By the end of 2011, the China Ministry of Health estimated that there were approximately 780,000 people living with HIV/AIDS in China, of whom 46.5% were infected through heterosexual transmission.1 A large proportion (52.2%) of the 48,000 incident infections estimated for 2011 were transmitted through heterosexual sex.1 Female sex workers (FSWs) are a particularly vulnerable group for HIV infection. FSWs are not only at high risk of contracting HIV, but also pose a risk of bridging the epidemic to the general population through sex with clients and regular sexual partners.1–4 HIV prevalence among FSWs in detention centers (where FSWs were detained if they were arrested, with more drug-using FSWs than community sites) in Yunnan Province has increased from 0.5% in 1995 to 4.0% in 2007, and HIV prevalence rates among FSWs in community sites was 1.5%, 1.5%, and 1.9% in 2005, 2006, and 2007, respectively.5 Characterizing the dynamics of the HIV epidemic among FSWs is critical in order to inform prevention interventions and policy decisions.
Many cross-sectional studies have been conducted in China on HIV and sexually transmitted infection (STI) risk factors among FSWs.6–12 Although examining the risk factors associated with HIV prevalence helps to understand the characteristics of the HIV epidemic, determining HIV incidence and the associated factors helps clarify how behaviors relate to HIV acquisition. To our knowledge, there have only been 3 studies that have estimated HIV incidence among Chinese FSWs.13–15 These studies, however, used HIV subtype B, E and D-enzyme immunoassay13,15 or a relatively short follow-up time.14 The current study aims to inform future HIV prevention efforts in Yunnan Province, a high-risk area of China, by estimating HIV incidence in a prospective cohort of FSWs and explores the risk factors associated with HIV acquisition. The study was conducted in Kaiyuan City, Yunnan Province, a city with a population of 292,000 and large population of drug users and sex workers.10
MATERIALS AND METHODS
The Chinese Center for Disease Control and Prevention (China CDC) and the Yunnan provincial CDC conducted behavioral surveys and HIV/STIs testing of FSWs biannually from March 2006 to November 2009. Local CDC outreach workers recruited FSWs in Kaiyuan City who worked out of any of the known sex work venues in the area (attempts were made to survey all venues, including streets walkers, temporary sublets, beauty salons, saunas, karaoke clubs, hotels, and night clubs). Outreach workers explained the study purpose, procedures, as well as the risks and benefits of participation to eligible FSWs and their bosses. Women, who were aged ≥16 years, self-reported commercial sex work within the previous 3 months, were willing to provide written informed consent, and agreed to undergo HIV/STIs testing and counseling were eligible to participate. All women who met the inclusion criteria were invited to participate in the research study and FSWs were compensated 50 RMB (7 USD) on completion of the survey. This study received approval from both the China CDC National Center for AIDS/STD and the Yunnan Provincial CDC institutional review boards.
Specialists from China CDC and the Yunnan Provincial CDC trained local staff members from the Kaiyuan CDC on protection of human subjects, obtaining informed consent, safeguarding confidentiality, and providing HIV/STIs pre- and posttest counseling.
Information regarding FSW demographics, as well as sexual and drug use behavior was elicited in face-to-face interviews. In order to maximize participant retention, the study schedule was thoroughly explained and was reemphasized at subsequent follow-up surveys. Contact information of FSWs was collected and confirmed at each study visit. Attempts were made to contact all study participants through provided contact information 1 month in advance to remind them to return for follow-up surveys. Subjects who were initially HIV negative and completed 2 or more surveys constituted an open cohort.
