SEXUALLY TRANSMITTED DISEASES (STDs) were reportedly eliminated in China in 19641,2 but have had a significant resurgence since the early 1980s.3,4 Between 1989 and 1998, the number of newly infected STD cases nationwide was increased by approximately 20% per year.5 In 2002, a total of 744,848 new STD cases (gonorrhea, syphilis, nongonococcal urethritis [NGU], genital herpes, genital warts, chancroid, and lymphogranuloma venereum [LGV]) were reported to the Chinese National Center for AIDS/STD Prevention and Control.6 The majority of STD cases were infected through unprotected sexual contact with their heterosexual partners.3–6
In late 2002, the Chinese government acknowledged that more than one million people in China had become infected with HIV.7 Approximately 220,000 people had already died of AIDS since the first case in China was diagnosed in June 1985, and 840,000 people were living with HIV at the end of 2002, giving a prevalence among the general population somewhere between 0.06% and 0.07%.8 By the end of September 2004, the cumulative number of reported HIV-positive cases was 89,067 with significant increases in reported infections since 2002.8 Needle sharing among drug users was the dominant transmission route of HIV,8–11 and only 17,813 cases or 0.2% of all confirmed HIV/AIDS cases were men who have sex with men (MSM).8 The United Nations Program on AIDS (UNAIDS) projects China could have between 10 and 15 million HIV cases by 2010 unless effective prevention measures are taken.12
Some cross-sectional studies have documented high STD prevalence among MSM in China with syphilis ranging from 9.04% to 20.8%,13,14 low HIV prevalence ranging from 0% to 3.1%,14–18 and common sexual risk behaviors such as multiple sexual partners and unprotected anal intercourse (UAI).19–23
Jiangsu is one of the most densely populated provinces in China with 74.4 million people and located at the eastern part of the Yangtze River Delta, next to Shanghai.24 By the end of 2000, a total of 106 HIV cases had been reported since the first case was detected in 1991.25 In 2004, 78,178 new STD cases were reported in Jiangsu Province with a 34% increase compared with 58,302 in 2003.26 In this article, we report the prevalence of STDs, including HIV infection, and sexual risk behaviors among MSM in Jiangsu Province using a convenience sample of men recruited from gay bars.
Sampling and Recruitment
All gay bars in five cities (Nanjing, Yangzhou, Changzhou, Wuxi, and Suzhou) in Jiangsu Province were identified through key informant interviews during informative research. After obtaining agreements from the owners/managers, a survey of MSM was conducted between February and July 2003 in 10 of 17 gay bars.
Every Friday night during the study period, except for a 10-week gap between March and May resulting from severe acute respiratory syndrome (SARS) outbreak in China, researchers from the Institute of Dermatology, Chinese Academy of Medical Sciences, visited a gay bar and approached men who appeared to be 18 or older and invited them to participate in the study as part of an HIV/AIDS/STD education program. Men who were 18 years of age or older and had ever had sex with a male in the past were eligible for the study.
Men who agreed to participate in the study were asked to complete a short anonymous, self-administered questionnaire after the researchers introduced the study and obtained the written informed consents. Questions covered sociodemographic characteristics, history of STDs, alcohol use, and sexual risk behaviors. Men who reported having had insertive and/or receptive anal intercourse with their male sexual partners in the past 3 months but failed to report consistent condom use were considered engaging UAI. After participants completed the questionnaire, the researchers used the manager’s office to perform a genital examination to check for the presence of urethral discharge, genital ulcers, and genital warts. Genital warts were diagnosed by direct visual examination applying acetic acid to the areas of suspected infection. A urethral swab and a blood sample were also taken for detecting the presence of STD and HIV infection. Study participants and men who were not willing to participate in the study were provided HIV/AIDS/STD counseling and education individually or in a small group.
