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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e3181aac23d
Articles

Prevalence and Correlates of HIV and Syphilis Infections Among Men Who Have Sex With Men in Chongqing Municipality, China

Xiao, Yan MD, DrPH*; Ding, Xianbin MD, MPH†; Li, Chunmei MD, MPH‡; Liu, Jianbo MD, MPH†; Sun, Jiangping MD, PHD*; Jia, Yujiang MD, DrPH§

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From the *National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China; †Chongqing Municipality CDC, Institute for AIDS/STD Control and Prevention, Chongqing, 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

The authors thank Meredith Bortz from the Vanderbilt Institute for Global Health for manuscript assistance and also thank Lei Xu from the Department of Biostatistics of Vanderbilt University for the statistics assistance.

Supported 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, the Institute for Global Health and Department of Pediatrics, School of Medicine, Vanderbilt University.

Correspondence: 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: jpsun@chinaaids.cn, and Yujiang Jia, MD, DrPH, Institute for Global Health and Department of Pediatrics, Vanderbilt University School of Medicine, 2525 West End Avenue, Suite 750, Nashville TN 37203-1783. E-mail: Yujiang.Jia@vanderbilt.edu.

Received for publication January 8, 2009, and accepted April 15, 2009.

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Abstract

Objective: To examine the prevalence and correlates of HIV/syphilis infections and sexually transmitted diseases (STDs) among men who have sex with men (MSM) in Chongqing, China.

Method: Cross-sectional surveys were conducted to provide information, including sociodemographics, sexual and drug use behaviors, HIV knowledge, and HIV-related services in 2006 and 2007, respectively. Multiple methods, including venue-based recruitment, community outreach, Internet advertisements, and peer referral, were used to identify men in Chongqing willing to participate in this study.

Results: Of the 1692 participants, 10.8% were HIV-infected (range by district: 7.0%–15.0%), 8.6% were syphilis-infected, and 15.3% self-reported STD-related symptoms. HIV infection was associated with older age, recruitment from bathhouses/saunas, less education, more male sex partners, sex with a woman in the past 6 months, syphilis infection, and STD-related symptoms. Syphilis infection was associated with older age, less education, inconsistent condom use with a man, STD-related symptoms, and HIV infection. STD-related symptoms were associated with older age, being of nonlocal residency, inconsistent condom use with a humans, having ever paid for sex with a humans, HIV infection, and being from District 1.

Conclusions: HIV and syphilis infections have reached alarmingly high rates in Chongqing’s MSM population. Better targeted, in-depth and comprehensive intervention strategies are needed urgently, including education, condom promotion and distribution, STD control, drug use-related intervention, and advocacy for HIV counseling and testing with bridges to HIV prevention and care services. Widespread testing for HIV, syphilis, and other major STDs in this risk group should be considered as measures for control.

The HIV epidemic in china continues to expand. Half of the estimated new cases in 2007 were transmitted sexually, 11% of them via unsafe sex between men.1–5 Disturbing HIV prevalence rates from 1.0% to 5.8% among men who have sex with men (MSM) have been reported in several major Chinese urban cities.2,4,6–9 MSM, a traditionally ignored risk group, are now becoming a more visible part of society and becoming more socially connected with each other, especially in large and midsized Chinese cities and areas with large concentrations of migrants.1,2,5,10

Most studies among MSM have been conducted in large cities in China, particularly Beijing,2,4,11 Shanghai,12 and Guangzhou.13 Increased prevalence of high-risk behaviors were observed among this group; 1 study found that 70% of MSM reported having sex with more than 1 partner in the past 6 months and only 30% used condoms for anal sex, while about half reported not using condoms when they had commercial sex with a male.1 Studies demonstrated the high rates of syphilis infection in this group in the regions with both high and low HIV prevalence rates.3,5,14 Sexually transmitted diseases (STD), particularly genital ulcer diseases, e.g., syphilis and herpes, are strongly associated with HIV acquisition.15–18 MSM has become the second most at-risk group in China for HIV infection following injection drug users.19

Those data collected through surveillance and epidemiologic studies face the challenge of accessing and sampling MSM.20–22 Effective comprehensive prevention intervention programs on MSM were constrained by the lack of reliable information, such as HIV and syphilis epidemics and behavior characteristics among this group. Little is known about the prevalence of HIV, syphilis infections, and other STDs among MSM in Chongqing Municipality. This is the first large study conducted in Chongqing to examine the prevalence and correlates of HIV/syphilis infections and self-reported STD-related symptoms among MSM.

