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Relationship Between Syphilis and HIV Infections Among Men Who Have Sex With Men in Beijing, China

Ruan, Yuhua PhD*; Li, Dongliang MD; Li, Xinxu MD*; Qian, Han-zhu MD, PhD; Shi, Wei MD, PhD; Zhang, Xiaoxi MD; Yang, Zhenkai MD; Zhang, Xiaoyan MD, PhD*; Wang, Chen MD; Liu, Yingjie MD; Yu, Miao MD; Xiao, Dong BS; Hao, Chun MD*; Xing, Hui MS*; Hong, Kunxue MD, PhD*; Shao, Yiming MD, PhD*

Sexually Transmitted Diseases: August 2007 - Volume 34 - Issue 8 - p 592-597
doi: 10.1097/01.olq.0000253336.64324.ef

Background: Little is known about risk of HIV and other STDs among men who have sex with men (MSM) in China.

Objective: To survey the prevalence and risk factors of HIV and syphilis and evaluate correlation of two infections among MSM in the Chinese capital city.

Methods: A community-based sample of 526 MSM was recruited in 2005 through Internet advertising, community outreach, and peer referring. Interviewer-administered interviews were conducted to collect information on demographics and sexual and other risk behaviors, and blood samples were collected to test for syphilis and HIV infections.

Results: Seventeen (3.2%) participants were HIV seropositive and 59 (11.2%) syphilis seropositive. Sixty-four percent of participants were migrants who did not have Beijing residence. Forty percent had >10 lifetime male sex partners and 28.8% reported having ever had sex with women. Consistent condom use with primary male sex partners ranged from 21% to 24%, with nonprimary male sex partners from 35% to 42%, and with female partners around 33%. Illicit drug use was not common; only 2.5% reported using Ecstasy or ketamine in the past 6 months. Multivariate logistic regression analyses demonstrated that >10 lifetime male sex partners were independently associated with seropositivity of both syphilis (OR, 1.9; 95% CI, 1.1–3.4) and HIV (OR, 4.3; 95% CI, 1.4–13.6). In addition, HIV infection is significantly associated with syphilis seropositivity (OR, 3.8; 95% CI, 1.3–10.8).

Conclusions: High mobility, multiple sexual partners, and high prevalence of unprotected sex behaviors and syphilis infection suggest a potential rapid spread of HIV in Chinese MSM.

Average prevalence for a group may be misleading, since persons face disease prevalence within their own network. Such prevalence may differ from the average based on the disease and the characteristics of individuals.

From the *State Key Laboratory for Infectious Disease Prevention and Control, and National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; †Chaoyang Center for Disease Control and Prevention, Beijing, China; and ‡Division of Preventive Medicine, Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama

We are grateful to the editor and two anonymous referees for their critical review of this manuscript.

This study was supported by grants from the Ministry of Science and Technology of China (2004BA719A01), China Integrated Programs for Research on AIDS (CIPRA, U19AI51915), the National Institute of Allergy and Infectious Diseases, National Institutes of Health, USA.

Correspondence: Yiming Shao, MD, PhD, State Key Laboratory for Infectious Disease Prevention and Control, and 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:

Received for publication July 27, 2006, and accepted October 27, 2006.

INJECTION DRUG USE and unhygienic plasma-collecting practices, which together have contributed to over 70% of 141,000 cumulatively reported cases of HIV infection in mainland China as of 2005, have been primary risk factors.1 However, China is facing an increasing risk of sexual transmission, either heterosexual through female sex workers (FSWs) or male-to-male sexual transmission among men who have sex with men (MSM).2 Unprotected male-to-male sexual contacts account for <1% of reported cases,1 but the estimated rate is 7.3% out of the 650,000 total cases by 2005.3 While data on HIV/AIDS epidemic among FSWs are increasingly available from the national HIV sentinel surveillance system2 and epidemiologic studies,4–6 little is known about MSM. A convenience sample of 481 MSM in the capital city Beijing showed that 3.1% respondents were HIV positive,7 and none of 144 bar-attending MSM in five eastern Chinese cities was infected with the virus.8

