Objectives: To explore and evaluate a sexually transmitted disease (STD)/HIV intervention program targeting female sex workers working in entertainment establishments in five different settings in China.
Design and method: A prospective, community-based, pre/post, intervention trial set in entertainment establishments (karaoke bars, massage parlours, dance halls, beauty parlours) where sex workers operate at sites in five provinces of China: Anhui, Beijing, Fujian, Guangxi and Xinjiang. The participants were all sex workers working in targeted entertainment establishments. A Women's Health Clinic was set up near participants' places of work at each site. Clinic-based outreach activities, including awareness-raising, condom promotion, and sexual health care, were developed and delivered to sex workers. Cross-sectional surveys at baseline and post-intervention were used to evaluate changes in condom use with the last three clients, and the prevalence of chlamydia and gonorrhoea.
Results: In total, 907 sex workers were surveyed at baseline and 782 at 12 months post-intervention. Outreach teams made 2552 visits to the target entertainment establishments, approached 13 785 female sex workers, and distributed 33 575 copies of education material and 5102 packets of condoms. The rate of condom use with the most recent three clients increased from 55.2% at baseline to 67.5% at 12 months evaluation. The prevalence of gonorrhoea fell from 26% at baseline to 4% after intervention, and that of chlamydia fell from about 41 to 26%.
Conclusion: The intervention was effective for increasing condom use and reducing STD among sex workers. The results were used to develop national guidelines on sex worker interventions for nationwide scale up.
From the aNational Center for AIDS/STD Control and Prevention, Chinese Center for Diseases Control and Prevention, Beijing, China
bXinjiang Center for Diseases Control and Prevention, Xinjiang, China
cFujian Center for Diseases Control and Prevention, Fujian, China
dFuyang Center for Diseases Control and Prevention, Fuyang, China
eGuangxi Center for Diseases Control and Prevention, Guangxi, China
fBeijing Shijingshan Institute for STD Control, Beijing, China
gNational STD Reference Laboratory, Nanjing City, Jiangsu, China.
Correspondence to Zunyou Wu, MD, PhD, Director, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 27 Nanwei Road, Beijing 100050, China. E-mail: firstname.lastname@example.org or email@example.com or firstname.lastname@example.org
Although China managed to virtually eliminate prostitution in the 1950s, since the country reopened its doors to the West in the late 1970s there has been a rapid resurgence of the sex work industry [1,2]. Sex workers are an important reservoir for sexually transmitted diseases (STD), including HIV . Among sex workers in re-education centres in Sichuan, for example, 48.8% of inmates had an STD, the most common being gonorrhoea, found in 20.4% of participants . Lower rates have been more commonly reported. For example in Henan, 20% of sex workers in a community sample reported ever having had an STD , in Guangxi 21% had a STD history and at a Shenzhen re-education centre, this figure was 14.5% . Chlamydia and gonorrhoea are the most commonly reported STD, but trichomoniasis, syphilis, herpes and genital warts are also prevalent. Rates of HIV are generally lower than for other STD; however, sex workers who are also drug users are at greatest risk; drug use has been an important risk factor for HIV infection among sex workers to date .
In China, sex workers generally operate in karaoke bars, dance halls, hotels, massage parlours, saunas, hair and beauty salons, and some solicit clients from the street or in parks [3,6,8,9]. While many sex workers are unmarried, a significant proportion are engaged in relationships or have sex partners who are not paying clients [3,10]. They frequently work outside their home towns, so their husbands or boyfriends in their home towns may be unaware of their sources of income; male partners may implicitly trust that their wives/girlfriends are not having unprotected sex with anyone else, making it difficult for the sex workers or former sex workers to initiate condom use with them [11,12]. In general, condom use is low with steady partners, but higher with clients, especially new clients [5,6,8,13–15]. Consistent condom use with clients among sex workers in entertainment establishments has been reported to range from close to 50% in Fujian  to 30.1% in Guangdong  and to 17% in Guangxi .