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METHODS

Study Settings

This study was conducted in 3 districts located in the urban area of Chongqing Municipality. These 3 districts comprise 5.3% of Chongqing’s 32 million people. Chongqing, located in midwestern China, is the largest and most populous of China’s 4 provincial-level municipalities.

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Participants

Cross-sectional surveys were conducted among MSM from July to September in both 2006 and 2007, respectively. Social demographic mapping was performed. All potential venues in 3 study districts were listed. The sizes of MSM populations were estimated by “multiplier method” for all mapping communities. There are 6 gay-oriented volunteer workgroups, 6 gay bars, 4 bathhouses, more than 100 clubs, bars, saunas, and 4 gay websites in these 3 districts. There are an estimated 60,000 MSM in 3 study districts, which account for 12.5% of the total number of estimated MSM in Chongqing Municipality. Participants were recruited by trained research staff through multiple methods: venue-based recruitment, Internet advertisements, community outreach, and peer referral using “snowball” techniques. Participants were recruited from gay-oriented venues such as night clubs, bars, tea bars, bathhouses, saunas, and nonvenue-based communities via the Internet, clinics, and grassroots organizations. A total of 1365 eligible participants were recruited using venue-based recruitment from bars, night clubs, tea bars, bathhouses, and saunas; and 327 were recruited using the Internet, clinics, community outreach, and peer referral using “snowball” techniques by grassroots organizations. All potential participants were invited for eligibility assessments and interviews in community-based voluntary counseling and testing centers and/or STD clinics. The experienced health professionals, with the assistance of the trained research staff from the gay community, conducted the interviews. After the introduction of the study purpose and informed consent, structured questionnaire-based interviews were administered by the health professional in a single private room. Survey information was collected anonymously and remained confidential. The enrollment criteria were: male, 18 years of age or older, self-reported having anal or oral sex with another male in the past 12 months, were willing to complete the study, and provided written informed consent. Blood samples were collected for all eligible participants. The study was approved by the Chongqing Municipality Institutional Review Board and the Institutional Review Board of Vanderbilt University.

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Measures

Structured questionnaire-based interviews provided socio-demographics, sexual and drug use behaviors, HIV knowledge, and HIV-related prevention services. Socioeconomic characteristics included: age, marital status, residency, ethnicity, education, and sexual orientation. Respondents were further asked how they perceived their sexual identity. The level of HIV-related knowledge was assessed by using 5 questions that were related to modes of HIV transmission and 3 questions that were related to misconceptions about HIV prevention. All questions were weighted equally. Participants who correctly answered ≥6 questions indicated greater knowledge of HIV transmission. The participants were then stratified into 2 groups, according to whether 6 or more appropriate responses were given to the 8 questions. The participants were also asked whether they received HIV testing and other HIV-related services (free condoms, lubricants, peer education, HIV/STD-related education materials, and STD examination and/or treatment) in the past 12 months. The interviewer asked the participants whether they had STD-related symptoms in the past 12 months. The interview was conducted by the health professional (public health physicians) with assistance from trained research staff from the gay community. Interviews were taken place in a single private room. Self-reported symptoms of STDs were determined according to whether the participants reported symptoms such as chronic pelvic pain, painful and disturbing genital blisters, discharge and painful urination, causing painful, tender blisters on the vaginal or perineal skin, an itchy, foul discharge, a painless ulcer, etc. The interviewer marked “yes” or “no” on the questionnaire based on the report participants provided. The survey took approximately 10 minutes to complete. The survey instrument questions and the method of stratification were based on the China National Comprehensive Surveillance Survey Guideline, which was recommended by a panel of national surveillance experts.

