Risk behaviours and prevalences of HIV and sexually transmitted infections among female sex workers in various venues in Changzhou,China

Abstract

Female sex workers (FSWs) play an important role in the heterosexual transmission of HIV and sexually transmitted infections (STIs) in China. We conducted a cross-sectional study of 609 FSWs from various venues in Changzhou to investigate risk behaviours and prevalences of HIV and STIs among FSW subgroups. Structured questionnaires were used in face-to-face interviews to collect information. Blood and cervical specimens were collected to test for HIV, syphilis, Neisseria gonorrhoeae (NG) and Chlamydia trachomatis (CT) infections. The overall prevalences of syphilis, NG and CT were 5.6, 2.3 and 17.0%, respectively. The highest prevalence of syphilis (13.8%, P < 0.001) was observed among FSWs in low-class (LC) venues. No case of HIV infection was found. Less than half of all FSWs (40.7%) reported consistent condom use with clients during the last month. A multivariate analysis revealed a 13-fold increased risk for FSWs with NG infection to be infected with syphilis and a four-fold increased risk for FSWs aged 30–39 years to have a CT infection relative to FSWs aged 15–20 years. The prevalences of STIs were high, and risky sexual behaviours were common, especially among FSWs in LC venues. More tailored and comprehensive prevention programmes should be developed for specific FSW subgroups.

Keywords

Female sex worker risk behaviours HIV sexually transmitted infections venues

Introduction

Since the first case of HIV infection was reported in 1985,¹ China has experienced a rising HIV epidemic, with the number of people living with HIV and AIDS increasing from 650,000 in 2005 to 780,000 in 2011.² Additionally, heterosexual contact has become the predominant mode of HIV transmission since 2007, constituting 52.2% of the 48,000 new HIV infections in 2011.² Female sex workers (FSWs) contribute largely to the heterosexual transmission of HIV and other sexually transmitted infections (STIs) in China. A review of studies on FSWs carried out across China between 1996 and 2010 revealed a relatively high HIV prevalence (median: 0.6%) among FSWs compared with the national HIV prevalence of 0.058% and even higher prevalences of a variety of STIs, with syphilis ranging between 0.8 and 12.5% (median: 6.9%), chlamydia ranging between 3.9 and 58.6% (median: 25.7%) and gonorrhoea ranging between 2.0 and 85.4% (median: 16.4%).³ The presence of STIs could facilitate the acquisition and transmission of HIV through sexual contact.^4,5 A megaproject conducted in eight cities of China has suggested the importance of integrating HIV with STI prevention programmes to reduce the incidence of HIV and other STIs among FSWs.^6,7

Jiangsu province, located in the eastern part of China, belongs to the largest economic zone – the Yangtze River Delta. Changzhou, consisting of seven districts, is a city in the south of Jiangsu with a total population of 4.6 million. Of its population, over 1.5 million are migrants, and approximately 80% of the migrants are from rural regions. Commercial sex flourishes in Changzhou, in addition to rapid economic development, residents’ increased disposable income, substantial rural-to-urban migration and evolving notions of sexuality.^8,9 In response, the government has created two national HIV/AIDS sentinel surveillance sites in two districts of Changzhou to monitor the seroprevalence of HIV/syphilis and risk behaviours of FSWs annually. However, the periodic surveillance system does not cover all seven districts, and common STIs such as Neisseria gonorrhoeae (NG) and Chlamydia trachomatis (CT) infections have not been included. Moreover, previous studies have mostly explored FSWs as one group, while it is actually a highly heterogeneous population that includes FSWs from various venues.^10,11 Hence, our study recruited FSWs from all seven districts of Changzhou and categorized them into high, middle and low tiers based on their type of work venue, examining the prevalences of HIV, syphilis, NG and CT infections among the subgroups and exploring factors that were correlated with the infections.

