BioMed Research International

Volume 2014 (2014), Article ID 620431, 12 pages

http://dx.doi.org/10.1155/2014/620431

Review Article

Prevalence of HIV and Syphilis Infection among Men Who Have Sex with Men in China: A Meta-Analysis

Yunhua Zhou,¹ Dongliang Li,² Dabing Lu,¹ Yuhua Ruan,³ Xiao Qi,² and Ge Gao¹

¹Department of Epidemiology and Health Statistics, School of Public Health, Suzhou University, Suzhou, Jiangsu 215123, China

²Chaoyang Center for Disease Control and Prevention, Beijing 100021, China

³State Key Laboratory for Infectious Disease Prevention and Control, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, Beijing 100026, China

Received 28 September 2013; Accepted 6 January 2014; Published 23 April 2014

Academic Editor: Muktar Aliyu

Copyright © 2014 Yunhua Zhou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Objectives . To figure out the most current prevalence of HIV and syphilis in MSM in China. Methods. A meta-analysis was conducted on the studies searched through PubMed, CNKI, and Wanfang published between 1 January 2009 and 11 April 2013. Results. Eighty-four eligible studies, either in Chinese or in English, were included in this review. The pooled prevalence of HIV and syphilis infection in MSM in China was 6.5% and 11.2%, respectively. The subgroup analyses indicated that the prevalence of HIV infection was higher in the economically less developed cities than that in the developed cities (7.5% versus 6.1%, ). In contrast, the prevalence of syphilis infection was lower in less developed cities than in developed cities (8.6% versus 15.1%). Studies with a sample size smaller than 500 had a lower prevalence of HIV and syphilis infection than those with a sample size greater than 500 (5.9% versus 7.2% for HIV; 11.0% versus 11.5% for syphilis, respectively). Conclusions. HIV and syphilis infection are prevalent in MSM in China. The different prevalence of HIV and syphilis infection between developing and developed cities underscores the need to target prevention strategies based on economic conditions.

1. Introduction

The human immunodeficiency virus (HIV) and syphilis infection epidemics present an intractable problem to the world. This is also true in China, where there is a marked increase of people living with HIV/AIDS, from 740,000 in 2009 to 780,000 in 2011. Approximately 17.4% of new HIV cases are attributed to homosexual transmission [1]. It was said that the epidemic of HIV infection among men who have sex with men (MSM) has been the gravest of the six newborn HIV/AIDS challenges in China [2]. From 2009 to 2013, the prevalence of HIV among MSM ranged from 1.7% to 21.0% in China [3, 4]. A recent meta-analysis reported that almost 5.3% (95% CI: 4.8%–5.8%) of MSM in China were living with HIV, which was more than 90 times higher than the general public [5]. The prevalence of syphilis in MSM increased from 6.9% to 11.8% between 2003 and 2009 [6, 7].

The fast growth of the HIV epidemic has been observed in some reports [5, 8]. Although there have been several meta-analyses on prevalence of HIV and syphilis in MSM [5, 8, 9], the most recent meta-analysis only included studies until 2008. Thus, it is important for us to have a better and more thorough understanding of the current prevalence of HIV and syphilis. Therefore, we performed a meta-analysis of all available literature published from 2009 to 2013.

Given the poor awareness of AIDS-related knowledge in economically developing cities, which may lead to higher prevalence of marriage and bisexuality and lower condom use than economically developed cities, we also carried out a subgroup analysis to explore the differences in HIV and syphilis prevalence between developing and developed cities in China. Results from the analyses may guide future policies for more rational allocation of prevention and treatment resources.

2. Methods

2.1. Search Strategy

A systematic review of published articles was conducted by searching the following database: PubMed, Chinese National Knowledge Infrastructure (CNKI), and Wanfang from January 1, 2009, to April 11, 2013. Search terms included HIV, AIDS, syphilis, STD, sexually transmitted disease, prevalence, MSM, homosexual, gay, sex between men, and China. Reference lists were also referred to for additional articles. This review was conducted according to the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) statement issued in 2009.

