JAIDS Journal of Acquired Immune Deficiency Syndromes:
Prevalence and Correlates of HIV and Syphilis Infections Among Men Who Have Sex With Men in Seven Provinces in China With Historically Low HIV Prevalence
Xiao, Yan MD, DrPH*; Sun, Jiangping MD, PhD*; Li, Chunmei MD†; Lu, Fan MD, PhD*; Allen, Katherine L MSc‡; Vermund, Sten H MD, PhD‡; Jia, Yujiang MD, DrPH‡
From the *National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of China; †Department of Epidemiology and Biostatistics, School of Public Health, Hebei Medical University, Shijiazhuang, Hebei Province, People's Republic of China; and ‡Institute for Global Health and Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN.
Supported partly by the China Global Fund AIDS Program Round Five, the National Center for AIDS/STD Control and Prevention, the Chinese Center for Disease Control and Prevention, and the Institute for Global Health and Department of Pediatrics, Vanderbilt University School of Medicine.
Correspondence to: Jiangping Sun, MD, PhD, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 27 Nanwei Road, Xuanwu District, Beijing 100050, China (e-mail: firstname.lastname@example.org).
Objectives: To assess HIV and syphilis infection among men who have sex with men (MSM) in Chinese regions with historically low HIV prevalence.
Method: A cross-sectional survey was conducted in 20 cities or districts across 4 provinces, 2 autonomous regions, and a municipality. Socioeconomic/behavioral risk factors were measured. Blood samples were tested for HIV via enzyme-linked immunosorbent assay and Western blot confirmation and syphilis via rapid plasma reagin and passive particle agglutination test for detection of Treponema pallidum Antibodies.
Results: Of 4983 MSM participants, 2.9% were HIV infected (range: 0%-15.1%) and 9.8% were syphilis infected (1.3%-29.3%). Syphilis infection was associated with older age [adjusted odds ratio (AOR) = 2.9; 95% confidence interval (CI): 2.0 to 4.3], not being married or cohabiting (AOR = 0.7; 95% CI: 0.5-0.9), less education (AOR = 1.3; 95% CI: 1.0 to 1.7), inconsistent condom use during anal sex with men (AOR = 1.4; 95% CI: 1.0 to 1.8), and living in inner Mongolia (AOR = 23.9; 95% CI: 9.7 to 58.6), Jilin (AOR = 7.9; 95% CI: 3.4 to 18.3), Heilongjiang (AOR = 7.1; 95% CI: 3.1 to 16.6), Liaoning (AOR = 6.1; 95% CI: 2.6 to 14.2), or Chongqing (AOR = 5.9; 95% CI: 2.5 to 13.9). HIV infection was associated with older age (AOR = 3.7; 95% CI: 2.0 to 6.7), less education (AOR = 2.9; 95% CI: 1.8 to 4.7), inconsistent condom use during anal sex with men (AOR = 1.9; 95% CI: 1.2 to 3.2), syphilis infection (AOR = 2.1; 95% CI: 1.3 to 3.4), and living either in Liaoning (AOR = 8.2; 95% CI: 1.1 to 61.4) or Chongqing (AOR = 57.2; 95% CI: 7.9 to 414.4).
Conclusions: HIV and syphilis have reached alarming rates in China's MSM population, thus, appropriate responses are urgently needed.
