 137 HIV prevalence estimates (Table 1). There were 9, 69, and 59 reported HIV prevalence estimates among MSM in China in the time periods 2001–2003, 2004–2006, and 2007–2009, respectively.

The sample size of selected studies varied from 1916 to 2738.36 The mean sample size was 344.5 (median: 240), and nearly half of the studies (49%) were conducted in MSM venues (particularly in gay bars), whereas 39% of studies used venue-based method to recruit MSM participants.

Prevalence of HIV Infection Among MSM

Our pooled estimate across all studies suggests that HIV prevalence among MSM countrywide in China has increased substantially: it was 1.4% (0.8%–2.4%) during 2001–2003, 2.3% (2.0%–2.6%) during 2004–2006, and 5.3% (4.8%–5.8%) during 2007–2009 (Fig. 2). However, there has been substantial epidemiologic variation between different geographical regions. HIV prevalence during 2001–2003 ranged from 0.3% (0.0%–5.3%) in the East to 2.1% (1.0%–4.1%) in South Central (Fig. S1a, Supplemental Digital Content, online only, available at: https://links.lww.com/OLQ/A22). During the period 2004–2006, Northwest region had the lowest HIV prevalence among MSM (1.0%, 0.5%–1.7%) and Southwest China had the highest HIV prevalence (4.0%, 2.8%–6.5%) compared to other Chinese regions (Figs. 3, S1b, Supplemental Digital Content, online only, available at: https://links.lww.com/OLQ/A22). This increasing trend continued in the following years across all regions. HIV prevalence among MSM in the Southwest increased rapidly by nearly triple, reaching the high level of 11.4% (9.6%–13.5%) during 2007–2009. HIV prevalence in the North and Northeast regions doubled to 4.8% (3.5%–6.6%) and 3.9% (2.8%–5.4%), respectively; and it tripled to 3.5% (2.5%–4.8%) in the Northwest in comparison with levels in 2004–2006 (Fig. 3). HIV prevalence in East and South Central China also experienced significant increases to 3.5% (2.6%–4.7%) and 4.3% (3.7%–5.0%), respectively (Figs. 3, S1c, Supplemental Digital Content, online only, available at: https://links.lww.com/OLQ/A22).

Figure 3.
Figure 3.:
Estimated HIV prevalence among MSM in each Chinese region and countrywide during 2001–2009 among 91 studies. Each column represents the pooled estimate from meta-analyses over all studies for the given region and time period. The error bars represent standard deviation of the percentages.

The pooled HIV prevalence estimated over all studies for each Chinese region and nationwide over the past decade is summarized in Figure 3. All geographical regions, except Beijing (P = 0.12), experienced a significant increase in HIV prevalence over this period (P < 0.05). MSM in the Northwest region have the lowest HIV prevalence. MSM in the Southwest region have the highest HIV prevalence since 2004 and have experienced the fastest growing HIV epidemic.

Heterogeneity and Publication Bias Across Studies

Among 18 regional subgroups analyses, 8 exhibited significant heterogeneity (Beijing 2004–2006; North 2007–2009; East, Northeast, and Southwest in both 2004–2006 and 2007–2009). The inconsistency varied and is moderately large in these 8 regional subgroups (I2 = 39.92–84.96, indicating that approximately 40%–85% of the total variability is caused by the true population heterogeneity rather than sampling error). Conversely, 6 out of 18 regional subgroups reported I2 = 0% heterogeneity (East, Northeast, South Central, and Northwest during 2001–2003; South Central 2004–2006; and Beijing 2007–2009). Out of 3 national groups, 2 experienced significantly high heterogeneity (I2 were 82% and 87% for National 2004–2006 and 2007–2009, respectively). There were no significant publication biases observed (P = 0.095, 0.132, and 0.311 during 2001–2003, 2004–2006, and 2007–2009, respectively).

DISCUSSION

We report findings from a review of available literature on HIV prevalence among MSM across the 7 geographical regions of China. Our meta-analyses showed that HIV prevalence among MSM in China has substantially increased since 2001. The national prevalence increased from 1.4% (0.8%–2.4%) during 2001–2003 to 2.3% (2.0%–2.6%) during 2004–2006, to 5.3% (4.8%–5.8%) during 2007–2009. This trend is indicative of trends that occurred across all regions in China. However, we found significant variation in the magnitude in different regions. Of particular note, HIV prevalence has increased to alarmingly high levels among MSM in the Southwest region which is currently at 11.4%.

Our estimated national HIV prevalence (5.3%) is consistent with the prevalence of 5.0% reported by a recent national epidemiologic survey over 61 major cities in China in 2009,98 but is higher than a previous meta-analysis estimate of 2.5% published by Gao et al. in 2009.99 This previous study did not account for the clear time trend in HIV prevalence estimates and pooled measures from 2001 to 2008 countrywide, and hence is likely to be an underestimate of the current prevalence. Another recent study published in Chinese by Tang et al.100 estimated annual HIV prevalence, 2002–2006, but they did not detect an increasing trend. This is likely due to over categorization of temporal divisions, grouping of diverse geographical regions, and not including recent years (after 2007) when prevalence was observed to increase most rapidly. Our study, with more than 90 collated studies from different regions during 2001–2009, provides a thorough estimate of the level and trend of HIV epidemics among MSM across China.