The reasons cited for not using condoms with clients include refusal by clients, availability, expense, embarrassment, faster sex, ability to charge a higher fee, not wishing to be suspected of having a disease, and loss of clients [5,6,8,11,12]. Owners of the establishments out of which the girls work may also be unsupportive [11,16]. In many cases, the women are simply unaware of the risk; the majority are young, from rural areas and with limited education, particularly about sex, which is not taught in schools, and some have sex for the first time while working [8,11,12]. Myths surrounding STD and prevention of infection are easily propagated. Complementary or alternative prevention methods may be used to prevent infection or pregnancy, including douching, frequent use of antibiotics, or judging a client's ‘cleanness’ [11,12,17].
Programs that promote the use of condoms among sex workers and include education about and testing for, STD have demonstrated their efficacy to reduce HIV and STD transmission, most notably in Thailand  and Zaire . Condom use to control the spread of HIV and other STDs in China has been officially promoted since 1998 , but the degree of active promotion varies between provinces, depending on the attitude of the local government and the severity of the local STD/HIV epidemic. There is an urgent need to develop effective, feasible and sustainable interventions that can be supported with local resources. Such interventions can then be promoted on a large scale in China, thereby having a significant impact on the STD and HIV epidemics. This study reports on a demonstration intervention project that was conducted in five sites in Anhui, Beijing, Fujian, Guangxi and Xinjiang.
Participants and methods
Five sites in two provinces, one municipality, and two autonomous regions were chosen for the intervention. These were the downtown areas of Fuyang prefecture in Anhui province, Shijingshan district in the Beijing municipality, Huian county in Fuzhou province, Beihai city in Guangxi Zhuang Autonomous Region and Hami city in Xinjiang Uygur Autonomous Region (Fig. 1). The predominant routes of HIV infection vary in these venues (Fig. 1).
Mapping of all entertainment establishments and drug stores in each site was conducted before the pre-baseline survey, before the implementation of the intervention and again before the final evaluation survey. The number of venues in each site at pre-baseline is shown in Fig. 1.
A qualitative study was conducted before the baseline survey to gather background information about the five sites. The study used in-depth interviews with sex workers and establishment owners to collect information about condom use, preferences for using private/public clinics and pharmacies, how clients are introduced to sex workers, and their thoughts on how and when the intervention should be conducted. Five to six sex workers and three establishment owners were interviewed privately in each site. Two focus group discussions were held in each site, one each for sex workers and establishment owners. This information was used to inform the development of the intervention materials.
Special sexually transmitted disease clinics and outreach program
Based on inputs from sex workers in the qualitative study, each site selected one clinic to support the project: a ‘Women's Health Clinic and Counselling Service’. The five clinics provided sexual health care services, including counselling to women, and sex workers and were equipped with simple laboratory equipment (e.g., a microscope and stains) to perform STD tests. Clinicians were trained in the diagnosis, treatment and management of STD, on appropriate attitudes towards sex workers and in counselling. Each clinic also had one to two outreach teams with two members who visited targeted establishments every afternoon. Coupons that offered discounts for clinic services were developed and distributed to sex workers to encourage them to actively seek check-ups for the early diagnosis and treatment of STD. Coupons were given to sex workers by outreach workers and to sex workers who visited the clinic.
Four video compact discs (VCD) discussing basic sexual health, reproductive health, STD and their prevention, and HIV/AIDS prevention were provided to the clinics to play in their waiting rooms. Four educational flyers were printed and distributed: two specifically for sex workers and two for the general public. Five cartoon educational folders about HIV/AIDS, condom use and STD were developed and distributed: two targeting female sex workers and three for the general public including sex workers. Two more cartoon educational folders were developed during the implementation of the trial: one which focused on knowledge about pregnancy and contraception, and another which focused on health seeking behaviours. These two educational folders were developed based on feedback generated from supervision visits to the sites.
Prior to the trial, condoms used by female sex workers were usually purchased by themselves from local pharmacies and clinics. From April 2000, outreach staff began promoting 100% condom use among sex workers by initially distributing free condoms, followed later by the direct sale of condoms at discounted prices.
A baseline cross-sectional survey was carried out in late February and early March 2000. All sex workers in each venue included in the trial were invited to participate. Participants were interviewed anonymously using an interviewer-administrated questionnaire and informed consent was obtained before interview. The questionnaire collected data on demographic characteristics, sexual practices, condom use, drug use, HIV/AIDS knowledge, contact with and knowledge about the project, and clinic attendance and opinion of the services provided.