The HIV epidemic in China continues to grow, expanding beyond injection drug users.1-3 Half of all new cases in 2007 were transmitted sexually.2,4 Of particular concern is increasing transmission among men who have sex with men (MSM). HIV prevalence in this group is estimated between 1% and 5%.4-7 Between 2005 and 2007, the cumulative reported HIV cases attributed to MSM increased from 0.4% to 3.3%.2 Unsafe sex between men accounted for 11% of the estimated new HIV cases in 2007, which is an increase from previous years.2 Given that MSM in China are not a highlighted high-risk group, this trend is worrisome. Emerging data suggest that MSM are increasing risky activities. Massive internal migration from rural areas to urban cities has occurred, resulting in MSM being more visible and socially connected.2,4,7,8 This is especially true in large-sized and medium-sized cities with large concentrations of migrants.2,4,7,8 This social transformation has been associated with higher risk for HIV infection in MSM.2,4,7-9
In addition to rising HIV prevalence, high syphilis prevalence (∼10%) has been documented in urban MSM.4-7,10-13 High prevalence of both of these infections can be attributed to high-risk behaviors in MSM. For example, 70% of urban MSM reported having sex with more than 1 partner in the past 6 months.2 Only 30% used condoms for anal sex, and about half reported not using condoms when having paid sex with a male.2 A significant number (>25%) of MSM have also had sex with females.4 These prevalent high-risk behaviors, coupled with increasing syphilis prevalence, make MSM a particularly vulnerable risk group for HIV. Sexually transmitted infections (STIs), particularly, for example, syphilis and herpes, are strongly associated with HIV acquisition.14-17 Recognition and treatment of syphilis are crucial to both HIV and syphilis control and prevention. Without decisive action, MSM could become the second highest prevalent risk group, behind injection drug users, for HIV infection in China.18
Most studies examining HIV, STIs, and risk behaviors among MSM were conducted in large Chinese cities, particularly Beijing,4,6,19 Shanghai,20 and Guangzhou.21 Few studies have been conducted in provinces/autonomous regions in China with historically low HIV prevalence, due to difficulties in accessing and enrolling MSM for both surveillance and epidemiological studies.1,22,23 This prevents the creation of evidence-based policies for HIV and STI risk reduction. To effectively guide and evaluate prevention programs, systematic data on MSM throughout China is needed. We sought to examine prevalence of HIV and syphilis and their socioeconomic/behavioral risk factors among MSM in 4 provinces, 2 autonomous regions and a municipality where data on HIV and syphilis infections is limited. Despite their distinction in status, we will refer to provinces, autonomous regions, and municipalities as “provinces” in this article because China's public health system treats them similarly.
This study was conducted in 20 large and mid-sized urban cities (or districts) across 7 provinces (Fig. 1). These cities (or districts) are located in Western and Northern China and were previously regarded as low HIV prevalence regions. MSM have gradually become more visible in the urban cities of these regions, but insufficient information about this risk group has resulted in a lack of MSM public health programs before 2006. Surveys in other Chinese cities have suggested that HIV prevalence among MSM is on the rise, indicating a need for the present survey.
A cross-sectional survey was conducted among MSM in 7 provinces from July to September 2006. The sizes of MSM populations were estimated in each community, and site recruitment venues were mapped. Participants were recruited by trained staff through venue-based recruitment, complemented by internet advertisement, community outreach, and peer referral using “snowball” techniques. Participants were recruited from gay-oriented venues including clubs, bars, parks, and bathhouses. All potential participants were invited to eligibility assessments and interviews in community-based voluntary counseling and testing centers or STI clinics. Survey information was collected anonymously and remained confidential. The enrollment criteria were: male, 14 years of age or older, reported having had oral or anal sex with another male in the past year, willing to finish the study, and provided written informed consent. The study was approved by the institutional review board of Vanderbilt University.
Measures and Test
Questionnaire-based interviews were used to provide socioeconomic and behavioral information. Socioeconomic characteristics included age, marital status, residency, ethnicity, education, and sexual orientation. Behavioral information was gathered about sexual activities and HIV risk behaviors. Assessing a subject's awareness of 3 major transmission routes for HIV was done by categorizing 3 questions identifying modes of transmission. Blood samples were collected for HIV and syphilis tests. Two screening tests were used to diagnose HIV: an enzyme-linked immunosorbent assay (Vironostika HIV Uni-Form II Ag/Ab; BioMérieux Corporate, Marcy l'Etoile, France) and a confirmatory test using the HIV-1/2 Western blot assay (HIV Blot 2.2 WB; Genelabs Diagnostics, Singapore). Syphilis seropositivity was determined using rapid plasma reagin and a Passive Particle Agglutination Test for Detection of Antibodies to Treponema pallidum (Treponema pallidum Antibodies; Rong Sheng Biostix Inc, Shanghai, China).