Methods

Study design and participants

From November 2010 to January 2011, a cross-sectional study was conducted in Changzhou, Jiangsu province. To recruit a representative sample of FSWs, sex work venues in the city were mapped and stratified into high, middle and low classes based on the minimum charge in venues. High-class (HC) venues (minimum charge ≥ 300 RMB) referred to hotels, bars and nightclubs; middle-class (MC) venues (minimum charge between 100 and 300 RMB) referred to saunas and karaoke bars and low-class (LC) venues (minimum charge ≤ 100 RMB) referred to bathhouses, roadside hair salons/barber shops, roadside motels and rental houses. Within all seven districts, FSWs were recruited from the three classes of venues located in their areas. Convenience sampling was used to recruit potential participants from each tier of these venues. Eligible participants were females aged 15 years or above, reported providing vaginal, oral or anal sex to male clients for money or goods within the past year and were able to provide informed consent. The study time frame of FSWs’ sexual behaviours with regular partners and non-paying non-regular partners was also within one year. This study was approved by the Medical Ethics Committee of the Chinese Academy of Medical Sciences Institute of Dermatology.

Procedures and measures

With the cooperation of local health supervision institutes, we informed the gatekeepers (e.g. establishment owners, managers or pimps) of selected venues about the purpose of our survey and asked them to help mobilize FSWs in their establishments to participate in the investigation. Participants were assessed for eligibility by trained investigators according to the inclusion criteria. Once eligible subjects were confirmed, they were asked to sign an informed consent form after receiving a brief introduction about the survey. Then, a face-to-face interview using an interviewer-administered structured questionnaire was conducted to collect data on sociodemographic characteristics and risk behaviours within the past year. The sociodemographic characteristics included age, ethnicity, education, marital status and residential status. The behavioural information included sexual partnership, condom use with clients, regular and non-regular non-paying partners and drug use.

After completing a structured questionnaire within 15–20 min, each participant had 5–7 ml venous blood drawn by qualified nurses for HIV and syphilis testing. Cervical swabs were collected for NG and CT testing, except among those who were menstruating. Each participant was assigned a unique identifier for the questionnaire, blood sample and cervical swab. An incentive package of free condoms and HIV/STI prevention pamphlets was provided to every participant for completing the questionnaire. Additionally, 30 RMB (approximately 4.5 U.S. dollars) were provided as compensation for blood and cervical specimens.

Laboratory tests

The blood specimens were tested for HIV and syphilis at local CDC laboratories, while cervical specimens were tested for NG and CT at the National STD Reference Laboratory in Nanjing. Screening for HIV antibodies was performed using an HIV-specific enzyme-linked immunosorbent assay (ELISA) kit (Wantai Biopharmacy Co., Ltd, Beijing, China). Negative results from the ELISA were recorded as HIV-negative, while positive results were confirmed via Western blot (Singapore MP Biopharmacy Asia Pacific Pty Ltd). Positive results from both the ELISA and Western blot were recorded as HIV-positive. Screening for syphilis antibodies was performed using a Treponema pallidum ELISA (Wantai Biopharmacy Co., Ltd, Beijing, China), and positive results were confirmed with a Toluidine Red Unheated Serum Test (TRUST, Rongsheng Biotechnical Company, Shanghai, China). If the results from the TRUST were positive, titres of non-treponemal-specific antibodies were recorded. Syphilis infection was defined as having positive results on both the ELISA and TRUST. Detection of NG and CT was performed with an Amplicor CT/NG polymerase chain reaction (PCR) kit (Roche Diagnostic Co., Ltd., USA), and NG or CT infection was defined as having a positive PCR assay result.

