Feng, Yuji MD, PhD*; Wu, Zunyou MD, PhD†; Detels, Roger MD, MS*; Qin, Guangming BS‡; Liu, Li MD, PhD‡; Wang, Xiaodong BS§; Wang, Jun BS§; Zhang, Linglin MD‡
Men who have sex with men (MSM) have been harshly and disproportionately impacted upon by HIV and continue to be a major driver of the HIV/AIDS epidemic in the world. In the United States, MSM accounted for approximately 45% of newly reported HIV/AIDS diagnoses in 2006 and nearly 54% of cumulative AIDS diagnoses.1 In Australia, New Zealand, and most western European countries, MSM accounted for as much as 70% of all HIV infections.2 In Indonesia, MSM represent 15% of reported AIDS cases, 29% in Singapore, 32% in Hong Kong, and 33% in the Philippines.3
By 2007, the major groups infected with HIV in China were injection drug users (IDUs; 38.5%), former blood donors (19.3%), and promiscuous heterosexuals (17.8%).4 However, recent data indicated an emerging epidemic among MSM in the main cities.5-8 According to the China Ministry of Health, 2%-4% of adult males in China are primarily homosexual in their sexual behaviors which corresponds to 5-10 million men.9 By the end of 2005, it was estimated that 47,000 MSM were living with HIV/AIDS, accounting for 7.3% of the total number of estimated HIV cases in China.10
Surveys among MSM have been rare in China. In Beijing, an increasing HIV prevalence among MSM has been observed in the past 3 years, from 0.4% in 2004 to 4.6% in 2005 and to 5.8% in 2006.7 This trend agreed with the results of another study in a northern city of China that showed a slight increase of HIV prevalence among MSM from 1.3% in 2002 to 2.2% in 2006.5 Studies across China have reported high levels of sexually transmitted disease (STD) infections, a high prevalence of multiple sexual partners, and low consistent condom use.5,7,11-14 In a study conducted in 6 large cities in China, only 32.5% of 1389 participants had always used condoms when having anal intercourse. The average number of their male sex partners was 5.7, including 4.4 unfamiliar sex partners in the past 6 months, 11.6% had participated in group sex in the past 6 months.12
Limited data on HIV among MSM in Sichuan indicated that high-risk behaviors occur within this population. One survey reported that 84.7% MSM had had sex with male partners in the past 6 months and that the median number of partners for anal sex and oral sex were 4.4 and 4.2, respectively. About 62% of those who engaged in anal sex reported having 3 or more partners in the past 6 months and 20% of them had paid for sexual services during the same period. Condom use with different male partners varied significantly. The proportions of consistent condom use with regular, casual, and commercial male partners were 15.8%, 16.3%, and 32.3%, respectively. Only 18.3% of participants reported having been tested for HIV antibody in the past 12 months.15,16
With support of the China-United Kimgdom HIV/AIDS Prevention and Care Project and the Sichuan Center for Disease Control and Prevention, the Chengdu Gay Community Care Organization (CGCCO) has provided HIV voluntary counseling and testing and high-risk behavior surveillance among MSM in Chengdu since 2002. Data indicated that HIV prevalence surged from 0.64% in 2003 to 6.58% in 2006, and the percentage of consistent condom use when having anal sex remained at about 40% after the 4-year intervention effort.17 A cross-sectional survey was conducted from March to June 2007 in Chengdu to update the prevalence of HIV and STDs among MSM and the factors associated with HIV infection.
Study Design and Sampling
The snowball sampling method was used to recruit participants from the Chengdu MSM community. According to the formative study carried out before the quantitative survey, the major venues for MSM activities in Chengdu included internet chatrooms, bars, tea bars, money boy (MB) brothels, public restrooms, public bathhouses, and parks. Fifteen seeds were selected to cover all types of venues. Because some seeds “died out” soon after the survey started, 4 more seeds were recruited later in the process using the same procedure. All seeds were MSM at least 18 years old, fluent in both Mandarin and the Chengdu dialect, and had patronized MSM venues frequently.
MSM eligible for the study were at least 18 years, had been living in Chengdu in the past 3 months, and had had oral or anal sex with other men. All of the participants were given the option of either completing the written questionnaire by themselves or undergoing a face-to-face interview in either the Mandarin or Chengdu dialects. The information collected in the questionnaire included demographic characteristics, sexual history with other men and women including unprotected anal intercourse, commercial sex, self-reported STD infection history and specific symptoms of STD infections in the genital track or anus in the past 6 months, past HIV testing, HIV knowledge and attitudes, and assessment of depression [Center for Epidemiologic Studies Depression Scale (CES-D)].