Data were double entered and evaluated for congruency using EpiData software (version 6.4; EpiData Association; Odense, Denmark). SPSS software (Version 16.0; SPSS Inc, Chicago, IL) was used for analysis. χ2 or T tests were employed for bivariate analysis of sociodemographic and behavioral variables. Multivariable logistic regression model were constructed using a stepwise backward sequence. Variables with P < 0.05 in bivariate analysis were considered statistically significant and included in the multivariable model.
General Description of Participants
Of the 5442 participants enrolled in this study, 459 (9.2%) were excluded from analysis due to missing survey responses (Table 1). The remaining 4983 eligible participants were included in the study. The age of participants ranged from 15 to 68 with a mean age of 28.4 years. Nearly three-quarters of participants were local residents of their study site, 19.0% lived in other cities in the same province, and 7.8% resided in a different province. The majority (92.0%) belong to the Han ethnic group. Among 4657 participants who reported their sexual orientation, 64.1% self-identified as homosexual, 34.3% bisexual, and 1.5% heterosexual.
Among the participants, 60% had their sexual debut at less than 18 years old, with one-third having had their first sexual encounter with a female. Most participants (82.1%) reported having anal sex with a man in the past 6 months, and 39.2% reported greater than 3 sexual partners in the past 3 months. In the previous 6 months, 27.8% reported always using a condom during anal sex with a man. A quarter reported having had sex with a woman in the past 6 months, and only 18.2% reported always using a condom. Additionally, 5.9% reported paid sex with a man in the past 6 months, and 38.1% reported always using a condom.
Prevalence Rates of HIV and Syphilis Infections
HIV infection was observed in 2.9% of participants (range by site: 0%-15.1%), and 9.8% were syphilis infected (1.3%-29.3%). Coinfection with HIV and syphilis was found in 31 participants. HIV was more common among participants with syphilis [adjusted odds ratio (AOR) = 2.1, 95% confidence interval (CI): 1.3 to 3.4] (Table 2).
Predictors for Syphilis Infection
In multivariate analysis, factors associated with syphilis infection were middle and old age (AOR = 1.5; 95% CI: 1.1 to 2.0; 25-35 vs. <22 years of age and AOR = 2.9; 95% CI: 2.0 to 4.3; 36-68 vs. <22 years of age), not being married or cohabiting (AOR = 0.7; 95% CI: 0.5-0.9; married or cohabited vs. single), less than junior high education (AOR = 1.3; 95% CI: 1.0 to 1.7), inconsistent condom use during anal sex with a man in the past 6 months (AOR = 1.4; 95% CI: 1.0 to 1.8), and HIV infection (AOR = 2.4; 95% CI: 1.5 to 3.8). When compared with Gansu, the province with the lowest syphilis prevalence, living in inner Mongolia (AOR = 23.9; 95% CI: 9.7 to 58.6), Jilin (AOR = 7.9; 95% CI: 3.4 to 18.3), Heilongjiang (AOR = 7.1; 95% CI: 3.1 to 16.6), Liaoning (AOR = 6.1; 95% CI: 2.6 to 14.2), or Chongqing province (AOR = 5.9; 95% CI: 2.5 to 13.9) was significantly associated with increased syphilis risk (Table 3).