Statistical analysis

Data from the questionnaires and laboratory tests were entered twice into a database using EpiData software (version 3.1) to evaluate congruency, and multiple logic checks were conducted to ensure data quality. All of the data were analysed using SPSS software (version 17.0). Quantitative data that were not normally distributed (e.g. age of FSWs) were compared by the type of work venue using the Mann–Whitney U test. A Chi square test was used to explore the proportional differences of sociodemographic and behavioural characteristics and HIV/STI infections among the FSW subgroups, and Fisher’s exact test was used for the contingency table when more than 20% of the cells had expected counts less than five. The outcome variables were prevalence of HIV, syphilis, NG and CT infection. A univariate logistic regression analysis was performed to assess the association between each independent variable and the outcomes of interest. Variables with a significance level of P < 0.10 in the univariate analysis were included in the multivariate logistic regression analysis using stepwise backward elimination to identify variables that were independently associated with infection. An odds ratio (OR) and adjusted odds ratio (AOR) with 95% confidence intervals (CIs) were determined. A value of P < 0.05 was considered statistically significant.

Results

Sociodemographic characteristics

In total, 609 FSWs were recruited from 113 venues in the seven districts of Changzhou, including 144 (23.6%) FSWs from HC venues, 371 (60.9%) from MC venues and 94 (15.4%) from LC venues. The mean age of all participants was 27.7 years (standard deviation [SD], 7.0; range, 15–56 years), with 57.3% between 20 and 29 years old. The FSWs in LC venues (mean age ± SD, 31.7 ± 8.0) were significantly older than those in MC (28.2 ± 6.8, Z = 4.0, P < 0.001) and HC venues (23.6 ± 4.3, Z = 8.0, P < 0.001). The majority (98.9%) of FSWs were of Han ethnicity, and only 14.9% were local residents. Additionally, 46.5% of FSWs in HC venues had a high school level of education or above, which was significantly higher than that of FSWs in MC (24.0%, χ²= 36.25, P < 0.001) and LC venues (2.1%, χ²= 93.35, P < 0.001) (Table 1). More FSWs (68.1%) in LC venues were currently married, compared with those in MC (53.4%, χ²= 13.88, P = 0.001) and HC venues (19.4%, χ²= 75.43, P < 0.001), but only 34.4% of them were currently living with their husbands.

Table 1.

Sociodemographic characteristics of female sex workers in different classes of venues in Changzhou, Jiangsu Province, China (n = 609).

Characteristics^a	High-class venues (N = 144)	Middle-class venues (N = 371)	Low-class venues (N = 94)	χ ²	P value
Age group (years)				78.10	<0.001
15–19	14 (9.7)	22 (5.9)	7 (7.4)
20–29	116 (80.6)	203 (54.7)	30 (31.9)
30–39	13 (9.0)	122 (32.9)	41 (43.6)
≥40	1 (0.7)	24 (6.5)	16 (17.1)
Ethnicity				–	0.48^b
Han	141 (97.9)	368 (99.2)	93 (98.9)
Other	3 (2.1)	3 (0.8)	1 (1.1)
Education				103.99	<0.001
Primary school or below	4 (2.8)	68 (18.3)	44 (46.8)
Middle school	73 (50.7)	214 (57.7)	48 (51.1)
High school or above	67 (46.5)	89 (24.0)	2 (2.1)
Marital status				88.11	<0.001
Currently married	28 (19.4)	198 (53.4)	64 (68.1)
Divorced/widowed	2 (1.4)	17 (4.6)	9 (9.6)
Never married	114 (79.2)	156 (42.0)	21 (22.3)
Living with				68.46	<0.001
None	49 (34.0)	148 (39.9)	43 (45.7)
Spouse	15 (10.4)	122 (32.9)	22 (23.4)
Boyfriend	39 (27.1)	46 (12.4)	4 (4.3)
Family members	5 (3.5)	20 (5.4)	3 (3.2)
Others	36 (25.0)	35 (9.4)	22 (23.4)
Residential status				10.87	0.03
Changzhou city	15 (10.4)	64 (17.3)	12 (12.8)
Other cities of Jiangsu Province	46 (31.9)	73 (19.7)	23 (24.5)
Other Provinces	83 (57.6)	234 (63.1)	59 (62.8)
Venues				–	–
Hotel/restaurant	29 (20.1)	–	–
Sauna/bathhouse	–	242 (65.2)	53 (56.4)
Nightclub	34 (23.6)	–	–
KTV/bar	81 (56.3)	129 (34.8)	–
Roadside hair salon/barber shop	–	–	3 (3.2)
Roadside motel/rental house	–	–	38 (40.4)

Values are given as number (percentage).