Blood was collected and tested for HIV-1 antibodies (enzyme-linked immunosorbent assay [ELISA], Vironostika HIV Uni-Form plus O, bioMerieux, Holland), herpes simplex virus type-2 antibody (HSV-2, HerpeSelect-2 ELISA IgG, Focus, Hackensack NJ), and syphilis (rapid plasma reagin test, Diagnosis kit, Xinjiang Xindi Company, China). Positive HIV-1 ELISAs were confirmed by Western blot (Diagnostics HIV Blot 2.2, Genelabs, Redwood City, Calif) and positive rapid plasma reagin tests for syphilis were confirmed by the Treponema pallidum particle assay test (Serodia-P·PA-Fujirebio, Fuji, Japan). Endocervical swabs were collected and tested for Neisseria gonorrhoeae and Chlamydia trachomatis by polymerase chain reaction (PCR, AMPLICOR, Roche, Branchburg, NJ). Vaginal swabs were collected and a wet mount was prepared to detect Trichomonas vaginalis. Urine was collected for opiate screening (MOP One Step Opiate Test Device, ACON Laboratories, Inc, San Diego, Calif). Participants were classified as using illegal drugs if they self-reported drug use or tested positive for opiates through urine screening.
Subjects were scheduled for follow-up visits 4 to 6 weeks after the initial visit to receive test results and posttest counseling. FSW participants with STIs were referred to the Kaiyuan Dermatology Hospital, where participants were entitled to receive a 60% discount on STI treatment. Those who tested HIV-positive were referred to the Kaiyuan People’s Hospital, where antiretroviral therapy was offered through the support of the Clinton Foundation.
Statistical tests were performed using SAS 9.1 (SAS Institute Inc, Cary, NC). Those who were HIV positive at baseline were excluded from the analysis. χ2 tests were used to compare demographic and behavioral characteristics of participants who returned for follow-up and subjects who did not return. HIV incidence density was calculated for subjects who were HIV negative at baseline and completed at least 2 surveys, dividing the number of events of HIV seroconversion by the number of person-years (PY) of follow-up. The follow-up time for each FSW was calculated as the time between her first negative HIV test and the most recent negative HIV test or incident HIV infection if she seroconverted. Poisson 95% confidence intervals (CIs) were calculated for overall incidence density.
The exact date of seroconversion was unknown, thus the probability of seroconversion was assumed to occur uniformly along the interval between the date of last HIV-negative test and the first HIV-positive test. HIV infection was not assumed to take place on the midway of the interval, which may produce artificial fluctuations, as many of these intervals were long. For subjects who seroconverted, the contribution of PY to the denominator was proportional to the amount of time remaining until the end of that interval.
Univariate and multivariate Cox proportional hazards regression models with time-dependent variables were used to determine the factors associated with HIV seroconversion. Most factors could change during follow-up and were treated as time-dependent variables. Some characteristics, such as education level, nationality, and age at initiation of sex work, were treated as time-independent variables. Factors found significant in univariate analysis were included in a stepwise Cox proportional hazards multiple regression model with entry criteria of P < 0.2 and exit criteria of P > 0.05.
Higher risk venues were defined as locations where FSWs generally charged <100 RMB ($14 USD) per sexual service, including beauty salons, temporary sublets, and street-based venues. Lower risk venues were defined as locations where FSWs generally charged 100 RMB or more per sexual service, including karaoke clubs, nightclubs, saunas, and hotels.10
Study Participant Characteristics
From 2006 to 2009, a total of 2282 FSWs participated in at least 1 survey. Of these, 2051 (89.9%) participants were HIV negative at baseline and 851 (41.5%) initially HIV-negative FSWs returned for at least 1 follow-up visit.
Table 1 compares the baseline demographic, behavioral, and clinical characteristics of the FSWs retained in the cohort and those who were lost to follow-up. Among those in the cohort, the majority was Han ethnicity (69.8%), had registered residence in other cities in Yunnan (54.2%), had a low education level (35.0% had <6 years of education), and worked out of low-risk entertainment venues (63.3%). There were 81 (9.5%) injection drug users (IDUs) and 56 (6.6%) non-IDUs in the cohort. Of the 118 FSWs who tested urine opiate positive for drug use, 108 (92%) self-reported drug use. Correspondingly, of the 127 FSWs who reported any illegal drug use, 108 (85%) tested urine opiate positive. Self-reporting drug use had a high consistency with urine testing (κ = 0.86, 95% CI: 0.81– 0.91). Reported condom use last week was high for those in the cohort (86.0%), but there was a relatively high prevalence of STIs including N. gonorrhoeae (6.8%), C. trachomatis (21.6%), Trichomonas vaginalis (7.3%), HSV-2 (62.5%), and syphilis (7.9%). Compared with FSWs who did not report alcohol use, FSWs who reported alcohol use had higher condom use with clients in the past week, were more likely from lower risk venues, had higher fee-per-service, and fewer clients in the previous week.