All sex workers participating in the surveys were tested for chlamydia and gonorrhoea. Vaginal swabs were collected from subjects for laboratory test of STD. Chlamydia and gonorrhoea testing, using polymerase chain reaction (PCR) (Roche, Branchburg, New Jersey, USA), were performed in the National STD Reference Laboratory in Nanjing. This laboratory participated in a NIH/NIMH (US National Institute of Health, National Institute of Mental Health) supported five country STD/HIV prevention trial and was responsible for testing chlamydia and gonorrhoea, and for quality control of other STD tests in local laboratories . Rates were calculated as prevalence. HIV was not tested because national surveillance data at the time indicated a lower than 0.5% prevalence rate among SW.
A second cross-sectional survey was conducted after the intervention, between October and November 2001, which used the same questionnaire and collected bio-specimens in the same way. Differences in the demographic characteristics, condom use behaviours and STD prevalence were compared pre- and post-intervention, using chi-squared tests for categorical variables and t-tests for continuous variables. All analyses were done using Stata™ V6 (StataCorp, College Station, Texas, USA).
The study was approved by the Ethical Review Committee (i.e. Institute Review Board) in the Chinese Academy of Preventive Medicine (the Institute was re-organised as China Center for Disease Control and Prevention in 2002).
During the intervention, project staff made 2552 visits to targeted entertainment establishments, approached 13 785 female sex workers, distributed 33 575 copies of the educational materials and 5102 packets of three condoms, and provided 4128 check-ups and treatment for sex workers at the Women's Health Clinics. Between July and September 2000, there was a nationwide campaign to enforce strict disciplinary action against organized prostitution. As a result, the organization of the sex industry changed and became more individual entrepreneur-oriented; namely sex workers coordinated by a pimp or establishment owner using a paging service. This change made outreach more difficult.
Nine hundred and seven sex workers participated in the baseline survey (154 in Fujian, 207 in Guangxi, 167 in Beijing, 180 in Anhui, and 199 in Xinjiang) and 782 sex workers participated in the final evaluation survey (139 in Fujian, 203 in Guangxi, 160 in Beijing, 97 in Anhui, and 183 in Xinjiang). The demographic characteristics, in terms of residency, age group, education level and marital status, were similar in baseline and in final evaluation surveys (Table 1). Most sex workers (76.3% at baseline and 79.6% at follow-up) were from outside of the province (P = 0.11); 70.7 and 67.9% were younger than 25 years old (P = 0.21); 67.8 and 68.9% did not finish senior high school (P = 0.65); 25.4 and 29.4% were married; and 66.5 and 64.6% were never married (P = 0.10).
Knowledge about AIDS
Participants answered an average of 34.7% of HIV/AIDS knowledge questions correctly at baseline which increased to 79.8% at follow-up (P < 0.001). The percentage of correct answers for all individual questions increased, without exception (Table 2).
Sexual practices and condom use
Changes in risky sexual behaviour are described in Table 3. Significant changes were observed for the number of sex workers using condoms in the most recent sexual intercourse (from 55.2% at baseline to 67.5% at follow-up; P < 0.001), and the number agreeing to sex without a condom for higher payment (40.4 to 21.2%, P < 0.001). Changes were also observed for the types of non-client sex partners; reasons for using condoms and where participants bought condoms (see Table 3).
Sexually transmitted diseases
At baseline, 53.2% of sex workers reported a history of STD, and this figure was similar at follow-up (48.0%; P = 0.80). Among study participants, 827 out of 907 at baseline survey and 724 out of 782 at evaluation survey provided vaginal swabs for laboratory STD tests. Biological testing indicated that over the course of the intervention, the prevalence of each type of STD had decreased. The overall prevalence of gonorrhoea fell from about 26% at baseline to 4% after intervention, and the prevalence of chlamydia fell from about 41 to 26%.
Health seeking behaviours
The number of sex workers seeking monthly check-ups increased from 18.0% at baseline to 26.3% at follow-up (P < 0.001). However, the number seeking 2-monthly checkups reduced from 5.0 to 2.5%. (P = 0.016); the number seeking weekly checkups was also reduced, from 8.1 to 2.5% (P < 0.001); and the number never getting checkups remained similar, at 8.1 and 9.8% (P = 0.195).