Tested by Fisher’s exact test.

Risk behaviours

Less than half of all FSWs (40.7%) reported consistent condom use with clients during the last month. Fewer FSWs (57.8%) in HC venues reported condom use with clients during the last commercial sex act, compared with those in MC (76.0%, χ²= 15.85, P < 0.001) and LC venues (75.5%, χ²= 7.69, P = 0.006). Similarly, FSWs in HC venues (30.4%) least frequently reported consistent condom use with clients in the past month, followed by 36.2% of FSWs in LC venues (χ²= 2.70, P = 0.26) and 45.6% of FSWs in MC venues (χ²= 9.48, P = 0.01). Among FSWs who had regular partners, only 22.5% (120/533) had used a condom with their boyfriend or spouse during the last intercourse, and the proportion was lowest (6.0%) among FSWs in LC venues. Nearly half of all FSWs had non-paying non-regular partners, with whom 143 FSWs (51.1%) had used a condom during the last intercourse, and FSWs in LC venues also least commonly reported condom use (26.9%). Furthermore, 1.0% (6/603) of respondents admitted having used illicit drugs in the past year, and the main types of drugs used were methamphetamines, ketamine and ecstasy. None of the respondents reported injecting drugs in the past six months (Table 2).

Table 2.

Risk behaviours and prevalences of syphilis, NG and CT infections among female sex workers in different classes of venues in Changzhou.

Characteristics^a	High-class venues	Middle-class venues	Low-class venues	χ²	P value
Condom use with client at last sex	135	366	94	16.87	<0.001
Yes	78 (57.8)	278 (76.0)	71 (75.5)
No	57 (42.2)	88 (24.0)	23 (24.5)
Frequency of condom use with clients in the past month	135	366	94	13.14	0.01
Never	15 (11.1)	33 (9.0)	5 (5.3)
Sometimes	79 (58.5)	166 (45.4)	55 (58.5)
Always	41 (30.4)	167 (45.6)	34 (36.2)
Do you have regular partners (spouse or boyfriend)	141	368	94	34.26	<0.001
Yes	124 (87.9)	342 (92.9)	67 (71.3)
No	17 (12.1)	26 (7.1)	27 (28.7)
Condom use with regular partners at last sex	124	342	67	12.10	0.002
Yes	32 (25.8)	84 (24.6)	4 (6.0)
No	92 (74.2)	258 (75.4)	63 (94.0)
Do you have non-paying non-regular partners	138	366	94	17.28	<0.001
Yes	65 (47.1)	189 (51.6)	26 (27.7)
No	73 (52.9)	177 (48.4)	68 (72.3)
Condom use with non-paying non-regular partners at last sex	65	189	26	13.10	0.001
Yes	26 (40.0)	110 (58.2)	7 (26.9)
No	39 (60.0)	79 (41.8)	19 (73.1)
Ever used illicit drugs in the past year	142	369	92	–	0.85^b
Yes	1 (0.7)	5 (1.4)	0 (0)
No	141 (99.3)	364 (98.6)	92 (100)
Syphilis infections	142	370	94	19.12	<0.001
Yes	11 (7.7)	10 (2.7)	13 (13.8)
No	131 (92.3)	360 (97.3)	81 (86.2)
NG infections	79	290	67	–	0.50^b
Yes	1 (1.3)	6 (2.1)	3 (4.5)
No	78 (98.7)	284 (97.9)	64 (95.5)
CT infections	79	290	67	2.11	0.35
Yes	17 (21.5)	44 (15.2)	13 (19.4)
No	62 (78.5)	246 (84.8)	54 (80.6)

CT: Chlamydia trachomatis; NG: Neisseria gonorrhoeae.

