At the end of 2005, the Chinese Ministry of Health, UNAIDS and World Health Organisation (WHO) jointly estimated that China had 650 000 individuals infected with HIV – over four times the cumulative number of confirmed cases at that time (141 241). HIV/AIDS cases have been on the rise in recent years and sexual transmission is now the principal route of transmission, accounting for 49.8% of new infections in 2005. Same-gender sex is thought to be a major contributor, with an estimated 47 000 men who have sex with men (MSM) living with HIV/AIDS in 2005 .
HIV has been identified among MSM communities in various parts of China. In northeastern China, the prevalence of HIV has been reported at 1.38% among MSM in Harbin (the provincial capital of Heilongjiang) . Similar estimates have been described among MSM in east China (1.83% in Hefei, Anhui Province) , as well as in southern China . Recent data also suggest that the number of HIV infections among MSM in China is increasing. For example, in Beijing, the prevalence of HIV was 3.1% among MSM in 2001–2002 , while a more recent survey, conducted in 2005, found a higher prevalence of 4.6% . In 2006, the Chinese Ministry of Health estimated that there were 5–10 million MSM living in China, of which 1.35% were infected with HIV .
Although the prevalence of HIV among MSM in China is currently low, HIV could spread rapidly within the MSM community given high rates of unprotected anal sex. For example, in Hefei and Harbin, 84 and 85% of respondents, respectively, reported that they had not used a condom during anal sex in the previous 6 months .
Under significant pressure from society and family, most MSM will eventually get married. In a study which recruited MSM from around the country, 34.5% of respondents were or had been married, and close to half reported having had sex with women . Thus, there is the potential for MSM to serve as a sexual ‘bridge’ between high-risk men and low-risk women. This sexual mixing pattern may contribute to the sexual transmission of HIV to heterosexually active adults.
One group at particular risk of acting as this bridge is male sex workers (MSW). Due to political and cultural restrictions , as well as other barriers including official denial about their existence, social marginalization, and a lack of information about their needs and concerns, few studies have investigated the relationship between the male sex trade and HIV/AIDS, resulting in a lack of sufficient data and corresponding health interventions. MSW are particularly vulnerable to HIV/AIDS because they may engage in unsafe sexual behaviors with their clients, most of whom are gay or bisexual men, but who may also include women. Thus, the risk of HIV among gay or bisexual men could mirror concomitant risks among male sex workers.
The purpose of this study was to measure the prevalence of sexual behaviors known to facilitate HIV transmission among MSW.
Ethical approval was received from the Ethical Review Committee (i.e. Institute Review Board) in the Chinese Academy of Preventive Medicine (re-organized as Chinese Center for Disease Control and Prevention in 2002).
Study site and recruitment
The study was conducted in Beijing, the Capital City of China, and Qingdao, a coastal city in Shandong Province. The two cities were chosen because, according to the information from key informants, they are tourist destinations for both local and foreign tourists, have a more developed economy than most other areas in China, and are home to an increasing number of MSM.
Background information about the study sites, local MSM community and venues frequented by MSM and MSW was gathered through interviews with two key informants in each city. These men also assisted in recruiting study participants. The first author worked as a waiter in one of these venues and lived in a dormitory with other staff to establish a relationship with them and the venue's patrons, and invite them to participate in the study. The initial participants were then asked to refer friends. Eligible participants were aged 18 years or older and had engaged in sex in the year prior to the survey.
Participants completed a detailed questionnaire through face-to-face interviews. Interviews were conducted in a private room and informed consent was taken from each participant before the interview commenced.
The questionnaire included questions on: (1) demographic data, including age, ethnicity, housing status, education; (2) sexual risk behaviors, including insertive and receptive anal and oral sex with regular and commercial partners (both male or female), condom use, age at first sexual encounter; and (3) other risk behaviors, including alcohol and tobacco use, as well as use of illegal drugs (marijuana, cocaine, heroin, ketamine and ecstasy), and how they were administered (orally, smoked, injected, inhaled). Sex trade involvement was defined as the exchange of sex for money, drugs, goods, clothing or shelter.