Compared with FSWs lost to follow-up, the subjects who completed at least 1 follow-up survey were generally older, from other provinces, and living in rented apartments (as opposed to living with her family or in a brothel). Those retained in the cohort were more likely to engage in certain risk behaviors including injection and noninjection drug use. In addition, those in the cohort were more likely to have worked in the commercial sex industry for a longer duration and more likely to have HSV-2 or syphilis; however, this subset of participants also had fewer clients in the previous week and charged a higher fee-per-service.
HIV Prevalence and Incidence
As shown in Table 2, HIV prevalence was 10.1% among all enrolled participants. HIV prevalence was highest among IDUs (47.8%), but lower among non-IDUs (15.5%), and those who do not use any drugs (4.3%).
During the course of 3.5 years, 851 FSWs were followed an average of 1.55 (±0.38) years, for a total of 1319 PY, and 19 incident cases of HIV infection were diagnosed, yielding an overall incidence of 1.44 per 100 PY (95% CI: 0.87–2.24). Of the 19 participants who seroconverted, 5 were IDUs, 5 were non-IDUs, and 9 were nondrug users. It was thus estimated that at least 73.7% (14 nondrug users and non-IDUs of 19 new HIV cases) of subjects were infected through sexual transmission.
Factors Associated With HIV Acquisition
Table 3 presents the demographic and behavioral characteristics associated with HIV incidence in univariate analysis. Participants who lived at home with their family, were IDUs, were non-injection drug users, had ≥7 clients in previous week, and had inconsistently used condoms with clients in the previous week had an increased risk of HIV infection. Those who reported drinking alcohol were less likely to become infected with HIV.
Table 4 presents the significant factors identified in the multivariate Cox proportional hazards regression model. FSWs who were non-injection drug users, had inconsistently used condoms with clients in the previous week, and had ≥7 clients in the previous week were more likely to seroconvert. IDU was not a significant factor for HIV seroconversion after controlling for other factors, but this variable was retained in the multivariate model to demonstrate its relationship with HIV seroconversion.
This study found a relatively low incidence (1.44 per 100 PY, 95% CI: 0.87–2.24), but high prevalence (10.1% among the whole study population) of HIV among FSWs in Kaiyuan City, Yunnan. Non-injection drug use, inconsistent condom use, and the number of clients per week were independently associated with HIV seroconversion. Significantly, the majority of those who seroconverted were not self-reported IDUs, indicating that most subjects had acquired the virus sexually.
The HIV incidence rate identified in our study is similar to corresponding rates reported in previous research conducted among FSWs in China.13–15 Similar to the results of this study, the other 2 sites (Dehong Prefecture, Yunnan Province; and Xichang City, Sichuan Province) sampled in the aforementioned studies had high prevalences of HIV and drug use. However, whether the HIV incidence rate of 1.44 per 100 PY identified in this study is representative of the epidemic among Chinese FSWs in other heavy drug use areas is unknown. More prospective studies among FSWs should be done to know the HIV/STIs incidence in the future.