Values are given as number (percentage).

Tested by Fisher’s exact test.

Prevalences of HIV and STIs

In total, 606 (99.5%) blood specimens and 436 (71.6%) cervical specimens were collected. No case of HIV infection was found. The overall prevalence of syphilis was 5.6% and was highest among FSWs in LC venues (13.8%, P < 0.001), followed by 7.7% of FSWs in HC venues and 2.7% of FSWs in MC venues (Table 2). The overall prevalences of NG and CT were 2.3 and 17.0%, respectively, but no statistically significant differences in the prevalences of NG and CT infections between FSW subgroups were observed.

Factors associated with STIs

In the univariate analysis, variables related to syphilis infection included LC venues (OR: 3.75; 95% CI: 1.81–7.79, P < 0.001); low education (OR:3.11; 95% CI: 1.31–7.37, compared with middle school level of education, P < 0.05) and NG infection (OR: 5.04, 95% CI: 1.00–25.28, P < 0.05). Moreover, FSWs infected with syphilis seemed to have a greater risk of being infected with NG (OR: 5.04, 95% CI: 1.00–25.28, P < 0.05). Compared to FSWs aged 15–20 years, FSWs in older age groups were more likely to be infected with CT (30–39 age group, OR: 4.25; 95% CI: 1.65–10.95, P < 0.01). In the multivariate analysis (Table 3), the factor that was independently associated with syphilis infection was NG infection (AOR: 13.87, 95% CI: 1.22–157.63, P < 0.05); additionally, CT infection was significantly related to older age when older FSWs were compared with FSWs aged 15–20 years (30–39 age group, AOR: 4.25; 95% CI: 1.65–10.95, P < 0.01).

Table 3.

Factors independently associated with infections of syphilis, NG and CT by multivariate analysis among female sex workers in Changzhou.

	Syphilis infection		NG infection		CT infection
Factors	AOR (95%CI)	P value	AOR (95%CI)	P value	AOR (95%CI)	P value
Age group (years)		–		–		0.02
15–19	–	–	–	–	1.0 (Reference)	–
20–29	–	–	–	–	2.08 (0.92–4.72)	0.08
30–39	–	–	–	–	4.25 (1.65–10.95)	0.003
≥40	–	–	–	–	2.29 (0.67–7.76)	0.19
NG infection		0.03		–		–
Yes	13.87 (1.22–157.63)	–	–	–	–	–
No	1.0 (Reference)		–	–	–	–

AOR: adjusted odds ratio; CI: confidence interval; CT: Chlamydia trachomatis; NG: Neisseria gonorrhoeae.

Discussion

In China, FSWs have become a high-risk population for the acquisition and transmission of HIV and other STIs. Our study found significant differences in sociodemographic characteristics, risk behaviours and prevalence of HIV/STIs among the FSW subgroups. FSWs from LC venues were older, less educated and typically married. The majority of FSWs (85.1%) were migrants from other regions, which reflected the finding that over half of the currently married FSWs were not living with their spouses. On the one hand, most FSWs were inclined to move away from their hometowns to more developed cities for a higher income.¹² On the other hand, they wanted to conceal the fact that they were sex workers from their husbands and other family members by living apart.¹³ FSWs usually had multiple partners, including their clients, regular partners and non-paying non-regular partners. In our study, approximately half of the FSWs had non-paying non-regular partners. Clients could also be FSWs’ non-paying non-regular partners. They became ‘good friends’ and met each other after work once in a while to have non-paying sex.

