The prevalence of HIV among MSM in China: a large-scale systematic review


 Objectives：The prevalence of HIV among men who have sex with men (MSM) has shown a consistent upward trend in China and has become a significant public health challenge. The aim was to comprehensively estimate the national prevalence of HIV among MSM and its time trends through a large-scale systematic review.
Methods：Systematic search of Cochrane Library, PubMed, EMBASE, CNKI, VIP, and Wanfang Data databases without language restriction for studies on the prevalence of HIV among MSM published before March 2016. Studies were eligible for inclusion if they were published in the peer-reviewed literature and used validated assessment methods to assess the prevalence of HIV among MSM. Estimates were pooled using random-effects meta-analysis.
Results：Data were extracted from 325 cross-sectional studies (482,977 individuals) covered 59 cities from 30 provinces and municipalities of China. The overall national prevalence of HIV among MSM from 2001 to 2014 was estimated to be 6.32% (95% CI: 6.05–6.60%), with high between-study heterogeneity (I2 = 92.3%, P < 0.001). A dramatic increase was showed in HIV prevalence over the past 14 years, 1.31% (95%CI: 0.33–5.07%) in 2001, reaching a high of 11.44% (95%CI: 10.19%-12.83%) in 2014. HIV prevalence was the highest in those aged 50 years and older with HIV prevalence of 19.31 %( 95%CI: 13.14-27.44%). HIV was more prevalent in the illiterate population (16.76%), than in those who had received an education. Although the internet was a major venue for Chinese MSM seeking male sex partners (41.65%, 95%CI: 0.3947-0.4387), seeking MSM in bathhouses/saunas had the highest associated prevalence of HIV (14.58%, 95%CI: 11.40%-18.47%). The HIV prevalence among MSM varied by location: compared with other regions in China, HIV was highly prevalent among MSM in the southwest (11.06%, 95%CI: 10.22%-11.95%). Compared to participants who sometimes or always used condoms, participants who had never used a condom in the past 6 months had a higher risk of HIV infection, with odds ratios of 0.1 (95%CI: 0.08-0.14).Conclusions：Our analysis provided reliable estimates of China’s HIV burden, which appears to present an increasing national public health challenge. Effective government responses are needed to address this challenge and include the implementation of HIV prevention.


Introduction
Since the late 1990s, increasing numbers of men who have sex with men (MSM) have been diagnosed with HIV in the majority of countries with large and visible MSM communities [1][2][3]. Chinese scientists began studying HIV-related risk behaviours among MSM in 1993, but epidemiological studies assessing the prevalence of HIV were not conducted until 2000 [2]. A growing body of evidence from different time periods and locations has shown that MSM play an increasingly important role in China's HIV/AIDS epidemic. According to a report by the Chinese Ministry of Health, approximately 780,000 people were estimated to be living with HIV/AIDS in China in 2011, and 17.4% of the estimated HIV/AIDS cases were attributable to male-to-male sexual contact [3]. Recent national reports showed that HIV transmission in homosexual men accounted for 21.4% to 23.4% of the newly identified HIV/AIDS cases in some areas in China [2,4,5].
Estimations of the overall HIV prevalence among MSM in China have relied on several reviews conducted from 2001 to 2009, 2003 to 2009, and 2005 to 2010; these reviews found that MSM formed a high-risk population for HIV infection in China, with an overall prevalence ranging from 2.5% to 6.5%. Furthermore, these reviews identified a rising

Search strategy
A comprehensive literature search was conducted in the following databases to identify studies published up to March 2016: Cochrane Library, PubMed, EMBASE, Chinese National Knowledge Infrastructure (CNKI), VIP, and Wanfang Data. Two independent investigators performed the searches in parallel. We used combinations of keywords and medical subject heading (MeSH) terms as follows: ("HIV" or "AIDS" or "human immunodeficiency virus" or "acquired immunodeficiency syndrome") and ("homosexual" or "gay" or "men who have sex with men" or "MSM" or "bisexual" or "Tongzhi" [the Chinese term referring to homosexual men]) and ("China" or "Chinese") and ("prevalence" or "infection" or "associated risk" or "infection status" or "epidemic status" or "surveillance"). We also searched relevant reference lists and relevant journals manually and corresponded with authors to obtain the original data if necessary. We did not include grey literature (i.e., literature that had not been formally published). This systematic review and meta-analysis adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [347]. Table 1.

Characteristics of the selected studies
The 325 eligible articles included in this study covered 59 cities from 30 provinces and municipalities of China (no studies were from Tibet). The sample size of the selected studies ranged from 30 to 1,498,841 (mean 1486, 95% confidence interval [CI]: 538 -2434) [17,18]. Among the 325 selected articles, 6 reported results for multiple study sites, and 70 reported HIV prevalence estimates for more than 1 time period, resulting in a total of 572 HIV prevalence estimates. The first included study was reported in 2001 [12], with an HIV prevalence of 1.31%, and the studies provided overall estimates of the HIV prevalence among MSM in China from 2001 to 2014. We found a publication bias across the studies reporting the HIV prevalence (t=-3.25, p=0.0011) (Figure 2).