Although general estimates of HIV infection among Chinese FSWs have been much lower (1%–2%),16–20 the higher HIV prevalence in the current study may be because of regional and subject differences. Yunnan has one of the most concentrated HIV epidemics in China, and there was a high proportion of drug users in the current study sample,10 which may be why the HIV prevalence in the current study was higher than the average level in Yunnan province.5 The HIV prevalence among the current study’s nondrug using FSWs (5.2%) was comparable (somewhat higher) to the overall prevalence among FSWs in detention centers in Yunnan province (4% in 2007).5 Studies show that FSWs who also use drugs are at a much higher risk for acquiring HIV than FSWs who do not.21,22 Studies of Chinese FSWs show that up to 25% use drugs23 and HIV prevalence rates may differ based on the proportion of drug use. High HIV prevalence was also found in other countries, with high proportions of drug using FSWs.24–26 HIV prevalence was 11.6% among FSWs in Dimapur, Nagaland, a high HIV prevalence state of India, with 25% of the participants ever using and 5.7% ever injecting illicit drugs.24 In Indonesia, HIV prevalence averaged 10.5% among direct and 4.9% among indirect FSWs.25
Like other studies of Chinese FSWs,18,20,21,23 the current study found high rates of STIs; C. Trachomatis was the most common bacterial STI followed by T. vagnialis then N. gonorrhoeae, and somewhat higher rates have been found among FSWs in Yunnan (58.6%, 43.2%, and 37.8%, respectively)27 and Guangzhou (32%, 12.5%, and 8%, respectively).20 Geography, study dates, and sampling methods may account for these differences; for instance, in the Yunnan study, subjects were also recruited from STI clinics, yielding a slightly higher rate. The role of STIs in HIV transmission has been well reviewed.28–31 Early detection and treatment of STIs may be an effective strategy to reduce HIV transmission.
HIV prevalence was particularly high among IDUs (47.8% HIV positive). However, although IDU was significantly associated with HIV seroconversion in univariate analysis, it was no longer significant when controlling for other factors. This is surprising given previous research that has found IDU among Kaiyuan FSWs to be the most salient predictor for HIV infection in cross-sectional studies.10 About half of IDUs had been infected by HIV before participating in the current study, the remaining IDUs may have had lower risk. Needle exchange (initiated in 2005) and methadone programs (initiated in 2009) in Kaiyuan may play an important role, as these programs can reduce the risk of HIV transmission among IDUs. Moreover, the relatively small sample size of IDUs may have limited the power to detect a difference.
Although IDU was not found to be a predictor of HIV seroconversion, non-injection drug users were found to be 6 times more likely to seroconvert compared with nondrug users. Previous research has identified noninjection drug use to be associated with high-risk behaviors and prevalent HIV.32,33 Edlin et al has also highlighted the exchange of sex for money32 and as sex work is the primary source of income for many FSWs, some FSWs may compromise safe sexual practice or may take on a riskier client base to earn more money to support their drug use habits. Ostrow et al has also argued that illegal drug use may weaken the immune system, presenting a greater opportunity for infection.34 Underreporting of IDU may also be a reason for this surprising result, as IDUs classified as non-IDUs would increase the apparent risk of this group. The results of this study underscore the need for HIV interventions among drug users that incorporate sexual risk reduction.35
Not surprisingly, inconsistently using condoms with clients and having ≥7 clients in the previous week were independently associated with HIV seroconversion. Only 20.8% of participants retained in the cohort reported consistent condom use with their regular sexual partners. Condoms have been consistently shown to protect against HIV infection36,37 and low condom use, with regular partners could lead to a larger epidemic in the general population. Condom promotion programs among Chinese FSWs have shown increased condom use and decreased STI incidence rates,38,39 but these programs should emphasize the importance of condom use with all partners, including regular partners. FSWs who reported alcohol use were less likely to HIV seroconvert in univariate analysis, but this variable was not retained in the multivariate model. Alcohol use was associated with other HIV risk factors. FSWs who reported alcohol use had higher condom use with clients in the past week, were more likely from lower risk venues, had higher fee-per-service, and fewer clients in the previous week.
This study was subject to several limitations. Many risk factors, including condom use and illegal drug use, were self-reported and may thus be affected by social desirability and/or recall bias. To mitigate social desirability bias, biologic indicators were used to evaluate opiate use and prevalent STIs and HIV. However, IDU was only measured through self-report and thus may be under reported. To mitigate recall bias, we asked participants to recall their most recent behavior. Nearly 60% of eligible FSWs were lost to follow-up, and there were significant differences between the subjects who were retained in the cohort and those who were lost to follow-up. Participants in the cohort had a higher prevalence (in comparison with those lost to follow-up) of some factors that might increase their HIV risk, including illicit drug use, prevalent HSV-2, and prevalent syphilis, but also had a lower prevalence of other risk behaviors including having more clients in the previous week; thus, it is difficult to determine whether HIV incidence was overestimated or underestimated. Furthermore, low retention may contribute to the low incidence, but high prevalence of HIV found in this study.
