Figures
Abstract
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.
Citation: McLaughlin MM, Chow EPF, Wang C, Yang L-G, Yang B, Huang JZ, et al. (2013) Sexually Transmitted Infections among Heterosexual Male Clients of Female Sex Workers in China: A Systematic Review and Meta-Analysis. PLoS ONE 8(8): e71394. https://doi.org/10.1371/journal.pone.0071394
Editor: Sten H. Vermund, Vanderbilt University, United States of America
Received: June 22, 2012; Accepted: June 29, 2013; Published: August 12, 2013
Copyright: © 2013 McLaughlin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Support for this research came from an National Institutes of Health (NIH) Fogarty K01 Award (US NIH 1K01TW008200-270 01A1), the UNC Fogarty AIDS International Research and Training Program (NIH FIC D43 TW01039), the UNC Social Science Research on HIV/AIDS in China (NIH NICHD R24 HD056670-01), the UNC Center for AIDS Research, and the Harvard Institute for Global Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
China has a history of both large epidemics of sexually transmitted infections (STIs) and comprehensive population-based responses. In the 1950s, the Chinese government launched a massive campaign to eliminate STIs through screening, free penicillin, and suppression of the commercial sex industry [1], [2]. Although there were limited epidemiological investigations, by the 1960s STIs were thought to be extremely uncommon [2]. In the wake of extensive economic and social change since the 1980s, both commercial sex and STIs have experienced a marked resurgence in China [3]. The rising prevalence of syphilis and other STIs in the general population in China suggests the potential for the HIV epidemic in China to accelerate through sexual transmission [3]–[9]. Heterosexual transmission has emerged in recent years as the primary mode of HIV transmission in China, accounting for 62.6% of estimated new infections in 2009, compared to 11.3% prior to 2006 [10]–[12].
Subgroups of heterosexual men in China are likely at an increased risk for STIs and HIV infection. One male heterosexual risk group in China that has attracted concern is “mobile men with money”–wealthy businessmen and officials who purchase unprotected sex [13]. Another male heterosexual group believed to be at increased risk of STIs are “surplus men”–an increasing population of young, poor, unmarried men, resulting from China’s imbalanced sex ratio [14]. This group of men may be unable to afford a bride price but able to pay the price of a low-fee sex worker [14]. Understanding these and other subgroups of heterosexual Chinese men who purchase sex is important for designing effective STI/HIV prevention strategies. China’s national median prevalence of commercial sex purchased by men is 4.2% (95% confidence interval [CI], 3.5%–5.2%), exceeding the median prevalence of 2.4% among 55 other countries [15]. The existence of both a significant amount of data on the health and behavior of male clients and population-based data on STI prevalence makes China a uniquely appropriate place to study the STI/HIV risk of clients.
Despite the theoretical STI risk of heterosexual male clients of female sex workers (FSW), there are reasons why clients in China may not have high STI prevalence. Although the higher prevalence of STIs among FSW in China compared with the general population has already been well described [11], [16]–[18], clients often report higher rates of condom use with commercial sex partners compared with wives or other stable partners [10], [19]–[23]. Clients may also seek formal STI care more promptly than men who do not purchase sex [24]–[26]. Thus, research is needed to better understand the sexual risk and prevalence of STIs among clients.
Compared to the literature on FSW, relatively few published studies to date have examined heterosexual male clients of FSW in China [27]. Clients are a heterogeneous and sometimes transient group, making it difficult to sample from the population and produce generalizable findings. Additionally, in a setting where commercial sex work is punished and highly stigmatized [28], clients can be difficult to reach and hesitant to participate in surveys.
We abstracted cross-sectional prevalence data, recruitment methods, and other information on heterosexual men who purchase sex from FSW. The purpose of this study is to systematically assess the prevalence of HIV, syphilis, gonorrhea, and chlamydia among heterosexual male clients of FSW in China.
Methods
Search Strategy
Studies investigating the prevalence of STIs among heterosexual male clients of FSW were identified by searching for articles in the PubMed, Embase, China National Knowledge Infrastructure (CNKI), Wanfang Data, and CQVIP databases. CNKI, Wanfang Data, and CQVIP are China’s three major online bibliographic databases for searching Chinese-language biomedical journals. Combinations of terms for China, STIs, sex work, and sex workers were used to screen for potentially relevant studies (see Text S1). Chinese search terms incorporated the variety of local expressions for sex workers reported in the public health and social science literature [29]. Articles from all years were eligible for inclusion. All database searches were updated through December 31, 2012.
Following PRISMA guidelines, the list of publications obtained through this initial search was narrowed to studies relevant to our analysis (see Table S1) [30]. Studies that reported the quantitative prevalence of biomarkers of HIV, syphilis, gonorrhea, or chlamydia among male clients in mainland China or Hong Kong were included. Because the English and Chinese search terms did not limit the initial search to clients, the first round of exclusion based on article titles eliminated a large number of publications on the subject of female sex workers that did not report on heterosexual male clients. Male clients were defined as men who had ever purchased sex from a female sex worker in their lifetime. Although men who sell sex to men are also an important HIV risk group, this review included only studies of heterosexual male clients of FSW (referred to hereafter as “clients”). Reviews, intervention studies, modeling studies, and studies lacking sufficient details on methods were excluded. Studies were included if the sample consisted entirely of clients or if the sample was a more general group of men (e.g., miners or patients at STI clinics) but the reported STI prevalence was disaggregated by whether the men reported having purchased sex.
Data Extraction and Analysis
For all studies, two study authors (MMM and CW) independently extracted the following data: study location (province and city), population sampled, recruitment methods, total sample size, number of clients in the sample, years of data collection, age, income, marital status, definition of client, biomarkers examined, and prevalence of HIV, syphilis, gonorrhea, and chlamydia. The four STIs were defined according to national laboratory standards for diagnosis [31].