At baseline, 53.0% of sex workers had had an abortion and at follow-up this was 57.9% (P = 0.044). At follow-up 17.0% of women had had an abortion in the most recent 3 months compared with 11.2% at baseline (P < 0.001).
At baseline, 18 of the sex workers reported a history of drug use (2%), while in the final survey, six reported drug use (0.8%; P = 0.035).
Six hundred and twenty-five (80.0%) sex workers reported that they knew about the Women's Health Clinic. Among those who knew about the clinics, 34% (215) had attended. Among attendees, 45.9% thought the attitude of doctors was great; 45.9% thought the quality of services were good; and 11.5% commented that the clinics were good because they provided additional counselling services and were conveniently located. However, when asked where they would prefer to go for treatment, only 12.1% of women in study sites would go to the Women's Health Clinic.
At follow-up, 72.6% of sex workers had been in touch with outreach teams and 87% reported that an outreach team had visited their establishment. Eighty-two percent had received educational materials (33% once, 19% twice and 26% at least three times), and 55% reported receiving condoms from the outreach team (28.9% once, 12% twice and 13.7% at least three times)
This trial demonstrated the efficacy of a behavioural intervention among sex workers in five sites to increase HIV/STD knowledge, condom use and health-seeking behaviours, and to reduce STD. Although HIV/STD knowledge was significantly improved for all items, many sex workers continued to hold misconceptions about HIV and STD after the intervention. Most notably, fewer than half were able to distinguish the difference between HIV infection and AIDS and 65% continued to believe mosquitoes could transmit HIV. In contrast, four of the top five questions showing the greatest improvement in knowledge were related to reproductive health (questions 7, 10, 11 and 12). Moreover, the number of women reporting they used condoms to prevent disease increased, while the number using them only for contraception decreased. These data suggest that linking sexual and reproductive health education may be an important strategy for maintaining the interest of the target audience. This has already been demonstrated elsewhere in China  where women showed much greater interest in learning about how to prevent HIV/STD when they realised infection could affect their fertility.
As shown in Table 3, the numbers of women reporting condom use at last sex, and once or twice in the last three episodes improved significantly, but the improvements in consistent condom use (three out of three times) were not statistically significant. Condom use with the main sex partner increased, but this was not statistically significant and remained at < 30%. It appears that although sex workers can be convinced to use condoms with clients, it is more difficult for them to initiate condom use with non-paying partners.
Based on its demonstrated efficacy in these areas, the model was used to inform the development of national guidelines for conducting interventions among sex workers. Current figures for HIV/STD demonstrate the need for further scale up of these interventions among high risk groups, particularly sex workers. For example, in 2005 gonorrhoea and syphilis were the fourth and fifth most common diseases reported to the Ministry of Health and AIDS was the third biggest killer among reportable, infectious diseases . At the end of the same year, it was estimated that approximately 127 000 commercial sex workers and their clients were living with HIV/AIDS, accounting for 19.7% of total HIV infections . The government reiterated the call for interventions among this group in the 2006 Regulations on AIDS Prevention and Treatment  and in their associated five-year plan  that promotes the availability of condoms in establishments where sex workers operate.
We examined the efficacy of an intervention to promote condom use and increase HIV/STD knowledge among sex workers. The programme was successful at increasing condom use and reducing the prevalence of STD amongst the sex workers surveyed. The results were used to inform the development of national guidelines that are in current use in China.
Sponsorship: This project was supported by the World AIDS Foundation grant number WAF 195(99-011). The Preparation of the manuscript was supported by the China Multidisciplinary AIDS Prevention Training Program with NIH Research Grant # U2R TW06918 funded by the Fogarty International Center, National Institute on Drug Abuse, and the National Institute of Mental Health.
1. Zou K. The “Re-education Through Labour” system in China's legal reform. Criminal Law Forum 2002; 12:459–485.
2. Cohen MS, Henderson GE, Aiello P, Zheng H. Successful eradication of sexually transmitted diseases in the People's Republic of China: implications for the 21st century. J Infect Dis 1996; 174(Suppl 2):S223–S229.
3. Gil VE, Wang MS, Anderson AF, Lin GM, Wu ZO. Prostitutes, prostitution and STD/HIV transmission in mainland China. Soc Sci Med 1996; 42:141–152.
4. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2004; 2:33–42.
5. Ding Y, Detels R, Zhao Z, Zhu Y, Zhu G, Zhang B, et al
. HIV infection and sexually transmitted diseases in female commercial sex workers in China. J Acquir Immune Defic Syndr 2005; 38:314–319.
6. Lau JT, Tsui HY, Siah PC, Zhang KL. A study on female sex workers in southern China (Shenzhen): HIV-related knowledge, condom use and STD history. AIDS Care 2002; 14:219–233.
7. Chen XS, Yin YP, Liang GJ, Gong XD, Li HS, Poumerol G, et al
. Sexually transmitted infections among female sex workers in Yunnan, China. AIDS Patient Care STDS 2005; 19:853–860.
8. Qu S, Liu W, Choi KH, Li R, Jiang D, Zhou Y, et al
. The potential for rapid sexual transmission of HIV in China: sexually transmitted diseases and condom failure highly prevalent among female sex workers. AIDS Behav 2002; 6:267–275.
9. van den Hoek A, Yuliang F, Dukers NH, Zhiheng C, Jiangting F, Lina Z, et al
. High prevalence of syphilis and other sexually transmitted diseases among sex workers in China: potential for fast spread of HIV. AIDS 2001; 15:753–759.
10. Yang H, Li X, Stanton B, Liu H, Liu H, Wang N, et al
. Heterosexual transmission of HIV in China: a systematic review of behavioral studies in the past two decades. Sex Transm Dis 2005; 32:270–280.
11. Liao SS, Schensul J, Wolffers I. Sex-related health risks and implications for interventions with hospitality women in Hainan, China. AIDS Educ Prev 2003; 15:109–121.
12. Xia G, Yang X. Risky sexual behavior among female entertainment workers in China: implications for HIV/STD prevention intervention. AIDS Educ Prev 2005; 17:143–156.
13. Liu S, Fu J, Su S. A survey on characteristics of sexual behavior among women engaging in clandestine prostitution. Chin J STD/AIDS Prev Cont 2001; 7:294–295.
14. Zhu G, Sun J, Peng Z. Investigation of condom use among commercial sex workers. Chin J STD/AIDS Prev Cont 2003; 9:95–97.
15. Xu L, Yan Y, Chen L. Epidemiological study of HIV-related behaviors in high-risk population in Fuzhou city. Chin J STD/AIDS Prev Cont 2001; 7:220–222.
16. Yang H, Li X, Stanton B, Fang X, Zhao R, Dong B, et al
. Condom use among female sex workers in China: role of gatekeepers. Sex Transm Dis 2005; 32:572–580.
17. Rogers SJ, Ying L, Xin YT, Fung K, Kaufman J. Reaching and identifying the STD/HIV risk of sex workers in Beijing. AIDS Educ Prev 2002; 14:217–227.
18. Rojanapithayakorn W, Hanenberg R. The 100% condom program in Thailand. AIDS 1996; 10:1–7.
19. Laga M, Alary M, Nzila N, Manoka AT, Tuliza M, Behets F, et al
. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers. Lancet 1994; 344:246–248.
20. Ministry of Health of China, State Development Planning Commission, Ministry of Science and Technology, Ministry of Finance. Chinese national medium and long-term strategic plan on prevention and control of HIV/AIDS
. (1998–2010) State Council Document (1998) number 38. Beijing, 1998 (in Chinese).
21. NIMH Collaborative HIV/AIDS Prevention Trial Group. Sexually transmitted disease and HIV prevalence and risk factors in concentrated and generalized HIV epidemic settings. AIDS
2007; 21(Suppl 2)
22. Ministry of Health of China. Infectious disease annual report for 2005, and Monthly Reports for January and February 2006
. Beijing: Ministry of Health; 2006.
23. Ministry of Health of China, UNAIDS, WHO. 2005 update on the HIV/AIDS epidemic and response in China.
Beijing: Ministry of Health; 2006.
24. State Council of P.R. of China. Regulations on AIDS prevention and treatment
[in Chinese]. Beijing; State Council of P.R. of China; 2006.
25. State Council of P.R. China. China's action plan for reducing and preventing the spread of HIV/AIDS (2006-2010)
[in Chinese]. Beijing; State Council of P.R. of China; 2006.