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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Int J Infect Dis. Author manuscript; available in PMC Mar 1, 2010.
Published in final edited form as:
PMCID: PMC2650737
NIHMSID: NIHMS51280

Prevalence and Predictors of HIV Infection among Female Sex Workers in Kaiyuan City, Yunnan Province, China

Abstract

Background

Sexual transmission is the fastest growing route of HIV transmission in China.

Methods

Cross-sectional study of 737 female sex workers (FSW) in Kaiyuan City, Yunnan Province, China from March-May 2006 to describe risk factors for HIV infection and to determine the commercial sex venues where FSWs were most at risk of being infected with or infecting others with HIV.

Results

Overall HIV prevalence was 10.3%, but prevalence varied with the sex venue with 25.8% of FSWs working on streets being HIV-positive and none of the FSWs working in night clubs. Adjusted odds ratios (OR) of HIV infection were 9.1 (95% CI: 4.67–17.55) for injection drug use; 3.3 (95% CI: 1.46–7.37) for non-injection illegal drug use; 2.7 (95% CI: 1.25–5.93) for duration of sex work ≥5 years; 2.2 (95% CI: 1.05–4.70) for infection with herpes simplex virus type 2; and 2.0 (95% CI: 1.12–3.47) for working at a higher risk entertainment venue. Although condom use was not a significant risk factor in the overall model, FSWs in lower risk venues who reported consistent use with clients had a 70% reduction in HIV infections (OR: 0.30; 95% CI: 0.12–0.90).

Conclusions

Illegal drug use, particularly with injection drugs, is the single greatest risk factor for HIV infection among FSWs in Kaiyuan City, China. FSWs working on the street or in temporary sublets, beauty salons or saunas are at particularly high risk for transmitting and being infected with HIV. HIV prevention efforts among FSWs should target illegal drug users and these other subgroups.

Keywords: female sex workers, sex work venues, HIV, injection drug users, condom, sexually transmitted infections, China

Background

The China Ministry of Health currently estimates that about 700,000 people are infected with the human immunodeficiency virus (HIV) in China. Among the 50,000 estimated new infections in 2007, 45% were heterosexual and 42% were through injection drug use (IDU) (1). National sentinel surveillance data and other reports suggest that, overall, about 1% of female sex workers (FSW) in China were HIV-positive in 2004 (25).

HIV infection rates are highest among FSWs in Yunnan Province in Southern China, near the borders with Vietnam, Thailand and Myanmar (6). Although the HIV epidemic there has been driven predominantly by injection drug use, sexual transmission has played an increasingly greater role (7). The National HIV Risk Population Survey in 2003 showed that the average prevalence of HIV among FSWs in Yunnan was 3.7% (8). The major goal of this study was to inform future HIV prevention efforts in this high risk area of China by assessing the current prevalence of HIV in FSWs, determining the role of injection drug use in the epidemic, and describing other risk factors for HIV infection. The study was conducted in Kaiyuan City, Yunnan with a population of 292,000 and large numbers of drug users and sex workers.

Methods

This study was conducted by the Chinese Center for Disease Control and Prevention (China CDC) in Beijing in conjunction with provincial and local CDC staff in Yunnan. With approval from both the national and local Yunnan institutional review boards, we conducted a cross-sectional study of all women identified as FSWs in Kaiyuan City, Yunnan Province from March to May 2006. The FSWs were recruited by out-reach workers of Kaiyuan city who went to all sex work venues, explained the study purpose, procedures, and the risks and benefits of participation to FSWs and to their bosses; all women working as sex workers were invited to participate in this research. The inclusion criteria for the study were women ≥16 years old, self-reported to have sold sex for money within the previous three months, and agreement to testing and counseling for HIV, other sexually transmitted infections (STI), and use of illegal drugs. After providing informed consent, participants were asked standardized questions about their demographics, basic medical history, and potential HIV risk factors.

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, USA), and syphilis (rapid plasma reagin (RPR) test, Diagnosis kit, Xinjiang Xindi company, China). Positive HIV-1 ELISAs were confirmed by western blot (Diagnostics HIV Blot 2.2, Genelabs, USA) and positive RPR tests for syphilis were confirmed by the Treponema pallidum particle assay (TPPA) 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, USA). Vaginal swabs were collected and a wet mount prepared to detect Trichomonas vaginalis.