In contrast to previous studies,^14,15 our study showed that FSWs in HC rather than LC venues least commonly reported consistent condom use with clients. A possible explanation for this result was that clients of HC venues were usually wealthy and preferred to pay more money for sex without a condom. Most FSWs did not refuse this economic incentive. A qualitative study in China revealed that one FSW earned double her regular earnings when she forewent using a condom.¹⁶ Nevertheless, FSWs tended to assess risk based on their own assumptions and the appearance of the client.¹⁶ Most clients of HC venues were wealthy, well educated and neatly dressed. Hence, FSWs believed that they were ‘clean’ and ‘safe’ and were more inclined to have sex with them without a condom.^17,18 Further research is needed to explore FSWs’ condom use with clients in HC venues.

Consistent with previous literature, condom use among FSWs was less frequent with regular partners than with clients. The proportion of all FSWs who reported condom use with clients at last intercourse was three times greater than their reported condom use with regular partners. This phenomenon was even more apparent among FSWs in LC venues, with 75.5% reporting condom use with clients and only 6.0% reporting condom use with regular partners. ‘Trust in each other’ was reported to be the main reason that FSWs did not use condoms with their regular partners.^19,20 They were familiar with each other, felt ‘safe’ when having sex and thought condom use would reduce intimacy.^16,19 For married FSWs in LC venues, it was even more difficult to initiate condom use with their husbands because most husbands did not like to use condoms and because condom use was perceived as a sign of distrust and unfaithfulness in marriage.^16,21 The proportion of FSWs using a condom with non-paying non-regular partners (51.5%) at last intercourse was between 22.5% with regular partners and 71.8% with clients. This reflected a compromised risk perception when having sex with non-paying non-regular partners. Therefore, future condom promotion programmes should focus on FSWs’ condom use not only with clients but also with regular and non-regular non-paying partners.

The proportion of FSWs (1.0%) who reported using illicit drugs in the past year in the study area was much lower than that of FSWs (5.1–23.6%) in a number of other cities in China.^6,22,23 Methamphetamines, ketamine and ecstasy, also referred to as club drugs,²⁴ were the main types of drugs used by FSWs in our study. In fact, China has seen an increase in the use of club drugs among FSWs in many regions.^25–27 The use of drugs before or during commercial sex could impair FSWs’ judgement²⁸ and ability to negotiate safe sex with clients,^29,30 leading to a greater risk for HIV/STI transmission between FSWs and their clients.^25,31 Therefore, control and prevention of drug use should be addressed in future intervention programmes for the purposes of helping FSWs realize the harms and risks of drug use altering their risky behaviour.

No case of HIV infection was found, which confirmed the low prevalence of HIV among FSWs in Changzhou. In fact, while the HIV prevalence was consistently low among FSWs in most regions of China, it was higher than 1% in specific regions such as Yunnan, Xinjiang, Guangxi, Sichuan and Guizhou provinces in the south and southwest, where drug abuse, especially injection drug use, was common.² The overlap between commercial sex and drug use exacerbated the HIV epidemic in those areas.^2,3,32 Only 1.0% of participants in our study reported using drugs in the past year, which could be the main factor contributing to the low HIV prevalence among FSWs in Changzhou.

However, our study revealed a prevalence of syphilis at 5.6%, NG at 2.3% and CT at 17.0%. The prevalences of STIs varied among FSWs in different classes of venues, showing a higher prevalence of syphilis, NG and CT infections among FSWs in LC venues. FSWs in LC venues were older, which to some extent suggested a longer duration of sex work.^7,33 The multivariate analysis indicated a fourfold increased risk for FSWs aged 30–39 years to have a CT infection relative to FSWs aged 15–20 years. In addition, older FSWs usually earned less, thus needing to serve more clients and have more frequent sex.^4,32 They also could have had less access to health care services.¹⁴ All of these factors led to a higher risk of STIs among FSWs in LC venues. The multivariate analysis also showed a 13-fold increased risk for FSWs with NG infection to be infected with syphilis. This was in accordance with the fact that the presence of any type of STI could enhance the risk for other STIs and HIV infection through unprotected sexual contact.^14,34 Hence, periodic screening and prompt treatment for STIs should be emphasized in future HIV intervention programmes, especially among FSWs in LC venues.