At the beginning of the survey, the interviewer briefly introduced himself and the study, then went through a series of formalities with the participant including the importance and nature of confidentiality, issues related to the collection of information, the right not to participate and to withdraw from participation without penalty, incentive distribution, referral information related to sexual health issues, and access to the final report. Participants were not asked to sign the informed consent form to maintain the anonymity of this study. After the interview, a 2.5-mL blood sample was drawn from each participant for HIV, herpes simplex virus 2 (HSV-2), and syphilis testing.
Collected specimens were tested by the Sichuan Provincial Center for Disease Prevention and Control for antibodies to HIV, HSV-2, and syphilis. Antibody to HIV was detected by the enzyme-linked immunosorbent assay (ELISA; Livzon Group Reagent Factory, Zhuhai, China), and positive results were confirmed by Western blot (Singapore MP Biomedical Asia Pacific Ltd Singapore). IgG antibody to syphilis was tested by ELISA (Beijing Kinghawk Pharmaceutical Co, Ltd Beijing, China). HSV-2 IgG was also tested for ELISA using the only reagent approved by Food and Drug Administration (Focus Technologies, Cypress, CA).
Ethical Considerations and Incentives
The survey was anonymous, no names or other personal identifying information were collected from the participants. Each participant was assigned a unique study number and identified only by this number during the process. A private room in the CGCCO office was used for the interviews. Participants were given a prenumbered card with an appointment date for receiving their test results and posttest counseling. Referral for treatment for the positives was provided as needed. Fifty Chinese Yuan (US $6.5) was given to the participants as compensation for their time or the equivalent value in condoms and lubricants.
The study protocol was reviewed and approved by the Institutional Review Board of the University of California, Los Angeles and the Chinese Center for Disease Control and Prevention (China CDC).
Descriptive analyses were conducted to describe the demographic characteristics of the sample, prevalence of HIV and STDs, and the risk factors for HIV infection. Univariate and multivariate logistic regressions analyses were used to assess the associations between the risk factors and HIV infection. Variables in the multivariate analysis were selected based on the results of univariate analysis and prior knowledge. When variables were significantly correlated, only those variables best explaining the relationships were used for model fitting. All statistical analyses were performed using the Statistical Analysis System, version 9.1.3 for Windows.
A total of 538 MSM were recruited to the study among whom 513 (95.4%) completed the questionnaire. All 538 blood samples were tested for HIV and HSV-2, although only participants who finished the questionnaire were tested for syphilis. The HIV (confirmed only), HSV-2, and syphilis prevalences of the total sample were 9.1% [49 of 538; 95% confidence interval (CI): 6.7% to 11.5%], 24.7% (133 of 538; 95% CI: 21.1% to 28.4%), and 28.1% (144 of 513; 95% CI: 24.2% to 32.0%), respectively. Prevalences of both HIV and HSV-2 were higher among those who refused to respond to the questionnaire (HIV: 16.0% vs. 8.8%; HSV-2: 32.0% vs. 24.4%). However, because the sample size was small and no personal information was collected for nonrespondents, no further conclusions could be made.
Because no information was obtained from those who refused to answer the questionnaire, only 513 participants were included in the final analysis. The age of the participants ranged from 16.8 to 44.5 years, with a median age of 24 years. More than half (57.5%) were younger than 25 years, and 48.2% had some college or higher education. The majority (80.8%) of the sample had never been married. The primary reason for getting married was to satisfy their parents' wishes (54.4%) followed by the desire to conceal their homosexual orientation (27.9%). Some participants indicated that they did not know their sexual orientation before getting married. For those who had never married, 50.5% wanted to be married in the future. Approximately, 70% of them thought the most important reason to marry would be to satisfy their parents' wishes. The second most important reason was that they also loved females (26.8%). Only 12.2% reported that the most important reason to be married was to conceal their sexual orientation.
Almost two-thirds (63%) of the participants identified themselves as either absolutely homosexual or bisexual. Forty-three (8.4%) did not state their sexual orientation or “did not know.” However, when asked which gender(s) they preferred to have sex with, 9 of the 43 preferred only males, 15 preferred mostly males, 13 both equally, 4 mostly female, and 2 only females. Sexual orientation of those who did not reveal their sexual orientation was defined according to these preferences.
The most popular strategy to find male sexual partners was the internet (63.1%), followed by through friends (51.9%), in bars (19.5%), and in public bathhouse (10.6%). When asked which one above had been used most, 54.2% of participants selected internet and 27.6% through friends.
