Since 2008, heterosexual contacts have become the predominant mode of human immunodeficiency virus (HIV) transmission in China, accounting for 46.5% of the estimated 740,000 people living with HIV and AIDS in 2011.1 Female sex workers (FSWs) are one of the key populations to facilitate increase of HIV epidemic and likely to determine how fast the HIV epidemic will spread from high-risk groups to the general population. However, because of the difficulties of accessibility, FSWs who solicit clients on the streets or other public outdoor places are poorly covered by the current HIV/STD surveillance and intervention programs.2 In addition to increased risk related to injection drug use among FSWs, previous studies have shown that prevalence of syphilis and other STDs varies among FSWs recruited from different types of sex-work venues in China,2–4 but the HIV prevalence among different kinds of sex workers has not been well reported. In this article, we present a multisite cross-sectional study on prevalence of HIV infection and its correlates associated with sociodemographic characteristics among FSWs from different types of venues in China.
The study was conducted during June to September 2009 in 6 cities in southern China (Guangxi, Guangdong, and Hainan provinces). In each study site, sex-work venues were mapped and selected for recruiting a convenience sample of FSWs. Eligibility to participate in the study included age >16 years; ability to give an informed consent; and having provided commercial sex for money or goods within the previous 3 months. Sex-work venues were categorized into 3 tiers, i.e., high tier (HT) including karaoke bars, or hotels; middle tier (MT) including hair salons or barber shops, massage parlors, foot bathing shops, roadside shops, guesthouses, or roadside restaurants; and low tier (LT) including street, or other public outdoor places. Each participant was interviewed using a structured questionnaire and then underwent a blood specimen collection for HIV and syphilis tests.
Serological tests of HIV and syphilis were conducted at local laboratories according to national guidelines. HIV infection was defined as being positive for HIV enzyme-linked immunosorbent assay and Western blot tests, and syphilis infection was defined as being positive for treponemal enzymelinked immunosorbent assay and nontreponemal toluidine red unheated serum test (TRUST) tests.
Univariate and multivariate logistic regression analyses using backward stepwise elimination were applied to evaluate factors associated with HIV infection. The variables attaining P < 0.10 significance in univariate analysis were included in the multivariate logistic regression analysis, retaining only variables achieving P < 0.05 significance in the final model. Adjusted odds ratio (AOR), with 95% confidence intervals (CIs), was determined. All statistical analyses were performed using SPSS (version 13.0, Chicago, IL) software. The study protocols were reviewed and approved by the Medical Ethics Committee of the Chinese Academy of Medical Sciences Institute of Dermatology.
A total of 5322 FSWs, including 1379 (25.9%) from HT venues, 2482 (46.6%) from MT venues, and 1461 (27.5%) from LT venues, were enrolled from 6 study sites. Age of FSWs in LT venues (mean ± standard deviation, 28.7 ± 8.0) was significantly older than those in MT and HT venues (25.2 ± 5.9 and 23.4 ± 4.5, respectively; F = 353.79, P < 0.001). More women in LT venues (41.9%) were local residents compared with those in MT and HT venues (26.5% and 10.6%, respectively, χ2 = 239.51, P < 0.001). About 5% of FSWs admitted that they used illegal drug in the past 12 months, and a small number (n = 20) reported a history of intravenous drug use in the past 6 months. A total of 28 FSWs infected with HIV were detected, giving an overall prevalence of 0.54% (95% CI, 0.37%–0.76%). Table 1 shows the results from univariate analysis of associations of HIV infection with selected sociodemographic characteristics and status of syphilis. The HIV prevalence was significantly associated with being older age, local residency, locating in Guangxi, working in LT venues, and having syphilis infection. The difference in HIV prevalence between FSWs who reported use and no use of a condom was not statistically significant (χ2 = 0.54, P = 0.46). In multivariate logistic regression analysis (Table 2), the variable statistically associated with HIV prevalence include being FSWs who work in LT venues (AOR = 2.73, 95% CI = 1.12–6.67, P = 0.028) and coming from Guangxi Province (AOR = 7.89, 95% CI = 1.65–37.64, P = 0.004).