Publication bias was examined by visually inspecting funnel plots for asymmetry; for each STI a plot of the prevalence (x-axis) and the sample size (y-axis) was examined [32]. The Begg and Mazumdar rank correlation was also used to evaluate publication bias (p-value <0.05 represents significant publication bias) [33]. Heterogeneity across studies was estimated by calculating I2, an index of the variation across studies that is due to heterogeneity as opposed to chance [34]. The studies were also categorized by population sampled (detainees vs. other), sampling strategy (convenience sample vs. other), region (southwest vs. other), and study period (2000–3, 2004–6, 2007–9, 2010–12), and these categories were examined for differences in the I2 statistic. Study locations were categorized based on official domestically used designations [35]. Detainees refer to men arrested for purchasing sex and detained in jail or detention facilities known as reeducation centers, where they may be tested for HIV and other STIs [28].
Random effect models were used to calculate the pooled prevalence estimates and 95% confidence intervals (CI) for HIV, syphilis, gonorrhea, and chlamydia. The pooled prevalence estimates were also calculated by population sampled, sampling strategy, location, and study period, and the chi-squared based Cochrane Q-test was used to compare the pooled prevalence estimates between subgroups. Odds ratios and 95% CI were calculated for the STI prevalence estimates to compare the risk of infection between clients and the general adult population in China. Comprehensive Meta-Analysis Version 2 (Biostat, Englewood, NJ) was used for all analyses.
Results
2376 publications were obtained through the literature search, of which 37 met the inclusion criteria (Figure 1). There were large differences in the prevalence of HIV, syphilis, gonorrhea, and chlamydia reported by the studies (Table 1).
The median number of clients included in the studies was 450 (interquartile range [IQR], 186–2033). The total sample size of clients for all 37 studies was 26,552. Among studies reporting median age or age distributions, the majority of clients sampled were between 25 years old and 45 years old, except for six studies reporting a higher proportion of clients over 45 years of age [36]–[41]. Among studies reporting marital status, the majority of clients were married or living with their regular partner; the proportion exceeded 50% in all studies except four [42]–[45] and exceeded 75% in eight studies. Only six studies reported the income levels of the clients sampled. Three studies reported a median annual income between 1300–2000 US$ [42], [45], [46]. In the other three studies, 40% of participants earned less than 1700 US$ per year [47], 65% earned less than 2900 US$ per year [43], and 33% earned less than 800 US$ per year [48].
Six studies were undertaken in south central China [45], [49]–[53], eleven in the southwest [12], [38], [42], [44], [46]–[48], [53]–[56], eleven in the east [36], [37], [39], [41], [57]–[63], and seven in the north [64]–[70]. Two studies were national [4] or multi-city samples [71]. There were no studies from northwestern or northeastern regions in China. Most studies used convenience sampling, but three studies used snowball sampling with female sex worker or client-client referrals [42], [47], [48], and one used stratified probability sampling [4]. Twenty-four studies sampled detainees [12], [36], [37], [39], [41], [49]–[52], [54], [57]–[70], but other studies sampled miners [46], clients at commercial sex venues [38], [41]–[43], [45], [47], [48], [56], [71], STI clinic attendees [38], [41], [47], [53], [55], [71], or the general population [4]. Four studies defined clients as men who reported purchasing sex in the previous year [4], [47], [48], [55]. Other studies defined clients as men who reported purchasing sex in the previous three months [43] or “recently” [71]. Two studies included only men who sought sex at a commercial sex venue at the time they were recruited [45], [56]. The remaining studies defined clients as men who reported ever purchasing sex [44], [46], [53] or did not specify the time period when sex was purchased.
The Begg and Mazumdar rank correlation test indicated that there was no publication bias among the studies reporting HIV (p = 0.353), syphilis (p = 0.331), gonorrhea (p = 0.139), or chlamydia (p = 0.322) prevalence. Visual inspection of the funnel plots also revealed no significant publication bias among the studies. There was no recognizable association observed between study size and reported prevalence. The prevalence of each STI was heterogeneous between studies, with an I2 statistic greater than 80 for gonorrhea and greater than 90 for HIV, syphilis, and chlamydia.
There was no significant change in the I2 statistic when the studies reporting syphilis prevalence were subdivided by study location, population sampled, or sampling method (Table 2). Among the studies reporting HIV prevalence, studies in southwest China showed greater heterogeneity than those undertaken in other regions (95.8 vs. 62.9), and studies of detainees showed less heterogeneity than those studying other populations of clients (60.3 vs. 94.2). There was no significant change in the I2 statistic when the studies reporting HIV prevalence were subdivided by sampling method (Table 3). For both HIV and syphilis, studies conducted between 2007 and 2012 had high heterogeneity (>65) whereas those conducted prior to 2007 had no significant heterogeneity. Forest plots of the prevalence of HIV, syphilis, gonorrhea, and chlamydia among clients of FSW are presented in the (see Figures S1 to S4 in File S1).
Among the 31 studies reporting HIV prevalence, the pooled estimate of HIV prevalence among clients was 0.68% (95% CI 0.36–1.28%) (Table 2). The HIV prevalence estimate among southwestern studies was higher than the HIV prevalence estimate among studies undertaken in other regions (2.54% vs. 0.24% p = 0.001). The estimated HIV prevalence among studies that used convenience sampling was significantly lower compared to those that used other sampling methodologies (0.50% vs. 4.56%, p<0.01). The estimated prevalence among studies that sampled detainees was lower than among studies that sampled other subgroups of clients (miners, STI clinic attendees, men at commercial sex work venues, or the general population) (0.30% vs. 2.00%, p<0.01). Among studies reporting data for one or two year intervals, there was a non-significant increase in HIV prevalence in later years (0.23% in 2000–3, 0.30% in 2004–6, 0.39% in 2007–9, 0.81% in 2010–12, p = 0.812). Clients were found to have 11.80 (95% CI 10.03–13.88) times greater odds of being infected with HIV than the general Chinese population (Table 4).
