Abstract
To estimate the prevalence of HIV and syphilis and to assess the predictors of unprotected anal intercourse (UAI) among men who have sex with men (MSM) in Beijing, a community-based survey recruited MSM in 2005 through internet advertisement, community outreach, and peer referral. Demographic, sexual, and HIV risk behavioral information were collected. Serospecimens were tested for HIV and syphilis infections. Of the 526 participants, 3.2% were HIV-positive, 11.2% syphilis-positive, 50% and 43.3% had UAI with regular and casual sex partners, respectively. Participants practicing UAI with regular male partners were independently associated with lower monthly income (adjusted odds ratio-AOR, 1.7; 95% CI, 1.0–3.0) and encountering male sex partners at bathhouses, public washrooms, and parks (AOR, 2.2; 95% CI, 1.0–4.9). Participants practicing UAI with casual male partners were associated with encountering male sex partners at bathhouses, publics washrooms, and park (AOR, 3.0; 95% CI, 1.8–5.2) and more male sex partners having receptive anal intercourse (AOR, 1.8; 95% CI, 1.1–2.9), and was inversely associated with receiving money for sex with men (AOR, 0.3; 95% CI, 0.2–0.7). Professional male sex workers were less likely to practice UAI in Beijing, suggesting the benefits of educational outreach to date. Further education, condom promotion, and prevention of sexually transmitted infections should be intensified urgently to combat the rising HIV epidemic among MSM in Beijing.
INTRODUCTION
An estimated 650,000 Chinese were living with HIV/AIDS in 2005; the trend of the epidemic is still on the rise (China MOH et al, 2005). By transmission categories, injection drug users (IDUs) accounted for the largest proportion of persons living with HIV (44.3%), followed by sex workers and their clients (19.6%), partners of HIV-positive individuals and members of the general population (16.7%), and former blood donors and recipients of blood products (10.7%), acknowledging that past cases were more likely to have been due to commercial blood and plasma donation and receipt of blood products (China MOH et al, 2005). Less data is available on men who have sex with men (MSM) in China, but about 47,000 MSM were estimated to be living with HIV/AIDS in 2005, accounting for 7.3% of persons living with HIV/AIDS (China MOH et al, 2005).
High
HIV prevalence rates reported among MSM in several Asian countries have drawn attention, including in Phnom Penh, Cambodia (8.9%), Chiang Mai, Thailand (15.3%), and Andhra Pradesh, India (18.2%) (CDC, 2006). There has been a rapid rise in HIV prevalence among MSM in Bangkok, from 17.3% in 2003 to 28.3% in 2005 (United Nations Program on HIV/AIDS, 2007). Recent studies suggest unprotected risk behavior or sexually transmitted diseases (STDs) among MSM have been found commonly in several cities in China (Zhang et al, 2000; Qu et al, 2002b; Choi et al, 2003; Gu et al, 2004; Cai et al, 2005; Qian et al, 2005; He et al, 2006; Jiang et al, 2006; Liu et al, 2006; Lu et al, 2006). Disturbing HIV prevalence rates from 1.0 to 5.0% among MSM have been reported in several urban cities (Qu et al, 2002b; Gu et al, 2004; Cai et al, 2005; Lu et al, 2006); higher than the overall prevalence (0.05%) for China. Without timely action, MSM could become the second most at risk group for HIV infection following injection drug users in China (Zhang and Chu, 2005).
Nationwide behavioral surveys among MSM conducted in 2001 found that 66.2% of participants reported having insertive unprotected anal intercourse (UAI) and 57.0% receptive UAI with male partners, and 18.5% reportes having group sex (Zhang et al, 2002). Other studies found that 15–30% of MSM were married or remarried largely due to social pressure, suggesting that MSM having unprotected sex and bisexual activities may be a bridge for transmission of HIV and other sexually transmitted diseases (STD) to the general population (Zhang et al, 2000; Qu et al, 2002b; Choi et al, 2003; Gu et al, 2004; Cai et al, 2005; Qian et al, 2005; CDC, 2006; He et al, 2006; Jiang et al, 2006; Liu et al, 2006; Lu et al, 2006; China MOH et al, 2007; United Nations Program on HIV/AIDS, 2007). The sexual risk behaviors among MSM are well described worldwide, but little is available concerning predictors for unprotected sex and other high risk behavior among MSM in China. This is of vital importance given the rising HIV prevalence in this population. Our study was to estimate the prevalence of HIV and syphilis infections and predictors for UAI among MSM in Beijing.