FSWs have become one of most-at-risk populations for HIV in many developing countries.5 More attention has been paid to typology of FSWs for developing HIV/STD surveillance and intervention programs in recent years,4,6 but studies on HIV/STD burden among FSWs in different types of venues are limited.2,3 FSWs in LT venues are a special segment of FSWs with more vulnerable nature in terms of sociodemographic characteristics, organization of sex work, employment and economic status, and relationship with clients.4,7 Our study found that the prevalence for HIV infection among FSWs in LT venues (1.37%) was much higher than that among those in MT (0.28%) and HT venues (0.07%), indicating about 3 times higher risk for HIV infection in LT venues than HT or MT venues. Previous studies have shown that the FSWs working in LT venues tended to have greater number of sexual clients, but infrequently used condoms due to extra payment for unsafe sex.8–10 FSWs in LT venues either independently solicit clients on streets or find clients through nearby construction sites and factories.7 They usually earn far less than what FSWs in MT or HT venues earn7 but engage in riskier behaviors when having sex with both commercial and regular nonpaying partners11 and are highly stigmatized and marginalized by society. In some areas of China, elder individuals are more likely to purchase commercial services from FSWs in LT venues.12 This may be one explanation for the increasing trends of HIV and STD infections among elders in recent years.13 As FSWs in LT venues continue to shoulder a greater burden of the diseases,careful attention should be given to this particular high-risk population in order to reduce morbidity and decrease HIV/STD transmission from this bridge population to sexual partners or general population.14,15 The high prevalence of HIV infections among FSWs in LT venues further emphases the importance of effective prevention and intervention programs for this population. However, the FSWs in LT venues are not yet well represented in current HIV and STD surveillance programs and are also less covered by current intervention programs in China. Geographic location of Guangxi was an independent factor statistically associated with HIV infection in multivariate logistic regression model. Guangxi Province is among the 6 provinces in China reporting the highest numbers of HIV/AIDS cases. The epidemic of HIV/AIDS was largely confined to injection drug users in Guangxi Province before 2007.16 However, heterosexual transmission has increasingly been the source of infections in recent years. In Guangxi Province in 2009, the most common transmission mode was heterosexual contact, accounting for >60% of reported HIV/AIDS cases.17 HIV prevalence at study sites in Guangxi (1.03%) was significantly higher than that in other sites (0.07%). This rate was higher than 0.8% reported by a study among FSWs in 4 cities in Guangxi18 but much lower than 2.3% reported in Liuzhou, which is located in a major drug trafficking-route in southern China and has a high HIV prevalence among local injection drug users.19 Moreover, nearly 10% of FSWs in Liuzhou re- ported having had sex with drug users.19
There are some limitations to be addressed. First, although the study was carried out in 6 sites covering 3 provinces, the socioeconomic and behavioral characteristics of FSWs in the study areas may be different from other areas in China, and most (26/28) of HIV-infected FSWs were detected in Guangxi. Any generalization of the study results should be made with caution. Second, the study was not able to use a random sampling method to recruit the FSWs, likely resulting in the sample bias. Third, 10% to 40% of FSWs to refuse participating in the study may result in potential selection bias. Fourth, the numbers of FSWs with some risk behaviors (such as injection drug use, sharing needle) were too small in the study population to do the subgroup analysis for determining potential associations between the infections and these risk factors. Fifth, the data regarding sexual behaviors and condom use are subject to self-reporting bias and social response bias.
Based on findings from the study, it can be concluded that a substantial prevalence of HIV infection is among FSW population and the behavioral risk of HIV infection varies across different types of sex work venues, indicating a highest risk among FSWs in LT venues. As this subgroup of FSWs has not been well covered by current control programs in China, the innovative and comprehensive interventions, including social supports, health education, condom promotion, HIV and syphilis screening, partner notification, and STD care, to access this hard-to-reach population for preventing HIV and other STDs should be urgently developed. Importantly, it should be noted that the categorization of FSWs according to the places they work is aimed to improve our understanding of systematic differences in risk behaviors and HIV/STD infections across subgroups of this population in order to develop targeted public health interventions. It is not our hope that by classifying the FSWs on streets or other public outdoor places as FSWs at low tier venues, they become further stigmatized and marginalized.