High-Risk Sexual Behaviors and Condom Use
The median age at first sex (oral, anal, and/or vaginal) was 19 years. More than 60% of the participants' first sexual partners were male (62.1%). Some of the participants started their sexual activities as early as 8 years old, although a few had their first anal intercourse with a male in their 40s. Table 1 shows the numbers of male sex partners with whom the participants had had oral or anal sex and female sex partners. More than half (55.5%) of the participants had had sex with female partners in their life.
A boyfriend (BF) was defined as somebody with whom the participant had had sex and desired a long-term relationship. The majority of the participants had only 1 or no BFs in the past 6 months. The numbers of BFs or female sex partners in the past 6 months were similar between HIV-positive and HIV-negative participants. However, HIV-positive participants tended to have more casual male partners (Table 1).
The most preferred sexual behavior with male partners was anal sex (82.7% with BFs and 77.7% with casual male partners). About half (44%) of the participants had always or almost always been insertive, whereas 32% were always receptive, and 22% were about the same for both.
In the past 6 months, 26 participants (5.1%) had paid for sex with FSWs, and 52 (10.2%) with “MBs,” whereas 10 (2.0%) had sold sex to female clients and 93 (18.3%) to male clients. The number of participants who had sold sex was higher than those admitting to be MBs, indicating that some of them might have been selling sex only occasionally.
The rate of consistent condom use (always used condoms when having sex) varied by type of sexual partners. The highest use was with casual male partners (38.6%), and the lowest was with wives or girlfriends (17.8%). About two-thirds (67%) had had anal sex as their most recent encounter, and condom use for the most recent sexual intercourse was 57.5% (289 of 503, 95% CI: 53.1% to 61.8%). The primary means to avoid HIV/STD infection when not using a condom was washing after sexual intercourse (52.9%) and avoiding having anal sex (28.3%).
Five questions were used to assess participants' knowledge of condom use (Table 2). Only 120 men (23.4%) gave the right answers to all 5 questions. One third (33.7%) of the participants thought that condoms could be tested for safety before sex by filling them with water, and 26.3% believed that HIV/STDs could be prevented by putting a condom on just before ejaculation.
Knowledge about HIV/AIDS was generally low (Table 2). No critical questions were answered correctly by more than 70% of the participants, including “a person with HIV/AIDS can look as healthy as other people” (66.3%), “persons with STDs are more likely to be infected with HIV” (63.9%), and “people with HIV cannot transmit the virus to others if not symptomatic” (67.7%).
Using lubricant when having anal sex prevents small tears and lesions in the anus lining reducing the risk of HIV transmission. In our study, 258 participants (50.4%) used only water-based lubricants when having anal sex, 60 (11.7%) used only oil-based lubricant, and 112 (21.9%) used both. When not having lubricant available, 218 (42.6%) avoided having anal sex, and 239 (46.7%) used other material for lubrication such as saliva, toothpaste, or oil.
Other Risk Behaviors
One fifth (21.6%) of participants often consumed alcohol before having sex among whom, 51 admitted to being drunk a few times. One quarter (124; 24.2%) of participants had used illegal drugs. The most popular was Ketamine (112 of 124, 91.1%) followed by amphetamine (68 of 124, 55.3%). Only 4 participants had used heroin of whom 2 had injected. Only 14 (2.7%) of participants had used drugs before having sex.
Sexually Transmited Diseases
One fifth (20.3%) of participants reported having been diagnosed as being infected with a STD. Only half (53.5%) received treatment in a regular clinic or hospital. Among those who denied being diagnosed with a STD, 24.2% had had symptoms in the genital track or anus 1-2 weeks after having oral, anal, or vaginal intercourse. According to the results of testing for HSV-2 and syphilis, 195 participants (36.2%) were infected with at least 1 STD of whom 74 (37.9%) had both HSV-2 and syphilis infections.
The shortened version of the CES-D was used to assess participants' mental health status. The CES-D is a 20-item, self-reporting depression scale. Items refer to the frequency of symptoms during the past week. The score for each person is calculated based on the answers to the questions. A score below 15 indicates that the participant does not seem to be experiencing high levels of depressive symptoms at that time. Scores between 15 and 21 indicate mild to moderate depression and more than 21 indicate possible major depression. In this study, 237 participants (46.3%) scored less than 15, 82 participants (16.0%) between 15 and 21, and 193 participants (37.7%) more than 21.
Risk Factors for HIV Infection
In the total sample, students comprised 14.8%, but none were found to be infected with HIV. Thirty HIV-infected participants (66.7%) were self-employed or in a service business and seven HIV-positive participants were MBs. HIV-positive persons tended to have had more lifetime sexual partners than negatives.