All participants were assigned a unique study identification number and given a telephone number and time they could call for their test results. Participants identified themselves on the telephone by identification number only. Men who tested positive for bacterial STD (gonorrhea, chlamydial infection, syphilis, or NGU) or genital warts were referred for treatment at the STD Service Center in the Institute of Dermatology, Chinese Academy of Medical Sciences, and those who tested positive for other viral STD (hepatitis B virus [HBV], hepatitis C virus [HCV], herpes simplex virus-2 [HSV-2], or HIV infection) were provided counseling over the phone by a trained counselor.
Urethral swabs were tested by polymerase chain reaction (PCR) for the presence of Neisseria gonorrhea and Chlamydia trachomatis using the Amplicor CT/NG test (Roche Diagnostics, Branchburg, NJ). This assay was also used to monitor PCR inhibition with an internal control (IC) provided in the kit. Ureaplasma urealyticum, Mycoplasma hominis, and Mycoplasma genitalium were detected by an in-house nested PCR with primers deduced from 16S rRNA gene sequence.27 The outer set of primers could detect Mycoplasmas species and U. urealyticum while avoiding crossreaction with other common bacterial species. The sequence of the forward primer was 5′-GAG TTT GAT CCT GGC TCA GC-3′ and the reverse primer 5′-ATT ACC GCG ACT GCT GGC AC-3′. Five microliters of DNA was added to 15 microliters of 1* PCR buffer (1 U Taq DNA polymerase, Promega; 1.5 mmol/L MgCl2; 0.5 mol/L of each primer; 200 mol/L dATP, dGTP, and dCTP). The PCR was performed with the GeneAmp PCR System 9600 (Applied Biosystem, Foster City, CA) under the following conditions: 93°C for 30 seconds (denaturation), 55°C for 30 seconds (annealing), and 72°C for 60 seconds (elongation) for 35 cycles. To improve the efficiency of PCR, a series of inner sets of primers were used for nested PCR. For U. urealyticum, the forward primer was 5′-GCG GCA TGC CTA ATA CAT GCA-3′ and the reverse primer 5′-CTT ATT CAA ATG GTA CAG TCA AAC-3′. For M. hominis, the forward primer was 5′-CAA TGG CTA ATG CCG GAT ACG-3′ and the reverse primer 5′-GGT ACC GTC AGT CTG CAA-3′. For M. genitalium, the forward primer was 5′-GCC ATA TCA GCT AGT TGG T-3′ and the reverse primer 5′-CTC CAG CCT TTG CCT GCT A-3′. The first PCR product was diluted 10 times and 5 L of the dilute product was added to 15 microliters of 1* PCR buffer (1 U Taq DNA polymerase; Promega; 1.5 mmol/L MgCl2; 0.5 mol/L of each primer; 200 mol/L dATP, dGTP, and dCTP). The PCR was performed under the following conditions: 93°C for 30 seconds (denaturation), 55°C for 30 seconds (annealing), and 72°C for 60 seconds (elongation) for 35 cycles. Amplicons were visualized after electrophoresis on 2% agarose gel and observed under Gel Doc EQ System (Bio-Rad, Hercules, CA). The expected length of amplified fragment was 456 bp for U. urealyticum, 335 bp for M. hominis, and 241 bp for M. genitalium. Positive results of M. genitalium were confirmed with the amplicon nucleotide sequencing (TaKaRa Biotechnology, Dalian, China).
Blood samples were tested for the presence of hepatitis B surface antigen (HBsAg) by enzyme immunoassay (EIA; Shanghai Kehua Biotechnology Ltd., Shanghai, China); syphilis was detected by treponema pallidum particle agglutination assay (TPPA; Fujirebio Diagnostics Inc., Tokyo, Japan) and rapid plasma region (RPR; Xinjiang Xinde Co., Xinjiang, China); the presence of HIV antibodies was demonstrated by EIA (Abbott Laboratories, Abbott Park, IL), and positive results were confirmed by Western blot (Abbott Laboratories, Abbott Park, IL); antibodies to HCV were detected by EIA (Shanghai Kehua Biotechnology Ltd., Shanghai, China); and antibodies to HSV-2 were detected by HSV-2 IgG enzyme linked immunoassay (ELISA; Focus Technologies, Cypress, CA). Western blot was performed in the HIV Confirmatory Laboratory at Jiangsu Provincial Center for Disease Control and Prevention, and all the other tests were performed in the STD Reference Laboratory at Chinese National Center for STD & Leprosy Control and Prevention in Nanjing.