Among the 31 studies reporting syphilis prevalence, the pooled estimate of syphilis prevalence among clients was 2.91% (95% CI 2.17–3.89%) (Table 3). The syphilis prevalence estimate did not differ significantly by region, sampling methodology, or population sampled. Among studies reporting data for one or two year intervals, there was a significant increase in syphilis prevalence in later years (0.28% in 2000–3, 0.30% in 2004–6, 1.13% in 2007–9, 8.79% in 2010–12, p<0.01). Clients were found to have 5.73 (95% CI 4.59–7.16) times higher odds of having syphilis infection compared to the general Chinese population (Table 4).
Among the 14 studies reporting gonorrhea prevalence, the pooled estimate of gonorrhea prevalence among clients was 2.16% (95% CI 1.46–3.17%). Among the eight studies reporting chlamydia prevalence, the pooled estimate of chlamydia prevalence was 8.01% (95% CI 4.94–12.72%). Subgroup analyses were not performed for gonorrhea and chlamydia because the number of studies was insufficient. Compared to the general Chinese population, clients were found to have 44.10 (95% CI 9.79–198.64) and 2.56 (95% CI 2.04–3.21) times greater odds of being infected with gonorrhea and chlamydia, respectively.
Discussion
While there have been a number of studies examining subsets of high-risk men, there have been few studies that systematically investigate clients of FSW. To our knowledge, this is the first systematic review of STI prevalence among heterosexual male clients of FSW in China. Our review revealed considerable variation in STI prevalence reported among clients in China, as well as substantial variation in sampling strategies used.
The pooled estimates of HIV, syphilis, gonorrhea, and chlamydia prevalence among male clients of FSW in this review exceed the prevalences previously reported in population-representative samples, large samples of low-risk groups, and national estimates in China. The prevalence of HIV in China is currently estimated to be 0.06%, corresponding to 11.8 times lower odds of HIV infection than clients in this review [11]. A large study of couples receiving compulsory premarital examinations found a low prevalence of syphilis across various study sites in China (0.33% to 0.71%) [72]. In comparison, clients in this review were found to have 5.7 times higher odds of being infected with syphilis. In their national stratified probability sample of Chinese individuals ages 20 to 64 years, Parish and colleagues found that among men, the prevalence of gonorrhea was 0.02% (95% CI 0.005–0.1%) and the prevalence of chlamydial infection was 2.1% (95% CI 1.3–3.3%) [48]. Clients in this review had 44.1 times and 2.7 times higher odds of being infected with gonorrhea and chlamydia, respectively.
The prevalence of STIs among clients in this review is lower than the prevalence among other at-risk groups in China reported in systematic reviews. The prevalence of HIV among FSWs in China is estimated to be 0.6%–3.0% [73], [74], compared to 0.68% among clients in our review. And the prevalence of syphilis, gonorrhea, and chlamydia among Chinese FSWs is estimated to be 5.0–6.9% [74], [75], 16.4% [74], and 25.7% [74], respectively, compared to 2.91%, 2.16%, and 8.01% among clients in our review. Among Chinese men who have sex with men, HIV prevalence is estimated to be 5.3% [76] and syphilis, 13.5% [77], compared to 0.68% and 2.91% among clients in our review. However, heterogeneity across studies and sampling limitations prevent definitive conclusions about how the prevalence of STIs in this population compares to the general population and other at-risk groups.
Most of the studies included in this systematic review used a convenience sample of detainees at jails or reeducation centers. The prevalence of HIV was lower among detainees compared to other populations. This trend is the opposite of what has been found among FSW in China. Systematic reviews have shown that incarcerated FSW have a higher prevalence of syphilis compared to FSW who have been sampled at entertainment centers, beauty salons, and other places of work [5], [28]. Moreover, the trend toward lower HIV infection among clients who have been detained is surprising given the literature on incarceration as a risk factor for STIs [78]–[85]. However, male client detainees in China differ from typical incarcerated populations in a crucial way–they are detained specifically for purchasing sex. In other contexts where prisoners have been detained for a variety of offenses, the reason for incarceration may affect the association between incarceration and STIs. Income and other variables may confound these relationships, but the high degree of heterogeneity among the studies in terms of both STI prevalence and reported demographic characteristics precluded a meta-analysis of income or other predictors. Additionally, a number of the studies that did not examine detainees sampled clients seeking care at STI clinics, a population that would be expected to have a higher prevalence of STIs, and this may in part explain the difference in HIV prevalence found between detainees and other subgroups.
Accurately sampling clients is challenging. Male clients of FSW comprise a heterogeneous group, representing men of varying income, education, and occupational categories [15], [86]. Men who frequently purchase commercial sex may be oversampled in studies of clients, which could lead to an overestimation of STI prevalence in the male client population. Stigmatization of commercial sex work and detention of clients during crackdown campaigns further complicates sampling and outreach programs. Similar problems identifying clients and enrolling them in research studies have been reported in other contexts [87], [88], [89]. Moreover, the definition of client that Chinese police have used for arrests has evolved over time, so the meaning of detainee is likely to be somewhat inconsistent across different time periods.