2.2. Study Selection

Studies were included if they met the following criteria: (1) published in Chinese or English language; (2) cross-sectional or cohort studies that reported either HIV or syphilis prevalence or both; (3) HIV and syphilis infection was diagnosed from at least two laboratory serologic testing methods; (4) articles that presented study design information, including study period, study site, and sampling method. Studies were excluded if (1) the study participants were MB (Money Boys) or young MSM (younger than 18 years old); (2) the sample size was smaller than 150. Studies with no specific study cities were also excluded from subgroup analyses. If articles with the same data were published in both Chinese and English, the English source was included.

2.3. Data Extraction

The first author extracted the following data from the included studies, which was later verified by the second author: the first author and published year, study period, study site, sampling methods, average age of MSM participants, sample size, and prevalence of HIV infection or syphilis infection or both. The study sites were divided into developing and developed cities (as assessed on the basis of based on per capita gross domestic product (GDP) for each city). Developing cities were defined as those with a per capita GDP lower than 15,000 RMB and developed cities were defined as cities with per capita GDP higher than 15,000 RMB. GDP of each city per person-year was obtained from http://tieba.baidu.com/p/2312163828. Disagreements were resolved by discussion. If no consensus could be reached, a third author would be referred to.

2.4. Validity Assessment

Validity assessments were accomplished by two workers. Studies were considered to be of high validity if they met the following criteria: (1) reported both HIV and syphilis infection; (2) used two or more recruitment methods; (3) sample size larger than 500; (4) published in English.

2.5. Statistical Analysis

Meta-analyses of the prevalence of HIV and syphilis infection among MSM were carried out by Meta-Analyst software (Beta 3.13). -test (significance level ) and (significance level ) statistics were calculated to measure homogeneity of studies. Studies that had either 0.25 were defined as heterogeneous. Potential publication bias was assessed by Begg’s test. Pooled prevalence of HIV and syphilis infection, 95% confidence intervals, and the relative weight for each study were calculated by using random effects models. Due to the heterogeneity which is commonly observed in meta-analysis concerning sensitive groups such as MSM, we conducted a meta-regression with 10,000 permutations in a Monte Carlo simulation to explore the sources of between-study heterogeneity with the following covariates: economy status, sampling methods, sample size, and published year. Subgroup analyses were conducted to obtain the prevalences of HIV and syphilis from different stratifications.

3. Results

3.1. Study Selection for Meta-Analyses

1222 articles were retrieved after the initial search from databases and another 6 articles were included from reference lists. A total of 1096 articles were removed after screening of titles and abstracts because they were not topically relevant (), were reviews (), and used the same data (). 151 articles were eligible for full-text screening and 67 were further excluded because they did not report the sampling methods or study site (), did not mention the study period (), had a sample size smaller than 150 (), included MB or young MSM (), presented neither HIV nor syphilis prevalence (), just used one method to diagnosis syphilis (), and tested HIV infection by urine (). The detailed process of data selection is illustrated by Figure 1.

Figure 1: Flow chart of the meta-analysis studies selection.

3.2. Study Characteristic

Eighty-four studies with estimates of HIV prevalence (English 18, Chinese 66) and seventy-six studies with estimates of syphilis prevalence (English 17, Chinese 59) were finally identified in this review, which covers 59 cities from 29 provinces and municipalities in China (no studies from Hainan, Tibet, Hong Kong, Macao, and Taiwan). The prevalence of HIV and syphilis ranged from 1.7% to 21.0% and 0.9% to 31.2%, respectively [3, 4, 10–89]. In the meta-analysis of pooled prevalence of HIV, the sample size ranged from 150 to 6101 (total 71,845), and in the estimating of syphilis prevalence, the sample size oscillated between 157 and 6101 (total 65,162). About half of them were located in developing cities (50.7% and 51.4% in analyses of HIV and syphilis prevalence, resp.,). The following sampling methods were used to recruit participants: snow ball (), respondent driven sampling (RDS) (), multiple sampling methods (), and others (). The basic information of the 84 included studies is represented in Table 1.