Finally, urine was collected for opiate screening (MOP One Step Opiate Test Device, ACON Laboratories, Inc., USA). Participants were classified as using non-injection illegal drugs if they self-reported as such or did not self-report but tested urine positive; injection drug use status was based only on self-report. All participants were scheduled for a follow-up visit 4–6 weeks later to discuss test results and for counseling.

Statistical tests were performed using SAS™ 9.1 software (SAS Institute Inc, Cary, NC, USA). We compared HIV prevalances and factors associated with HIV infections among FSWs working in the different sex work venues in order to classify venues as higher or lower in terms of HIV risks. T-tests, Fisher Exact tests, and chi-square tests were used to compare subjects infected or not infected with HIV, as well as to compare subjects whom we classified as working in higher or lower risk venues. Univariate associations between risk factors and HIV seropositivity were evaluated using simple logistic regression analysis. In addition, adjusted ORs were calculated for all FSWs and separately for FSWs working at lower and higher risk venues, building logistic models first by adjusting for the factors found to be significant in univariate analysis (P <0.02) and then limiting final multivariate models to risk factors or confounders that were statistically significant in the overall and venue specific analyses. The collinearity diagnostics were evaluated for the variables included in the final model by calculating the following indexes: tolerance, variance inflation factor, condition number and variance proportion. We multiplied the number of clients with whom HIV-positive FSWs had unprotected sex (condom was not used or broke or fell off during intercourse), by the probability of female-to-male transmission of HIV-1 per sexual contact (0.031) to arrive at estimate of the number of clients infected (9).

Results

Of the 756 FSWs screened for the study, 15 were excluded because they had not sold sex for money in the previous three months, and 4 others were excluded because blood specimens could not be obtained. Of the 737 FSWs included in the study, 393 (53%) returned for test results and post-test counseling.

Table 1 shows the behavioral characteristics of FSWs working in the various sex work venues. Based on these characteristics we classified streets walkers, temporary sublets and beauty salons as the higher risk venues in terms of HIV risks and the other four venues as lower risk venues. About half (48.6%) of FSWs worked in karoke clubs, and about a quarter (26.7%) worked in beauty salons. HIV prevalences were substantially higher in the higher risk venues, with the exception of hotels, for which numbers were small. The mean earnings per client was lower in what we classified as higher risk venues, and mean numbers of clients per week also tended to be higher here. The percentages of FSWs reporting injection drug use were substantially higher in the higher risk venues, particularly among street walkers. Although we classified saunas as a lower risk venue based on the injection drug use, mean cost per client, and HIV prevalence of FSWs working here, they shared several characteristics more in common with the higher risk venues, including the mean numbers of clients per FSW in the previous week.

Table 1
Comparison of major factors associated with HIV risks for female sex workers (FSW) according to their usual venue for sex work: classification of venues as higher and low risk.

Table 2 describes the demographic and behavioral characteristics of HIV-positive and –negative FSWs and according to whether they were classified as working in higher-or lower-risk venues. Not surprisingly, because HIV prevalence was a key factor in the classification of venues as higher or lower risk, FSWs working in higher, as opposed to lower, risk venues were at a significantly greater risk of HIV infection (17.9% vs. 5.7%; P < 0.0001). FSWs were primarily of Han ethnicity with permanent residences in Yunnan. We found significantly higher HIV infection rates among FSWs living in their family home rather than in an apartment (27.1% vs. 7.7%), reporting tooth extractions or fillings (15.4% vs. 9.3%), tattoos (13.6% vs. 8.0%), seeing 7 or more clients a week compared to fewer (17.6% vs. 8.6%), engaging in paid sex for 5 years or more compared to less than one year (29.6% vs. 5.6%) and always using vs. sometimes or never using condoms with every client in the previous week (9.1% vs. 16.5%). The median duration of sex work was 46 months for HIV-positive subjects and 18.5 months for those who were HIV-negative (P < 0.0001). FSWs working in higher risk venues were significantly more likely to be from Yunnan province, to have worked as a FSW for a longer time, and to have reported not using condoms with all clients in the previous week.