This study identified a relatively low HIV incidence among a prospective cohort of FSWs. Although previous research among this population has found IDU to be the most salient predictor for HIV infection, the current study did not find IDU to be significantly associated with HIV acquisition, which may indicate a shift in the local epidemic from IDU to sexual transmission. Future interventions should continue to focus on sexual risk reduction among FSWs. Traditional HIV prevention methods among FSWs such as condom promotion should be emphasized, considering the high prevalence of STIs. Screening and treatment of STIs are also an important strategy for reducing the risk of HIV transmission, especially when sexual transmission has become the main route of transmission. Significant attention should focus on the drug-using FSWs with overlapping risk, for whom needle exchange and methadone or other drug reduction treatment should be reinforced.
2. Wang H, Wang N, Bi A, et al.. Application of cumulative odds logistic model on risk factors analysis for sexually transmitted infections among female sex workers in Kaiyuan city, Yunnan province, China. Sex Transm Infect 2009; 85: 290–295.
3. Cote AM, Sobela F, Dzokoto A, et al.. Transactional sex is the driving force in the dynamics of HIV in Accra, Ghana. AIDS 2004; 18: 917–925.
4. Plummer FA, Nagelkerke NJ, Moses S, et al.. The importance of core groups in the epidemiology and control of HIV-1 infection. AIDS 1991; 5 (suppl 1): S169–S176.
5. Jia M, Luo H, Ma Y, et al.. The HIV epidemic in Yunnan Province, China, 1989–2007. J Acquir Immune Defic Syndr 2010; 53 (suppl 1): S34–S40.
6. 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 Immune Defic Syndr 2010; 53 (suppl 1): S48–S53.
7. Lu F, Jia Y, Sun X, 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.
8. Ngo TD, Laeyendecker O, Li C, et al.. Herpes simplex virus type 2 infection among commercial sex workers in Kunming, Yunnan Province, China. Int J STD AIDS 2008; 19: 694–697.
9. Wang H, Wang N, Chen RY, et al.. Prevalence and predictors of herpes simplex virus type 2 infection among female sex workers in Yunnan Province, China. Int J STD AIDS 2008; 19: 635–639.
10. Wang H, Chen RY, Ding G, 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.
11. Xu JJ, Wang N, Lu L, et al.. HIV and STIs in clients and female sex workers in mining regions of Gejiu City, China. Sex Transm Dis 2008; 35: 558–565.
12. Lau JT, Ho SP, Yang X, et al.. Prevalence of HIV and factors associated with risk behaviours among Chinese female sex workers in Hong Kong. AIDS Care 2007; 19: 721–732.
13. Duan S, Shen S, Bulterys M, et al.. Estimation of HIV-1 incidence among five focal populations in Dehong, Yunnan: A hard hit area along a major drug trafficking route. BMC Public Health 2010; 10: 180.
14. Tian LG, Ma ZE, Ruan YH, et al.. Incidence rates of human immunodeficiency virus and syphilis as well as the rate of retention in a 6-month follow-up study of female sex workers in areas with heavy drug use in Xichang of Sichuan province, China [in Chinese]. Zhonghua Liu Xing Bing Xue Za Zhi 2006; 27: 939–942.
15. Xu J, Wang H, Jiang Y, et al.. Application of the BED capture enzyme immunoassay for HIV incidence estimation among female sex workers in Kaiyuan City, China, 2006–2007. Int J Infect Dis 2010; 14: e608–e612.
16. Ding Y, Detels R, Zhao Z, et al.. HIV infection and sexually transmitted diseases in female commercial sex workers in China. J Acquir Immune Defic Syndr 2005; 38: 314–319.