Blood samples were collected from all eligible participants 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 immune assay (HIV Blot 2.2 WB; Genelabs Diagnostics, Singapore). Syphilis infection was determined using rapid plasma reagin (Beijing Wantai Biologic Production Company, Beijing, China) and a Passive Particle Agglutination Test for Detection of Antibodies to Treponema pallidum (Rong Sheng Biostix Inc, Shanghai, China). Syphilis testing algorithm is described in Figure 1.

Figure 1
Figure 1
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Statistical Analysis

Questionnaire-based data and serological testing results were double entered into a computer database. The data collected in the 2 cross-sectional studies were combined with the exclusion of the previous enrollment in 2006 for the enrollment in 2007. We also used data validation tools available in SPSS to check the duplicate data entry. Data were evaluated for congruency using the EpiData software (EpiData 6.4 for Windows, The EpiData Association Odense, Denmark). Univariate and multivariable logistic regression analyses were performed using the SPSS software (Version 16.0; SPSS Institute Inc., Chicago, IL) to evaluate the correlates for HIV/syphilis infections and self-reported STD-related symptoms. Variables with P <0.05 in multivariable analysis were considered statistically significant.

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RESULTS

Characteristics of Participants

Of the 1692 eligible participants enrolled in this study (Table 1), 81 participants were excluded due to failure to provide blood samples (3 participants), being under 18 years of age (53), unwilling to answer the sensitive sex-related questions (12), and repeated participation (13). The age of the participants ranged from 18 to 68 years, with a mean age of 27.7 (SD: ±8.7) years. Of the participants, 17.1% reported being married or cohabiting, 6.0% were separated, divorced or widowed; 22.4% were nonlocal residents; 98.0% belonged to the Han ethnic group; and 86.5% received high school or higher education. Of the 1647 participants, 65.0% self-identified as homosexual, 34.0% as bisexual, and 1.0% as heterosexual (Table 2).

Table 1
Table 1
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Table 2
Table 2
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Sexual and Drug Use Behaviors

One-third (31.2%) of the participants reported having had their first sex at <18 years of age; 41.6% had their first sex with a female partner (Table 3). Most (81.6%) of the participants reported having had anal sex with a male in the past 6 months, with 65.1% reporting more than 2 sex partners (median: 2) and 63.4% reporting inconsistent condom use during anal sex with men. One-fifth reported having had sex with women in the past 6 months, with 76.5% reporting inconsistent condom use. Of the participants, 5.0% reported paying for sex with men in the past 6 months, with 40.0% reporting inconsistent condom use; 6.3% received money for sex with men, with 31.5% reporting inconsistent condom use. Of the participants, 5.2% reported using drugs in the past 6 months, with 5.7% injecting drugs.

Table 3
Table 3
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Table 3
Table 3
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HIV Knowledge and Prevention Services

The majority (91.8%) of the respondents answered at least 6 of the 8 HIV-related questions correctly (Table 3). More than half of the participants received HIV education material (60.4%), half received free condoms (52.3%) and peer education (51.7%), and one-third (35.9%) had received examination and/or treatment for STDs in the past 12 months. Of the participants with STD-related symptoms in the past 12 months, 58.7% sought STD services, 23.5% self-treated, and 17.8% received no treatment. Only 29.6% of the participants received a test for HIV in the past 12 months with three-quarter received pretest counseling.

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Prevalence of HIV, Syphilis Infections, and Self-Reported STD-Related Symptoms

Of the participants, 10.8% were HIV-infected (ranging from 7.0% to 15.0% by district), 8.6% were syphilis-infected (from 7.0% to 9.6% by district) and 15.3% (11.8%–19.9% by district) self-reported having STD-related symptoms in the past 12 months. HIV was more common among participants with syphilis infection (adjusted odds ratio, AOR = 1.7; 95% CI: 1.1–2.9) and with STD-related symptoms (AOR = 1.7; 95% CI: 1.1–2.7) than those without (Table 4).