In the past decades, China has also observed a remarkable increase of sexually transmitted diseases (STDs); for example, the annual reported cases of eight reportable STDs (including syphilis and HIV/AIDS) increases from 48 in 1980 to 157,108 in 1990 and further skyrockets to 859,040 in 2000 and 742,022 in 20049–11. Syphilis accounts for about 10% of the reported epidemic, e.g., 9.9% in 2000 and 10.9% in 2004.9,10 There is a particular concern about ulcerative STDs including syphilis, which have been found to increase, by two- to fivefold, the risk for HIV infections.12,13 HIV, in turn, may increase the acquisition of other STDs and alter the natural history and response to standard therapy of ulcerative STDs, resulting in “epidemiologic synergy” between HIV and STDs.14,15 Sparse prevalence data suggest that STDs may be common among MSM in China. Of 144 men recruited from gay bars in eastern China, 6.9% had active syphilis, 7.8% were infected with herpes simplex virus-2, and 13.2% had genital warts.8 Meanwhile, studies have documented a high prevalence of risky sexual behaviors among MSM. In a nationwide survey of 1109 MSM, >80% of respondents had unprotected oral sex, >60% had unprotected anal intercourse, and nearly 10% were involved in commercial sex in the previous year.16 Under social pressure, most MSM hide their sexual orientation and many of them are married.2,17,18 About one third are married, and even a higher proportion of Chinese MSM have ever had sex with women.17,18 Therefore, MSM may play a bridging role in spread of HIV and other STDS from their high-risk male sexual partners to their low-risk female partners such as wives.2 This study aims to survey the prevalence and risk factors of HIV and syphilis and evaluate correlation of these two infections among a community-based sample of MSM in Beijing, China.

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Study Participants and Recruitment

This cross-sectional study was conducted from June to November 2005 in China's capital city, Beijing. Study participants were recruited in three ways. The first method was though advertising at the websites of National Center for AIDS/STD Control and Prevention ( and a nongovernmental AIDS volunteer group ( Second, 15 peer recruiters were hired and trained to reach out to clubs, bars, parks, and bath houses frequented by MSM and distribute flyers with study-related information. Third, study participants were encouraged to refer their peers to participate in the study. All potential participants came to a district HIV testing and counseling clinic in downtown Beijing for eligibility assessment. Eligibility criteria included self-reported same-gender sex in the past 6 months, Beijing residence, and willingness to provide written informed consent. Written informed consent was obtained from all study participants before they were interviewed. Those who met the screening criteria then completed an HIV/STD risk assessment interview, received HIV pretest and risk-reduction counseling, and had blood drawn to test for HIV and syphilis antibodies. Participants were also given HIV posttest counseling when they subsequently returned for their HIV test results. The study protocol and informed consent form were approved by the institutional review board of the National Center for AIDS/STD Control and Prevention of the China Center for Disease Control and Prevention.

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Data Collection

Data were collected using an interviewer-administered questionnaire on the basis of a one-to-one interview in a separate room of the district clinic. Each study participant was assigned a unique and confidential identification code for the questionnaire and specimens. Major demographic variables collected were age, ethnicity, education, employment, current marital status, income, housing, and residence. Questions pertaining to behavior and practices included sexual orientation, age of initiating sex with men, lifetime number of male sex partners. Questions also addressed the following behaviors in the past 6 months: commercial sex with male sex partners, any new male sex partners, unprotected insertive anal sex with primary or nonprimary male sex partners, unprotected receptive anal sex with primary or nonprimary male sex partners, unprotected vaginal sex with primary or nonprimary sex partners, and illicit drug use.

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Laboratory Analysis of HIV and Syphilis Infections

All participants provided a blood specimen, which was tested for both HIV and syphilis antibodies. Blood samples were tested for HIV antibody with an enzyme-linked immunosorbent assay (ELISA) (Beijing Wantai Biologic Medicine Company, China) and positive results were confirmed by an HIV-1/2 Western Blot immune assay (HIV Blot 2.2 WB, Genelabs Diagnostics, Singapore). Syphilis antibodies were screened by using an ELISA (Beijing Wantai Biologic Production Company, China). Reactive samples were confirmed by a Passive Particle Agglutination Test for Detection of Antibodies to Treponema pallidum (TPPA, Omega, UK). HIV subtype analysis was based on the sequences from the env and gag regions of the HIV RNA envelope.