The heterogeneity in the populations sampled and the prevalence of STIs reported across the studies reviewed represents a limitation of the present review and underscores the challenge of sampling clients. This variation across studies also highlights a limitation of systematic review research, as the findings can vary based on the databases and search terms selected. The high degree of heterogeneity also limited our ability to evaluate publication bias, and it is possible that publication bias may have been unidentified. Another limitation was the inclusion of a number of studies of men detained for purchasing sex. Although according to national policies detainees give informed consent for routine health exams that include STI/HIV testing [90], many of the studies did not provide sufficient detail to allow us to evaluate the consent process. Our comparison of the prevalence of STIs among clients versus the general population is limited because a number of client studies sampled men attending STI clinics, who would be expected to have a higher risk of STI infection. Additionally, the data on chlamydia and gonorrhea prevalence in the general population is more than ten years old, so we assumed that these two epidemics have been stable in recent years. Finally, differences among the studies in terms of the definition of male client also limit the findings of this review. Most studies defined a male client as a man who reported ever purchasing sex, and some studies did not specify the definition of client. Future studies examining the prevalence of STIs among clients should consider reporting STI prevalence by frequency of purchasing sex and type of sex worker or commercial sex venue frequented.
This study highlights the need for further community-based sampling strategies among male clients. Differences in the reported prevalence of HIV and syphilis by sampling strategy and population sampled suggest the limitations of convenience sampling. In comparison, population-based probability sampling, used by Parish and colleagues [4], is a more rigorous sampling methodology. Despite its limitations for sampling purposes, detention offers an opportunity for intervention for this hard-to-reach population. Every country will have its own unique policy, but in China, where a large number of men are detained for purchasing sex, detention is an occasion when clients could receive routine STI screening and services.
Much of the HIV and STI prevention agenda has focused on women and men who have sex with men, both in China and worldwide. Heterosexual men–including male clients of FSW– are often left out of this agenda. Whereas female sex workers have been the target of numerous STI prevention strategies in China [91], their clients have attracted considerably less public health attention and prevention resources. The higher pooled estimates of HIV, syphilis, gonorrhea, and chlamydia prevalence among clients in this review, compared to the prevalence estimates previously reported for the general population in China, suggest that greater attention to the sexual risk of male clients of female sex workers may be needed. However, the prevalence of STIs in this population is poorly appreciated using conventional study designs, and additional research is needed to characterize their sexual risk and STI prevalence.
Supporting Information
Table S1.
PRISMA checklist for systematic reviews and meta-analyses.
https://doi.org/10.1371/journal.pone.0071394.s001
(PDF)
Text S1.
English and Chinese search terms used for the systematic review.
https://doi.org/10.1371/journal.pone.0071394.s002
(PDF)
File S1.
Forest plots for HIV, syphilis, gonorrhea, and chlamydia. Forest plots showing unadjusted estimates (squares) with 95% confidence intervals (bars) for HIV (Figure S1), syphilis (Figure S2), gonorrhea (Figure S3), and chlamydia (Figure S4) among male clients of female sex workers in China. The pooled prevalence estimate is represented as a red diamond.
https://doi.org/10.1371/journal.pone.0071394.s003
(PDF)
Acknowledgments
We thank Huang Yingying for her helpful comments in the preparation of this manuscript. We thank Liu Fengying and Hong Xuan for their help with the database searches.
Author Contributions
Conceived and designed the experiments: MMM JDT. Performed the experiments: MMM CW EPFC YW JDT. Analyzed the data: MMM CW EPFC LZ JDT. Contributed reagents/materials/analysis tools: CW EPFC. Wrote the paper: MMM EPFC CW LY BY JZH YW LZ JDT.
References
- 1.
Cohen MS, Henderson GE, Aiello P, Zheng H (1996) Successful eradication of sexually transmitted diseases in the People’s Republic of China: implications for the 21st century. J Infect Dis (Suppl 2): S223–229.
- 2. Cohen MS, Ping G, Fox K, Henderson GE (2000) Sexually transmitted diseases in the People’s Republic of China in Y2K: back to the future. Sex Transm Dis 27(3): 143–145.
- 3. Chen ZQ, Zhang GC, Gong XD, Lin C, Gao X, et al. (2007) Syphilis in China: results of a national surveillance programme. Lancet 369(9556): 132–138.
- 4. Parish WL, Laumann EO, Cohen MS, Pan S, Zheng H, et al. (2003) Population-based study of chlamydial infection in China: a hidden epidemic. JAMA 289(10): 1265–1273.
- 5. Lin CC, Gao X, Chen XS, Chen Q, Cohen MS (2006) China’s syphilis epidemic: a systematic review of seroprevalence studies. Sex Transm Dis 33(12): 726–736.
- 6. Chen XS, Yin YP, Tucker JD, Gao X, Cheng F, et al. (2007) Detection of Acute and Established HIV Infections in Sexually Transmitted Disease Clinics in Guangxi, China: Implications for Screening and Prevention of HIV Infection. J Infect Dis 196(11): 1654–1661.
- 7. Cheng JQ, Zhou H, Hong FC, Zhang D, Zhang YJ, et al. (2007) Syphilis screening and intervention in 500,000 pregnant women in Shenzhen, the People’s Republic of China. Sex Transm Infect 83(5): 347–350.
- 8. Wong SP, Yin YP, Gao X, Wei WH, Shi MQ, et al. (2007) Risk of syphilis in STI clinic patients: a cross-sectional study of 11,500 cases in Guangxi, China. Sex Transm Infect 83(5): 351–356.
- 9. Chen XS, Gong XD, Liang GJ, Zhang GC (2000) Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 27(3): 138–142.
