Inequalities in socioeconomic status, behaviors, healthcare services and vulnerability to HIV/STIs between brothel-based and street-based female sex workers in Yunnan, China

Background: Commercial sex plays a critical role in the transmission of HIV/ST I infections in mainland China because female sex workers (FSWs), who tend to be either street-based (SSWs) or brothel-based (BSWs), are extremely prevalent. These two groups had different behaviors and treatment. Few studies investigated due to SSWs group is difficult to reach. Methods: A cross-sectional survey was conducted in Yunnan Province of China with 129 street-based and 185 brothel-based participants. Peer educators conducted anonymous, face-to-face interviews to collect data on socio-demographic characteristics, HIV/STIs-related knowledge, sex work history, sex behaviours, experience of receiving healthcare service, and experience of abuse from clients. Blood samples were taken for HIV and syphilis testing. Urine samples were taken for gonorrhoea and chlamydia testing. Results: Significant differences on socio-economic characters and HIV/STIs prevalence are found between the two types of FSWs. SSWs are older than BSWs; have less education, more dependents, and more clients in one week; receive less healthcare services; and have a higher prevalence of HIV/STIs. Binary logistic regression model results showed that venue for sex trade and experience of HIV testing were significantly associated with the prevalence of HIV/STIs Conclusions: The SSWs are at lower socio-economic status and have high HIV/STIs mobility, who are more marginalized, receive less healthcare and are, thus, more vulnerable. China’s next step in healthcare intervention should focus on the most hard-to-reach-marginalised groups. HIV/STIs testing and socio-psychological support programmes are urgent needed for these neglected people.


Background
Even though China has made significant progress in HIV/AIDS control and prevention, the epidemic is a continuing challenge [1] . With the changing trends in transmission routes, more than 90% of new HIV infections was sexually transmitted path, which is now the primary driver [2] . Commercial sex, in particular, plays a critical role in the sexual transmission of HIV/STDs in China. Although the epidemic is largely characterised by a low national prevalence of 0.037% [3] , the prevalence of HIV among 5 all sex workers was 0.19% in 201 [4] , with certain regions having higher prevalence, especially in low-fee female sexual workers (FSWs) was much higher at 4.7% [5] .
The sex industry was virtually eliminated in the 1950s in China but re-emerged and be periodic crackdowns since the 1980s. This increasing trend is from the implementation of open-door and market-economic policies, flourishing synchronously with rapid economic development [6,7] . Several socioeconomic changes are driving commercial sex in China. Rural-to-urban migration had increased, resulting in more women turning to commercial sex and men engaging in high-risk sex with FSWs.
Attitudes towards sex are also becoming more liberal with an increase in premarital and extramarital sex [8,9] .It has estimated the number of FSW in China between 2 and 20 million [10][11][12] . Some studies estimated the (FSWs) population to be as high as 3.6% of the total adult female population (15-49 years old) in some areas of China, higher than the proportions in other Asian countries or anywhere else in the world [13,14] FSWs in China are a heterogeneous group, usually divided by work venue. The two main groups are the brothel-based sex workers (BSWs) who encounter their clients in various entertainment and service establishments (e.g., bars, hotels, guesthouses, saunas, massage parlors, etc.) and the street-based sex workers (SSWs) who solicit on streets or in parks [15] . Some studies have estimated the socio-demographics 6 characteristics, HIV-related knowledge, risky behaviors, and prevalence of HIV/STIs among BSWs and their clients [16][17][18][19][20] . However, less studies [21][22][23][24][25] , have looked at the SSWs, because of their high mobility and secrecy resulting in challenges in gaining access to them.
There were few studies [26,27] in China focus on both SSWs and BSWs. Therefore, we have conducted the much deeper comparative study in China that targets both SSWs and BSWs, comparing socioeconomic factors, sexual behaviors and risky practices, like the experience of verbal or physical abuse, HIV/STIs-related knowledge, HIV/STIs prevalence and their influencing factors, and the efficacy of their health-care.

Study site and field management
This study was conducted between August and September 2010, in Lingxiang County of Yunnan province, southeast China. Yunnan province has one of the highest HIV prevalence in China, Lingxiang County being one of the epidemic centres [28] . Four FSW peer educators working for an NGO were recruited into the study team.
They helped in the mapping out the two FSW groups, recruitment, and interviews using a structured questionnaire after obtaining written informed consent. Blood and urine samples were collected by laboratory staff from the local CDC for HIV/STIs testing.
HIV/STIs-related pre-test-post-test counseling, informing of test results, and free STI and Antiretroviral therapy ART treatment are all provided by certified medical staff with the local CDC. This study received approval from the local Yunnan institutional review boards.

