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Prevalence of Syphilis and Human Immunodeficiency Virus Infections Among Men Who Have Sex With Men in Shenzhen, China: 2005 to 2007

Feng, Tie-Jian MD*; Liu, Xiao-Li MD*; Cai, Yu-Mao MPH*; Pan, Peng MD*; Hong, Fu-Chang MD*; Jiang, Wei-Na MD*; Zhou, Hua MD; Chen, Xiang-Sheng MD, PhD

doi: 10.1097/OLQ.0b013e31818600f4

From the *Shenzhen Center for Chronic Disease Control and Treatment and Shenzhen Institute of Dermatology, Shenzhen, People's Republic of China; †Baoan District Hospital of Maternal and Child Health, Shenzhen, People's Republic of China; and ‡National Center for STD Control, Chinese Academy of Medical Sciences and Peking Union Medical College Institute of Dermatology, Nanjing, People's Republic of China

The authors thank all participants of this study for their cooperation. We also thank Kathryn E. Muessig, a doctoral candidate of the Johns Hopkins Bloomberg School of Public Health and the NIH Fogarty International Center Research Scholar, for English editing.

Supported by grants from the Shenzhen Sciences and Technology Program.

Correspondence: Yu-Mao Cai, MPH, Shenzhen Center for Chronic Disease Control, 2021 Buxin Road, Luohu District, Shenzhen, Guangdong Province 518020, People's Republic of China. E-mail:

Received for publication April 4, 2008, and accepted June 25, 2008.

IN CHINA, THERE HAS BEEN an emerging epidemic of HIV and syphilis infections among men who have sex with men (MSM). Multiple surveys conducted in recent years have shown a high prevalence of syphilis infections among MSM in China.1,2 A rapid increase of HIV prevalence has been demonstrated among MSM in some areas, including in China. For example, the prevalence of HIV had increased from 0.4% in 2004 to 5.8% in 2006 in Beijing, China.3 A high HIV prevalence has also been found among MSM in other Asian countries including Phnom Penn, Cambodia (8.9%), Chiang Mai, Thailand (15.3%), and Andhra Pradesh, India (18.2%).4 In 2007, homosexual transmission has accounted for 12.2% of the 50,000 estimated new HIV infections in China.5 Risk of HIV transmission is a particular concern in the context of current syphilis epidemic because infection with ulcerative STDs, including syphilis, has been shown to increase the risk of HIV transmission 3- to 5-fold.6 HIV may also increase the acquisition of other STDs and alter the natural history and response to standard therapy of ulcerative STDs, resulting in an “epidemiologic synergy” between HIV and STDs.7 For these reasons there is particular concern about the potentially increasing transmission of HIV and syphilis among MSM.8 Because of overlaps in sexual networks between the MSM and non-MSM population, it is also predicted that the transmission of HIV and syphilis among MSM may play an important role on driving the epidemic of HIV and syphilis in China in the future.

This article presents results from 3 consecutive prevalence surveys of HIV and syphilis infections among MSM in Shenzhen of Guangdong, China. This study aimed to understand the magnitude of HIV and syphilis infections among MSM, trends in infection over time, and the main corrects for infections in order to inform policy makers and develop an evidence-based syphilis control program.

The study subjects were recruited from 3 MSM saunas, 3 MSM bars, and 1 MSM clinic affiliated to the Shenzhen Center for Chronic Diseases Control (Shenzhen Institute of Dermatology) in Shenzhen City between 2005 and 2007. Eligible participants were those men who self-reported having sex with other men. All eligible MSM participants were informed of the study and its purposes. Those who agreed to participate in the study gave verbal informed consent and were enrolled. Participants completed a short interview-administered questionnaire that included socio-demographic and sexual behavior questions. The interview was conducted one-to-one by a trained doctor from the STD clinic, or a trained outreach worker with previous experience in HIV/STD prevention services at MSM saunas and bars. In addition to completing the questionnaire, blood was drawn for syphilis and HIV serology testing. Unlinked, anonymous screening was conducted on each blood sample. For syphilis, toludine red unheated serum test (TRUST, Rongsheng Biotech Inc, Shanghai, China) was used for initial screening and Treponema pallidum particle agglutination test (Fujirebio Inc. Japan) was used for confirmation of those with positive TRUST results. Cases with positive TRUST and Treponema pallidum particle agglutination test results were defined as serologically positive for syphilis, i.e., syphilis infection. HIV infection was identified by screening with ELISA and confirmation with Western blot for positive ELISA specimens. The study was approved by the Medical Ethics Committee of the Shenzhen Center for Chronic Disease Control/Shenzhen Institute of Dermatology. Data from questionnaires and laboratory tests were entered using the EpiData software (EpiData Association, Denmark). For each survey year, we present crude and population-adjusted point prevalence and 95% confidence intervals (CIs) of HIV and syphilis infections. Data about prevalence of syphilis by year was compared using χ2 test. Univariate analysis was used to identify variables associated with syphilis infection. Crude odds ratios (OR) are given with corresponding 95% CIs. Variables that were significant at P < 0.10 in univariate analyses were included for multivariate logistic analysis. Multivariate model variables with a probability level of P ≤ 0.05 were considered statistically significant. All statistical analysis was conducted with SPSS for Windows 11.0 (SPSS Inc., Chicago, IL).