Significantly high levels of heterogeneity in national group analyses were not unexpected. Variations in HIV prevalence estimates between studies in the national groups could be explained by the different characteristics between studies. Geographical regions and study times are the 2 main factors contributing to the high heterogeneities. Secondary factors including sample sizes and methodology of MSM recruitment also likely result in substantial heterogeneities across studies in the regional subgroup analyses. As the majority of studies were conducted in MSM venues, participants are more likely to have high-risk sexual behavior than otherwise. This may overestimate the actual HIV prevalence.

Despite the rapid increasing trend of HIV prevalence among MSM in China, levels are relatively low compared to other Asian countries. For example, HIV prevalence among MSM in Cambodia, Indonesia, and Thailand are estimated to be 7.8%, 9.0%, and 24.6%, respectively.101

To our knowledge, this study is the first time that HIV prevalence among MSM in China was reviewed by geographical regions over time. This geographical-specific analysis provides important implications for understanding the past spread, current situation and projecting the future epidemic trend of HIV in this important population group. These estimates provide valuable data for disease surveillance in China and can assist in planning for the allocation of public health resources to prevent further transmission among the most at-risk populations.

Several limitations in this study should be noted. First, sentinel surveillance of HIV transmission among MSM is limited in China, especially in Northwest China. Sentinel sites in most Chinese provinces did not cover MSM until 2003 and some sites have not yet initiated any surveillance targeting MSM.102 HIV prevalence among MSM has not been reported in 6 out of 31 provinces in China (Fig. S1, Supplemental Digital Content, online only, available at: https://links.lww.com/OLQ/A22) and this limits our analysis of prevalence trends in these regions. Second, HIV prevalence data predominantly originated from studies conducted in major cities in urban China but not in rural areas. There may be significant differences between urban and rural areas due to numerous factors including sexual behaviors, size of MSM populations, levels of education, and degree of societal discrimination.103 Further study of HIV among Chinese MSM in rural areas is required. Third, very few studies were identified in some particular regions for specific time periods. For example, HIV prevalence estimates in the East (0.3%) and Northwest (0.6%) regions during 2001–2003 were based on 1 study and in other regions and time periods some estimates were based on studies in limited numbers of cities. Fourth, our study results may have publication bias whereby some prevalence data may exist but are have not been published or detected by our search strategy. Fifth, heterogeneity existed between studies reviewed due to different survey methodologies, demographics of MSM recruited and sampling sizes in different studies. The meta-analyses could not take all of these variations across individual studies into account. Limited reporting of HIV prevalence in recent years, as a result of delay in publication, is also a potential factor affecting our results.

HIV prevalence in the Southwest is remarkably high in comparison with other regions. Consistent with our findings, the proportion of all reported diagnosed cases who are attributed to male homosexual exposure in the city of Kunming of Southwest China has increased from 2.2% in 2000 to 42.2% in 2007.4 The high HIV prevalence among MSM in the Southwest may be associated with the early and relatively large HIV epidemic among people who inject drugs in this region104 or prevalence of other risk factors associated with higher HIV transmission. High-risk behaviors are common among MSM in China as evident from a large study of sexual behaviors among 2250 MSM across China conducted in 2006, which revealed that only 40% of MSM used condoms in anal sex acts consistently in the last 6 months.10 Routine behavioral surveillance to identify trends in underlying factors for the rapid increase in prevalence in the Southwest, and elsewhere, is required.

The consistently growing trend of HIV epidemics among Chinese MSM suggests that the epidemic could increase further in the absence of effective public health strategies targeted for MSM. As homosexuality is becoming more open and accepted in Chinese society, a substantially increasing number of gay websites and newsletters have appeared and social networking has significantly expanded across the country. Venues specifically designed for MSM such as gay bars and saunas have also become more visible in the major urban cities. These factors may facilitate further spread of HIV infections. Furthermore, according to one study, approximately 35% of unmarried and 70% to 80%105,106 of married MSM had sex with women in the last 6 months and only 16% to 29% of these MSM consistently used condoms.10 Consequently, MSM may also act as bridge of HIV transmission to their regular female sex partners.

China did not launch large-scale prevention efforts among MSM until the initiation of the China-Gates Cooperative HIV Prevention Program in 2009, which targets homosexual men in 14 major cities. Before this program, only Yunnan and Sichuan in Southwest region had coordinated HIV prevention strategies for MSM. Currently, the Chinese government has little experience in HIV prevention among MSM and is only beginning to implement community-based health education. The Chinese government will require active engagement and participation of the gay community for sustainable and effective interventions to mitigate the further spread of HIV among MSM.

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