Data collection instrument
A structured questionnaire for FSWs based on The Family Health International Behavioral Surveillance Survey (FHI-BSS) 2000(see the supplementary files), was used to collect data on socio-demographic characteristics, HIV/STI-related knowledge, risk perception, sex work history, sex behavior with clients and sex partners, self-report STI symptoms, and experience of receiving healthcare services. Knowledge of transmission and prevention of HIV/AIDS was measured by seven true/false/unknown questions.
One point was given for each correct answer, with the score ranging from 0 to 7 points.
Knowledge about symptoms of other STIs was similarly measured by ten questions, 9 with the score ranging from 0 to 10 points. Both focus group discussions and in-depth interviews with FSWs and peer educators were conducted to check the appropriateness of the questionnaire.

Laboratory testing
Blood samples were taken for HIV and syphilis testing. HIV was tested using the enzyme-linked immunosorbent assay (ELISA) for screening and the western blot test for confirmation. Screening for syphilis was performed using the rapid plasma reagin (RPR) test and the treponema pallidum particle agglutination (TPPA) test. Positive RPR and TPPA constitute a diagnosis of active syphilis. Urine samples were taken for gonorrhea and chlamydia testing by real-time fluorescent quantitative PCR (FQ-PCR) assay. Our study outcome was defined as testing positive for one or more of these four STIs (HIV, syphilis, gonorrhea, and chlamydia).

Means and proportions compared by using the Mann-Whitney U-test and the
Chi-square test. A binary logistic regression model with crude odds ratios (OR), adjusted OR, and 95% confidence intervals (CI) of related factors associated with HIV/STIs were calculated. All analyses were carried out with the SPSS11.5 (IBM SPSS Co., USA). P<0.05 was considered statistically significant (two-sided).

Sociodemographic characteristics and sex worker history
The sociodemographic characteristics of SSWs and BSWs showed in Table 1.
SSWs were older, more of them married, had received less education, and had to support more dependents than BSWs (P<0.001). They had begun sex work at an older age, had longer sex worker careers (P<0.01), and received a lower fee per client than BSWs (P<0.001). Consistently, they solicited many more clients per day (P<0.001) than their BSW counterparts.

Sex behaviors and risky practices
Risky practices and condom usage described in Table 2  The HIV/AIDS-related knowledge score was high in both FSW groups, although without the significance. Conversely, the score of knowledge on STIs was low, and a significant difference found between the two groups (P<0.001). Compared with BSWs, SSWs had received less HIV/STIs related health-care services, such as free condom distribution, STIs testing, and treatment, and HIV counseling and testing (37.0 vs. 64.4%, P<0.001) (). About two-thirds of the subjects in both groups had had HIV testing in the past (68.5 vs. 65.5%, NS) (

HIV/STIs prevalence and related risk factors
Five of the SSWs and none of the BSWs were confirmed to be infected with HIV (P<0.01). Syphilis prevalence was higher in SSWs (7.0 vs. 1.1%, P<0.01). Overall, 37.2% of SSWs and 24.9% of BSWs were found to be HIV/STIs infected (Table 4, P<0.05).
A binary logistic regression model developed for all of the participants. As independent variables, the exposure variable of interest and all variables independently associated with the total number of STI infections were included (Table 5). SSWs are at a higher risk of having STIs compare with those BSWs (OR =2.07, 95% CI 1.22-3.50), HIV testing is a protective factor for HIV/STI infections (OR=0.42, 95% CI 0.24-0 .71).

