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Behaviour
Original article
Prevalence of HIV, syphilis, and HCV infection and associated risk factors among male clients of low-paying female sex workers in a rural county of Guangxi, China: a cross-sectional study
  1. Chen Zhang1,
  2. Xiaoming Li2,
  3. Shaobing Su2,
  4. Liying Zhang2,
  5. Yuejiao Zhou3,
  6. Zhiyong Shen3,
  7. Zhenzhu Tang3
  1. 1Department of Epidemiology, Vanderbilt University, Nashville, Tennessee, USA
  2. 2Wayne State University School of Medicine, Detroit, Michigan, USA
  3. 3Guangxi CDC, Nanning, China
  1. Correspondence to Chen Zhang, Department of Epidemiology, Vanderbilt University, 2525 West End Avenue, Suite 725, Nashville, TN 37203, USA; chen.zhang.1{at}vanderbilt.edu

Abstract

Background The purpose of this study was to examine prevalence of HIV, syphilis and hepatitis C virus (HCV) infection as well as related risk factors among a group of male clients of low-paying female sex workers (FSW) (eg, women who usually encounter their clients on the street or small establishments in rural or less developed areas, or who charge low fees for each sexual service) in a rural county of China.

Method Cross-sectional study conducted in 2011 in a rural county of Guangxi in China. A total of 102 clients who reported information on demographics and HIV risks (eg, inconsistent condom use) and provided blood sample to test for HIV, HCV and syphilis were included in the data analysis. Both bivariate and multivariate analyses were employed to explore risk factors of HIV, HCV and syphilis infection.

Results Most of participants were of Han ethnicity with a mean age of 61.8 years. The majority of them lived in rural areas and worked as farmers with limited disposable cash incomes. The sample reported a high rate of unprotected sex with FSW in the last sex episode (83.7%) and inconsistent condom use in the last 6 months (95.9%). The overall prevalence of HIV, HCV and syphilis was 1.9%, 1.0% and 18.4%, respectively.

Conclusions Findings suggest that male clients, especially the elderly ones, are at a high risk of HIV infection given prevalent unprotected sex and high prevalence of syphilis. Culturally-appropriate, age-specific interventions are urgently needed to curb the HIV/sexually transmitted infection epidemic among this at-risk population in China.

  • EPIDEMIOLOGY (GENERAL)
  • HIV
  • HEPATITIS C
  • SYPHILIS
  • SEXUAL BEHAVIOUR

https://doi.org/10.1136/sextrans-2013-051275

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    Introduction

    Although China remains as a low-prevalence country in the HIV epidemic, the number of new infections has increased gradually each year.1 Heterosexual transmission becomes a dominant route of transmission accounting for 62.6% of the 48 000 new infections in 2011 in China.1 Female sex workers (FSW) constitute one of the most at-risk populations for HIV infection and transmission.2 Based upon different methodologies, an estimated four to six million FSW work hierarchically in China.3–7 Numerous studies have documented the high risk of HIV infection among FSW and also repeatedly call for attention to their male clients.8 ,9

    In the HIV epidemic in China, male clients of FSW may play an important role in the escalating heterosexual transmission.10–12 Limited literature has documented a high prevalence of HIV and other sexually transmitted infections (STIs) as well as high risk behaviours (eg, unprotected sex) among male clients.4 ,12–14 In addition, existing studies among male clients in China have suggested different patterns of demographic characteristics, risk behaviours (eg, unprotected sex) and HIV/AIDS knowledge among male clients who visit FSW working at different hierarchies of the commercial sex.13–15 Men who visited high-paying FSW usually had a high socio-economic status (eg, business men or government officers). They might be more concerned about their health and more likely to practice protected sex.10 ,16 On the other hand, men who patronised low-paying FSW might be at a higher risk of HIV infection as low-paying FSW were usually less likely to practice safe sex compared with their peers who worked at high-paying venues.10 ,17 ,18 Client of low-paying FSW were usually featured as less educated with low socio-economic status.10 For instance, Lau et al (2009) reported that the rate of inconsistent condom use was as high as 77.0% among a group of male clients who patronised low-paying FSW in the last 6 months.15

    In addition to their unprotected sex with FSW, many male clients also practice unprotected sex with their non-commercial sexual partners including wives, girlfriends and non-paying casual sexual partners.19 ,20 For instance, in a study of mine workers in China, 61.2% and 84.1% of the participants reported never using a condom with FSW and their regular partners, respectively.20 The multiple, often concurrent, partnerships, coupled with high rates of unprotected sex, render male clients a potentially bridging role of transmitting HIV/STI from ‘high-risk’ groups to the general population.