The total numbers of MSM enrolled were 242 in 2005, 458 in 2006, and 676 in 2007. Among the 1376 MSM who participated in the study, more than half (53.1%) were recruited from one STD clinics, 31.6% from 3 sauna venues, and 15.3% from 3 gay bars. Average age was 28.5 ± 7.2 (standard deviation, SD) years with a range of 17 to 68 years. The majority of the participants (96.6%) came from Shenzhen or areas near Shenzhen, though not all of these individuals possessed a valid Shenzhen household registration card (hukou).

In terms of sexual orientation, 37.9% reported bisexual behaviors. Regarding homosexual (anal intercourse) activities, 34.3% reported being the insertive partner, 15.6% the receptive partner, and 50.1% reported both insertive and receptive anal sex behaviors. In total, 46 participants tested positive for HIV, and 264 tested positive for syphilis. The adjusted prevalence rate of syphilis infection among MSM showed a statistically significant increase from 10.1% in 2005 to 20.0% in 2006 and 19.60% in 2007 (P < 0.01). The adjusted prevalence rate of HIV infection also had an increasing trend between 2005 and 2007 (1.7% in 2005, 2.6% in 2006 and 3.8% in 2007) though this difference was not statistically significant (P = 0.2).

Demographic characteristics (age, education level, marital status, and residence status) were comparable across the 3-year period. There was a statistically significant decrease in the proportion of MSM reporting heterosexual orientation between 2005 and 2006, and between 2006 and 2007 (20.6%, 9.6%, and 2.3%, respectively). In univariate analysis, cases with syphilis infection were significantly more likely to be elder (P = 0.03), have ever married (P = 0.03), patronize sauna (P < 0.001), have homosexual (P < 0.001) or bisexual (P < 0.01) orientation, and test positive for HIV infection (P < 0.01) (Table 1). In multivariate logistic analysis, syphilis infection was significantly associated with patronizing sauna (OR = 3.37; 95% CI, 1.33–8.52, P = 0.05), and testing positive for HIV (OR = 6.38; 95% CI, 2.00–20.37, P = 0.001) (Table 1).



Recently, there have been some improvements in monitoring the prevalence of HIV infection among MSM through China's national HIV sentinel surveillance system.9 However, to our knowledge, there have been very few regularly implemented, cross-sectional studies published that examine the trends in the HIV and syphilis epidemics among MSM in China.

In the current study of an MSM population, we noted an overall crude HIV prevalence of 3.3%, 66-fold greater than the average level (0.05%) in the general population. The HIV and syphilis coinfection prevalence (crude prevalence of 1.7%–4.6% and adjusted prevalence of 1.7%–3.8%) found in our study population is similar to that found in some areas in China (1.47% in Shanghai,2 2.2% in Harbin,10 3.2% and 2.1% in Beijing1,11) but significantly higher than that observed in Guangzhou, a neighboring city of Shenzhen (0%)12 and in Jinan (0.5%).13 However, the prevalence of syphilis (crude prevalence of 9.9%–22.6% and adjusted prevalence of 10.1%–20.0%) in our MSM population is higher than those found in most of these studies.1,3,11,12 These high prevalences support the existence of substantial HIV/STD-related risk behaviors among this population, and justify more detailed research about risk behaviors among MSM population in China.

Among MSM in the current study, a significant association was found between syphilis infection and entertainment venue (4.3% in gay bars and 17.5% in gay saunas). This information will be not only useful for guiding programmers to tailor venue-based intervention activities targeting MSM population but also helpful for reminding epidemiologists to carefully consider and select appropriate venues for surveillance activities among MSM. We found that there was a significant association of syphilis and HIV infections, and that 8.5% (22/260) of the participants with syphilis were also infected with HIV. The data of high proportion (37.9%) of bisexuality further confirms concerns regarding the bridging effects of this population between the MSM population and their heterosexual partners.

By the end of October 2007, a total of 2515 cumulative cases of HIV/AIDS had been reported in Shenzhen. Of these cases, 93.5% were migrants from other areas.13 The HIV problem in Shenzhen is still less serious than areas in southwest of China. However, sexual contact has become the major route of HIV transmission in the study area, opening up the potential for spread of HIV from populations that have previously been considered high risk to the general population.13 Comprehensive intervention strategies to cover not only these traditional high risk populations (e.g., sex workers and their clients, and injecting drug users), but also those men with homosexual or bisexual behaviors, are urgently needed. Detection and treatment of syphilis among MSM are important public health measures and are crucial to both HIV and syphilis control and prevention. Currently, the Shenzhen Institute of Dermatology has developed a special program based on a combination of the outreach services to MSM settings and MSM clinic-based services to provide health education, behavioral change communication, voluntary counseling and testing (VCT) of HIV and syphilis, and consequent referral services.

Some limitations in the current study should be addressed. First, this study included only limited information on risk behaviors, and did not ask about drug use behaviors. However, this is likely of minimal concern as previous research found very low levels of illicit drug use in this population.14 Second, participation bias and reporting bias are potential concerns. In addition, there were some missing data as a result of the reluctances of interviewees to provide personal information. Shenzhen is a “special economic zone” located in south coastal China and adjacent to Hong Kong Special Administrative Region. The socio-demographic characteristics of its MSM population may be different from with other Chinese cities. Any generalization of the results from this study should therefore be made with caution.

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