MATERIALS AND METHODS
Participants and recruitment
A community-based cross-sectional study was conducted among MSM in Beijing from June to November of 2005. The participants were recruited through website advertisements (http://www.Chinaids.org.cn and http://www.hivolunt.net) and peer recruiters trained for outreach among MSM in clubs, bars, parks, and bathhouses. All potential participants were invited to a community-based voluntary counseling and testing (VCT) clinic for eligibility assessment. Enrollment criteria included male sex, reports of having sex with other males in the past 6 months and willingness to finish the study and provide written informed consent. The study proposal was approved by the institutional review board (IRB) of the National Center for AIDS/STD Control and Prevention of the China Center for Disease Control and Prevention (CDC) and the IRB of Vanderbilt University Medical Center.
Data collection
Questionnaire-based interviews were conducted in a private room in a local district clinic. Data were collected including sociodemographic information (eg, age, ethnicity, education, employment, marital status, and income), sexual, and HIV risk behavioral information (eg, sexual orientation, age of initiating sex with men, lifetime number of male sex partners, commercial sex with male sex partners, new male sex partners, insertive UAI with regular or casual male partners, receptive UAI with regular or casual male sex partners, unprotected vaginal sex with regular or casual sex partners, and illicit drug use).
HIV and syphilis infection tests
Blood samples were collected from all participants for HIV and syphilis. HIV infection status was determined by enzyme immunoas-say (EIA) (Beijing Wantai Biological Medicine Company, China) testing and confirmed with a HIV-1/2 Western Blot (HIV Blot 2.2 WB™, Genelabs Diagnostics). Syphilis infection was determined using an EIA (Beijing Wantai Biological Production Company, Beijing, China) and confirmed with a Passive Particle Agglutination Test for Detection of Antibodies to Tre -ponema pallidum (TPPA™, OMEGA, UK).
Statistical analysis
EpiData software (EpiData 3.0 for Windows™, The EpiData Association Odense, Denmark) and Statistical Analysis System (SAS 9.1 for Windows™, SAS Institute Inc., Cary, NC, USA) were utilized for data analysis. Prevalence rates of HIV and syphilis and 95% confidence intervals (CI) were calculated by the exact binomial procedure. Multivariable logistic regression models were constructed to identify the independent risk factors for UAI with both regular and casual male sex partners, controlling for potential confounding and interacting factors.
RESULTS
Participants and enrollment
Five participants refused to participate in this study and seven withdrew; refusing to answer the sensitive questions regarding sexual behavior. A total of 526 participants were eligible and completed the study (Table 1), HIV prevalence was 3.2%, and syphilis prevalence was 11.2%. Of the 526 participants, 65.8% were from age 21 to 30 years, 94% belonged to Han ethnic group, 62.0% received college or higher level of education, 18.0% were married or cohabited with male or female sex partners, and non-Beijing residents accounted for 64.3%.
Table 1.
Characteristics of men who have sex with men in Beijing, China.