1. MOH/UNAIDS/WHO. 2011 Estimates of HIV/AIDS Epidemic in China. Beijing: China Ministry of Health, 2011.
2. Chen XS, Wang QQ, Yin YP, et al.. Prevalence of syphilis infection in different tiers of female sex workers in China: Implications for surveillance and interventions. BMC Infect Dis 2012; 12: 84.
3. Li Y, Detels R, Lin P, et al.. Difference in risk behaviors and STD prevalence between street-based and establishment-based FSWs in Guangdong Province, China. AIDS Behav 2012; 16: 943–951.
4. Li J, Chen XS, Merli MG, et al.. Systematic differences in risk behaviors and syphilis prevalence across types of female sex workers: A preliminary study in Liuzhou, China. Sex Transm Dis 2012; 39: 195–200.
5. Baral S, Beyrer C, Muessig K, et al.. Burden of HIV among female sex workers in low-income and middle-income countries: A systematic review and meta-analysis. Lancet Infect Dis In press.
6. Buzdugan R, Halli SS, Cowan FM. The female sex work typology in India in the context of HIV/AIDS. Trop Med Int Health 2009; 14: 673–87.
7. Huang Y, Henderson GE, Pan S, et al.. HIV/AIDS risk among brothel-based female sex workers in China: Assessing the terms, content, and knowledge of sex work. Sex Transm Dis 2004; 31: 695–700.
8. Wang Q, Yang P, Gong XD, et al.. Syphilis prevalence and high risk behaviors among female sex workers in different settings. China J AIDS STDs 2009; 15: 398–400.
9. Yang X, Xia G. Gender, work, and HIV risk: Determinants of risky sexual behavior among female entertainment workers in China. AIDS Educ Prev 2006; 18: 333–347.
10. Yang X, Xia G, Li X, et al.. Social influence and individual risk factors of HIV unsafe sex among female entertainment workers in China. AIDS Educ Prev 2010; 22: 69–86.
11. Li Y, Detels R, Lin P, et al.. Prevalence of HIV and STIs and associated risk factors among female sex workers in Guangdong Province, China. J Acquir Immun Defic Syndr 2010; 53 (Suppl 1): S48–S53.
12. Pearline RV, Tucker JD, Yuan LF, et al.. Sexually transmitted infections among individuals over fifty years of age in China. AIDS Patient Care STDS 2010; 24: 345–347.
14. Huang ZJ, Wang W, Martin MC, et al.. “Bridge population”: Sex workers or their clients?–STI prevalence and risk behaviors of clients of female sex workers in China. AIDS Care 2011; 23 (suppl 1): 45–53.
15. Hesketh T, Zhang J, Qiang DJ. HIV knowledge and risk behaviour of female sex workers in Yunnan Province, China: Potential as bridging groups to the general population. AIDS Care 2005; 17: 958–966.
16. Wang L, Wang N. HIV/AIDS epidemic and the development of comprehensive surveillance system in China with challenges. Chin Med J (Engl) 2010; 123: 3495–3500.
17. Yang X, Abdullah AS, Wei B, et al.. Factors influencing Chinese male’s willingness to undergo circumcision: A cross-sectional study in western China. PLoS ONE 2012; 7: e30198.
18. Zhu BY, Bu J, Huang PY, et al.. Epidemiology of sexually transmitted infections, HIV, and related high-risk behaviors among female sex workers in Guangxi Autonomous Region, China. Jpn J Infect Dis 2012; 65: 75–78.
© Copyright 2012 American Sexually Transmitted Diseases Association
19. Lu F, Jia Y, Sun X, Wang L, et al.. Prevalence of HIV infection and predictors for syphilis infection among female sex workers in southern China. Southeast Asian J Trop Med Public Health 2009; 40: 263–272.