The possible risk factors for HIV infection were assessed by logistic regression. Because HSV-2 and syphilis infections were correlated in the sample (OR = 6.59, 95% CI: 4.24 to 10.24), STD infection was defined as either one of them or both. Table 3 shows the results of univariate and multivariate logistic regression. After controlling for other variables, participants who had a college or higher education level were 3 times more likely to be infected with HIV (OR = 3.17, 95% CI: 1.44 to 6.97). Those who had a history of being infected by either HSV or syphilis were more than 4 times more likely to be HIV positive (OR = 4.48, 95% CI: 2.02 to 9.96). Not knowing how to use condoms properly also significantly increased the risk for HIV infection (OR = 2.65, 95% CI: 1.27 to 5.54). Compared with clerks or students, the risk of HIV infection for MBs was 6 times higher (OR = 6.43, 95% CI: 1.54 to 28.86). For those who had lived in Chengdu for more than 5 years, the risk of HIV infection was 2.5 times higher (OR = 2.47, 95% CI: 1.06 to 5.76).
Chengdu is one of the largest city in southwest China. Studies have estimated that Chengdu has more than 71,000 MSM among whom at least 10,000 are sexually active.18 Surveillance data among MSM in Chengdu indicated that the HIV prevalence has increased dramatically from 0.64% in 2003 to 6.58% in 200617 and was 9.11% in our study in 2007.
HSV-2 and/or syphilis infection significantly increased the risk of being infected with HIV. After controlling for other risk factors, participants who had been infected with either HSV or syphilis were 4 times more likely to be infected by HIV. In our study, about 20% of participants self-reported having had a diagnosed STD infection in the past, but only half had been treated in a regular clinic.
High-risk behaviors were common in this population. Only half of the participants used a condom during their last sexual intercourse. Consistent condom use was low even with casual male sex partners (38.6%). Only 23% of participants were able to correctly answer all the questions about how to use condoms properly. When not using a condom during sex, more than half of them just washed after sex to avoid being infected with HIV/STDs.
MBs were 6 times more likely to be infected with HIV compared with government employees, clerks, or students. Some participants who did not identify themselves as MB also reported occasional behaviors of selling sex for extra money. Among those who were self-employed or worked in a service business, 18.1% had engaged in commercial sex with male clients in the past 6 months, which was higher than among clerk/government employees (3.7%) or students (2.7%), putting this group at higher risk of HIV infection.
MSM living in Chengdu for more than 5 years were twice as likely to be infected with HIV compared with those living there a shorter time. This may reflect a shorter cumulative exposure time. The internet has become the most popular method for MSM seeking sexual partners, followed by through friends. In addition to focusing on the venues patronized by MSM, such as bars, parks, and bathhouses, intervention activities targeting MSM should target the internet and personal networks. Programs also need to reach MSM with STDs who do not attend STD clinics.
By the end of 2007, the major HIV transmission mode in Sichuan was still injection drug use. In our study, about one fourth of the participants had tried illegal drugs. However, drug use was not found to be a risk factor for HIV infection in our study, possibly because most of them used Ketamine or amphetamine instead injecting heroin. Thus, the HIV epidemic among MSM and IDUs seemed to be independent, so far.
Limitations of This Study
Because of the biases associated with the snowball sampling method, participants in this study were not likely to have been a representative sample of MSM in Chengdu. Possible bias may also derive from the choice of the initial seeds because most of them were volunteers from the Chengdu Gay Care Organization, were young, and had a college degree or higher level of education. Participants wanting to hide their sexual orientation such as those who were married or had a high social status were probably less likely to be recruited to this study. Therefore, compared with the entire MSM population in Chengdu, our sample might have been younger, better educated, and less likely to be married. The IgG antibodies of syphilis were tested by an ELISA assay and were not confirmed by treponema pallidum hemagglutination assay (TPHA) testing. Therefore, the syphilis prevalence in this study might be overestimated. A positive result of syphilis testing only indicated a history of infection, not necessarily active syphilis.
HIV prevalence among MSM in Chengdu has been increasing rapidly in the past few years. STD infections were also very high in this population and significantly increased the risk for being infected with HIV. To prevent HIV/STDs, promotion campaigns of condom use are needed not only to boost the frequency of condom use but also to educate MSM about proper condom use. Certain subpopulations, such as those infected with STDs or who engage in commercial sex, require more attention and intervention. To reach the most sexually active MSM, more efforts should target the internet and the personal networks in this population.
The authors are grateful to the people who participated in this study. We especially thank CGCCO for their heartily assists and helpful input in this study. Appreciation also goes to Dr. Abdelmonem Afifi, Dr. Thomas Coates, Dr. Li Li, Dr. Pamina Gorbach, and Dr. Marc Bulterys for their review, comments, and inspiring suggestions.
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