| Variables | N | % |
|---|---|---|
| Overall sample size | 526 | |
| Age | ||
| 17–20 | 78 | 14.8 |
| 21–30 | 346 | 65.8 |
| 31–54 | 102 | 19.4 |
| Ethnicity | ||
| Han | 494 | 93.9 |
| Minoritya | 32 | 6.1 |
| Education | ||
| Junior high school or less | 65 | 12.4 |
| Senior high school | 135 | 25.7 |
| Some college or higher | 326 | 62.0 |
| Marital status | ||
| Single/Bachelordom | 408 | 77.6 |
| Married/Cohabited with male or female sex partners | 95 | 18.1 |
| Separated/Divorced/Widowed | 23 | 4.4 |
| Beijing permanent residents | 188 | 35.7 |
| Sexual orientation | ||
| Exclusively homosexual | 365 | 69.4 |
| Predominantly homosexual | 128 | 24.3 |
| Predominantly heterosexual | 33 | 6.3 |
| Lifetime number of male sex partners | ||
| 1–5 | 198 | 37.6 |
| 6–10 | 113 | 21.5 |
| 11–20 | 77 | 14.6 |
| >20 | 138 | 26.2 |
| Number of male sex partners in P6M | ||
| 1 | 181 | 34.4 |
| 2–5 | 208 | 39.5 |
| 6–10 | 76 | 14.4 |
| >10 | 61 | 11.6 |
| Ever had sex with female sex partners | 152 | 28.9 |
| Had sex with female sex partners in the past six months | 56 | 10.6 |
| Participated in male group sex in the past six months | 59 | 11.2 |
| Gave money for sex with men in the past six months | 22 | 4.2 |
| Received money for sex with men in the past six months | 45 | 8.6 |
| Unprotected sex with male or female sex partners in the past six months | ||
| Had unprotected insertive anal sex with regular male sex partners | 189 | 35.9 |
| Had unprotected receptive anal sex with regular male sex partners | 140 | 26.6 |
| Had unprotected insertive anal sex with casual male sex partners | 188 | 35.7 |
| Had unprotected receptive anal sex with casual male sex partners | 177 | 33.6 |
| Had unprotected sex with regular female sex partners | 29 | 5.5 |
| Had unprotected sex with casual female sex partners | 15 | 2.8 |
| Used illicit drugs in the past six monthsb | 13 | 2.5 |
| HIV positive | 17 | 3.2 |
| Syphilis positive | 59 | 11.2 |
including Hui, Manchu, Uigur, Dai, Salar, Yao, and Zhuang
including: Ecstasy, Ketamine, and Marijuana
Participants identified as exclusively homosexual and predominantly homosexual accounted for 69.4% and 24.3%, respectively, whereas 6.3% of the participants were identified as predominantly heterosexual with only incidentally homosexual activities. Approximately 26.0% previously had more than 20 male sex partners and 30.0% previously had sex with female sex partners during their the lifetime. During the previous 6 months, about 12.0% of participants had more than 10 male sex partners and 11.0% had sex with female sex partners; 11.2% participated in male group sex; 4.2% paid and 8.6% received money for sex with men. Participants reported had insertive and receptive UAI with regular male sex partners accounted for 35.9% and 26.6% in the previous 6 months, respectively. Participants had insertive and receptive UAI with casual male sex partners in 35.7% and 33.6%, respectively. Participants had UAI regular and casual female sex partners in 5.5% and 2.8%, respectively. 2.5% of participants used illicit drugs in the previous 6 months.
Sexual behavior with regular or casual male sex partners
Of the 526 participants, 64.0% and 69.0% had previously engaged in anal intercourse with regular or casual male sex partners in the previous 6 months, respectively. These participants were more likely to have the UAI (78.6% vs 63.2%, p<0.001), insertive UAI (78.1% vs 58.6%, p<0.001), or receptive UAI (76.4% vs 64.6%, p<0.01) with regular male sex partners than with casual male sex partners (Table 2).
Table 2.
Sexual behaviors by regular or casual male sex partners among men who have sex with men in past six months in Beijing, China.
| Variables | Regular male sex partners |
Casual male sex partners |
p | ||
|---|---|---|---|---|---|
| % | n/N | % | n/N | ||
| Any unprotected anal intercourse | 78.6 | 264/336 | 63.2 | 228/361 | <0.0001 |
| Insertive anal intercourse | 72.0 | 242/336 | 66.2 | 239/361 | 0.10 |
| Unprotected insertive anal intercourse | 78.1 | 189/242 | 58.6 | 140/239 | <0.0001 |
| Receptive anal intercourse | 73.2 | 246/336 | 75.9 | 274/361 | 0.40 |
| Unprotected receptive anal intercourse | 76.4 | 188/246 | 64.6 | 177/274 | 0.003 |
Predictors of practicing UAI with regular or casual male sex partners
Bivariate analyses found that practicing UAI with regular male sex partners was associated with lower monthly income, encountering male sex partners at bathhouses, public washrooms, or parks, or using illicit drugs (Table 3). Practicing UAI with casual male sex partners was associated with younger participants, lower monthly income, encountering male sex partners at bathhouses, public washrooms, or parks, more male sex partners in the previous 6 months, receiving money for sex with men in the previous 6 months, and more male sex partners of receptive anal intercourse in the previous 6 months. Multivariable logistic regression analyses showed that practicing UAI with regular male partners was independently associated with lower monthly income (OR, 1.7; 95% CI, 1.0–3.0) and encountering male sex partners at bathhouses, public washrooms, or parks (OR, 2.2; 95% CI, 1.0–4.9). Practicing UAI with casual male partners was associated with encountering male sex partners at bathhouses, public washrooms, or parks (OR, 3.0; 95% CI, 1.8–5.2) and having more male sex partners with receptive anal intercourse (OR, 1.8; 95% CI, 1.1–2.9), and was inversely associated with receiving money for sex with men (OR, 0.3; 95% CI, 0.2–0.7).