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Statistical Analysis

Questionnaire data were double entered and compared with EpiData software (EpiData 3.0 for Windows; The EpiData Association Odense, Denmark). After corrections, data were then converted and analyzed using Statistical Analysis System (SAS 9.1 for Windows; SAS Institute Inc., NC).

We calculated HIV prevalence and confidence interval (CI). Variables significant at a level of 0.1 in bivariate logistic regression analyses were fitted into multivariate models. Multivariate logistic regression models were constructed through backwards elimination to select independent risk factors for HIV and syphilis infections separately, while controlling for potential confounding factors. Both odds ratio (OR) and CI were obtained for each explanatory variable in the final models.

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General Characteristics

Five MSM refused to participate in the study, and seven participants withdrew from the study because they were unwilling to answer the sensitive questions regarding sexual behaviors. Of the 526 study participants, 43.0% were recruited through community outreach, 38.6% through peer referring, and 18.4% through Internet advertising. The average age was 26.2 years (standard deviation, 6.5), with a range of 17 to 54 years; 93.9% were majority Han ethnics and 6.1% were other minority ethnics. Two percent of participants had primary school or less, 10.3% attended junior high school (9 years), 25.7% attended senior high school (12 years), and 62.0% had some college or above. A total of 77.6% participants were single, 6.5% were married, 0.4% cohabited with a female friend, 11.2% cohabited with male sexual partner, and 3.0% were divorced, respectively. About 20% of participants were students, and 11.2% had no job; 35.7% had a Beijing resident card. The median monthly income of the participants was $200US. Only 2.5% reported using illicit drugs (mainly ecstasy and ketamine) in the past 6 months.

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Sexual Behaviors

Most MSM had their first sex with men at the age of around 20 years. About two thirds of MSM had both primary and secondary sexual partners in the past 6 months, and the median number of sexual partners was 2. However, commercial same-sex practices were not less than 10%. Ten percent reported having sex with women in the past 6 months. About one fifth reported consistently using condoms with primary male partners and one third with other sexual partners (Table 1).



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Syphilis Infection and Correlates

Of 526 participants, 11.2% (59) were infected with syphilis, as shown in Table 2. In bivariate analyses, factors significantly associated with syphilis infection were age, occupation other than students, college and higher education, lifetime number of male sex partners, type of recruitment, a history of STDs, and illicit drug use. Beijing residence, sex with women, condom use, and way of finding sex partners were not significantly associated with syphilis infection (P >0.05). Multivariate logistic regression analysis demonstrated that older age (OR, 2.2; 95% CI, 1.3–3.9) and >10 lifetime male sex partners (OR, 1.9; 95% CI, 1.1–3.4) were associated with higher risk of syphilis infection, while nonpeer-recruit route (OR, 0.5; 95% CI, 0.3–0.8) was associated with lower risk.



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HIV Infection and Correlates

Of 526 participants, 3.2% (17) were infected with HIV, as shown in Table 3. Factors significantly associated with HIV infection were college and higher education, Beijing residence, lifetime number of male sex partners and syphilis infection. Age, occupation other than students, type of recruitment, sex with women, condom use, a history of STDs, way of finding sex partners, and illicit drug use were not significantly associated with HIV infection (P >0.05). Multivariate logistic regression analysis demonstrated that >10 lifetime number of male sex partners (OR, 4.3; 95% CI, 1.4–13.6) and syphilis seropositive status (OR, 3.8; 95% CI, 1.3–10.8) were associated with increased risk of HIV infection. Of the 10 specimens that could be typed, 9 (90%) were reactive to HIV-1 subtype B and 1 was reactive to subtype CRF01-AE.