Table 4
Table 4
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Correlates for HIV Infection

In the multivariable logistic regression model, HIV infection was independently associated with older age (AOR = 1.6, 95% CI: 1.1–2.5, 25–34 years of age vs. younger; AOR = 2.3, 95% CI: 1.4–3.7, ≥35 vs. <25 years of age), being recruited from bathhouses or saunas (AOR = 2.1, 95% CI: 1.0–4.4), less education (AOR = 2.2; 95% CI: 1.5–3.3), more than 2 male sex partners in the past 6 months (AOR = 1.8; 95% CI: 1.2–2.7), sex with a woman in the past 6 months (AOR = 1.4; 95% CI: 1.0–2.5), syphilis infection (AOR = 1.7; 95% CI: 1.1–2.9), and self-reported STD-related symptoms in the past 12 months (AOR = 1.7, 95% CI: 1.1–2.7) (Table 4).

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Correlates for Syphilis Infection and Self-Reported STD-Related Symptoms

In the multivariable logistic regression model, syphilis infection was independently associated with older age (AOR = 1.9; 95% CI: 1.1–3.4; ≥35 vs. <25years of age), less education (AOR = 1.7; 95% CI: 1.1–2.6), inconsistent condom use during anal sex with a male (AOR = 1.5, 95% CI: 1.1–2.3, sometimes vs. always), self-reported STD-related symptoms (AOR = 1.6; 95% CI: 1.0–2.4), and HIV infection (AOR = 1.7; 95% CI: 1.1–2.8) (Table 4). Self-reported STD-related symptoms were independently associated with older age (AOR = 0.5, 95% CI: 0.3–0.7; ≥35 vs. <25years of age), being a nonlocal resident (AOR = 1.6, 95% CI: 1.2–2.2), inconsistent condom use during anal sex with a male (AOR = 2.5, 95% CI: 1.6–3.9, never vs. always), having paid for sex with a male in the past 6 months (AOR = 1.9, 95% CI: 1.1–3.5), HIV infection (AOR = 1.7, 95% CI: 1.1–2.6), and being from district 3 (AOR = 2.1, 95% CI: 1.3–3.4, vs. district 1) (Table 4).

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DISCUSSION

Our study found that HIV prevalence was alarmingly high in Chongqing’s MSM; the rates are significantly higher than those reported in the past in the same districts (0.5% in 2004 and 3.0% in 2005).23 This rate also greatly exceeds any other reports in China.2,3,5,6,8,24,25 High HIV prevalence rates among MSM in Asia have drawn attention recently in Phnom Penn, Cambodia (8.9%); Chiang Mai, Thailand (15.3%); and Andhra Pradesh, India (18.2%),26 especially the rising HIV prevalence among MSM in Bangkok, which was up from 17.3% in 2003 to 28.3% in 2005.27 Rising prevalence in Chongqing signals that MSM have emerged as a high-risk group for HIV and the epidemic has further spread among this population in China.

In this study, syphilis was detected at 8.6% among MSM. Consistently high prevalence rates of syphilis from 6.9% to 19.1% were reported among MSM populations in different studies in urban cities.3,6,12,13 However, the HIV epidemic among MSM has a wide geographic variation, with concentrated epidemics in several cities in China. A systematic review has suggested the prevalence of syphilis infection among MSM has increased in China.28 A high prevalence of self-reported STD-related symptoms (15.3%) was also documented, which nearly doubled the prevalence rates of syphilis infection found in this study.

