Sexually Transmitted Diseases

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Sexually Transmitted Diseases:
doi: 10.1097/01.olq.0000218881.01437.99

Syphilis Among Female Sex Workers in Southwestern China: Potential for HIV Transmission

Ruan, Yuhua PhD*; Cao, Xiaoyun MS*; Qian, Han-Zhu MD, PhD†; Zhang, Li MS*; Qin, Guangming BS‡; Jiang, Zhengqing§; Song, Benli§; Hu, Wei§; Liang, Shu BS†; Chen, Kanglin§; Yang, Ye MS*; Li, Xinxu MS*; Wang, Jun MS*; Chen, Xi MS*; Hao, Chun MS*; Song, Yanhui MS*; Xing, Hui MS*; Wang, Ning MD, PhD*; Shao, Yiming MD, PhD*

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From the *State Key Laboratory for Infectious Disease Prevention and Control and the National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; the †Division of Preventive Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama; the ‡Sichuan Provincial Center for Disease Control and Prevention, Chengdu, Sichuan Province, China; and the §Xichang Center for STD and Leprosy Control, Xichang City Sichuan Province, China

This study was supported by grants from the Ministry of Science and Technology of China (2004BA719A01, 2004BA719A02), the Ministry of Health of China (WA2003-13), and the National Natural Science Foundation of China (30571612, 10501052).

Correspondence: Yiming Shao, MD, PhD, State Key Laboratory for Infectious Disease Prevention and Control, and National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China., 27 Nanwei Road, Xuanwu District, Beijing 100050, China. E-mail:

Received for publication August 30, 2005, and accepted March 10, 2006.

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Objective: The objective of this study was to investigate the prevalence and risk factors of syphilis infection among female sex workers in a southwestern Chinese city along a drug trafficking route.

Methods: From December 2004 to January 2005, 343 female sex workers (FSWs) were recruited through community outreach and peer referring. Confidential questionnaire interviews were administered to collect information on sexual and other sexually transmitted diseases/HIV risk behaviors. Cervical and blood samples were collected to test for syphilis and HIV antibodies and Neisseria gonorrhoeae infection; Condyloma acuminatum infection was diagnosed clinically.

Results: Of 343 FSWs, 15.7% were infected with syphilis. The prevalence of HIV, gonorrhea, and C. acuminatum was 0.6%, 2.0%, and 1.5%, respectively. The subtype of 2 HIV-1 infections was both CRF 07BC. Nearly 10% of FSWs reported using illicit drugs. Consistent use, inconsistent use, and never use of condoms with commercial sex clients in the last month were reported by 53.9%, 38.5%, and 7.6% FSWs, respectively. Longer duration of sex work (odds ratio [OR] = 1.98; 95% confidence interval [CI] = 1.08–3.62), working at low-end establishments (OR = 2.03; 95% CI = 1.10–3.76), and if primary sex partners had sex with other women in the past 6 months (OR = 2.06; 95% CI = 1.08–3.91) were independently associated with syphilis infection.

Conclusions: High prevalence of syphilis and overlapped unprotected commercial sex and drug using behaviors among FSWs along a drug-trafficking route may suggest a potential for rapid spread of HIV from injection drug users to FSWs and then to the general population and underscore the urgency of preventive interventions to break the bridge of FSWs for HIV/sexually transmitted disease spread.

SINCE CHINA ADOPTED A FREE market economy and an open door policy in 1978, commercial sex activities have flourished across the country. The Chinese Public Security Office estimated that there are 4 to 6 million sex workers nationwide in 2000, an increase of 160-fold in number compared with 1985.1 During this period, the annual cases of 8 reportable sexually transmitted diseases (STDs, including syphilis and HIV/AIDS) increased by 147-fold from 5838 to 859,040.2 The skyrocketing STD epidemic is becoming an increasingly important public health problem in China. Furthermore, studies have shown several STDs may increase HIV susceptibility. Ulcerative diseases such as syphilis are more likely than nonulcerative ones such as Neisseria gonorrhoeae and Chlamydia trachomatis infections to facilitate HIV transmission.3,4 Syphilis is a common STD in China, which accounts for approximately 10% of the reported STD cases nationwide, for example, 9.9% in 2000 and 10.9% in 2004.2,5