Table 2
Comparison of demographic and behavioral characteristics of 737 HIV-positive and HIV–negative female sex workers and comparison of sex workers working in higher or lower risk venues.*

HIV infection rates were particularly high among injection drug users (49.3% positive) and non-injection drug users (19.6% positive). Of the 114 FSWs who tested urine opiate positive for drug use, 82 (72%) of them self-reported drug use. Correspondingly, of the 88 FSWs who reported any illegal drug use, 82 (93%) tested urine opiate positive. Among all FSWs, the median duration of sex work was 19.4 months (Interquartile Range, IQR: 8.1–40.5 months) and median number of paid clients in the preceding week was three (IQR: 1–5).

Fifty-two percent of women reported a “regular partner”, defined as a male with whom she had regular sexual relations without compensation, such as a boyfriend or spouse. Of the subjects who said they had a regular sex partner, 84% said they did not use condoms routinely with him, and there was no association between using condoms with regular sex partners and being HIV-infected. Among the 38 HIV-positive FSWs with regular sex partners, only 7 (18.4%) said they always used condoms with them in the previous week. In contrast, 56 (73.7%) of the 76 HIV-positive FSWs said they used condoms with all paid sex partners in the previous week. The overall HIV prevalence was significantly lower in those reporting consistent condom usage with clients (9.1% vs. 16.5% for those not always using condoms with clients).

The median number of paid sex partners in previous week before participating in the study was 4 for HIV-positive FSWs (and 5 and 3 for HIV-infected FSWs working in higher and lower risk venues). It was estimated that 2.79 clients would be infected in a week by sexual transmission, 2.17 and 0.62 clients in higher and lower risk venues, respectively. The prevalence of STIs other than HIV was also very high in this study (Table 2). About two-thirds of FSWs were positive for HSV-2 and about one-third for C. trachomatis (respectively, 74.5% and 29.7% of those working in higher risk venues and 64.2% and 23.6% of those working in lower risk venues). Trichomonas vaginalis and HSV-2 infections were significantly more common among women infected with HIV.

Table 3 shows adjusted odds ratios (OR) and 95% confidence intervals (CI) of HIV infection for potential risk factors or confounders that remained statistically significant after we included in the multivariate logistic models all variables that were significant in the univariate analysis; ORs are shown for all FSWs together and according to their venue of sex work. Overall, IDUs had a 9-fold greater risk of HIV infection than FSWs who did not use drugs; risks were higher for FSWs working in higher, as opposed to lower, risk venues (OR 10.2 vs. 6.9). Non-injection drug users were at 3.3-fold greater risk than FSWs not using drugs, but this association was significant only for FSWs working in higher risk venues and not for those working in lower risk venues. These results for non-injection drug users remained statistically significant when FSWs who did not self-report drug use but tested urine positive were excluded from the analysis. Compared to working in commercial sex for less than one year, working for five or more years was associated with 2.7-fold greater risk of HIV infection.

Table 3
Odds ratios (OR) and 95% confidence intervals (CI) of HIV infection among all female sex workers and according to location of sex work in higher or lower risk venues.*

Vaginal douching was a strong risk factor among women working in higher risk venues (OR 3.8; 95% CI 1.06–13.68), but this was not a significant risk factor among FSWs working in lower risk venues. FSWs reported douching with soapy water (27% HIV-positive), spermicide (23% infected), toothpaste (20% infected), water (20% infected), medical disinfectant (19% infected), and salt water (18% infected; there were no significant differences between HIV infection status and the douche product used). The potential risk factors and confounders that were statistically significant in the univariate analysis but not in the multivariate analysis are listed in a footnote to Table 3.