Descriptive analyses were conducted to illustrate the sociodemographic characteristics, alcohol use, sexual orientation, sexual risk behaviors, and prevalence of STDs, including HIV infection. Bivariate analyses were performed to assess the risk factors associated with UAI and newly acquired STDs. Unlike viral infections, bacterial STD such as gonorrhea, chlamydial infection, and syphilis were more likely acquired within months. Assessing the risk factors of these newly acquired infections would help us find some potential predictors for future infections, including HIV. In our study, men who tested positive for gonorrhea, chlamydial infection, or active syphilis (TPPA positive and RPR titer ≥1:8) were considered cases of newly acquired STDs. Adjusted odds ratios (AOR) were also computed using multivariate logistic regression models to evaluate risk factors associated with UAI and newly acquired STDs controlling for age, education, and marital status. All statistical analyses were performed using the Statistical Analysis System (SAS) software version 8.02 for Windows.28
The study protocol was reviewed and approved by the Institutional Review Board (IRB) at the Institute of Dermatology, Chinese Academy of Medical Sciences & Peking Union Medical College.
A total of 167 men were approached during the study period, and 144 agreed to participate giving a participation rate of 86.2%. Table 1 shows the sociodemographic characteristics, alcohol use, and sexual risk behaviors of the sample. Approximately half (49.3%) men were between 18 and 29 years, and 49.5% received some college or higher education. Forty-one men (28.5%) were married and living with their wives; and 12.5% were separated or divorced. Approximately one in five (18.2%) men were considered heavy drinkers, who frequently consumed five or more drinks in the past 3 months.
The Kinsey scale was used to define men’s sexual orientation.29 A total of 83 (58.1%) men identified as exclusively homosexual or predominantly homosexual, whereas 31 (21.7%) men identified as predominantly heterosexual with only incidentally homosexual encounters. Only 17.0% of the men had their first sex encounter with another male before age 18.
In the past 3 months, 94.4% of participants were sexually active with men and 45.5% had sex with women. Approximately two in five (41.3%) men had sex with both men and women. Fifty (34.7%) men reported four or more male sexual partners, and nine (6.3%) men reported four or more female sexual partners. More than half (55.2%) of the men reported having insertive or receptive anal intercourse with men, and 83.5% (66 of 79) of them reported UAI.
Among 112 men who provided a urethral swab, one man was diagnosed with gonorrhea, seven with C. trachomatis infection, and two with coinfection of N. gonorrhea and C. trachomatis. One fourth (27.7%) of the men were diagnosed with nonchlamydial nongonococcal urethritis showing the presence of at least one of the following pathogens: U. urealyticum, M. hominis, and M. genitalium (Table 2).
Six men who reported negative test results for HIV, syphilis, and HBV tests during recent blood donations and refused to provide blood sample for the study were considered negative for all these three infections without drawing blood for additional confirmatory testing. A blood sample was taken from the remaining 138 men to test for HIV, syphilis, HBV, HCV, and HSV-2 infections. No one tested positive for HIV or HCV infections. The prevalence of syphilis seropositivity was 18.8% (95% confidence interval [CI]: 12.7–26.1) with a positive TPPA test result, and the prevalence of active syphilis was 6.9% (95% CI: 3.4–12.4) with a positive TPPA test result and RPR titer of 1:8 or higher (Table 2).
Table 3 shows that UAI was not associated with age or educational background. Although not statistical significant at the level of 0.05, men who were divorced or separated from their wives, heavy drinkers, and men who had their first sex with a male before age 18 were more likely to engage in UAI with their male sexual partners. Both bivariate and multivariate analyses showed that men with four or more male sexual partners in the past 3 months were more likely to report UAI (OR = 3.09, 95% CI: 1.51–6.31; AOR = 3.34, 95% CI: 1.60–6.99).