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Our study showed a moderate prevalence of HIV (3.2%) and a high prevalence of syphilis (11.2%) among MSM in the capital city Beijing. The HIV prevalence is similar as one in a previous study in the same city (3.1%),7 but seems to be higher than those in other Chinese regions, for example, 0.0% in Dalian City and 1.3% in Ha'erbin (northeastern China),19,20 0.0% in five cities of Jiangsu Province (eastern China),8 and 1.6% in Shenzhen City (southern China).21 A high prevalence of syphilis was also observed among MSM in other Chinese cities, such as 16.7% in five cities of Jiangsu Province,8 19.1% in Shenzhen City,21 and 11.1% in Guangzhou City (southern China).22

Contrary to the scenario in China that MSM are not among HIV heavily infected subgroups, MSM account for a large portion of HIV cases in many Western countries. In the United States, over 40% of cumulative reported AIDS cases through 2004 are related to male-to-male sexual contact.23 MSM accounts for 27% of new HIV cases during 2003–2004 in France, 40% from 2001 to 2005 in Germany, 49% in 2003–2004 in Netherlands, and 32% in 2004 in the UK.24 Syphilis epidemics declined in North America and Western Europe during early 1990s but rose in the past years.25,26The recent epidemics have largely involved MSM.25,26 Wide access to highly active antiretroviral therapy (HAART) since the middle1990s in Western countries has improved the health and survival of AIDS patients and led to HAART-related treatment optimism,27 which may partially explain the resurgence of risky sexual behaviors and the rising syphilis epidemic among MSM in some large cities of these countries in recent years.28,29

Illicit drug use is uncommon among Chinese MSM, which may be another difference from their counterparts in many Western countries. Only 2.5% of participants in our study used illicit drugs in the past 6 months; another Chinese study found that only one of 201 MSM (0.5%) was adrug injector.22 It seems that there is little overlap of two populations—drug users and MSM in China. On the contrary, drug abuse is common among MSM in Western countries and often constitutes a major risk for HIV spread in this population.23,30,31 Drug use may relax safer sex norms and increase unprotected anal sex and risk of acquiring HIV.30,31

Although drug use may not be a significant contributor to HIV transmission among Chinese MSM based on available data, high prevalence of syphilis and risky sexual behaviors are potential risk factors. Studies have demonstrated the connection between HIV and syphilis infections. A case–control study in New York City found that MSM with primary and secondary syphilis were sevenfold more likely than controls to be infected with HIV;32 a prospective cohort study in Pune, India, showed that the elevated risk of HIV-1 infection was associated with incident syphilis.33 Our data also indicated a possible correlation between HIV and syphilis infections. HIV prevalence was higher among participants with syphilis infection (10.2%) than those without infection (2.4%; P <0.05), although caution should be taken for interpretation of this relationship due to small number of HIV cases in our study. Syphilis may increase risk of HIV acquisition through various mechanisms: syphilitic ulcers ease the passage of HIV, local inflammation and gathering of CD4+ cells increase the possibility of HIV transmission, and activated host immunologic response enhances HIV republication.34 Highly prevalent syphilis infection and risky sexual behaviors, including multiple sexual partners and low condom use as shown in our study and other studies, may suggest a potential rapid spread of HIV among Chinese MSM, considering the fact that HIV has been introduced to this population. Intervention programs are urgently needed with focuses on reducing risky sexual behaviors and treating syphilis and other sexually transmitted infections.

The subtype analysis in our study showed that the 90% of HIV-strains was B and 10% and CRF01-AE. A subtype of 12 specimens during 1998–2001 among HIV-infected MSM in Beijing was B, which lasted for about 10 years; its origin was from Europe or America.35 Continued monitoring of HIV-1 subtype is needed for tracking cross-group transmission, for example, from injection drug uses to MSM.

MSM are a hidden subgroup in China. It is difficult to survey a representative sample of this population. Previous studies often use convenience samples7,19–21. We used multiple approaches to recruit study participants, and our study subjects may represent a wider spectrum of MSM in Beijing. Seventy percent of participants in our study received some college or higher education, and 64.3% did not have a Beijing resident card. These proportions are higher than those in other Chinese big cities19,21). Condom use among MSM in our study is similar to that in other Chinese cities19–21. Beijing is the capital of China, which represents more higher education and floating population.

Due to the nature of cross-sectional study, we can not ascertain causal association between syphilis and HIV infections. Longitudinal studies are needed to assess the temporal relationship. Considering the facts that MSM have multiple sex partners and are highly mobile, analysis of social and sexual networks may help understand the transmission of HIV/STDs within and beyond this population.36 Our study is a one-site study; the prevalence rates of syphilis and HIV infections may not necessarily represent the situation in other areas. MSM should be included in the Chinese HIV sentinel surveillance system.

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