The most important risk factors for FSWs working in higher risk venues were injection drug use (OR 10.2), duration of sex work for ≥5 years (OR 5.2), non-injection drug use (OR 4.9), and vaginal douching (OR 3.8). Consistent use of condoms with clients or regular sex partners was not significantly associated with HIV risks in this group. In comparison, the major risk factors for FSWs working in lower risk venues were injection drug use (OR 6.9), history of blood transfusion (OR 4.7), and trichomoniasis (OR 4.4). FSWs working in lower risk venues who said they used condoms with all clients in the previous week showed a 70% reduction in HIV risk that was statistically significant (OR 0.3; 95% CI 0.12–0.90). For the variables that remained in the multivariate model, the collinearity diagnostic was run, and the key indicators showed no collinearity between these variables. The condition number was 4.16 (less than 10); tolerance exceeded 0.8, and the variance inflation factor was less than 1.2.

Discussion

Our results suggest that while HIV infections of FSWs in Yunnan are primarily driven by illegal drug use and the sharing of drug injection equipment. Also our results suggest that, the risk of transmission of HIV from FSWs to their clients and regular sex partners is high because condoms are infrequently used. Our results also suggest that there are important differences both in HIV prevalence and in the risk factors for HIV infection according to the venue where sex work occurs.

Overall 10.3% of the 737 FSWs included in this study were infected with HIV, with infections significantly more frequent among FSWs working in higher risk venues (beauty salons, temporary sublets, and on the street; 17.9% HIV-positive) as opposed to the venues we defined as lower risk (karaoke clubs, night clubs, saunas, and hotels; 5.7% HIV-positive). Based on a female to male HIV transmission risk of 0.031 from a Thailand study (9) and taking into account condom use among clients, client frequency and HIV prevalence, we estimate that 2.79 clients per week would be infected with HIV by FSWs in this study with about 2.17 or 78% of the infections being passed by FSWs working in higher risk venues. Thus, to better prevent HIV infections of clients and the entry of HIV into the general population of China, prevention efforts among FSWs should particularly focus on FSWs working on the street, in temporary sublets or in beauty salons. Saunas should also be considered for prevention efforts since they shared some of the high risk characteristics of the other venues we classified as higher risk.

Adjusting for significant covariates, HIV risk factors were also found to differ by venue. While injection drug use was a significant risk factor in both higher and lower risk venues (OR: 10.2 and 6.9, respectively), non-injection drug use (OR: 4.9), was also a significant risk factor for HIV infection among FSWs working in higher risk venues. Although a much higher percentage of FSWs working in higher risk venues used injection drugs than those working in lower risk venues (17.9% vs. 4.2%), our results suggest that public health measures addressing illegal drug use, in particular needle exchange and drug treatment programs, are needed for FSWs in Yunnan, regardless of the venue in which they work.

We found that using condoms with all of the previous week’s clients was only a significant protective factor among FSWs working in lower risk venues (OR 0.3), and not among FSWs working in higher risk venues. Consistent condom use with clients was significantly more common among FSWs working in the lower risk venues (88% vs. 76%; P < 0.0001). We also found that among HIV-positive FSWs, only 18.4% consistently used condoms with their regular sex partners and 73.7% with their clients. Condoms have been consistently shown to protect against HIV infection (10, 11), so FSWs need to be counseled to use condoms to protect both their paying and non-paying sex partners and themselves, especially if their sex partners are known to use injection drugs.

Vaginal douching was practiced by 84% of the FSWs in our study, a finding consistent with results from another study of FSWs in China, which found that 65% of them douched (12). This same study identified an association between vaginal douching and decreased use of condoms and increased self-reported history of STI. Our finding that, among FSWs working in higher risk venues, those who douched were at 3.8-fold greater risk of HIV infection after adjusting for other key risk factors, suggests that douching is being substituted for condoms by FSWs working in higher risk venues, particularly since the prevalence of HIV was similar regardless of the douching agent used. Although the association between douching and HIV infection is controversial (1315), douching should never be substituted for condom usage.

Our results are consistent with other studies of FSWs in China. Although general estimates of HIV infection in FSWs have been much lower, about 1–2% (35, 16, 17), studies show that FSWs who also use drugs are at a much higher risk for acquiring HIV than FSWs who do not (18, 19). Studies of Chinese FSWs show that up to 25% use drugs as well (20) and HIV prevalence rates will differ according to what proportion also use drugs. One study identified a 10% HIV prevalence among FSWs in Kunming, the capital of Yunnan Province, with all HIV-infected also being drug users and a significant association between drug use and HIV infection (P <0.01) (21). Another study quantified drug use as a significant risk factor for HIV infection (OR 8.0, 95% CI 2.1–30.3) but found that trichomonas infection was an even larger risk factor (OR 11.2, 95% CI 2.9–42.7) (17). In our study, drug use is the single largest risk factor for HIV acquisition among FSWs, much larger than any risk factor traditionally associated with sex work, such as condom use rates, numbers of partners, and STIs.

