Syphilis has made a dramatic resurgence in China during the past two decades [1]. Heterosexual contacts have become one of primary modes of HIV transmission in China [2, 3]. Syphilis has been considered as one of factors to facilitate HIV transmission [4]. Female sex workers (FSWs) are more at risk of having HIV, syphilis and other sexually transmitted infections (STIs). Syphilis has been ranked as the third most prevalent notifiable infectious disease in China. Thus, the syphilis epidemic holds important relevance for infectious disease burden control in China and the region. Assessing the disease burden of syphilis among FSWs is necessary for planning primary and secondary prevention control measures. Syphilis surveillance in China has relied largely on case reports submitted by hospitals or clinics through a website-based case-reporting system [1]. Syphilis prevalence monitoring among specific high-risk populations including FSWs is conducted through HIV sentinel surveillance surveys to provide trends for gauging the effectiveness of prevention efforts [5]. The reported incidence of primary and secondary syphilis (reflecting the intensity of recent transmission) was 11.7 cases per 100, 000 residents in 2009, which had increased by 2.1 times since 2005 [6]. However, case report data may underestimate the true burden of syphilis due to inadequate screening among asymptomatic infected persons and underreporting of the diagnosed cases. Current sentinel surveillance for HIV and syphilis infections among FSWs in China is usually based on recruitment of a convenience sample of FSWs working in entertainment establishments. Based on a list of establishments which are typically used for interventions through outreach work, some venues are selected for recruiting a convenience sample of FSWs for a questionnaire survey and specimen collection. Freelance FSWs are usually not included in the surveillance of most sentinel sites. In this case, the FSWs working at luxurious sex venues (e.g. karaoke bars or hotels) are usually disproportionately recruited. In this paper, we present a multi-site epidemiological study on the prevalence and risk factors of syphilis among FSWs recruited from different typologies of venues in China, and discuss the implications of these findings for surveillance and interventions.

A total of 7,118 FSWs, including 2,144 (30.1%) HT-FSWs, 3,227 (45.3%) MT-FSWs and 1,747 (24.5%) were enrolled from eight study sites to participate in a baseline survey during June and September 2009. The rates to refuse participating in the study were 8-12% in HT-FSWs, 20-25% in MT-FSWs and 30-35% in LT-FSWs. Overall, 7,118 specimens underwent syphilis ELISA testing followed by TRUST testing for those with positive ELISA. The prevalence of syphilis infection in the study population was 5.0% (95% CI, 4.5%-5.5%).

Commercial sex is illegal in China. By 2005, the Chinese Center for Disease Control and Prevention (CDC) estimated that there were 2.8 to 4.5 million FSWs nationwide [8]. Risk behaviors and socio-demographic characteristics of FSWs linked to the sex trade may be associated with risk of STI infection, health care seeking behaviors, and/or social stigma [9, 10]. There have been several ways to classify women who provide sex for money or gifts. A study has categorized FSWs into seven typologies according to their workplace and organization, income and demographics, and approximate sexual risk [11], while other studies have categorized them into 3 tiers simply based on sex work venues and socio-economic contexts [12, 13]. Despite the fact that no consensus on FSW typologies has been met in China, typology of FSWs is important for design of surveillance and intervention programs.