Table 3.
Prevalence of unprotected anal Intercourse (UAI) and associated predictors by regular or casual male sex partners among men who have sex with men in the past six months (P6M) In Beijing, China
| Variable | Anal sex with the regular male sex partners | Anal sex with the casual male sex partners | |||||||
|---|---|---|---|---|---|---|---|---|---|
| N | UAI (%) | OR (95% CI) | AOR (95% CI) | N | UAI (%) | OR (95% CI) | AOR (95% CI) | ||
| Overall | 336 | 78.6 | 361 | 63.2 | |||||
| Age (median, years) | ≤26 | 215 | 76.7 | 1.0 | 225 | 58.7 | 1.0 | ||
| >26 | 121 | 81.8 | 1.36(0.78–2.39) | 136 | 70.6 | 1.69(1.07–2.66)b | |||
| Ethnicity | Han | 313 | 79.6 | 1.0 | 340 | 63.5 | 1.0 | ||
| Minority | 23 | 65.2 | 0.48(0.20–1.19) | 21 | 57.1 | 0.76(0.31–1.87) | |||
| Education | Senior high school or Iess | 110 | 78.2 | 1.0 | 165 | 64.8 | 1.0 | ||
| Some college or higher | 226 | 78.8 | 1.03(0.60–1.80) | 196 | 61.7 | 0.87(0.57–1.34) | |||
| Monthly income | >200 US dollars | 170 | 73.5 | 1.00 | 1.00 | 178 | 57.9 | 1.00 | |
| ≤200 US dollars | 166 | 83.7 | 1.85(1.08–3.16)b | 1.74(1.01–2.98) | 183 | 68.3 | 1.57(1.02–2.41)b | ||
| Married/Cohabited with male or female partners | |||||||||
| No | 262 | 77.1 | 1.0 | 310 | 62.3 | 1.0 | |||
| Yes | 74 | 83.8 | 1.53(0.78–3.04) | 51 | 68.6 | 1.33(0.70–2.50) | |||
| Had Beijing residence card | |||||||||
| No | 210 | 77.1 | 1.0 | 244 | 63.1 | 1.0 | |||
| Yes | 126 | 81.0 | 1.26(0.73–2.18) | 117 | 63.2 | 1.00(0.64–1.59) | |||
| Ever found male sex partners through Internet | |||||||||
| No | 81 | 76.5 | 1.0 | 114 | 64.9 | 1.0 | |||
| Yes | 255 | 79.2 | 1.17(0.64–2.12) | 247 | 62.4 | 0.90(0.56–1.42) | |||
| Ever found male sex partners through bathhouse, public washroom, and park | |||||||||
| No | 267 | 76.0 | 1.0 | 1.0 | 250 | 56.0 | 1.0 | 1.0 | |
| Yes | 69 | 88.4 | 2.40(1.09–5.29)b | 2.22(1.00–4.91) | 111 | 79.3 | 3.01(1,78–5.07)a | 3.02(1.76–5.17) | |
| Number of male sex partners, P6M | |||||||||
| ≤2 | 205 | 80.0 | 1.0 | 109 | 54.1 | 1.0 | |||
| >2 | 131 | 76.3 | 0.81(0.48–1.37) | 252 | 67.1 | 1.72(1.09–2.73)b | |||
| Participated in male group sex, P6M | |||||||||
| No | 295 | 80.0 | 1.0 | 305 | 63.6 | 1.0 | |||
| Yes | 41 | 68.3 | 0.54(0.26–1.10) | 56 | 60.7 | 0.88(0.49–1.59) | |||
| Gave money for sex with men, P6M | |||||||||
| No | 318 | 78.3 | 1.0 | 343 | 63.3 | 1.0 | |||
| Yes | 18 | 83.3 | 1.38(0.39–4.92) | 18 | 61.1 | 0.91(0.34–2.41) | |||
| Received money for sex with men, P6M | |||||||||
| No | 308 | 79.2 | 1.0 | 318 | 65.4 | 1.0 | 1.0 | ||
| Yes | 28 | 71.4 | 0.66(0.28–1.56) | 43 | 46.5 | 0.46(0.24–0.87)b | 0.34(0.17–0.68) | ||
| Number of male sex partners of insertive anal intercourse, P6M | |||||||||
| ≤2 | 260 | 78.1 | 1.0 | 230 | 59.6 | 1.0 | |||
| >2 | 76 | 80.3 | 1.14(0.60–2.16) | 131 | 69.5 | 1.54(0.98–2.44) | |||
| Times of the insertive anal sex with male sex partners, P6M | |||||||||
| ≤5 | 184 | 76.1 | 1.0 | 228 | 64.9 | 1.0 | |||