- 10. Yang H, Li X, Stanton B, Liu H, Liu H, et al. (2005) Heterosexual transmission of HIV in China: a systematic review of behavioral studies in the past two decades. Sex Transm Dis 32(5): 270–280.
- 11.
Ministry of Health of the People’s Republic of China (2012) 2012 China AIDS Response Progress Report. Beijing, China: Ministry of Health. Available: http://www.unaids.org/en/dataanalysis/knowyourresponse/countryprogressreports/2012countries/ce_CN_Narrative_Report[1].pdf. Accessed 2013 February 26.
- 12.
Jia M, Luo H, Ma Y, Wang N, Smith K, et al.. (2010) The HIV epidemic in Yunnan Province, China, 1989–2007. J Acquir Immune Defic Syndr (Suppl 1): S34–40.
- 13. Uretsky E (2008) ‘Mobile men with money’: the socio-cultural and politico-economic context of ‘high-risk’ behaviour among wealthy businessmen and government officials in urban China. Cult Health Sex 10(8): 801–814.
- 14. Tucker JD, Henderson GE, Wang TF, Huang YY, Parish W, et al. (2005) Surplus men, sex work, and the spread of HIV in China. AIDS 19(6): 539–547.
- 15.
Pan S, Parish WL, Huang Y (2011) Clients of female sex workers: a population-based survey of China. J Infect Dis (Suppl 5): S1211–1217.
- 16. Chen XS, Yin YP, Liang GJ, Gong XD, Li HS, et al. (2005) Sexually transmitted infections among female sex workers in Yunnan, China. AIDS Patient Care STDS 19(12): 853–860.
- 17. van den Hoek A, Yuliang F, Dukers NH, Zhiheng C, Jiangting F, et al. (2001) High prevalence of syphilis and other sexually transmitted diseases among sex workers in China: potential for fast spread of HIV. AIDS 15(6): 753–759.
- 18. Ruan Y, Cao X, Qian HZ, Zhang L, Qin G, et al. (2006) Syphilis among female sex workers in southwestern China: potential for HIV transmission. Sex Transm Dis 33(12): 719–723.
- 19. Yang C, Latkin C, Luan R, Nelson K (2010) Condom use with female sex workers among male clients in Sichuan Province, China: the role of interpersonal and venue-level factors. J Urban Health 87(2): 292–303.
- 20. Xu JJ, Wang N, Lu L, Pu Y, Zhang GL, et al. (2008) HIV and STIs in clients and female sex workers in mining regions of Gejiu City, China. Sex Transm Dis 35(6): 558–565.
- 21. Zhao R, Wang B, Fang X, Li X, Stanton B (2008) Condom use and self-efficacy among female sex workers with steady partners in China. AIDS Care 20(7): 782–790.
- 22. Tunthanathip P, Lolekha R, Bollen LJ, Chaovavanich A, Siangphoe U, et al. (2009) Indicators for sexual HIV transmission risk among people in Thailand attending HIV care: the importance of positive prevention. Sex Transm Infect 85(1): 36–41.
- 23.
Cai Y, Shi R, Shen T, Pei B, Jiang X, et al.. (2010) A study of HIV/AIDS related knowledge, attitude and behaviors among female sex workers in Shanghai China. BMC Public Health 10377.
- 24. Morris CN, Ferguson AG (2007) Sexual and treatment-seeking behaviour for sexually transmitted infection in long-distance transport workers of East Africa. Sex Transm Infect 83(3): 242–245.
- 25. Lau JT, Wong WS (2002) HIV antibody testing among male commercial sex networkers, men who have sex with men and the lower-risk male general population in Hong Kong. AIDS Care 14(1): 55–61.
- 26. Wang B, Li X, Stanton B, Fang X, Lin D, et al. (2007) HIV-related risk behaviors and history of sexually transmitted diseases among male migrants who patronize commercial sex in China. Sex Transm Dis 34(1): 1–8.
- 27. Yang C, Latkin C, Luan R, Nelson K (2010) Peer norms and consistent condom use with female sex workers among male clients in Sichuan province, China. Soc Sci Med 71(4): 832–839.
- 28. Tucker J, Ren X, Sapio F (2010) Incarcerated sex workers and HIV prevention in China: social suffering and social justice countermeasures. Soc Sci Med 70(1): 121–129.
- 29. Huang Y, Henderson GE, Pan S, Cohen MS (2004) HIV/AIDS risk among brothel-based female sex workers in China: assessing the terms, content, and knowledge of sex work. Sex Transm Dis 31(11): 695–700.
- 30.
Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339b2535.
- 31.
Chinese National Centers for Disease Control and Prevention (2006) Operational Standards and Laboratory Testing Methods for STDs. Nanjing: Chinese National CDC, National STD Control Center.
- 32. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109): 629–634.
- 33.
Thornton A, Lee P (2000) Publication bias in meta-analysis: its causes and consequences. J Clin Epidemiol 53207–216.
- 34. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414): 557–560.
- 35.
Lin C, Hendrischke H (2002) The Territories of the People’s Republic of China. London: Europa Publications.
- 36.
Zhang Y, Wu RH (2007) Shanghai di qu mai yin piao ke ren yuan xing bing fa bing qing kuang diao cha yu fen xi [Survey and analysis of the outbreak situation of sexually transmitted infections among prostitutes and clients in Shanghai]. Jian Yan Yi Xue [Laboratory Medicine] 22(3).
- 37. Hua YZ (2006) 832 ming mai yin piao chang ren yuan mei du gan ran qing kuang fen xi [Analysis of the syphilis infection situation among 832 prostitutes and clients]. Jiangsu Wei Sheng Bao Jian [Jiangsu Health Care] 8(5): 12.
- 38.