Table 1: Meta-regression and subgroup analyses of HIV and syphilis prevalence among men who have sex with men in China.

Study characteristic
Stratified meta-analysis

HIV
Syphilis

Prevalence (95% CI)
Meta-regression (, value)
Prevalence (95% CI)
Meta-regression (, value)

Sample size

    500
5.9% (5.0–7.0%)
1.017
11.0% (9.3–12.9%)
1.007

    500
7.2% (5.8–8.9%)

11.5% (9.8–13.5%)

Sampling methods

    RDS
7.4% (5.7–9.7%)
0.996
9.1% (7.1–11.6%)
1.009

    Snow ball
7.2% (5.4–9.4%)

13.3% (10.8–16.2%)

    Multiple Methods
5.9% (4.5–7.7%)

10.5% (8.2–13.3%)

    Others
6.2% (5.6–7.4%)

12.2% (10.0–14.9%)

Economy status

    15,000$
7.5% (6.5–8.6%)
0.971
8.8% (7.7–10.0%)
1.074

    15,000$
6.1% (4.7–8.0%)

15.5% (13.0–18.3%)

Published year

    2009-2010
5.9% (5.1–6.9%)
1.017
12.1% (10.6–13.7%)
−0.980

    2011–2013
7.6% (6.1–9.5%)

9.6% (7.6–12.1%)

3.3. Pooled Prevalence of HIV and Syphilis

According to our meta-analyses, the estimates of HIV prevalence in MSM in China ranged from 1.7% to 21.0%. The pooled prevalence of HIV infection was 6.5% (95% CI 5.6% to 7.4%), as seen in Figure 2, with substantial heterogeneity (. Estimates of syphilis prevalence ranged from 0.9% to 31.2% and the overall prevalence was 11.2% (95% CI 10.0% to 32.6%), as shown in Figure 3, with substantial heterogeneity observed .

Figure 2: Forest plot showing the meta-analyses of pooled prevalence of HIV among men who have sex with men in China.

Figure 3: Forest plot showing the meta-analyses of the pooled prevalence of syphilis among men who have sex with men in China.

3.4. Meta-Regression and Subgroup Analyses

Results of meta-regression indicated that economic status and sample size contributed to the heterogeneity between studies (Table 2).

Table 2: Basic information of the 84 included studies.

First author, published year
Sample size
Sampling methods
Location
Economy status
Prevalence (%)