| >5 | 152 | 81.6 | 1.39(0.82–2.37) | 133 | 60.2 | 0.82(0.52–1.27) | |||
| Number of male sex partners of receptive anal intercourse, P6M | |||||||||
| ≤2 | 251 | 78.9 | 1.0 | 192 | 57.3 | 1.0 | 1.0 | ||
| >2 | 85 | 77.6 | 0.93(0.51–1.68) | 169 | 69.8 | 1.72(1.11–2.67) á | 1.80(1.13–2.86) | ||
| Times of the receptive anal sex with male sex partners, P6M | |||||||||
| ≤5 | 181 | 76.8 | 1.0 | 214 | 63.1 | 1.0 | |||
| >5 | 155 | 80.6 | 1.26(0.74–2.13) | 147 | 63.3 | 1.01(0.65–1.56) | |||
| Used Illicit drugs, P6M | No | 329 | 79.3 | 1.0 | 348 | 63.8 | 1.0 | ||
| Yes | 7 | 42.9 | 0.20(0.04–0.89)b | 13 | 46.2 | 0.49(0.16–1.48) | |||
OR: odds ratio; CI: confidence interval; AOR: adjusted odds ratio
P<0.01
0.01<P<0.05
DISCUSSION
Our study found a large proportion of participants had a college or higher education (62.0%) or were non-local residents (64.0%). Two thirds of the participants were ≤26 years old, which is consistent with other studies in Beijing (Qu et al, 2002b; Choi et al, 2003; Cai et al, 2005). The number of participants in this study with exclusively homosexual activities was more than that of those with predominantly homosexual or heterosexual activities, which differs from previous studies. Two studies found the number of MSM who were self-identified as gay or homosexual surpassed those who identified themselves as bisexual or heterosexual in absolute numbers (Zhang et al, 2002; Choi et al, 2003), yet another study found the opposite (Gu et al, 2004).
Homosexual activities are not illegal in China, but they are not socially acceptable. Homosexual or bisexual activities are highly stigmatized, and MSM are often married and under social pressure to hide their sexual orientation (Liu and Choi, 2006; Wong et al, 2006). Education regarding safer sex practices and exploring research among MSM are huge challenges since they are socially marginalized and hard to reach. Three quarters of participants in this study were single, one fifth were married or cohabited, which is similar to other studies among MSM in China (Qu et al, 2002b; Choi et al, 2003; Gu et al, 2004; Cai et al, 2005; Liu and Choi, 2006; Lu et al, 2006). We also found 5.5% of participants had unprotected sex with female partners. These married MSM and bisexual men may serve as a potential bridge for HIV transmission to women (Qu et al, 2002a), especially when HIV prevalence rates reach relatively high levels, and risky sexual practices are common.
High prevalences of multiple male sex partners and commercial sex workers were found in several cities in China, suggesting a potential risk for rapid spread of HIV among MSM (Choi et al, 2003; Choi et al, 2004; He et al, 2006; Wong et al, 2006). Our findings showed that 40.0% of participants had more than 10 male sex partners in their lifetime, 26.0% had more than 5 male sex partners in the previous 6 months, and nearly 4.0% paid and 9.0% received money for sex with men, respectively.