Predictors for HIV Infection
Significant factors associated with HIV and included in the model were middle and old age (adjusted odds ratio AOR = 2.3; 95% CI: 1.3 to 4.0; 23-35 vs. <22 years of age and AOR = 3.7; 95% CI: 2.0 to 6.7; 36-68 vs. <22 years of age), less education (AOR = 2.9; 95% CI: 1.8 to 4.7; junior high school or lower vs. college or higher), syphilis seropositivity (AOR = 2.1; 95% CI: 1.3 to 3.4), and inconsistent condom use during anal sex with a man in the past 6 months (AOR = 1.9; 95% CI: 1.2 to 3.2; sometimes vs. always). When compared with Gansu, living either in Liaoning (AOR = 8.2; 95% CI: 1.1 to 61.4) or Chongqing (AOR = 57.2; 95% CI: 7.9 to 414.4) province was significantly associated with increased HIV risk (Table 2).
To our knowledge, this is the first large population-based HIV survey conducted among MSM in China. We demonstrate that HIV prevalence is high within this population. We provide additional information about the syphilis epidemic among MSM and risk factors for HIV and syphilis transmission among this high-risk group.
HIV was detected in 2.9% (range by site: 0%-15.1%) of MSM in 7 provinces with historically low HIV prevalence. This overall prevalence is similar to prevalence seen in large Chinese cities, for example, Beijing (3.1%-5.8%)4,6,24 and Shanghai (3.0%),24 but it greatly exceeds other reports examining this risk group.5,7,10,12,21 We also found an astonishingly high HIV prevalence of 15.1% in Yuzhong, a district in Chongqing Municipality.
Syphilis prevalence was also high, with a mean prevalence of 9.8% (range by site: 1.3%-29.3%). This is comparable to the prevalence observed in 4 other studies and a systematic review examining syphilis infection among high-risk and low-risk groups in China.5,10,20,21,25 However, syphilis prevalence varied greatly between provinces. Inner Mongolia had syphilis prevalence of 29.3%, whereas prevalence in the remaining provinces ranged from 1.3% to 12.8%.
This study found that age, junior high education or less, inconsistent condom use during anal sex with men in the past 6 months, syphilis infection, and study province were all independently associated risk factors for HIV infection. Similar risk factors were also associated with increased syphilis risk and included age, junior high education or less, inconsistent condom use during anal sex with men in the past 6 months, HIV infection, and study province.
We also demonstrated a correlation between HIV and syphilis infection. HIV prevalence was higher among participants with syphilis infection (6.3%) than those without infection (2.5%; P < 0.01). Although not unexpected, these findings are worrisome. Syphilis is a marker for engaging in high-risk sexual practices (eg, unprotected sex with multiple partners), and syphilis is known to facilitate HIV transmission.14-17 High prevalence of potential risk factors concurrently with the high prevalence of syphilis suggest that MSM in these provinces are at increased risk for HIV infection.
Our data indicate that 1.6% of participants use illicit drugs and that drug use was associated with HIV infection (odds ratio = 2.8; 95% CI: 1.2 to 6.6, P < 0.05), but this increased risk was not significant in multivariate analysis. This is consistent with other studies, suggesting drug use is not a significant contributor to HIV transmission among Chinese MSM.7 Overall, a small proportion of MSM reported illicit drug use with one-third having injected in the past 6 months. Previous studies found even less drug use among MSM.4 What is alarming, however, is high illicit drug use in 2 districts in Chongqing; these districts also had the highest HIV prevalence. In Jiulongpo and Yuzhong, illicit drug use was reported in 5.8% and 9.4% of participants, and HIV prevalence was 9.4% and 15.1%, respectively. These findings suggests that although illicit drug use is not a significant risk factor for HIV, increased illicit drug use amongst MSM in China could result in the HIV epidemic beginning to resemble that of western countries where drug use is a major risk for HIV transmission among MSM.4,26,27
Knowledge about HIV transmission routes was high (72.8%), suggesting partial success of HIV education programs. However, high-risk behavior coupled with high HIV and syphilis prevalence among this population suggest that education is not translating into behavior modification. This suggested that risk reduction education alone cannot help MSM make lasting behavioral changes. In addition to providing accurate and up-to-date information on risky behaviors, effective community-based prevention programs not only make condoms available and accessible but also focus on enhancing individuals' motivation to change their behavioral patterns, teaching concrete strategies, and behavioral skills to reduce risk, providing tools for risk reduction, and reinforcing positive behavior change.