All data were double-entered and validated in EPI-DATA. Univariate analyses were first conducted using χ2 tests for categorical variables. Multivariate models were explored to identify independent risk factors associated with condom use in the sex trade. Variables that were significant in the univariate analyses (P ≤ 0.05) were entered into the multivariate model. Backwards, stepwise, logistic regression was used, with removal of variables based on P > 0.20. All reported P-values are two-sided.
Socio-demographic characteristics of male sex workers
Eighty-five male sex workers finished the face-to-face interview. Median age was 22 years (range: 18–40 years). The majority (67%) were the 20–24 years age group. Nearly all participants were Han (94%), which is the major ethnic group in China. Most were unmarried (98%), had at least a high school education (61%) and were unemployed (59%). Of those who were employed, 21% were waiters or bartenders, and a further 12% were studying at a university. Forty-five per cent reported living in rented apartments, while 40% were living in the same venues where they worked as sex workers (Table 1).
Forty-four percent of interviewees identified themselves as homosexual, 44% identified as bi-sexual and 12% said they were heterosexual.
Drug use was common, with 44% reporting they had used illegal drugs. The majority (86%) took drugs orally, while only 3% injected and the remainder inhaled/smoked. The most commonly used drug was ecstasy, but use of heroin and ketamine was also reported. The median age of initial drug use was 20 years (range: 14–31 years).
Commercial sex behaviors and condom use in past 3 months
Participants began working in the sex trade at a median age of 20 years old (range 7–26 years). At the time of interview, most participants had been engaging in commercial sex for more than 12 months (mean: 29 months). More than 71% became involved in the trade by introduction from a friend, and 21% by internet. For most (62%), their first commercial sexual encounter was a pleasant experience.
Most MSW (82%) reported that they only engaged in sex with clients of the same gender, while the remainder served both male and female clients. The median number of clients in the past month was seven.
Oral sex with clients was the most frequently reported sexual practice (66%), followed by receptive (58%) and insertive (48%) anal sex and, lastly, vaginal sex (14%) (Table 2). Condom use was lowest for oral sex, with 66% reporting that they did not use condoms when practicing oral sex with clients. Consistent condom use was 53 and 71% for receptive and insertive anal sex, respectively. Among those having sex with women, half never used a condom. Thirty-five percent of the participants did not know that condoms could protect them from getting HIV infection.
The main barrier to consistent condom use was that clients thought it inhibited sensation. Some of the interviewees reported that if they met a client that they were attracted to and wanted to impress, they would be less inclined to use a condom lest they be less appealing to him.
High risk sexual behaviors with regular vs. commercial partners
Male sex workers were significantly more likely to practice passive oral sex and to engage in unprotected insertive anal sex with regular partners than with clients (passive oral sex: 44 vs. 18%, P < 0.01; unprotected insertive anal sex: 57 vs. 29%, P < 0.05). No significant differences were observed in other types of sexual behaviors.
Factors associated with condom use
Results of the multivariate analysis are shown in Table 3. When having commercial receptive anal intercourse, consistent condom use was associated with having regular partners, regretting getting involved in the sex trade, serving both male and female clients, and being required to use a condom use by their clients. Factors associated with condom use in commercial insertive sex included age group ≥ 20 years (13-fold increase), knowledge that condoms could protect them from HIV infection, and being required by clients to use a condom.
To the best of our knowledge, few studies on high risk behaviors among MSW have been reported in China. This group is characterized by minority status and marginalization, both of which are closely linked with increased HIV prevalence [11–13].
In this study, risk behaviors were common. Male sex workers engaged in a combination of HIV risk behaviors that include high risk sex, especially receptive anal intercourse; multiple sex partners, including males and females; and drug abuse. Our report supports other studies among high risk males previously reported [14–16].