    Despite potentially significant role of male clients in HIV/STI epidemic, few studies have focused on this population in China as well as other developing countries;12 ,20 ,21 studies among male clients of low-paying FSW are even scarcer.18 ,22 ,23 In the current study, we aim to examine prevalence of HIV, syphilis and hepatitis C virus (HCV) infection and its associated risk factors among a group of male clients of low-paying FSW in a rural county of China.

    Method

    Study design

    We employed a cross-sectional study design in the current study.

    Study setting

    Data in the current study were collected from June to August of 2011 from a rural county (‘County A’) in Guangxi Zhuang Autonomous Region (Guangxi). Guangxi has experienced a rapid increase of HIV prevalence since the first case of HIV infection was diagnosed in 1996. A total of 69 548 HIV/AIDS cases were reported as of June of 2011, which placed Guangxi second in terms of cumulative HIV seropositive cases among all provinces in China.24 County A is located in the northeast of Guangxi with a population of 430 000, among which 18% are ethnic minorities and nearly 15% are elderly people who are 60 years or older.25 As County A is primarily an agriculture county, the average monthly disposable cash income for each rural household is about ¥230 (approximately US$35 at the time of this study).25 Similar to the trend in Guangxi, the HIV epidemic in County A is mainly driven by heterosexual transmission.24

    Participants and recruitment

    Prior to data collection, our research team worked closely with local public health workers to identify low-paying commercial sex venues that were known to public health officials in the county. Consistent with a previous study that was conducted in the same region, we defined low-paying FSW as ‘women who usually encounter their clients on the street or small establishments in rural or less developed areas, or who charge low fees for each sexual service’.18 A total of 63 low-paying sex venues including road-side restaurants, mini-hotels, rental houses, hair salons, card-playing houses and elderly activity centres were identified by the research team. After establishing rapport with venue owners, we explained the purpose of the study and asked for their permission to conduct survey in their premises. Once we received the permission, trained health workers from the local Center for Disease Control and Prevention (CDC) approached eligible FSW working in these venues and asked for their help to recruit their male clients for the study. Eligible participants (1) were males who were 18 years or older and (2) ever visited FSW at least once in the past 6 months. An estimated 25% of the venues and 30% of the women who were approached refused to participate. A total of 113 FSW participated and referred their clients. Once these clients were identified and referred by the FSW, local health workers met these male clients at the venue and asked them to participate in this research study.

    An estimated 10% of the male clients who were approached refused to participate. A total of 103 men provided written informed consents and completed a self-administered anonymous short survey. We included 102 participants who provided blood samples for HIV, syphilis and HCV testing in the data analysis. To reduce social desirability bias and assure the confidentiality, the survey was conducted in separate rooms or private spaces at or near venues where the participants were recruited. No one was allowed to stay with participants during the survey except the interviewer who provided participants with assistance when necessary. The survey took about 15 min to complete. Participants were provided with a small gift (eg, soaps, detergents) with a cash value equivalent to US$4.50 as a token of appreciation for their participation. In addition, treatments and referral services were provided for participants who tested positive for HIV, HCV or syphilis. The study protocol was approved by the Institutional Review Board at Guangxi CDC, China.

    Measures

    Demographic information

    Participants were asked to provide information of their age, ethnicity, current occupation, educational attainment, marital status and monthly disposable cash income in Chinese currency yuan (eg, less than ¥200, ¥201–500, ¥501–1000 or more than ¥1000). For the purpose of data analysis in the current study, we categorised ethnicity into Han and non-Han, educational attainment into no more than middle school versus at least middle school, marital status into currently married (including cohabited) versus currently not married (including divorced or widowed), occupation into farmers versus non-farmers, and monthly disposable cash income into less than ¥200 versus at least ¥200. In addition, for the purpose of data analysis, we divided clients into three groups based upon their age distribution with equal proportions for each group: younger than 50-years-old, 50–70-years-old and older than 70-years-old.

    Sexually risky behaviours

    Participants were asked if they also had sex with non-commercial partners such as stable partners or casual non-paying partners. We further asked them if they used a condom in their last sex act and the frequency of using condoms in the past 6 months (never, sometimes and always). Respondents who did not answer ‘always’ to the second question were considered using condoms inconsistently. In addition, we asked participants to identify reasons why they did not want to use a condom with FSW during their sexual episodes. The reasons, in a form of checklist, included ‘affecting sex pleasures’, ‘believing both persons are healthy’, ‘no need for contraception’, ‘affecting intimacy with partners’, ‘saving money’ and ‘just did not want to use’. Participants were also asked whether they had a history of STI, ever used any illegal drugs, ever had any sexual partners who had an STI, ever sold blood (eg, whole blood, blood components) prior to 1998 (the year Chinese government banned commercial blood donation) and ever had tested for HIV.