Our study was subject to several limitations. First, convenience sampling was used to recruit FSWs from different classes of venues, resulting in compromised representativeness of the sample for the target population. Any generalization of the results from this study should be made with caution. Second, information on risk behaviours was self-reported in the face-to-face interview; thus, self-report bias and social desirability bias may exist. For example, considering the illegality of drug use in China and the protection of personal privacy, the FSWs might have underreported their use of illicit drugs. Third, due to the limited time and the length of the questionnaire, some information on sexual behaviours, such as average number of clients per week and duration of sex work, was not included in the interview.

In conclusion, FSWs in different classes of venues varied in terms of sociodemographic characteristics, risk behaviours and STI prevalence. While HIV prevalence was low among FSWs in Changzhou, the prevalences of other STIs such as syphilis, NG and CT infections were relatively high, and risky sexual behaviours were common, especially among FSWs in LC venues. Therefore, more tailored and comprehensive intervention programmes, including knowledge dissemination and education; condom distribution and promotion; control and prevention of drug use; and screening, counselling and treatment for STIs, need to be developed.

Footnotes

Acknowledgements

The authors thank all the staff for their hard work and all the participants for their time and trust. We also greatly appreciate the support from owners, managers and mommies of venues, and local health supervision institutes in the coordination, mobilization and implementation of the survey.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the Mega Project of China National Science Research for the 11th Five-Year Plan (2008ZX10001-005) from China Ministry of Health and the Ministry of Sciences and Technology.

References

Wang

. Overview of the HIV/AIDS epidemic, scientific research and government responses in China. AIDS 2007; 21: S3–S7.

China Ministry of Health (CMOH), Joint United Nations Programme on HIV/AIDS (UNAIDS), and World Health Organization (WHO). 2011 estimates of HIV/AIDS epidemic in China, Beijing, 2011.

Poon

Wang

et al.

Review of HIV and other sexually transmitted infections among female sex workers in China. AIDS Care 2011; 23: 5–25.

Ruan

Cao

Qian

et al.

Syphilis among female sex workers in southwestern China: potential for HIV transmission. Sex Transm Dis 2006; 33: 719–723.

Galvin

Cohen

. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2004; 2: 33–42.

Wang

Yin

et al.

The effect of a structural intervention for syphilis control among 3597 female sex workers: a demonstration study in South China. J Infect Dis 2012; 206: 907–914.

Chen

Yin

Liang

et al.

The prevalences of Neisseria gonorrhoeae and Chlamydia trachomatis infections among female sex workers in China. BMC Public Health 2013; 13: 121–121.

Hong

. Behavioral studies of female sex workers in China: a literature review and recommendation for future research. AIDS Behav 2008; 12: 623–636.

Yang

Xia

. Gender, migration, risky sex, and HIV infection in China. Stud Fam Plann 2006; 37: 241–250.

10.

Ramesh

Moses

Washington

et al.

Determinants of HIV prevalence among female sex workers in four south Indian states: analysis of cross-sectional surveys in twenty-three districts. AIDS 2008; 22: S35–S44.

11.

Chen

Merli

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.

12.

Wang

Chen

Sharp

et al.

Mobility, risk behavior and HIV/STI rates among female sex workers in Kaiyuan City, Yunnan Province, China. BMC Infect Dis 2010; 10: 198–198.

13.

Hong

Yang

et al.

HIV/AIDS-related sexual risks and migratory status among female sex workers in a rural Chinese county. AIDS Care 2009; 21: 212–220.

14.

Jin

Chan

Ding

et al.

Prevalence and risk behaviours for Chlamydia trachomatis and Neisseria gonorrhoeae infection among female sex workers in an HIV/AIDS high-risk area. Int J STD AIDS 2011; 22: 80–84.

15.

Stanton

et al.