Study quality assessment
In the quality assessment, 190 of the included studies were considered "good" quality (values between 67% and 100%), 135 were considered "satisfactory" (values between 33% and 66%), and none were considered "poor" (values between 0% and 33%).

Demographic information
The demographic characteristics are detailed in Table 1

Chronological prevalence of HIV infections among MSM
Based on the study years selected for our investigation, the data were classified annually from 2001 to 2014, and then, homogeneity was assessed. The pooled estimates across all studies suggested that the HIV prevalence in this population increased substantially (Table 2). This increasing trend continued in subsequent years, reaching a peak of 11.44% (95% CI: 10.19-12.83%) in 2014.
Relationships between HIV prevalence and age, education, marital status, occupation, ethnicity, and sexual debut partner Table 3 shows the age-specific prevalence of HIV. For each 10-year increase in age, the prevalence of HIV also increased from 6.12% in people aged <20 years to 9.20% in people aged 20-29 years to the highest prevalence (19.31%) in those aged >50 years.
The prevalence of HIV decreased with increasing years of education, with a prevalence in the illiterate group of 16.76% (95% CI: 6.38-37.31%), which was higher than the prevalence rate among those who had received an education. Of the assessed occupations (including teacher, office staff, farmer, service business employee, unemployed and jobseeking, and worker), the prevalence of HIV was highest among farmers at 14.75% (95% CI: 3.78-43.22%).
The odds ratio (OR) of HIV for those whose first sexual encounter was with a male compared to those with a first sexual encounter with a female was 0.60 (95% CI: 0.53-0.69), suggesting that in China, MSM with a female sexual debut partner had a higher HIV prevalence than those with a male sexual debut partner. Drug use was not a significant contributor to HIV transmission among Chinese MSM (OR: 1.14, 95% CI: 0.31-4.21).

Geographical characteristics of the HIV prevalence
To determine the geographical characteristics of the HIV prevalence in China, we analysed the differences in prevalence by geographical divisions in China based on its provinces or municipalities. The number of studies, total HIV-positive population, and pooled sample size were summarized for the different geographical divisions (Table 4).

Condom use information (in the last 6 months)
Participants who had engaged in unprotected sex in the past 6 months had a higher risk of HIV infection than those who reported protected sex (either sometimes or always using a condom). The ORs for participants who never used a condom during sex with men, during commercial sex with men, and during sex with a woman in the past 6 months were 0.1074 (95% CI: 0.0829-0.1380), 0.1121 (95% CI: 0.0944-0.1326), and 0.0670 (95% CI: 0.0307-0.1397), respectively.