    HIV/AIDS knowledge

    Knowledge of HIV/AIDS was assessed with eight questions regarding possible transmission routes (eg, blood transfusion, needle sharing and vertical transmission during delivery), non-transmission routes (eg, having meals together, mosquito bites), preventive measures (eg, consistent condom use, maintaining only one sexual partner) and a general question regarding whether a person can be determined of the infection status by his/her appearance. For each question, the response was coded as 1=correct answer or 0=incorrect answer. The composite score of the HIV/AIDS knowledge was calculated by summing correct answers to all eight questions with a higher score indicating a higher level of HIV/AIDS knowledge.

    HIV, syphilis and HCV testing

    Following the standard protocol and laboratory methods established by the China National Center for AIDS/STI Control and Prevention,26 participants were tested confidentially for HIV, syphilis and HCV antibody.

    Data analysis

    First of all, participants’ demographic characteristics were tabulated by age groups. Second, χ² tests were employed to detect participants’ sexual behaviours and reasons of not using a condom, HIV knowledge, HIV risks, and results of HIV/STI testing by age groups, marital status, educational attainment and levels of monthly disposable cash income. Finally, bivariate and multivariate logistic regression models were employed with HIV, HCV and syphilis infection as the dependent variables. HIV risks (eg, inconsistent condom use, multiple partnerships) and potential confounders including demographics (eg, age, marriage status and ethnicity) served as independent variables. We only included variables that showed bivariate significance (p<0.10) in the multivariate logistic regression model. All statistical analyses were performed using SPSS V.17.0 for Windows.

    Results

    Sample characteristics of the male clients

    As shown in table 1, participants (n=102) had a mean age of 61.8 years (median=63.0, SD=15.6) with a range of 27–90. The majority of them (84.3%) were of Han ethnicity. Almost half (42.2%) of the participants were currently married or cohabited, only 24.5% had middle school education or above, 93.1% were working as farmers and nearly half of them had a monthly disposable cash income less than ¥200. Male clients between 50 and 70 years of age had the lowest monthly disposable cash income among all participants in the three age groups (p<0.05).

    View this table:
    Table 1

    Demographics and HIV risks among MCFSW

    Sexual behaviours and reasons of not using a condom

    Among the 102 participants, a third had sex with non-commercial partners in the past 6 months. Among participants who had sex with non-commercial sex partners, 97.1% did not use a condom in the last sex act and 97.1% reported inconsistent condom use in the past 6 months. Table 2 revealed the pattern of sexual behaviours with their commercial sex partners: 83.7% of male clients reported not using a condom in the last sex act and 95.9% reported inconsistent condom use in the past 6 months. The top three reasons of not using a condom were ‘believing both persons are healthy’ (67.3%), ‘affecting sex pleasure’ (36.7%) and ‘no need for contraception’ (17.3%).

    View this table:
    Table 2

    Sexual behaviours and reasons of not using condoms with FSW among clients by age, education, cohabiting status and household disposal incomes

    HIV knowledge, HIV risks and HIV/STI testing

    The composite score of HIV knowledge is 3.24 (SD=3.06) among the 102 male clients. About 40% of male clients knew the three transmission routes of HIV correctly. Participants were less knowledgeable of the non-transmission routes compared with other routes of transmission. Less than half of male clients knew the preventative methods of HIV. Participants who were older than 50-years-old, had less educational attainment with less monthly disposable cash income had poorer HIV knowledge compared with their peers (p<0.05). Among all 102 participants, a third reported concurrent partnerships, 8.7% of them reported a history of STI, 1.0% reported ever using illegal drugs, 1.0% ever sold blood before 1998 and 2.9% ever had HIV testing. The prevalence of HIV, HCV and syphilis was 1.9%, 1.0% and 18.4%, respectively (table 3). The final multivariate logistic regression analyses revealed no significant associations among HIV, syphilis and HCV infection and other risk factors (eg, inconsistent condom use, illicit drug use).

    View this table:
    Table 3

    HIV knowledge and HIV risks among MCFSW by age, education, cohabiting status and household disposal incomes (N=102)

    Discussion

    To the best of our knowledge, this study was one of the first efforts to examine sexual behaviours, HIV knowledge and HIV risks among clients of low-paying FSW in China. Findings from the current study suggest clients of low-paying FSW featured as old (average age is older than 60-years-old), pursuing labour-intensive work (eg, farmers) with low monthly disposable cash income, and are particularly vulnerable for HIV risks given their high-risk behaviours (eg, unprotected sex) and high prevalence of syphilis. The unique characteristics of male clients of low-paying FSW raise a concern for increasing the HIV/STI epidemic among the elderly in China.1 ,27 ,28 With the low-cost of visiting low-paying FSW,21 ,28 ,29 availability of medications for sexual dysfunction25 and peer influence,12 ,25 older men are more likely to patronise low-paying FSW for sex services. These were also the plausible reasons for the skewed age distribution in the current sample.