Some MSW reported having both male and female clients. Sexual activity with men who also engaged in same-sex sexual behaviors put female clients at a high risk of exposure to HIV, and increases the possibility of transmission into the general heterosexual population. Furthermore, the pressure to marry and have a family is high in a developing country like China, usually making marriage with women inevitable for most MSW. Between 70 and 80% of urban, well-educated MSW will be or were married, while this proportion might be close to 90% in rural areas . This sexual mixing pattern may create a bridge for HIV transmission from high-risk men to common, low-risk families.
Male sex workers in our study were also found to have higher frequencies of passive oral sex and lower rates of consistent condom use in insertive anal intercourse with regular partners. This practice might contribute to the significantly higher HIV prevalence and incidence rates observed among MSW, putting their clients and other sexual partners at risk of HIV infection.
The factors associated with consistent condom use among MSW in this study included age (older than 20 years), knowing the protective effect of condom use, having regular partners, regretting getting involved in the sex trade, serving both male and female clients and being required to use a condom by clients. These results were similar to a study that was done on risk behaviors among MSM in Qingdao, which reported that younger age, low or no-income; poor education and being unmarried were associated with engagement in paid sex and high-risk behaviors .
The men interviewed had a diverse range of sexual networks. Male sex workers are not isolated from other sexual networks, but engage in more risks than other MSM, and are thus more vulnerable to HIV/AIDS and sexually transmitted disease (STD) . Our study highlights the need for personalized preventive measures linked with more realistic and acceptable HIV prevention and intervention efforts, especially for male sex workers.
Our study identified a significant proportion of participants using both injection and non-injection drugs, although the vast majority were not injecting. Drug abuse is associated with increased risk of HIV infection, both parenterally, through needle sharing, and sexually, through unprotected sex [19,20]. Prostitution has been reported as an economic necessity for drug users, both male and female . The relationship between onset of drug use and entry into sex work varies, with one study demonstrating that substance abuse precedes entry into prostitution , while another showed that sex was traded to earn enough money to maintain drug use [23–25]. In China, male drug users have also been reported to trade sex for drugs or money . De Graff and colleagues  reported that drug addicts were too weak to screen for good clients and drug desire increased the possibility of performing sexual acts without using condoms. Substance abuse among participants in our study was characterized by the consumption of party drugs, such as ecstasy, ketamine and methamphetamine. Methamphetamine use was associated with increased likelihood of engaging in sexual risk behaviors. Heavy methamphetamine users were more likely to report having had sexual intercourse before age 13 and with multiple partners . Thus drug education is urgently needed for MSW.
This survey aimed to collect behavioral information related to HIV/AIDS infection, without the support from laboratory data about HIV or STD infection. Although we had initially intended to collect biospecimens, MSW were very reluctant to provide us with urine and blood samples necessary for these tests, and so in light of recruitment difficulties we did not do any testing. This is a significant weakness of the study. However, the study has identified that MSW engage in sexual risk behaviors and thus are likely to be at increased risk of HIV infection.
A further limitation to the study was selection bias. Due to the sensitivity of the topic, it was difficult to achieve cooperation with all venue owners or patrons in these two cities, and so participants were recruited from just seven venues. Furthermore, most of our participants had good knowledge about HIV/AIDS. This means they may be more likely to volunteer to participate, but may also be more likely to be able to negotiate safer sex with their clients, thus leading to an overestimation for the rate of consistent condom use and an underestimation of the rate of high risk behaviors. Being HIV-aware, they may also be more likely to underestimate their engagement in sexual risk behaviors, leading to social desirability bias.
HIV-related high-risk behaviors were common among MSW, along with a low rate of condom use. Male sex workers should be the target of specific preventive activities, given their particular vulnerability and because infections are likely to disseminate into the general population given the high proportion of bisexual activity and marriage.
The authors would like to thank the venue owners, MSW and clients who participated in this study. They would also like to thank Ms Sheena Sullivan for help with the preparation of this manuscript.
Preparation of the manuscript was partly supported by the China Multidisciplinary AIDS Prevention Training Program with NIH Research Grant # U2R TW06918 funded by the Fogarty International Center, National Institute on Drug Abuse, and the National Institute of Mental Health.
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