A substantial prevalence of syphilis was found among FSWs in the study areas. These findings are consistent with the results reported elsewhere among FSWs with 5.3% in Sichuan [14], and 3% in Shandong [15], but are much higher than the median level of national prevalence (0.5-1.8%) [5]. The prevalence varies significantly by different tier of FSWs, showing a higher prevalence among LT-FSWs (9.7%) than MT-FSWs (4.3%) or HT-FSWs (2.2%). A systematic review of published studies found that low-tier FSWs are approximately twice as likely to have syphilis [16]. Some studies have found extremely high syphilis prevalence in this group, ranging from 10-38% [13, 17]. Studies have shown that the FSWs working in low-tier venues tended to have greater number of clients, but infrequently used condoms due to extra payment for unsafe sex [17–19]. Low-tier FSWs either independently solicit clients on streets (street-walking FSWs) or find clients (some knew each other) through nearby construction sites and factories [11]. Our results further indicate that older women are more likely to be infected with syphilis, and the women with less education are at a greater risk of infection. A 2006 national probability survey among men 15-49 years old indicated that the prevalence of visiting FSWs in the previous year was 4.2% overall, with 7.2% in urban areas and 1.8% in rural areas [20]. Although we do not have data on the percentages of Chinese men who visit each of the different tiers of FSWs, it has been found from observations in several areas that the clients of low-tier FSWs are usually migrants and elder men. It is known from our study that there are significant differences in terms of socio-demographic characteristics between different tiers of FSWs, indicating that low-tier FSWs tend to be older women with low education levels, and the women from local areas and non-Han minorities. These differences are important determinants for designing surveillance and intervention programs. The low-tier subgroups of FSWs are less well represented in current HIV and STI surveillance programs and are also less likely to be covered by current intervention programs in China. The significant differences in terms of demographic characteristics and prevalence of syphilis between FSWs recruited from low-tier sex work venues and those from middle or high-tier venues warrants consideration of what kind of population we should recruit and/or where we should recruit them to represent the FSWs for surveillance purposes. However, the interpretation of epidemiological and behavioral data emerging from such settings is challenging due to significant selection bias. The high prevalence of the syphilis infections in the study populations further emphases the importance of effective curative and preventive STI services for the FSW population. Syphilis surveillance and monitoring of the response to the STI epidemic may be improved by carefully considering and selecting appropriate target populations to represent women at high risk.

The strengths of this study include (1) the inclusion and classification of different tiers of FSWs in the study; (2) the utilization of community-based or outreach-based recruitment strategies; and (3) the multi-site survey consisting of 8 middle-size cities in China. There are also limitations to be addressed. First, although the study was carried out in eight cities, the socio-economic and behavioral characteristics of FSWs in the study areas may be different from other Chinese cities. Any generalization of the results from this study should therefore 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, high rates of FSWs to refuse participating in the study (i.e., 8-12%, 20-25% and 30-40% among HT-, MT- and LT-FSWs, respectively) may result in potential selection bias. Fourth, the sample size for this study may not be large enough for the subgroup analysis to show potential associations between the infections and some risk factors. Fifth, this study included only limited information on risk behaviors, and data regarding sexual behaviors and condom use is subject to self-reporting bias and social response bias due to the sensitivity of these topics. Finally, this study did not ascertain an association between syphilis and HIV infection because the number of FSWs with HIV infection was small, although some studies in China have shown that HIV infection is independently associated with syphilis infection [20]. In addition, some potential factors related to the infection, such as condom use with regular non-client sexual partners and the number of clients per week, were not included in the study.

As FSWs are an important source of infection and probably the bridge population for the heterosexual transmission of syphilis and HIV, the findings of this study have a number of important implications. First, this study shows a substantial prevalence of syphilis infection among FSWs and much higher prevalence among LT- and MT-FSWs. The patterns of infection suggest the importance of prioritizing the MT- and LT-FSWs in the current program for interventions (health education, condom promotion and STI care services) in FSWs. Second, this study suggests a re-appraisal of the current HIV/STI surveillance system in terms of sampling of women at high risk in China to enable more representative, valid and reliable prevalence estimates to be generated. Third, this study highlights our limited knowledge of the epidemiology of syphilis and likely other STIs among LT-FSWs in China. LT-FSWs are thought to be a potential and key co-factor for sustaining the spread of STIs in high-risk populations and for bridging the epidemic from high-risk groups to the general population. However, they are usually neglected by routine intervention programs. This underscores the urgency of including this neglected population in preventive interventions for reducing STI infection. The current HIV/STI intervention programs for female sex workers are urgently needed to improve for increasing access to MT- and LT-FSWs in China through providing a comprehensive intervention package. The package should include not only health education materials and condoms but also STI and reproductive health care including syphilis testing and counseling; and delivery of the package should be conducted by not only the solitary CDC outreach teams but also medical personnel and non-governmental organizations.

A substantial prevalence of syphilis in FSWs, particularly in low-tier FSWs, is a serious public health concern. Syphilis control in this population through universal screening of syphilis and integrating syphilis testing into VCT services, STI risk reduction education, and aggressive condom promotion programs are urgently needed. Much can and should be done to stem the syphilis epidemic and potential uptake of the co-epidemic of syphilis and HIV in FSWs. The Chinese Ministry of Health has already issued a national 10-year plan for syphilis control and prevention, where strengthening the surveillance system in high risk groups as well as comprehensive interventions among FSWs are priorities in order to curb the epidemic in China.