Although HIV prevalence rate among MSM in Chongqing is higher than many areas in China but the rate of syphilis is not as high as that in many areas, why? Because the “open door policy” and economic reforms were initiated in 1978, the social structure of China has been changing dramatically. Commercial sex activities have flourished across the country and STDs, including syphilis, have reemerged as a major public health problem 30 years after their near-elimination in China. Although high HIV prevalence rates have been found among MSM in some parts of China, the syphilis epidemic may not reach high levels in some areas where HIV infections are prevalent. Syphilis has just introduced into Chongqing’s MSM population; this rate is lower than many reports among MSM in other parts of China. Still, Chongqing’s MSM face a potential threat for rapid spread of syphilis infection due to the prevalent unprotected sex that have led the rapid spread of HIV.

Our study found that older age, less education, more male sex partners, bisexual behaviors, and recruitment from bathhouses or saunas were independent factors for HIV infection, these are consistent with other studies.24,29 Similar factors and inconsistent condom use were associated with syphilis infection and a history of STD-related symptoms. In China, MSM are a hidden subgroup in mainstream society. In fact, the challenges of even identifying MSM, such as stigma, discrimination, denial and ignorance, aggravate an already difficult situation. Most MSM married women to cover up their sexual orientation. Our study found that one-third of the participants self-identified as bisexual, 17.1% were married or cohabiting, and one-fifth had sex with women in the past 6 months. Moreover, the rate of consistent condom use with women was lower than with men. The high portion of men who have sex with both men and women could serve as a potential “bridge” in spreading HIV from high-risk MSM to their female partners. Lack of consistent condom use coupled with multiple sexual partners, common bisexual practices, and high mobility suggested that the epidemic could further spread among MSM and their low-risk female sex partners. Our study also found that older and less educated people are more likely to be infected with HIV and syphilis and participants recruited at bathhouses or saunas had higher HIV prevalence and more sexual partners than participants from other venues; this is consistent with other recent reports.30,31 These underline the need to explore more specifically designed education methods, condom promotion and distribution, and intervention programs to target the most vulnerable group.

Data showed that China faces a growing risk for HIV through sexual transmission, either heterosexually (through casual or commercial sex) or homosexually (among MSM).1 The nation recognizes the HIV/AIDS needs of more easily identifiable risk groups (e.g., injections drug users, female sex workers, and former blood/plasma donors), but neglects the needs of the emerging high-risk group, MSM.1,20,32–34 In Western countries, unsafe sex between men has been the most common route of transmission since the epidemic started. In the United States, more than half of new HIV infections (53%) in 2006 were among MSM.35,36 In Canada, unsafe sex between men continues to account for the largest proportion of new HIV infections (45% in 2005 compared with 42% in 2002).37 In central Europe, one-quarter of reported HIV cases were among MSM (27%) in 2006.38 Syphilis epidemics declined in North America and Western Europe during the early 1990s, but rose in the past years, underlining the need for inventive and better-targeted prevention in this community.39 Both the syphilis and HIV epidemics have largely involved MSM.40,41

This study found that 5.2% of participants reported ever using illicit drugs; other studies found much lower rates (0.5%–0.7%).2 Although no statistically significant relationship was found between HIV/STD infection and illicit drug use in this study, we believe that the rate of illicit drug use is worthy of recognition. There were no HIV or syphilis-infected participants found among injecting MSM, we found that 10.2% and 9.1% of drug users were infected HIV and syphilis, respectively; there is no significant difference between drug users and nondrug users. Drug use has been the predominant transmission route for HIV and high HIV prevalence (>30%) in Chongqing’s injection drug users, as reported in several sentinel surveillance sites.42 Data from many Western countries demonstrated that drug abuse is common among MSM and often constitutes a major risk for HIV; studies have established the association between substance abuse and sexual risk for HIV in various ethnic MSM communities.43–46 Drug use could relax safer sex norms and increase unprotected anal sex and the risk of acquiring HIV.44,45 However, the role of substance abuse in sexual behavior and the acquisition of HIV and other STDs among MSM is not well understood in the Chinese context. Much needs to be done to clarify the determinants of drug use among this group, whether drug use relates to sexual behavior, and the factors that account for the relationship between the 2 behaviors. STD risk reduction strategies, education, and behavior intervention have traditionally ignored MSM. Further investigation of these relationships may allow efforts and resources to be directed toward individuals whose behavior places them at risk.