Discussion
To the best of our knowledge, this study is the first large-scale systematic analysis of the epidemiology of HIV infection among MSM in China up to 2016. The study included 325 eligible studies that covered 59 cities from 30 provinces and municipalities. All the studies were of "satisfactory" or "good" quality, and the results of these studies were heterogeneous. Significant publication bias (Begg's test, t=-3.25, p-value=0.0011) existed across the studies reporting the prevalence of HIV. The national estimate of HIV prevalence among MSM from 2001 to 2014 was 6.32% (95% CI: 6.05%-6.60%), with study prevalence rates ranging from 0% (95% CI: 0.1-2.53%) to 22.91% (95% CI: 18.08-28.34%) [10,331]. The prevalence of HIV among MSM increased substantially between 2001 and 2014. These findings might have important policy implications because the prevalence also differed by age, education, occupation, and condom use. The data from this study indicated that the HIV prevalence differed by region, and a high burden of HIV infection was observed among MSM in southwest China, especially in Chongqing city. Although the internet was a major venue used by Chinese MSM to search for male sex partners, MSM who sought partners at bathhouses, saunas, and massage rooms had the highest HIV prevalence. Studies using snowball sampling had a higher prevalence of HIV infection than studies using RDS, convenience sampling, or multiple sampling methods. A possible explanation for this finding is that individuals with high-risk behaviours are more likely to accept HIV testing through snowballing sampling [2].
The present study provides insights into the national HIV prevalence among MSM over the past 14 years and proposes a critical suggestion for China's health department to implement more effective prevention strategies and policies in the future.  [336]. Remarkably, our study showed a dramatic, nearly 9-fold increase in the HIV prevalence (from 1.31% in 2001 to 11.44% in 2014) over the past 14 years, and this growth should receive a greater amount of attention. The increasing HIV prevalence may be associated with several factors: 1) the increasing migration for better employment opportunities and living conditions from regions with a high HIV prevalence, such as from southern China or from the countryside, to large cities, which have a relatively open culture and convenient sexual venues (e.g., bars, saunas, parks, and sex clubs.) [196]; 2) the gradual changes in attitudes towards sex and increased openness of male homosexuality in China with changes in Chinese society, although homosexuality is still not widely accepted by the general population [337]; and 3) the common occurrence of marriage between MSM and women because MSM might act as a bridge for HIV transmission from other MSM to the general population [9]. Additionally, to some extent, the increased HIV prevalence may be due to an increase in the testing rates because HIV testing among Chinese MSM has increased over the past decade.
A better understanding of the mechanisms underlying the age-related risks of HIV infection can help address the situation in practice. The findings presented in this article confirmed the notable increase in the HIV prevalence with increasing age in China because HIV was most prevalent in those aged 50 years and older; these results demonstrated a prominent age-dependent increase in HIV. The distribution of HIV cases by age differed somewhat from that of other countries [338]. A higher HIV prevalence was found among MSM aged 15-19 and 20-24 years in the United States and among 15-to 24-year-old MSM in the United Kingdom [337,339]. The reason for the increasing HIV prevalence in older MSM may be that older MSM have longer durations of exposure to HIV; additionally, unprotected anal intercourse (UAI) is more common among older MSM than in their younger counterparts, who may also have received a higher level of education [340]. Therefore, behavioural scientists and practitioners alike must address the implications of these findings when developing targeted prevention interventions and treatment services for older MSM [341].
Importantly, the largest subgroup of MSM in this study was those aged 20-29 years, who accounted for 52.69% of the MSM (95% CI: 50.92-54.46%) ( Table 1) Our study found that those who had less education, sought sexual partners at bathhouses or saunas, were farmers and were divorced or widowed were more likely to be infected with HIV. Regarding economic considerations, MSM with less education experience a lack of appropriate health messages and support and are more inclined to seek partners at bathhouses, saunas, or massage rooms due to their low costs [253]. The prevalence of HIV among farmers was 14.75%, which was the highest of all occupations examined. One possible explanation for this high prevalence is that farmers have a lower chance of receiving an education than other occupations in China. Yang et al. found that condom use was clearly higher among MSM with a higher level of education, such as college students or teachers, than that among others and that these more educated groups could volunteer to promote HIV intervention efforts and facilitate a reduction in the HIV infection rate among MSM [343].
Our study indicated that 22.32% of MSM were married to women; these MSM may conceal their sexual orientation due to the traditional values and social stigma present in China, making it unlikely that they can be reached by traditional prevention measures targeting the general MSM population. Although the proportion of divorced or widowed MSM was only 4.58%, the HIV prevalence appeared to be higher (15.16%) in this population than in the single, married, and cohabitating groups. This higher prevalence may be because MSM who are divorced or widowed no longer have access to a legitimate, routine sexual life and are thus more prone to illegal sexual behaviour and have greater exposure to high-risk environments [320].
Interestingly, HIV knowledge was high in the MSM population (91.07%, 95% CI: 89.52-92.41%), but consistent condom use was low, reflecting the complexity of the hypothesis that knowledge transfer and behavioural change are keys to HIV prevention. The study revealed that the rate of consistent condom use was lower when MSM had sex with women (29.56%) than when they had sex with men (41.46% for sex with men and 52.10% for commercial sex with men) over the past 6 months (Table 1). Therefore, MSM are vulnerable to HIV infection from both genders and can serve as a bridge for HIV transmission from one gender to the other. Han et al. reported that MSM who had sex with women were more likely to be married and that once they were HIV carriers, they were likely to exhibit commercial sexual behaviour [112]. This study confirmed that in addition to distribution of accurate and up-to-date information on risky behaviours and effective community-based prevention programmes that make condoms available and accessible, concrete strategies that illustrate and highlight the harm and dangers of not using a condom during penetrative sex need to be implemented to enhance individuals' motivations to change their behavioural patterns and skills and reduce their HIV risk [344].
Our data indicated that drug use was not a significant contributor to HIV transmission among Chinese MSM (OR: 1.14, 95% CI: 0.31-4.21), suggesting that drug use did not significantly contribute to overall HIV transmission among MSM. However, the increased illicit drug use among Chinese MSM may perpetuate the HIV epidemic, and this relationship may be similar to those in Western countries where drug use is a major risk for HIV transmission [345].
This systematic review and meta-analysis had several limitations. First, the scarcity of existing research did not allow for subgroup analyses of HIV prevalence by number of sexual partners or for analyses of the differences in condom use among MSM when purchasing or selling sex. Second, this study represented a wide spectrum of MSM in China; the included studies used snowball sampling, RDS, time venue sampling, convenience sampling, and multiple sampling methods. However, few studies in Jilin province (n=1) and Tibet (n=0) were included, which might have affected the regional HIV prevalence among MSM. Finally, significant publication heterogeneity (p-value=0.0011) was observed in our analysis. Differences between sampling methods, sample sizes, and study locations may explain some of these inconsistencies. Therefore, readers should be aware that they may be viewing a biased sample of experimental results and should moderate the strength of the conclusions accordingly [346].

Competing interests
The authors declare no conflicts interest.

Funding
This article was funded by the National Natural Science Foundation of China (No.

Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.