A multilevel analysis of gatekeeper characteristics and consistent condom use among establishment-based female sex workers in Guangxi, China. Sex Transm Dis 2010; 37: 700–705.

16.

Zhou

et al.

A qualitative exploration of barriers to condom use among female sex workers in China. PLoS One 2012; 7: e46786–e46786.

17.

Cai

Shi

Shen

et al.

A study of HIV/AIDS related knowledge, attitude and behaviors among female sex workers in Shanghai China. BMC Public Health 2010; 10: 377–377.

18.

Ghimire

Smith

van Teijlingen

et al.

Reasons for non- use of condoms and self-efficacy among female sex workers: a qualitative study in Nepal. BMC Women’s Health 2011; 11: 42–42.

19.

Parriault

Basurko

Melle

et al.

Predictive factors of unprotected sex for female sex workers: first study in French Guiana, the French territory with the highest HIV prevalence. Int J STD AIDS 2015; 26: 542–548.

20.

Voeten

Egesah

Varkevisser

et al.

Female sex workers and unsafe sex in urban and rural Nyanza, Kenya: regular partners may contribute more to HIV transmission than clients. Trop Med Int Health 2007; 12: 174–182.

21.

Lau

Tsui

Siah

et al.

A study on female sex workers in southern China (Shenzhen): HIV-related knowledge, condom use and STD history. AIDS Care 2002; 14: 219–233.

22.

Yao

Yang

Chu

et al.

Associations between drug use and risk behaviours for HIV and sexually transmitted infections among female sex workers in Yunnan, China. Int J STD AIDS 2012; 23: 698–703.

23.

Fan

Liu

Zhang

et al.

HIV, other sexually transmitted infections, and risk behaviors among female sex workers in Liuzhou, China. Int J Gynecol Obstet 2015; 128: 18–22.

24.

Colfax

Guzman

. Club drugs and HIV infection: a review. Clin Infect Dis 2006; 42: 1463–1469.

25.

Liao

Jiang

Zhang

et al.

Syphilis and methamphetamine use among female sex workers in Shandong Province, China. Sex Transm Dis 2011; 38: 57–62.

26.

Laidler

. The rise of club drugs in a heroin society: the case of Hong Kong. Subst Use Misuse 2005; 40: 1257–1278.

27.

Wang

Brown

Wang

et al.

Knowledge of HIV seropositivity is a predictor for initiation of illicit drug use: incidence of drug use initiation among female sex workers in a high HIV-prevalence area of China. Drug Alcohol Depend 2011; 117: 226–232.

28.

Corsi

Booth

. HIV sex risk behaviors among heterosexual methamphetamine users: literature review from 2000 to present. Curr Drug Abuse Rev 2008; 1: 292–296.

29.

Loza

Patterson

Rusch

et al.

Drug-related behaviors independently associated with syphilis infection among female sex workers in two Mexico-US border cities. Addiction 2010; 105: 1448–1456.

30.

Lau

JTF

Zhang

et al.

Comparing prevalence of condom use among 15,379 female sex workers injecting or not injecting drugs in China. Sex Transm Dis 2007; 34: 908–916.

31.

Couture

Evans

Sothy

et al.

Correlates of amphetamine-type stimulant use and associations with HIV-related risks among young women engaged in sex work in Phnom Penh, Cambodia. Drug Alcohol Depend 2012; 120: 119–126.

32.

Wang

Chen

Ding

et al.

Prevalence and predictors of HIV infection among female sex workers in Kaiyuan City, Yunnan Province, China. Int J Infect Dis 2009; 13: 162–169.

33.

Wang

Smith

Brown

et al.

Prevalence, incidence, and persistence of syphilis infection in female sex workers in a Chinese province. Epidemiol Infect 2011; 139: 1401–1409.

34.

Reynolds

Risbud

Shepherd

et al.

High rates of syphilis among STI patients are contributing to the spread of HIV-1 in India. Sex Transm Infect 2006; 82: 121–126.