Feng L, Liu L, Lai WH, Huang J, Hu Y, et al.. (2010) 2008–2009 nian Sichuan sheng piao ke ai zi bing shao dian jian ce jie guo fen xi [Sentinel surveillance of commercial sex clients in Sichuan, 2008–2009]. Yu Fang Yi Xue Qing Bao Za Zhi [Journal of Preventive Medicine Information] 26(9).
- 39.
Zhu LD (2007) 1011 li xing zui cuo ren yuan ai zi bing ji qi zhi xin xing de diao cha [Survey of AIDS and knowledge, beliefs, and behavior among 1011 sexual criminals]. Zhongguo Re Dai Yi Xue [Chinese Tropical Medicine] 7(1).
- 40. Jiang WY (2000) Zhoushan shi 300 ming xing bing gao wei ren qun jian ce jie guo fen xi [Surveillance analysis of 300 persons at high risk for sexually transmitted infections in Zhoushan city] Ji Bing Jian Ce [Disease Surveillance]. 15(6): 221–222.
- 41. Liu J, Liang QX, Feng XX, Yang YZ, Shan GS, et al. (2012) 2012 nian Liuzhou shi 400 ming piao ke ai zi bing shao dian jian ce jie guo fen xi [Sentinel surveillance of AIDS among 400 commercial sex clients in Liuzhou City in 2012]. Zhong Hua Ji Bing Kong Zhi Za Zhi [Chin J Dis Control Prev] 16(12): 1060–1063.
- 42. Jin X, Smith K, Chen RY, Ding G, Yao Y, et al. (2010) HIV prevalence and risk behaviors among male clients of female sex workers in Yunnan, China. J Acquir Immune Defic Syndr 53(1): 131–135.
- 43. Ma WJ, Wang JJ, Reilly KH, Bi AM, Ding GW, et al. (2010) Estimation of probability of unprotected heterosexual vaginal transmission of HIV-1 from clients to female sex workers in Kaiyuan, Yunnan Province, China. Biomed Environ Sci 23(4): 287–292.
- 44. Zhang H (2010) Ji yu an chang shou ji xing ban jing ye jian ce HIV de ke xing xing ji xiang guan yin su fen xi [Analysis of the feasibility and relevant factors associated with monitoring semen collected by sex workers from sex partners]. Zhong Hua Liu Xing Bing Xue Za Zhi [Chinese Journal of Epidemiology] 31(5): 534–537.
- 45. Liu Q, Gou J, Li F (2012) Xing chan ye zhong lao nian ke ren qun ti ai zi bing feng xian ji xing wang luo qing kuang–ji yu Guangxi mou bian jing xian de shi zheng fen xi [HIV risk and sexual network among the elderly clients of the sex industry: the case of Guangxi]. Ren Kou Yan Jiu [Population Research] 36(2): 60–70.
- 46.
Zhang G, Wong M, Yi P, Xu J, Li B, et al.. (2010) HIV-1 and STIs prevalence and risk factors of miners in mining districts of Yunnan, China. J Acquir Immune Defic Syndr (Suppl 1): S54–60.
- 47.
Yang C, Latkin C, Luan R, Wang C, Nelson K (2010) HIV, syphilis, hepatitis C and risk behaviours among commercial sex male clients in Sichuan province, China. Sex Transm Infect 86559–564.
- 48. Reilly KH, Wang J, Zhu Z, Li S, Yang T, et al. (2012) HIV and associated risk factors among male clients of female sex workers in a Chinese border region. Sex Transm Dis 39(10): 750–755.
- 49. Zhang CJ, Xu SL, Ding J (2001) 96 ming mai yin piao chang ren yuan STD jian cha jie guo fen xi [Analysis of STD examination results for 96 prostitutes and clients]. He Nan Yu Fang Yi Xue Za Zhi [Henan Journal of Preventive Medicine] 12(6): 347.
- 50. Zhu JC (2006) Changsha shi mai yin piao chang ren yuan mei du xue qing jian chu qing kuang bao gao [Report of the syphilis blood inspection of prostitutes and clients in Changsha city]. Zhongguo Xing Ke Xue [The Chinese Journal of Human Sexuality] 15(4): 46.
- 51. Lu JC, Liu HJ, Ren Y, Ping J (2008) Zhuhai shi 2546 li xing bing gao wei ren qun xing chuan bo ji bing liu xing bing xue fen xi [Epidemiological analysis of sexually transmitted diseases in 2546 high risk persons in Zhuhai city]. Ling Nan Pi Fu Xing Bing Ke Za Zhi [Southern China Journal of Dermato-Venereology] 15(3): 178.
- 52. Wang XX, Zhang QL, Chen BF, Fang XJ (2008) Guangdong sheng Dongguan shi bu fen xing zui cuo ren yuan ai zi bing bing du/mei du jian ce bao gao [Report of HIV/syphilis surveillance among sexual criminals in Dongguan city, Guangdong province]. Ji Bing Jian Ce [Disease Surveillance] 23(8): 490.
- 53. Yang YL, Li QY, Yu XQ, Wang YC, Ruan G (2011) Gao wei xing xing wei yu xing bing ai zi bing zhi shi ji gan ran zhuang kuang diao cha [Investigation on AIDS/STD knowledge, infection and high risk behavior among clients]. Gong gong wei sheng yu yu fang yi xue [J of Pub Health and Prev Med] 22(2): 51–53.
- 54. Zhang ZH, Xi DR (2006) Mai yin piao chang ren yuan xing bing ai zi bing xue qing xue jian ce fen xi [Analysis of sexually transmitted infections and AIDS blood examination among prostitutes and clients]. Yi Xue Xin Xi [Medical Information] 19(1): 169.