Risk of HIV/AIDS in China is shifting from illegal plasma/blood-collecting practices and injection drug use to sexual contacts.1 Heterosexual transmission of HIV through female sex workers (FSWs) is of particular concern. National sentinel surveillance data showed that average prevalence of HIV among FSWs increased from 0.02% in 1996 to 0.93% in 2004.6 Epidemiologic studies found a wide range of STD prevalence among FSWs, for example, HIV ranges from 0% to 10.3%.7–10 Use of different sampling methods and geographic variation of HIV infection may explain the results. We conducted a community-based survey among FSWs in a southwestern Chinese city located on a drug-trafficking route, where HIV and syphilis infections are common among injection drug users (IDUs).11–13 This article presents the prevalence of STDs with a focus on syphilis infection.

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Study Design and Study Population

This cross-sectional study was conducted between December 2004 and January 2005 in Xichang City, Sichuan Province, aiming to estimate baseline prevalence of HIV and other STDs among FSWs, describe their STD/HIV risk behaviors, and set up a cohort. Xichang City is located on a major drug-trafficking route.13,14 Its total population is 617,000 and 10% are Yi minority people. Local STD Control Center estimates that there are approximately 2800 FSWs and 3200 IDUs in Xichange City. The prevalence of HIV and syphilis among IDUs in 2000 was 11.3% and 15.3%, respectively,11,12 and HIV incidence was 3.17 per 100 person-years during a 12-month follow up.13

The sites of sex work in Xichang City were systematically mapped. Study participants were primarily recruited using community-based outreach. Project outreach workers reached out to the entertainment places, distributed study-related information to FSWs, and invited them to voluntarily participate in the study. Outreach workers also invited brothel managers and FSWs to refer other FSWs to the study. Eligibility criteria included: 1) female; 2) self-report of commercial sex in the past 6 months; 3) will stay in Xichang for the next 12 months; 4) able and willing to provide informed consent; 5) able and willing to provide contact information for follow up. Written informed consent was obtained from all study participants. Eligible participant completed HIV/STD risk assessment interview and received HIV pretest and risk-reduction counseling, cervical sample was collected, and blood specimen was drawn. Participants were given HIV posttest counseling when they returned for their test results. Study protocol and informed consent were approved by the Institutional Review Board of the National Center for AIDS/STD Control and Prevention of the Chinese Center for Disease Control and Prevention.

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Data Collection

Data were collected using an interviewer-administered questionnaire. Each study participant was assigned a unique and confidential identifier code for her questionnaire and specimens. Demographic variables included age, gender, ethnicity, education, previous employment, current marital status, income, birth area (rural or urban), and current residence. Sexual or other behavioral variables included age at sex debut, age at first commercial sex, establishment of sex work, frequency and number of sex with primary sex partner or commercial sex clients in the past 6 months, condom use in the last month, number of new sex partners in the past 6 months, average charge per sex trade, and drug use in the past 3 months.

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Laboratory Analysis and Sexually Transmitted Disease Diagnosis

All blood specimens were tested for both HIV and syphilis antibodies. HIV antibody was tested by enzyme-linked immunosorbent assay (ELISA, Beijing Jinhao Biologic Production Co., China) and was confirmed by an HIV-1/2 Western Blot immune assay (HIV Blot 2.2 WB; Genelabs Diagnostics, Singapore). Antibody to Treponema pallidum antigen (p15, p17, and p47) was screened by ELISA (Beijing Jinhao Biologic Production Co.) and retested by T. pallidum passive particle agglutination (TPPA; Fujirebio Inc., Japan). HIV subtype analysis was based on the sequences from the env and gag regions of the HIV RNA envelope. Cervical samples were tested for the presence of N. gonorrhea by blood agar culture. Condyloma acuminatum infection was clinically diagnosed based on Chinese STDs Diagnosis Guidelines.