Like other studies of Chinese FSWs (5, 17, 18, 21), we found high rates of STIs in this group and significant associations between HIV and other STIs. Adjusting for the key covariates, we found that FSWs with HSV-2 were at a 2.2-fold, statistically significant, greater risk of HIV infections than FSWs who were negative for HSV-2, an association that was consistent, but not statistically significant, in the venue-specific analysis (OR of HIV for HSV-2: 1.7 and 2.4 for FSWs working in the higher and lower risk venues, respectively). We also found that FSWs working in lower risk venues were at a statistically significant 4.4-fold greater risk of HIV if they were infected with T. vaginalis. These results are consistent with those of van den Hoek, et al. who reported an adjusted OR of 11.2 (95% CI 2.9–42.7) of HIV for trichomoniasis in China (17). The role of STIs in HIV transmission has been well reviewed (22) with many studies specifically associating both HSV-2 and trichomonas infection with HIV acquisition (2325). Suppressive therapy of HSV-2 has been shown to reduce genital and plasma HIV RNA levels in dually infected women (26) and studies are underway to determine if treatment of HSV-2 will reduce HIV transmission (27). Screening and treatment of STIs may be an effective public health intervention to reduce HIV transmission.

The HIV-positive participants who returned for their testing results were referred to the Kaiyuan People’s Hospital for further evaluation. The hospital provided antiretroviral therapy through the support of the Clinton Foundation to those individuals who met the national treatment guidelines. Although sex work is prohibited in China, the government has developed interventions to reduce HIV infections, including condom distribution programs, HIV/AIDS education programs, and provision of free HIV treatment for HIV-infected FSWs. Additionally there are a number of programs supported by foreign countries to provide free treatment for HIV-infected FSWs, which also reduces their risk of infecting others. However, because many FSWs in China do not know their infection status, they cannot be treated for HIV or advised to alter their risk behaviours. Thus, HIV screening programs for FSWs are needed.

Our study has several limitations. Because some of the data collected was based on self-report, some risk factors, such as use of condoms and injection drug usage, may be misclassified. To minimize this effect, we asked questions about recent events, such as condom use in the previous week, and we conducted objective tests of risk factors as much as possible, such as urine testing for opiates and laboratory tests for STIs. Second, because this was a cross-sectional study temporality cannot be determined. Whether the HIV infected, drug using FSWs were infected primarily through their drug use or sex work is not known and requires further study. Finally, although our results are consistent with other studies from China, as described above, few studies examining the association of drug use and sex work in China have been published and other studies are needed in more parts of China.

In summary, we find that the prevalence of HIV is high in FSWs in Yunnan, particularly among those who also use illegal drugs, work in higher risk entertainment establishments, have been in commercial sex for ≥5 years, or are HSV-2 antibody positive. We also find that many HIV-infected FSWs do not consistently use condoms with either clients or their regular sex partners, putting both sides at risk of infection. Infected clients may serve as the bridging population from HIV-positive FSWs to their low risk wives. Reports of HIV prevalence >1% in antenatal clinics from certain high risk areas in Yunnan (6) provides evidence that this bridging is already occurring. Although traditional HIV prevention methods among FSWs such as condom promotion should continue to be emphasized, other interventions should be considered that target the highest risk FSWs and particularly those working on the street, in temporary sublets, in beauty salons or in saunas. Significant attention should focus on the overlap group of drug-using FSWs and needle exchange and methadone or other drug reduction treatment should be promoted to this cohort. Education regarding vaginal douching and STI symptoms and treatment should be provided.

Acknowledgments

Funding

National Institute of Allergy and Infectious Diseases, U.S. National Institutes of Health (U19 AI51915-05).

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