    In our study, the overall HIV prevalence among male clients is 1.9%, which is comparable with studies conducted among male mine workers in Yunnan (1.8%)11 and clients recruited from different tiers of sex venues in Sichuan (1.5%),12 but it is much higher than that in general populations of China (0.058% at the end of 2011).1 The syphilis prevalence of the current sample (18.4%) is about three times higher than a study conducted among clients from different tiers of sex venues in Sichuan province (5.3%).13 However, the prevalence of HCV in the current sample (1.0%) is much lower compared with their peers in Sichuan (8.7%).13 These discrepancies among different studies may be due to the different sampling strategies and lab testing techniques. More research is needed to explore reasons of the discrepancies among different samples of male clients. In addition, a third of the male clients in our study had sex with their non-commercial partners. And the majority of the male clients had unprotected sex with both their commercial and non-commercial partners. Thus, high rates of unprotected sex and concurrent sexual partnerships, coupled with high rates of syphilis and HIV infection, suggest that male clients could play a significant role in transmitting and spreading HIV/STI from high-risk to low-risk populations.

    In the current study, we found that the majority of male clients had low perceived risk and poor HIV knowledge, which is consistent with previous studies.10 The prevalent unprotected sex combining with low awareness of HIV risks indicated the urgency of implementing HIV/STI prevention programmes among this at-risk population. By further examining our data, we found that male clients above 50 years of age had even poorer HIV knowledge and lower risk perception but a higher rate of unprotected sex. Perhaps older adults in China are usually less educated and traditionally perceive condoms as a device for contraceptives rather than a method protecting them from HIV/STI.30 Therefore, age-specific intervention prevention programmes are urgently required.

    This study explored demographic and behavioural characteristics of male clients of low-paying FSW. The findings of the current study provided preliminary data to inform future research. However, our findings should be interpreted with caution because of several limitations. First, we may not be able to generalise the findings to other male client populations in China as the participants in the current study were recruited in a rural county in a multi-ethnic region of China. Second, due to the illegality of commercial sex in China, our data were subject to social desirability bias. Third, the recruitment strategy in the current study may have resulted in sampling bias as FSW might only be able to identify or refer clients who they were familiar with (eg, repeated clients). Fourth, the small sample size may lead to insufficient statistical power to detect significant associations among some of the measures.

    In summary, findings in our study provide preliminary data for health practitioners and suggest some future directions to curb the HIV/STI epidemic in China. First, considering the characteristics of men who visit low-paying FSW, HIV educational campaign should be expanded to cover both younger and older populations,27 especially the older male adults who were the typical clientele of low-paying FSW and often performed unprotected sex. In addition, tailored HIV/STI prevention messaging (eg, pro-condom use norms) should be delivered and disseminated among male clients with different levels of health literacy and various socio-economic backgrounds via feasible channels (eg, community-based outreach programmes, booklets, hospital-based seminars, voluntary counseling and testing (VCT) clinics or text message). Second, considering the high prevalence of HIV and syphilis, culturally-appropriate, age-specific, and non-judgmental counselling, screening and treatment services should be developed and provided to this growing and at-risk population. Third, because of the illegality of commercial sex, peer-led risk reduction interventions may be more receptive and effective among the male clients.29 Culturally and socially acceptable network-based interventions may be promising by targeting this at-risk group. Fourth, considering a large proportion of male clients also having sex with their non-commercial partners, interventions should consider engaging male clients’ regular or non-paying casual partners. Therefore, preventive education concerning condom use and HIV/STI prevention programmes should be provided to the low-paying FSW, and other women, especially women in rural areas.

    Key messages

    • Demonstrate unique characteristics of male clients who visit low-paying female sex workers in China.

    • Present prevalence of HIV, hepatitis C virus and syphilis infection as well as their associated risky behaviours among this at-risk population.

    • The preliminary data in the current study provide direction for future research among this at-risk population.

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    Supplementary materials

    • Abstract in Chinese

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

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    Footnotes

    • Handling editor Jackie A Cassell

    • Contributors CZ made substantial contribution to conception and design as well as manuscript development. XL supervised the project, and participated in its design and coordination and helped to draft the manuscript. SS and LZ performed data analysis and manuscript development. YZ, ZT and ZS collected research data. All authors read and approved the final manuscript.

    • Funding The study described in this report was in part supported by NIH Research Grant R01AA018090 by the National Institute for Alcohol Abuse and Alcoholism.

    • Disclaimer The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute for Alcohol Abuse and Alcoholism.

    • Competing interests None.

    • Patient consent Obtained.

    • Ethics approval IRB in Guangxi CDC.

    • Provenance and peer review Not commissioned; externally peer reviewed.