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Statistical Analysis

Huang and colleagues grouped Chinese FSWs into 7 categories.14 However, in reality, there is no clear cut in these categories because FSWs may move from one category to another. In this article, we categorized FSWs as high end if they worked in star hotels, big karaoke and dancing bars, saunas, and VIP clubs; or low end if they worked in hair salons, massage parlors, small hotels, and on streets.

Original questionnaire and laboratory testing data were double-entered into EpiData software (EpiData version 3.0; The EpiData Association, Odense, Denmark), then transferred into a SAS (SAS version 8.2; SAS Institute Inc., Cary, NC) database for analysis. STD seroprevalence rates were computed. Univariate logistic analyses were used to explore factors associated with syphilis infection. Variables that were significant in univariate models (P ≤ 0.05) or were biologically plausible were included in a multivariable logistic regression model. Those not significant in the multivariable model were eliminated in a stagewise manner, identifying variables that were independently associated with syphilis seropositivity.

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Sociodemographic Characteristics

Five of 99 establishments approached did not agree to participate; 28 FSWs refused to participate or withdrew from the study because of unwillingness to answer sensitive questions. Of the 343 study participants from 94 establishments, 91.8% were recruited through outreach, 6.4% through peer referring, and the remaining 1.8% through referring by establishment managers. Approximately half of participants were from high-end (49.3%) and low-end (50.7%) establishments, respectively. The average age was 23.7 years, ranging from 15 to 40 years; 70.3% participants were born in rural areas; 38.2% were local residents and the majority were from other parts of Sichuan Province (53.6%) or outside Sichuan (8.2%). Nine percent were Yi minority; the majority of participants had ever attended junior high school (52.5%) or primary school (26.2%); 56.3% were single, 22.7% married, and 15.7% currently divorced; 34.1% reported to be farmers before sex work, 21.3% were waitresses, and 23.6% were unemployed. Nearly 10% reported to be drug users, and 4.1% injected drugs in the past 3 months.

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Sexual Behaviors

The median age of initiating sex work was 21 years, ranging from 15 to 34 years. The median duration of sex work was 1 year. Sixty percent (203 of 343) had at least one primary sexual partner (spouse, boyfriend, or fiancée) and 24.5% had at least 2 primary sex partners in the past 6 months. Approximately one third (76 of 203) of those who had primary sex partners knew that their partners had sex with other women in the past 6 months. The median numbers of all clients and new sex partners in the past 6 months was 80 and 70, respectively. Approximately half of participants reported consistent use (53.9%) in the last month; the remaining reported inconsistent use (38.5%) or never use (7.6%). Consistent, inconsistent, or never use of condoms with primary sex partners were 41.9%, 8.6%, and 49.6%, respectively. Oral sex and anal sex were reported by 1.2% and 4.7% participants, respectively.

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Prevalence of Syphilis and Other Sexually Transmitted Diseases

Of 343 participants, 15.7% were infected with syphilis. The prevalence of HIV, gonorrhea, and C. acuminatum infection was 0.6% (2 of 343), 2.0% (7 of 343), and 1.5% (5 of 343), respectively. The overall prevalence of any STDs was 20.1%. One HIV-infected FSW was a drug user. Analysis of HIV-1 sequence from env and gag regions of the virus envelope indicated that HIV-1 subtype in these 2 positive participants was CRF_07BC.

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Factors Associated With Syphilis Infection

In univariate analyses, the only sociodemographic factor significantly associated with syphilis infection was low-end places of sex work. Age, ethnicity, years of education, previous occupation, yearly income, married status, birth place, current residence, and average charge per sex service were not significantly associated with syphilis infection (P > 0.05; Table 1). Several sexual behavioral factors were associated with syphilis infection, including duration of sex work ≥2 years and if the primary sex partner had sex with other women in the past 6 months (Table 2).