Since 2005, the Chinese government has made efforts to scale up intervention programs for MSM, which include condom promotion, counseling and testing, peer education, STI services, and follow-up outreach and care services for HIV-infected individuals.2 The government has also developed national guidelines on HIV prevention and control for MSM.2 However, based on the results of this study, these efforts are not translating into the behavior modification needed to reduce STI and HIV risk. Only 18.9% of participants reported having an HIV test, and only 77.8% received pretest counseling. Less than one-third reported seeking treatment for an STI at an appropriate clinic with 10.4% seeking no treatment at all for symptomatic STIs. Less than half (46.3%) reported having received educational information about HIV through free posters and brochures. Additionally, third quarter national statistics in 2007 showed that 88,082 MSM were reached by comprehensive HIV prevention interventions, which represents only 8.2% of the MSM population (MOH, unpublished data, October 2007). Although widespread stigma hinders MSM from seeking HIV-related and STI-related services, additional efforts are needed to ensure that targeted messages reach a high proportion of MSM to prevent HIV and STI transmission. Increasing access to both STI clinics and education is also necessary to ensure that those infections, which increase HIV risk, are properly diagnosed and treated. Without appropriate health messages and support, many MSM will continue to engage in risky sexual behavior and fail to seek treatment when needed.
HIV and other STI transmission through male homosexual sex is increasing dramatically1,2,28,29; however, MSM have not been effectively targeted in China. This group has been largely ignored by both social and public health structures for too long, given their highly disproportionate HIV burden.30 Discrimination and stigmatization against MSM also continue to fuel the epidemic, resulting in under-representation in prevention/care programs and surveillance systems.30 Increased efforts are needed to target MSM for these services and ensuring their inclusion in surveillance systems.
Strengths of this study include its substantial sample size, geographic diversity of recruitment venues, and geographic mapping of the targeted population with population size estimation. Our study subjects may represent a wider spectrum of MSM in China than previous studies, which relied on convenience sampling.10,12,24 The study also has limitations. The cross-sectional nature of the study prevents ascertainment of causal associations between variables of interest. Additionally, an analysis of the role of social and sexual networks was not conducted. MSM typically have multiple sex partners and are highly mobile. An analysis of these networks would have enabled us to better understand the role of MSM in HIV/STI transmission within and beyond this population. Our study only interviewed urban MSM and therefore might not be representative of the MSM population. However, MSM tend to congregate in urban areas, even if they live in rural areas, suggesting that our study can be representative of more than just urban MSM. Finally, our study does not examine all sociodemographic and behavioral characteristics that could be risk factors for both HIV and syphilis. Additional studies need to be conducted to increase our understanding of current syphilis and HIV epidemics among Chinese MSM. A better understanding of the epidemic is crucial for successful prevention.
Both HIV and syphilis infections have reached alarming rates in China's MSM population, even in previously low prevalence regions. Although awareness of HIV transmission routes is high, suggesting successful dissemination of HIV education, potential risk factors are extremely prevalent, indicating that more needs to be done. Both HIV and syphilis control is deserving of China's highest priority. Increased testing for HIV and STIs, particularly for MSM, should be considered a necessary component of the prevention strategy, along with better targeted education programs and greater access to treatment. Combined syphilis and HIV control is essential among MSM in Chinese cities not hitherto perceived to be in the epidemic mainstream. This study should serve as a call to redouble our efforts in increasing access to testing, prevention, and treatment programs for MSM in China.
Authors thank Dr. Kenneth James Drake and Ms. Meredith Bortz from Vanderbilt University for help preparing the article.
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China; drug abuse; HIV; MSM; sexual behavior; syphilis
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