Discussion
Our results indicated that significant inequalities found between SSWs and BSWs concerning socio-demographics and healthcare service coverage. FSWs both have a high HIV awareness and condom use rate with clients, however, the issue on frequent 13 condom slippage or breakage well all existed for BSWs and SSWs. The SSWs received a significantly lower level of healthcare service and they are consistently more vulnerable and suffering from a higher incidence of HIV/STI infections than are BSWs.
Our findings indicate that violence abuse is a significant risk factor for HIV/STIs infections in FSWs population. Consistent with studies in Zimbabwe [28] , Swaziland [29] , American [30] , our results suggest that efforts to reduce violence are a key component of STI/HIV prevention and control in this vulnerable population. Violence Abuse from FSW clients has little studied in China or in other parts of the world. The illegal status of FSWs, the strong stigma and discrimination toward them in Chinese traditional culture, the fear of having their profession unmasked to family and acquaintances, and gender inequality are all factors that have contributed to their marginal situation and their vulnerability to abuse and violence [31] . At the same time, human resources are seriously limited within local health sectors in China [32] . therefore, most interventions would occur among the BSWs. Compared to BSWs, SSWs usually have no protectors or permanent venue; hence, they are more marginalized [33] , usually excluded from public healthcare sectors and surveillance systems and they are much harder to get the protection. 14 We also found HIV testing to be a protective factor against HIV/STIs, which suggests that seeking testing should promoted strongly in both groups and that more studies promoting HIV testing should be encouraged in relation to this population [34,35] .
Promotion of HIV testing and counselling (VCT) through the social media now become a new strategy in mainland China [3,36] . In last decades, the number of HIV testing facilities increased from 7,600 to 30,500 and the annual number of HIV tests increased from 45 million to 201 million (from 3.4% to 14.5% of the whole population) [37] .
Our multivariate analysis results highlight the importance of socioeconomic support in relation to HIV/STIs infection. All the three independent factors-work venue, experience of HIV testing, and abuse from clients-are strongly related to the socioeconomic background of FSWs. Most of the previous AIDS-related studies and interventions in China have been limited to biomedical issues only, with ideas for preventive efforts being almost entirely limited to the health sector. Even fewer studies have integrated HIV/STIs-related problems with other public health issues by looking at multiple-sector cooperation or using multi-disciplinary approaches [38,39] . Consequently, the generalization of the research findings are usually limited, as well as the efficacy of prevention intervention. Therefore, socio-epidemiologic studies and interventions considering social-economic and sociocultural backgrounds should be encouraged for 15 examining future HIV/STIs preventive approaches in China. Social support approaches, such as professional re-training and re-employment support, social support networks, and cooperation with non-health sectors should considered for FSWs.
The difficulty of reaching this population is a challenge for AIDS prevention in many countries. SSWs usually are not included in routine AIDS-related healthcare intervention or sentinel inspection as a result of their high mobility, mistrust of government, and lack of manpower in local healthcare sectors. In current study, our experience in integrating governmental and grassroots resources suggests that involvement of such organizations and peer educators is important, that skill training should be developed for peers, and that the public health sector and NGOs should be encouraged to integrate their work. Many international and national NGOs are dealing with many sensitive healthcare issues, large space remains for promoting cooperation between government sectors and NGOs on HIV/STIs prevention among high-risk groups in China [40,41] . Through assigning some of the routine work with FSWs to NGOs, the governmental healthcare can encourage such NGOs to involve themselves through planning, management, and implementation of healthcare services. The NGOs, on the other hand, should feel free to avail themselves of China's CDC laboratories and technical support.
SSWs were more hard to reach than BSWs, through close cooperation between a local Chinese CDC and grassroots NGO, we gathered both biological and behavior indicators on participants. The participates in this study successfully represented the whole FSWs in Lingxiang County. Based on no one rejected the interview, we thought there was no response bias. However, in the questionnaire, there were some sensitive questions so that the information bias maybe not avoided. In the meantime, we did much more in-depth comparative research from the risky behavior (themselves to the clients and partners) by using the FHIBSS, which use reliable methods to track HIV risk behaviors over time as part of an integrated surveillance system, which monitors various aspects of the epidemic. They are especially useful in providing information on behaviors among sub-populations who may be difficult to reach through traditional household surveys, but who may be at especially high risk for contracting or passing on HIV, especially for sex workers and their clients. Our results, which demonstrate the efficacy of combining resources at various levels to access these hard-to-reach groups, suggested that outreach programs to these kinds of vulnerable groups are of the utmost importance. The main weakness of this study is its limited scale. As described above, this cross-sectional survey conducted only in one spot. Hence, generalization of the results is limited, and more studies on a broader scale needed. 17 Though the Chinese health sector has made much progress in health education and interventions with both the general population and high-risk-groups [32,37] efforts to reach the most marginal and highest risk FSWs remain poor. As this is a cross-sectional design study, the next step for researchers is to design an approach for accessing the hard-to-reach FSWs, as interventional studies needed to examine how to improve healthcare toward this vulnerable population.

Conclusion
The inequality between BSWs and SSWs is significant and quite visible. The Chinese healthcare system has made significant progress on AIDS/STIs-related interventions among high-risk populations, including health education and heightened condom use. However, more particular technical training and instruction on condom usage is need, and evaluation of the efficacy of intervention programs is need.    Knowledge score of STIs symptoms 0-2=0, 3-10=1 (n1=120, n2=170) <0.001¹