- 55. Lei SC, Wu Y, Deng QS, Xia Y, Jia Y, et al. (2011) Chongqing shi men zhen jiu zhen piao chang ren qun ai zi bing zhi shi he xing wei duo zhong xin diao cha [Multi-center survey of the AIDS-related knowledge and praxiology of the outpatient whoremasters in Chongqing]. Zhongguo Pi Fu Xing Bing Xue Za Zhi [Chin J Derm Venereol] 25(6): 450–453.
- 56. Yao Y (2008) Ji yu an chang shou ji piao ke te zheng ji qi jing ye biao ben jian ce HIV [HIV surveillance based on client characteristics and semen samples collected by sex workers]. Zhong Hua Liu Xing Bing Xue Za Zhi [Chinese Journal of Epidemiology] 29(7): 651.
- 57. Ni CM, Wu HP, Chen MF (2011) 2004 nian - 2008 nian Haiyan xian bu fen piao an chang xing bing gan ran de qing kuang [Surveillance on STD infection of some sex workers and their clients in Haiyan county during 2004–2008]. Zhongguo Wei Sheng Jian Yan Za Zhi [Chinese Journal of Health Laboratory Technology] 21(9): 2269–2270.
- 58. Zeng YB, Fang F, Wang HF, Quan Z, Zhao Y, et al. (2009) Shanghai shi Jinshan qu mai yin piao chang ren yuan 892 ren xing bing zhuang kuang fen xi [Prevalent analysis of sexually transmitted diseases in 892 prostitutes and whoremasters in Jinshan district of Shanghai]. Zhongguo Pi Fu Xing Bing Xue Za Zhi [The Chinese Journal of Dermatovenereology] 23(4): 228–230.
- 59. Xi XW, Zhu FH, Tang HL (2012) 2007–2011 nian Wuxi shi Huaishan qu xing luan ren qun STD/AIDS jian ce jie guo fen xi [Analysis on STD/AIDS monitoring results among sexual promiscuity group in Huishan District of Wuxi City from 2007–2011]. Zhi Ye Yu Jian Kang [Occup and Health] 28(20): 2514–2515.
- 60. Hong QY, Shen Z, Lu ZM (2010) 1227 li mai yin piao chang ren yuan zi liao fen xi [Analysis of 1227 sex workers and clients]. Zhongguo Wei Sheng Jian Yan Za Zhi [Chinese Journal of Health Laboratory Technology] 20(11): 3064–3065.
- 61. Qiu XM, Zhong CY, Shen L, Wang L, Kang YP (2011) Hangzhou shi 822 li xing gao wei ren qun xing chuan bo ji bing liu xing bing xue fen xi [Epidemiological characteristics of sexually transmitted diseases in high risk population in Hangzhou city]. Ji Bing Jian Ce [Disease Surveillance] 26(4): 295–297.
- 62. Wu RH, Zhang Y, Shu YY, Tang Q, Wu GH (2012) Shanghai shi 1142 ming mai yin piao chang ren yuan mei du yu lin bing huan bing qing kuang fen xi [An analysis of gonorhea and syphilis conditions among 1142 female sex workers and their clients in one district of Shanghai]. Zhongguo Ai Zi Bing Xing Bing [Chin J AIDS STD] 18(5): 325–326.
- 63. Chen Z, Xie J, He J (2012) 1172 li mai yin piao chang ren yuan STD/AIDS gan ran zhuang kuang diao cha [Survey of STD/AIDS among 1172 sex workes and clients]. Zhongguo Ai Zi Bing Xing Bing [Chin J AIDS STD] 18(7): 492.
- 64.
Hu XM (2002) 1086 ming xing zui cuo ren yuan xing bing liu xing bing xue fen xi yu dui ce [Epidemiological analysis and management of sexually transmitted infections among 1086 sexual criminals]. Zhongguo Wei Sheng Gong Cheng Xue [China Health Engineering] 2115–116.
- 65. Zhao YR (2003) Mai yin piao chang ren yuan STD shi yan shi jian ce jie guo fen xi [Laboratory analysis of STDs in sex workers and clients]. Zhongguo Ai Zi Bing Xing Bing [Chin J AIDS STD] 9(5): 310–314.
- 66.
Li DL, Ding HF, Luo FJ (2006) 2517 li mai yin piao chang ren yuan xing chuan bo gan ran liu xing bing xue diao cha fen xi [Epidemiological analysis of sexual transmitted infection in 2517 FSWs and their male clients]. Zhongguo Ai Zi Bing Xing Bing [Chinese Journal of AIDS & STD] 4344–346.
- 67. Liu YQ (2007) Beijing shi Huairou qu 2005 nian te shu ren qun mei du gan ran qing kuang [Syphilis in special populations in Huairou district, Beijing 2005]. Zhi Ye Yu Jian Kang [Occupation and Health] 23(16): 1430–1431.
- 68.
Li GY, Xia DY (2010) 2005–2008 nian Beijing piao ke ren qun gan ran ai zi bing de wei xian xing wei gai bian yan jiu [HIV risk behavior change research among clients in Beijing in 2005–2008]. Zhong Guo Ai Zi Bing Xing Bing [China J AIDS STD] 3251–254.
- 69.
Dong XY, Zhou N, Guo Y, Yu MH (2009) Tianjin shi 2007 nian an chang ji piao ke shao dian jian ce jie guo fen xi [Sentinel surveillance analysis of sex workers and clients in Tianjin city, 2007]. Hua Nan Yu Fang Yi Xue [South China Journal of Preventive Medicine] 240–41.