These findings are worrisome in that HIV infection was independently associated with either a syphilis infection or self-reported STD-related symptoms. A case–control study in New York City found that MSM with primary and secondary syphilis were 7-fold times more likely than controls to be infected with HIV.15 A prospective cohort study in Pune, India showed that the elevated risk of HIV-1 infection was associated with incident syphilis.47 Syphilis may increase the risk of HIV acquisition through various mechanisms: syphilitic ulcers ease the passage of HIV, local inflammation and gathering of CD4+ cells increases the possibility of HIV transmission, and activated host immunologic response enhances HIV replication.48 In this study high risk factors along with the overlap between HIV and syphilis infection among the participants demonstrates the consequences of risky behavior and poses a particular concern that syphilis could further facilitate the transmission of HIV.

Although the majority of participants have HIV-related knowledge, the rates of condom use, uptake of HIV testing, and use of prevention services were still low. Many MSM with STD symptoms did not seek proper treatment. This indicated that a large portion of MSM who may be infected with HIV do not know their status and could continue to spread the virus.20,49 Widespread stigma often prevents MSM from seeking or receiving essential HIV/AIDS prevention services and care. China has scaled up HIV control efforts since 200450; however, low HIV testing rates (≈20% nationwide) remain an impediment to prevention and care.49 This suggests 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 and services available and accessible, but also focus on enhancing individuals’ motivation to change their behavioral patterns, teaching concrete copying behavioral skills to reduce risk, providing tools for risk reduction, and reinforcing positive behavior change.

Strengths of this study include its substantial sample size, via multiple recruitment methods with mapping strategies. Data suggested that most MSM in Chongqing seek sexual partners through the Internet, and participants recruited from different venues have different risks for HIV infection,23 therefore, multiple recruitment methods could provide a more representative sample. This study found that HIV and syphilis prevalence rates are 10.2% and 7.4% for the participants recruited from bars, night clubs, and tea bars, respectively; but significantly higher rates for HIV and syphilis infections were found at 17.6% and 17.0% among participants recruited from venues of bathhouses and saunas, respectively. This is consistent with the finding of lower levels of knowledge and higher rates of unprotected sex and sex trade among the venues of bathhouse and saunas. Because there are more bathhouses and saunas in district 3, both venues have a significantly higher risk for HIV infection, therefore, the HIV prevalence rate is significantly higher among MSM from District 3 (data not shown). The sociodemographic and behavioral factors identified in our study are informative, giving us a stronger grasp of Chongqing’s current HIV and syphilis epidemic in MSM.

The study also has its limitations. The questionnaire data relying on retrospective self-reports was subject to recall bias. Cross-sectional research design precludes identification of causal relationships. The brevity of the interview cannot provide a complete view. The findings should be interpreted carefully when generalizing the larger MSM population or comparing results from other studies.

Various programs targeting MSM were conducted on condom promotion, counseling and testing, peer education, STD services and follow-up outreach, and care services for HIV-infected individuals in China.1,50 However, effective follow-up and prevention intervention were constrained by the lack of reliable information on MSM, such as size of the population, behavior patterns, and the HIV epidemic among this group.1 The coverage of comprehensive prevention packages to address high risk behaviors among this group is limited. The linkage between the identification of HIV status and referral to treatment and care services is weak and not standardized.1 As a result, insufficient information is available to provide follow-up treatment, care, and support.

In conclusion, HIV risk-reduction interventions for Chinese MSM need to address the overlapping epidemics of HIV/syphilis infections and other STDs. Better targeted, indepth and sustained comprehensive intervention are needed urgently, including education, condom promotion and distribution, STD control, drug use-related intervention, and advocacy for HIV counseling and testing with bridges to HIV preventive services and care. Widespread screening for HIV/syphilis infections and other major STDs in this risk group should be considered as measures for control.

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