Men with a separated/divorced marital status was the only statistical significant (P <0.01) factor associated with newly acquired STDs. In bivariate analyses (data not shown in tables), men with a separated/divorced marital status were more likely to engage in UAI with male sexual partners (OR = 2.67; 95% CI: 0.91–7.78; P = 0.07) without reporting more male sexual partners (OR = 0.81; 95% CI: 0.28–2.38; P = 0.70) compared with those who never married. Heavy drinkers, men who had their first sex with another male before age 18, having four or more male sexual partners, and engaging in UAI with male sexual partners showed some trend in association with newly acquired STDs, but none was statistically significant.
Since the late 1980s, China’s National STD Sentinel Surveillance Program has been monitoring the prevalence of STDs among four population groups: female sex workers, long-distance truck drivers, blood donors, and antenatal clinic attendees,30 whereas China’s National HIV Sentinel Surveillance Program has been tracking the prevalence of HIV among six population groups since 1995, including females sex workers, drug users, long-distance truck drivers, pregnant women, STD clinic attendees, and blood donors.31 Neither of these two programs include MSMs. Limited information from some cross-sectional studies have shown high STD prevalence, low but significant HIV prevalence, and sexual risk behaviors among MSMs in some parts of China based on samples recruited through various methods: online sampling,13 peer recruitment,17,18,21 and gay bar recruitment.14 To the best of our knowledge, this is the first study in Jiangsu Province to investigate the prevalence of STDs, including HIV infection, and risk behaviors among MSMs.
Our study documented a high prevalence of STD among MSM in Jiangsu Province: gonorrhea 2.7%, chlamydial infection 8.0%, nonchlamydial nongonococcal urethritis 27.7%, active syphilis 6.9%, HBV infection 9.1%, HSV-2 infection 7.8%, and genital warts 13.2%. Different from the studies conducted in other parts of China, we did not find anyone with HIV infection. This could be explained by the lack of statistical power as a result of our limited sample size (n = 144) or a different HIV epidemic scenario among MSM in Jiangsu Province. By the end of 2000, only 106 HIV-infected cases had been reported with the majority of injection drug users and paid plasma donors in Jiangsu Province with 74.4 million people.25 HIV epidemic among MSM in Jiangsu Province might be at its very beginning stage with a very low HIV prevalence. However, this should be regarded with extreme caution before a population-based study is conducted. Six participants refused to provide their blood samples for HIV testing saying they had a negative HIV test result during a recent blood donation. If the actual reason for some of them was that they had already found out they were HIV-infected and did not want the researcher to know their HIV infection status, although anonymity and confidentiality were assured, it would make the HIV prevalence in our sample similar to some other studies.16,18 Although we did not find anyone who was HIV-positive, the 95% CI (0–2.5%) of HIV prevalence in our sample still overlapped the point estimate (1.35%) reported by a recent study carried out in Northeastern China (Dr. Yuhua Wu, personal communication, April 2005).
Consistent with other studies,13–23 our sample reported a high level of sexual risk behaviors among MSM. One third of men reported four or more male sexual partners, and almost half (46.2%) of the men reported engaging in UAI with their male sexual partners in the past 3 months. Although the questions did not appear in the questionnaire, we asked some participants about the reasons for not using condoms. Their answers included, “I don’t think I am at risk of HIV infection since I have never heard of anyone around me to be infected”; “I know my partner very well”; “If I insist on using a condom, my partner may think I have an infection and he may not want to have sex with me”; and “Condoms were not handy when I wanted to have sex.” Given the high prevalence of STD and sexual risk behaviors, it is urgent to develop targeted intervention programs to correct their misconceptions about HIV and condom use, and promote condom use before the spread of HIV infection in this group.