17. Wei SB, Chen ZD, Zhou W, et al.. A study of commercial sex and HIV/STI-related risk factors among hospitality girls in entertainment establishments in Wuhan, China. Sex Health 2004; 1: 141–144.
18. Ruan Y, Cao X, Qian HZ, et al.. Syphilis among female sex workers in southwestern China: Potential for HIV transmission. Sex Transm Dis 2006; 33: 719–723.
19. Zhu TF, Wang CH, Lin P, et al.. High risk populations and HIV-1 infection in China. Cell Res 2005; 15: 852–857.
20. van den Hoek A, Yuliang F, Dukers NH, 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.
21. Yang H, Li X, Stanton B, 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.
22. Rekart ML. Sex-work harm reduction. Lancet 2005; 366: 2123–2134.
23. Chu TX, Levy JA. Injection drug use and HIV/AIDS transmission in China. Cell Res 2005; 15: 865–869.
24. Medhi GK, Mahanta J, Paranjape RS, et al.. Factors associated with HIV among female sex workers in a high HIV prevalent state of India. AIDS Care 2012; 24: 369–376.
25. Magnani R, Riono P, Nurhayati, et al.. Sexual risk behaviours, HIV and other sexually transmitted infections among female sex workers in Indonesia. Sex Transm Infect 2010; 86: 393–399.
26. Nhurod P, Bollen LJ, Smutraprapoot P, et al.. Access to HIV testing for sex workers in Bangkok, Thailand: A high prevalence of HIV among street-based sex workers. Southeast Asian J Trop Med Public Health 2010; 41: 153–162.
27. Chen XS, Yin YP, Liang GJ, et al.. Sexually transmitted infections among female sex workers in Yunnan, China. AIDS Patient Care STDS 2005; 19: 853–860.
28. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2004; 2: 33–42.
29. Freeman EE, Weiss HA, Glynn JR, et al.. Herpes simplex virus 2 infection increases HIV acquisition in men and women: Systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20: 73–83.
30. Rottingen JA, Cameron DW, Garnett GP. A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known? Sex Transm Dis 2001; 28: 579–597.
31. McClelland RS, Sangare L, Hassan WM, et al.. Infection with Trichomonas vaginalis
increases the risk of HIV-1 acquisition. J Infect Dis 2007; 195: 698–702.
32. Edlin BR, Irwin KL, Ludwig DD, et al.; The Multicenter Crack Cocaine and HIV Infection Study Team. High-risk sex behavior among young street-recruited crack cocaine smokers in three American cities: An interim report. J Psychoactive Drugs 1992; 24: 363–371.
33. Booth RE, Watters JK, Chitwood DD. HIV risk-related sex behaviors among injection drug users, crack smokers, and injection drug users who smoke crack. Am J Public Health 1993; 83: 1144–1148.
34. Ostrow DG, DiFranceisco WJ, Chmiel JS, et al.. A case-control study of human immunodeficiency virus type 1 seroconversion and risk-related behaviors in the Chicago MACS/CCS Cohort, 1984–1992. Multicenter AIDS Cohort Study Coping and Change Study. Am J Epidemiol 1995; 142: 875–883.
35. Strathdee SA, Sherman SG. The role of sexual transmission of HIV infection among injection and non-injection drug users. J Urban Health 2003; 80 (suppl 3): iii7–iii14.
36. Cayley WE Jr. Effectiveness of condoms in reducing heterosexual transmission of HIV. Am Fam Physician 2004; 70: 1268–1269.
37. Laga M, Alary M, Nzila N, 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.
38. Ma S, Dukers NH, van den Hoek A, et al.. Decreasing STD incidence and increasing condom use among Chinese sex workers following a short term intervention: A prospective cohort study. Sex Transm Infect 2002; 78: 110–114.
39. Rou K, Wu Z, Sullivan SG, et al.. A five-city trial of a behavioural intervention to reduce sexually transmitted disease/HIV risk among sex workers in China. AIDS 2007; 21 (suppl 8): S95–S101.