HIV
Syphilis

Liang, 2011 [35]
511
Multiple methods
Foshan
Developed
7.0
8.0

Sun, 2009 [50]
401
Multiple methods
Dalian
Developed
4.2
17.5

Yang, 2012 [72]
264
VCT
Fuyang
Developing
5.7

Chen, 2012 [15]
400
Snow ball
Guilin
Developing
3.5
4.0

Wen, 2010 [64]
452
Snow ball
Guangzhou
Developed
4.9
6.0

Huang, 2011 [32]
395
Snow ball
Hefei
Developing
3.0
13.4

Wang, 2009 [54]
1348
Multiple Methods
Heilongjiang
Developing
2.3
14.8

Wang, 2010 [61]
200
Snow ball
Lanzhou
Developing
7.0
12.5

Wang, 2012 [58]
400
RDS
Mianyang
Developing
11.0
23.5

Lu, 2011 [40]
354
RDS
Nanchang
Developing
4.2
7.9

Chen, 2010 [3]
469
Snow ball
Nanning
Developing
1.7
10.7

Bao, 2009 [11]
6101
RDS
14 cities
Classifieda
6.3
14.0

Chen, 2012 [16]
300
Snow ball
Yangzhou
Developed
7.3
22.0

Li, 2009 [34]
1773
Multiple methods
Chongqing
Developing
10.6
8.4

Guo, 2009 [27]
204
Venues-based
Tianjin
Developed
5.9
18.7

Liu, 2012 [90]
507
Snow ball
Changsha
Developed
4.3
25.1

Qu, 2011 [91]
805
Snow ball
2 cities
Developed
3.7
14.1

Chen, 2011 [12]
831
VCT
Kunming
Developing
11.4
13.6

Zhou, 2011 [83]
1166
Snow ball
Chongqing
Developing
14.8
8.7

Han, 2012 [92]
272
Venues-based
Taiyuan
Developing
8.5
13.6

Tang, 2011 [93]
408
Venues-based
Guilin
Developing
2.5
4.9

Xu, 2011 [69]
436
Venues-based
Liaoning
Dropped outb
3.0
5.0

Bai et al., 2011 [94]
280
Snow ball
Suzhou
Developed
7.1
15.0

Zhou, 2011 [95]
491
RDS
Chongqing
Developing
14.9
5.1

Fan, 2012 [47]
500
RDS
Beijing
Developed
8.0
22.0

Liao et al., 2011 [96]
2996
Multiple methods
Shandong
Developed
2.5
5.5

Feng et al., 2009 [97]
2044
Venues-based
Chongqing
Developing
11.5
8.9

He, 2009 [29]
423
RDS
Guangzhou
Developed
1.3
14.8

Eric, 2011 [98]
288
Snow ball
Yuxi
Developing
10.8

Zheng, 2012 [81]
157
Multiple methods
Beijing
Developed
2.5
7.0

Wei, 2011 [63]
220
Snow ball
Taizhou
Developing
13.4
14.5

Zhong et al., 2011 [99]
379
RDS
Guangzhou
Developed
5.2
17.5

Zhang, 2012 [74]
503
RDS
Chongqing
Developing
15.7
6.6

Xiao, 2009 [66]
1692
Multiple methods
Chongqing
Developing
10.8
8.6

Xiao, 2010 [67]
4983
Multiple methods
20 cities
Dropped outb
2.9
9.8

Zhang et al., 2011 [100]
302
Snow ball
Beijing
Developed
9.9
19.2

Zhang et al., 2012 [101]
3314
Snow ball
Chongqing
Developing
14.2
9.4

Zhang, 2013 [75]
463
Snow ball
Harbin
Developing
9.5
14.3

Guo et al., 2009 [102]
433
Venues-based
2 cities
Developed
5.8
27.7

Ruan et al., 2009 [103]
541
Multiple methods
Beijing
Developed
4.8
19.8

Zou et al., 2010 [104]
429
Internet
2 cities
Classifieda
4.8
11.4

Wang, 2011 [105]
2020
Surveillance
4 cities
Developing
2.3

Gao, 2012 [106]
962
Multiple methods
Beijing
Developed
6.3
17.7

Zhou et al., 2010 [107]
550
Multiple methods
Beijing
Developed
4.5

Zhou, 2012 [108]
294
VCT
Shanghai
Developed
6.1
9.5

Ouyang, 2009 [44]
617
RDS
Chongqing
Developing
16.8
10.9

Meng, 2010 [42]
287
Multiple methods
Changde
Developing
3.5
12.9

Tang, 2012 [52]
303
Multiple methods
Dazhou
Developing
3.6
1.7

Sun, 2012 [49]
2006
Multiple methods
Dalian
Developed
5.2
16.6

Dai, 2011 [109]
1315
VCT
Guangzhou
Developed
5.4
6.8

Mou, 2012 [110]
1526
Venues-based
Guangzhou
Developed
5.7

Wen, 2010 [64]
452
Snow ball
Guangzhou
Developed
4.9
6.0

Wang, 2011 [111]
300
RDS
Kunshan
Developed
5.3
25.0

Sun, 2010 [112]
1350
RDS
2 cities
Developing
5.2
7.3

Zhu, 2011 [88]
259
Surveillance
Wuxi
Developed
13.9
25.1

Zhang, 2009 [76]
231
RDS
Urumqi
Developing
2.2
10.8

Chen, 2011 [113]
889
Snow ball
Lanzhou
Developing
6.0
13.6

Hong et al., 2009 [114]