Because of traditional values about family and marriage in China, many MSM eventually get married and have children. Many men conceal their homosexuality from society and their families. It is quite common among MSM in China to be sexually active with both men and women.16,17,19 In our sample, 41.0% of all age groups and 76.7% of men over 30 were once married, and 41.3% reported having sex with both men and women in the past 3 months. This suggests that heterosexual transmission of HIV infection between MSM and their female sexual partners should be emphasized in any HIV intervention. We found that separated/divorced men were more likely to report UAI and test positive in newly acquired STDs. Further research is needed to investigate this group and develop targeted interventions tailored to their needs.
Although statistical power to detect risk factors associated with UAI was limited as a result of our small sample size (n = 144), some trends can be seen that heavy drinkers, men who had their first sex encounter with another male before age 18, and men with four or more male sexual partners were more likely to engage in UAI. The information will be very useful in developing our HIV intervention programs to reduce UAI in this group.
We considered men who were tested positive for gonorrhea, chlamydial infection, or active syphilis (TPPA positive and RPR titer ≥1:8) as cases of newly acquired STDs. Evaluating the risk factors of newly acquired STDs may help us understand who may be at high risk of future infection, including HIV. Heavy drinkers, first sex encounter with a male before age 18, four or more male sexual partners, and UAI are risk factors of newly acquired STDs. HIV/AIDS interventions need to identify men with these factors and provide them with targeted HIV/AIDS education and STD treatment to reduce their chance of being infected with HIV. Newly acquired STDs can also be used as an indicator of sexual risk behaviors to evaluate the effectiveness of HIV/AIDS intervention programs, especially at the early stage of HIV epidemic in this group.
Because all participants were recruited from gay bars, the results of our study may not be generalizable to the larger MSM community. One ethnographic study conducted in Beijing reported that MSM who visited gay bars were mostly middle class, and segments of MSM socialized separately and rarely mixed.32 Our study showed some evidence of their socioeconomic status (SES) and almost half (49.5%) of our sample received some college or higher education, whereas the percentage is only 3.92% for the general population in Jiangsu Province.24 Limitations of this study also include selection bias resulting from convenience sampling strategy and the lack of statistical power resulting from limited sample size. Despite these limitations, our study still provides valuable HIV/STD information about MSM in Jiangsu Province that have never been studied before. Because no significant differences were reported among men visiting different gay bars and a high response rate (86.2%) may suggest good representativeness of our sample, the results may be generalizable to gay bar attendees in Jiangsu Province. The intention of our study was to provide preliminary data on the prevalence of STDs, including HIV infection, and sexual risk behaviors among MSM in Jiangsu Province, and use these preliminary findings to support a larger study using a probability sample, which will help us better understand the population and develop more appropriate interventions.
STDs and high-risk sexual behaviors (multiple males sexual partners and UAI) were prevalent among MSM in Jiangsu Province. Although we did not find anyone infected with HIV, given the facts that HIV prevalence among MSM in other parts of China has been as high as 3%,18 STDs facilitate the transmission of HIV,33–35 and the high prevalence of STDs and sexual risk behaviors exist in this group, the potential for future spread of HIV is of a concern, and it is urgent to provide them STD services (diagnosis and treatment) and HIV/AIDS/STD prevention education and interventions.
1. Hu C, Ye G, Chen X. Control and eradication of syphilis in China. Beijing Sci Conference 1964; 126:167–177.
2. Cohen MS, Henderson GE, Aiello P, et al. Successful eradication of sexually transmitted diseases in the People’s Republic of China: Implications for the 21st century. J Infect Dis 1996; 174(suppl. 2):S223–S229.
3. Shao C, Xu W, Ye G. Sexually transmitted disease control in China (1949–1994). Chin Med Sci J 1996; 11:252–257.
4. Gong X, Wang Q, Zhang G, et al. Epidemiologic trends of sexually transmitted diseases and prevention strategies in China. Chin J STD AIDS Prev Control 2001; 7(suppl):46–51.
5. Chen X, Gong X, Liang G, et al. Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138–142.
6. Qin Q, Gong X, Lu F. Epidemiology of sexually transmitted diseases in China (2002). Chin J STD AIDS Prev Control 2003; 9:217–220.