- 70. Gao JM (2008) 2006 nian Beijing shi Huairou qu xing bing ai zi bing jian ce jie guo fen xi [Analysis on results of STD and AIDS surveillance during 2006 in Huairou of Beijing]. Zhi Ye Yu Jian Kang [Occupation and Health] 24(14): 1415–1416.
- 71. Wang L, Gao L, Guo W, Wang L, Li DM, et al. (2010) 2009 nian Zhongguo bu fen cheng shi she qu piao ke ren qun AIDS xiang guan xing wei yu HIV gan ran lu diao cha [Survey of AIDS-related behavior and HIV prevalence among commercial sex clients in urban China in 2009]. Zhongguo Ai Zi Bing Xing Bing [China J AIDS STD] 16(4): 364–367.
- 72. Hesketh T, Tang F, Wang ZB, Huang XM, Williams D, et al. (2005) HIV and syphilis in young Chinese adults: implications for spread. Int J STD AIDS 16(3): 262–266.
- 73.
Poon AN, Li Z, Wang N, Hong Y (2011) Review of HIV and other sexually transmitted infections among female sex workers in China. AIDS Care (Suppl 1): 5–25.
- 74.
Chen XS, Wang QQ, Yin YP, Liang GJ, Jiang N, et al.. (2012) Prevalence of syphilis infection in different tiers of female sex workers in China: implications for surveillance and interventions. BMC Infect Dis 1284.
- 75. Chow EP, Wilson DP, Zhang J, Jing J, Zhang L (2011) Human immunodeficiency virus prevalence is increasing among men who have sex with men in China: findings from a review and meta-analysis. Sex Transm Dis 38(9): 845–857.
- 76. Chow EP, Wilson DP, Zhang L (2011) HIV and syphilis co-infection increasing among men who have sex with men in China: a systematic review and meta-analysis. PLoS One 6(8): e22768.
- 77. Burton MJ, Reilly KH, Penman A (2010) Incarceration as a risk factor for hepatitis C virus (HCV) and human immunodeficiency virus (HIV) co-infection in Mississippi. J Health Care Poor Underserved 21(4): 1194–1202.
- 78. Flanigan TP, Beckwith CG (2011) The intertwined epidemics of HIV infection, incarceration, and substance abuse: a call to action. J Infect Dis 203(9): 1201–1203.
- 79. Hammett TM (2009) Sexually transmitted diseases and incarceration. Curr Opin Infect Dis 22(1): 77–81.
- 80. Khan MR, Epperson MW, Mateu-Gelabert P, Bolyard M, Sandoval M, et al. (2011) Incarceration, sex with an STI- or HIV-infected partner, and infection with an STI or HIV in Bushwick, Brooklyn, NY: a social network perspective. Am J Public Health 101(6): 1110–1117.
- 81. Mertz KJ, Finelli L, Levine WC, Mognoni RC, Berman SM, et al. (2000) Gonorrhea in male adolescents and young adults in Newark, New Jersey: implications of risk factors and patient preferences for prevention strategies. Sex Transm Dis 27(4): 201–207.
- 82. Sosman J, Macgowan R, Margolis A, Gaydos CA, Eldridge G, et al. (2011) Sexually Transmitted Infections and Hepatitis in Men With a History of Incarceration. Sex Transm Dis 38(7): 634–639.
- 83. Thomas JC, Levandowski BA, Isler MR, Torrone E, Wilson G (2008) Incarceration and sexually transmitted infections: a neighborhood perspective. J Urban Health 85(1): 90–99.
- 84. Willers DM, Peipert JF, Allsworth JE, Stein MD, Rose JS, et al. (2008) Prevalence and predictors of sexually transmitted infection among newly incarcerated females. Sex Transm Dis 35(1): 68–72.
- 85. Huang Y, Maman S, Pan S (2012) Understanding the diversity of male clients of sex workers in China and the implications for HIV prevention programmes. Glob Public Health 7(5): 509–21.
- 86.
Wang Y, Jiang Y, Lu L, Wang G, Bi A, et al.. (2010) Microbicide acceptability and associated factors among female sex workers and male clients in Kaiyuan county, Yunnan province, China. J Acquir Immune Defic Syndr (Suppl 1): S93–97.
- 87. Sabido M, Lahuerta M, Montoliu A, Gonzalez V, Hernandez G, et al. (2011) Human Immunodeficiency Virus, Sexually Transmitted Infections, and Risk Behaviors Among Clients of Sex Workers in Guatemala: Are They a Bridge in Human Immunodeficiency Virus Transmission? Sex Transm Dis 38(8): 735–742.
- 88. Nguyen NT, Nguyen HT, Trinh HQ, Mills SJ, Detels R (2009) Clients of female sex workers as a bridging population in Vietnam. AIDS Behav 13(5): 881–891.
- 89.
Wang Y, Jiang Y, Lu L, Wang G, Bi A, et al.. (2010) Microbicide acceptability and associated factors among female sex workers and male clients in Kaiyuan county, Yunnan province, China. J Acquir Immune Defic Syndr (Suppl 1): S93–97.
- 90. Wu Z, Sun X, Sullivan SG, Detels R (2006) Public health. HIV testing in China. Science 312(5779): 1475–1476.
- 91.
Hong Y, Poon AN, Zhang C (2011) HIV/STI prevention interventions targeting FSWs in China: a systematic literature review. AIDS Care (Suppl 1): 54–65.
- 92.
Zhang G (2004) Huabei di qu mi niao sheng zhi dao sha yan yi yuan ti gan ran qing kuang ji xiang guan wei xian yin su fen xi [The prevalence and risk factors of urogenital chlamydia trachomatis infection in Huaibei, Anhui]. Ji Bing Kong Zhi Za Zhi [Chinese Journal of Disease Control & Prevention] 8(433–434).