593
Venues-based
Changzhou
Developed
13.7
31.2

Liu, 2012 [37]
661
Snow ball
Nanjing
Developed
3.9
11.5

He, 2012 [115]
235
Multiple methods
Geermu
Developing
4.3
0.9

Gong, 2010 [24]
252
Snow ball
Quanzhou
Developing
2.6
2.2

Zhang, 2012 [77]
300
RDS
Shenzhen
Developed
7.0
12.0

Pan, 2012 [45]
675
Multiple methods
Shenzhen
Developed
8.0
41.2

Shi, 2010 [116]
906
Venues-based
Shenzhen
Developed
4.2
14.5

Cai, 2012 [117]
5232
VCT
Shenzhen
Developed
6.5
21.0

Wang, 2010 [55]
900
RDS
Shenyang
Developed
9.3
11.0

Wang, 2011 [118]
450
Venues-based
Shijiazhuan
Developing
2.2
7.6

Wang, 2010 [61]
150
Snow ball
Shijiazhuan
Developing
6.7
11.3

Bai et al., 2011 [119]
280
Multiple methods
Suzhou
Developed
7.3
22.0

Zhang et al., 2011 [73]
717
Multiple methods
Suzhou
Developed
8.1
14.6

Xu et al., 2012 [70]
211
Multiple methods
Taizhou
Developing
10.0
11.8

Wang et al., 2011 [57]
201
Snow ball
Urumqi
Developing
6.5
7.0

Liu et al., 2010 [38]
456
RDS
Wuhan
Developed
6.6
21.9

Zhang et al., 2011 [80]
404
Snow ball
Xining
Developing
7.2
8.4

Wang et al., 2010 [62]
750
Multiple methods
Yangzhou
Developed
9.3
22.8

Chen et al., 2012 [14]
218
Snow ball
Chongqing
Developing
16.5
15.1

Yang et al., 2011 [71]
305
Multiple methods
Dali
Developing
3.0
2.0

Luo et al., 2012 [41]
1237
Snow ball
13 cities
Developing
8.2
3.9

Xu, 2010 [68]
1864
Multiple methods
4 cities
Classifieda
6.7

Ding et al., 2010 [19]
743
Snow ball
Chongqing
Developing
16.6
8.5

Ding et al., 2010 [20]
202
Snow ball
Chongqing
Developing
12.9
5.0

Li, 2009 [34]
1691
Multiple methods
Chongqing
Developing
10.9
8.6

Feng, 2010 [22]
946
Snow ball
Chongqing
Developing
15.8

Guo et al., 2012 [25]
109
Surveillance
Zunyi
Developing
10.1
1.0

Study sites were classified into different economy status when subgroup analysis was conducted; bStudy was dropped out then subgroup analysis was conducted.

Four and two studies were further excluded because of the absence of specific study cities in the subgroup analyses of HIV and syphilis prevalence by different economic status, respectively. The prevalence of HIV infection was slightly higher in developing cities (7.5%) than in developed cities (6.1%), whereas the prevalence of syphilis was significantly lower in developing cities (8.6%) than in developed cities (15.1%). Studies with a sample size smaller than 500 had a lower prevalence of HIV and syphilis infection than those with a sample size greater than 500 (5.9% versus 7.2%, 11.0% versus 11.5%, resp.) (Table 2).

Although the published year and sampling methods did not contribute to between-study variance, we also conducted subgroup analyses based on them. Although we only divided the published year into two groups, an uptrend of HIV infection and a decrease in syphilis infection were still observed (Table 2).

4. Discussion

This is an updated meta-analysis that presents the most current prevalence of HIV and syphilis infection in MSM in China. In order to obtain the prevalence from developing and developed cities, we also carried out a subgroup analysis by different economic status according to meta-regression. To our knowledge, this is the first study to compare the prevalence of HIV and syphilis infection between developing and developed cities in China. A national study survey of 61 cities by Wu reported the prevalence of HIV in MSM from the southwest, east, south, and northeast of China but did not account for the different economic conditions of each city [6].