Similar to the findings among MSM in Seattle and San Diego (Choi et al, 2002), this study demonstrated a high prevalence of UAI with regular (80%) and casual (60%) male partners in the previous 6 months, and participants were more likely to have any UAI with regular male partners than with casual male partners. MSM in steady relationship may not always be monogamous, and HIV status of MSM couples may be discordant, so having UAI with regular male partners may expand HIV transmission (Elford et al, 1999; Dodds et al, 2004). Thus, future prevention programs for MSM should not ignore the UAI in regular male partners.
Multivariable logistic regression analysis in this study indicated that lower income, encountering male sex partners at bathhouses, public washrooms, or parks, and more male sex partners had an influence on MSM having UAI with regular or casual male sex partners, or both. A survey in India indicated that the lower the income MSM were more likely to not use a condom for anal sex (Dandona et al, 2005). Socioeconomic status has an influence on condom use. A study in Hong Kong revealed that being an internet sex networker was associated with having engaged in anal sex, and more than 60% of internet sex networkers who had engaged in anal sex had UAI (Lau et al, 2003). However, considering the economic status and education levels of MSM in mainland China, MSM who found male sex partners at bathhouses, public washrooms or parks were more likely to engage in UAI, which also were associated with not carrying condom in a public place (Hart et al, 2004).
It is interesting that this study showed professional male sex workers were less likely to engage in UAI with casual male sex partners, which is similar to the finding in San Francisco (Ekstrand et al, 1999), however our earlier studies in the same region concluded differently, that professional sex workers were more likely to engage in receptive UAI (Choi et al, 2004). As expected, this study found that MSM having more male sex partners were more likely to practice UAI, which is consistent with previous findings (Ruiz et al, 1998; Choi et al, 2002, 2004; Jiang et al, 2006).
Compared with many Western countries, the HIV prevalence rate among MSM in China is relatively low: 3.2% was found in this study. Cross-sectional surveys in London indicated ≈11% of MSM were HIV positive (Dodds et al, 2004), and almost 9% in California (Ruiz et al, 1998). MSM accounts for a large proportion of HIV cases in many western countries. Over 40% of cumulative reported AIDS cases in the United States through 2005 were related to male-to-male sexual contact (CDC, 2005). MSM accounts for 40% of AIDS cases from 2001 to 2005 in Germany, 49% in 2003–2004 for Netherlands, and 32% in 2004 for the UK (Van der Poel et al, 2007). Illicit drug use is not common among Chinese MSM. Only 2.5% of participants in our study used illicit drugs in the past 6 months, and 0.5% (1/201) were reported in another study in China (He et al, 2006). Little relationship has been demonstrated between drug users and MSM in China. Drug abuse is common among MSM in the western countries and often constitutes a major risk for HIV spread in this population (Bluthenthal et al, 2001; Thiede et al, 2003; Kral et al, 2005).
The large overlap between HIV and syphilis among the participants in this study demonstrates the consequences of unprotected risk behavior and it poses a particular concern that syphilis could further facilitate the transmission of HIV (Cohen, 2004). A case-control study in New York found that MSM with regular and secondary syphilis were sevenfold more likely than controls to be infected with HIV (Paz-Bailey et al, 2004). Our study found that 11.2% of participants were infected syphilis, which is similar to four studies (7–20%) in China (Gu et al, 2004; Cai et al, 2005; He et al, 2006; Jiang et al, 2006). A systematic review has suggested the prevalence rate of syphilis seropositivity among MSM increased among MSM in certain cities of China (Lin et al, 2006).
Our data were collected through multiple sampling methods instead of a random sampling method. The findings should be interpreted carefully when generalizing to the larger MSM population and compared with results from other studies.
Given that MSM practicing UAI are more likely to recruit other men for sex, and do so in public settings, suggests that interventions must be offered in outreach programs that actually reach men in these venues. Commercial male sex workers were less likely to practice UAI in Beijing, suggesting the benefits of educational outreach to date. The findings from this study further underscored that education, condom promotion, prevention and control of sexually transmitted infections should be intensified urgently to combat the rising HIV epidemic among MSM in Beijing.
ACKNOWLEDGEMENTS
This study was supported, in part, by grants from the Ministry of Science and Technology of China (2004BA719A01), the National Institute of Health (CIPRA, U19AI51915), and the Institute for Global Health, School of Medicine, Vanderbilt University.
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