Table 1
Table 1
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Table 2
Table 2
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Three factors significant in univariate analyses or biologically plausible were fitted into a multiple logistic regression model. Drug use was not entered into the final model. Low-end place of sex work (odds ratio [OR] = 2.03; 95% confidence interval [CI] = 1.10–3.76), longer duration of sex work (OR = 1.98; 95% CI = 1.08–3.62), and if the primary sex partner had sex with other women in the past 6 months (OR = 2.06; 95% CI = 1.08–3.91) were independently associated with syphilis infection (Table 3). Meanwhile, all of these 3 factors were associated with drug use (P < 0.001, not shown in the table).

Table 3
Table 3
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Prostitution is illegal in mainland China. Most Chinese studies among FSWs either recruited participants from detention or reeducation centers or used convenience samples.7,15,16 In our community-based study, the establishments of sex work in Xichang City were systemically mapped by the trained and experienced outreach workers who had participated in several outreach projects, including the Xichang IDU Study.12 Approximately 95% of establishments and 92% of FSWs approached by outreach workers participated in the study. Participants worked in different establishments such as a star hotel, big karaoke parlor, dancing bar, sauna, VIP club, hair salon, massage parlor, small hotel, and streets, which covered a wide spectrum of FSWs. Therefore, the participants should represent a community sample of this population in Xichang City.

The prevalence of syphilis among FSWs in this southwestern Chinese city (15.7%) was similar as those in other southern Chinese cities (14% in Guangzhou and 17.7% in Hainan)16,17 and was higher than those in inner provinces (10% in Xinjiang and 7.4% in Shangdong).15,18 The prevalence rates of other STDs were low: HIV 0.6%, gonorrhea 2.0%, and C. acuminatum infection 1.5%. The most worrisome finding from this study is the high prevalence of syphilis considering Xichang is located on one major drug-trafficking route. HIV has reached an epidemic level and is still on a rising trend among IDUs in Xichang.11,13 HIV has been introduced into the FSW population in this area. These 2 HIV-infected FSWs had HIV-1 subtype CRF_07BC, which is the same as that among IDUs in Xichang,13 which suggests a possible transmission of HIV across these 2 subgroups. Nearly 10% FSWs were drug users. High prevalence of syphilis, which can cause genital ulcers, could put FSWs at a high risk of acquiring and transmitting HIV through sexual contacts. The conditions for epidemiologic synergy exist. Today’s syphilis might mean tomorrow’s HIV in this study site.

Longer period of sex work, primary sex partners’ sex behavior (having sex with other women), and working at low-end establishments were independently associated with higher risk of syphilis infection among FSWs in this study. Longer period of work exposure to multiple commercial sex partners and complex sex networks may increase their chances of exposing to infected partners and therefore increase their risk of STDs. Generally speaking, FSWs at low-end establishments have low incomes and education and low frequency of condom use.14 In this study, nearly half of participants reported inconsistent or no condom use with commercial sex partners and even higher proportions with their primary sex partners. Lower protection and higher prevalence of syphilis among low-end FSWs underscore the need of giving special attention to them in intervention efforts.

Drug use is significantly associated with duration of sex work, type of establishments, and whether their primary sex partners had sex with other women, but drug use was not independently associated with syphilis infection. Syphilis is mainly transmitted by sexual contacts or through the mother-to-child route and rarely through sharing needles.19 However, drug use could be an important risk factor for HIV infection. In many countries, HIV has been initially spread among drug users, and then sexual transmission of HIV has become a significant or dominant route.20 High prevalence of syphilis and unprotected sex behaviors among FSWs along a drug-trafficking route may suggest a bridging role of FSWs in HIV transmission from IDUs to the general population. Comprehensive health education and behavioral intervention are urgently needed to target to both FSWs and IDUs and break their bridging networks for HIV transmission.

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