Overall, eighty-four articles published between January 1, 2009, and April 11, 2013 were included in this review. It was observed that the prevalence of HIV and syphilis infection among MSM in China was 6.5% (95% CI 5.6% to 7.4%) and 11.2% (95% CI 10.0% to 12.6%), respectively, which was lower compared to other countries and cities. For instance, the prevalence of HIV among MSM was 14.2% in Brazil, 10.6% in Kenya, 21.5% in Senegal, 9.0% in Indonesia, 14.7% in India, and 24.6% in Thailand [120–123].

In spite of the relatively lower prevalence, there was evidence for the uptrend of HIV and syphilis infection among MSM in China. A meta-analysis of Chow reported that HIV infection among MSM has increased over the past years, from 1.4% (95% CI 0.8%–2.4%) during 2001–2003, to 2.3% (95% CI 2.0%–2.6%) during 2004–2006, and to 5.3% (95% CI 4.8%–5.8%) during 2007–2009 [8]. Results from our study indicate that the prevalence of HIV among MSM is still increasing. The expanding epidemic may be associated with the special role of MSM in China. Homosexuality is still not widely accepted by the general population. Therefore, marriage between MSM and women remains common, nn which case MSM might act as a bridge for HIV transmission to other MSM and the general population. It was reported that the prevalence of bisexual behavior among MSM in China was as high as 31.2% [124].

The subgroup analyses showed that the prevalence of HIV infection was 7.5% from developing cities and 6.1% from developed cities, whereas the prevalence of syphilis was 8.6% from developing cities and 15.1% from developed cities. The exact reasons for this finding are unclear, but one possible reason is that syphilis is a curable disease and several large scale public health programs were conducted in several developing cities in the past few years [74].

Several limitations of our analyses must be kept in mind. First, substantial heterogeneity was observed in our analysis. We found that study site, sample size, and sampling methods contributed to the heterogeneities. These factors may also have contributed to the increasing trend of HIV and syphilis infection in MSM in China. A meta-analysis of Chow reported that articles published in English were more likely to present high prevalence than Chinese articles, which may have resulted in between-study variance. The presence of publication bias was also a considerable limitation in our analysis (Figure 4). With the strict inclusion criteria, we excluded studies with a sample size smaller than 150 and those with only one testing method to diagnose syphilis. There are also a large number of unpublished articles (e.g., government documents) and studies that reported relatively low prevalence. Third, there were few studies from rural areas, which may have led to an overestimation of HIV and syphilis prevalence. More studies of rural MSM studies are needed in the future. Fourth, several studies that did not specify the city location were excluded from the subgroup analysis, which may have increased the possibility of publication bias. Fifth, the economic classification of the cities was only based on the per capita GDP; results may only partially reflect the true economic status of the city.

Figure 4: Begg’s funnel plot showing the potential publication bias.

Despite the limitations listed above, our meta-analyses employed a strict inclusion criteria and valid search strategy in order to provide an objective, authentic, and current estimate of HIV and syphilis prevalence among MSM in China, with a large aggregate sample size of 75036. We also conducted a subgroup analysis to present the different prevalence rates of HIV and syphilis infection in developing and developed cities.

In conclusion, HIV and syphilis are prevalent among MSM in China; HIV prevalence is higher in developing cities than in developed cities, while the situation of syphilis is just the opposite. These results urgently indicate the need for strategies aimed at prevention, surveillance, and treatment. Moreover, corresponding policies should be drawn up by the local government on the basis of local economic status.

Conflict of Interests

There are no conflict of interests.

Acknowledgments

This work was supported by the National Nature Science Foundation of China no. 81273188 and the National Mega Projects on Key Infectious Disease Control of China Ministry of Science and Technology no. 2012ZX10004-904. The autors thank Zongda Jin, Wei Li, and Guochong Chen for their assistance with the literature search and Stephen Pan for the English editing. The authors are also grateful to Jiachen Shi and Yin Fu for data extracting and checking and all the authors of the original studies included in our analysis.

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