7. Xinhua News Agency. Number of HIV cases in China reaches 1,000,000. China Youth, October 21, 2002.
8. China State Council AIDS Working Committee Office and UN Theme Group on HIV/AIDS in China. A Joint Assessment of HIV/AIDS Prevention, Treatment and Care in China (2004). Available at: http://www.casy.org/engdocs/JAREng04.pdf
. Accessed April 11, 2005.
9. Liao S. HIV in China: Epidemiology and risk factors. AIDS 1998; 12(suppl B):S19–S25.
10. Zhang K, Ma S. Epidemiology of HIV in China. BMJ 2002; 324:803–804.
11. Wu Z, Rou K, Cui H. The HIV/AIDS epidemic in China: History, current strategies and future challenges. AIDS Educ Prev 2004; 16(suppl A):S7–S17.
13. Yang Z, Fang S, Cai W, et al. Syphilis, HIV infection and sexual risk behaviors among men who have sex with men. Chin Public Health 2003; 19:1292–1294.
14. Gu Y, Qu P, Su L, et al. HIV-related knowledge, attitudes, beliefs and practices among men who have sex with men in Shenyang, China. Chin Public Health 2004; 20:573–574.
15. Qu S, Zhang D, Wu Y, et al. HIV-related knowledge, attitudes, and behavior among men who have sex with men in northeastern China. Chin J STD AIDS Prev Control 2002; 8:338–340.
16. Qu S, Zhang D, Wu Y, et al. Prevalence of HIV infection and sexual risk behaviors among men who have sex with men in northeastern China. Chin J STD AIDS Prev Control 2002; 8:145–147.
17. Liu H, Liu Y, Xiao Y. HIV-related knowledge, attitudes, and behavior among men who have sex with men in Beijing, China. Chin J STD AIDS Prev Control 2001; 7:289–291.
18. Choi KH, Liu H, Guo Y, et al. Emerging HIV-1 epidemic in China in men who have sex with men. Lancet 2003; 361:2125–2126.
19. Choi KH, Gibson DR, Han L, et al. High levels of unprotected sex with men and women among men who have sex with men: A potential bridge of HIV transmission in Beijing, China. AIDS Educ Prev 2004; 16:19–30.
20. Tao X, Cai W, Cai Y, et al. Sexual risk behaviors among 114 men who have sex with men in Shenzhen, China. Mod Prev Med 2004; 31:247–248.
21. Zhang B, Liu D, Li X, et al. A survey of men who have sex with men: Mainland China. Am J Public Health 2000; 90:1949–1950.
22. Lin X, Liu Y, Huang G, et al. Sexually transmitted diseases, HIV infection and sexual risk behaviors among men who have sex with men. Mod Prev Med 2004; 31:618–619.
23. Lau JT, Kim JH, Lau M, et al. Prevalence and risk behaviors of Hong Kong males who seek cross-border same-sex partners in mainland China. Sex Transm Dis 2004; 31:568–574.
24. Jiangsu Statistics Bureau. Jiangsu Statistical Yearbook (2001). China Statistics Press, 2001.
25. Jia C, Yang H, Xu X, et al. Epidemiology of HIV/AIDS in Jiangsu Province. Chin J STD AIDS Prev Control 2002; 8:33–35.
26. Chinese National Center for AIDS/STD Control and Prevention. Epidemiology of sexually transmitted diseases in China (2004). Beijing, China: Chinese Center for Disease Control and Prevention, Chinese National Center for AIDS/STD Control and Prevention, 2005.
27. Jiang J, Ye S, Wang H, et al. Association of Mycoplasma genitalium
and Ureaplasma urealyticum
with nongonococcal urethritis. Chin J Lepr Skin Dis 2005; 21:85–88.
28. SAS System for Windows, release 8.02. Cary, NC: SAS Institute, 2001.
29. Kinsey AC, Pomeroy WB, Martin CE. Sexual Behavior in the Human Male. Philadelphia: WB Saunders, 1948.
30. Yu J, Liang G, Xia Q, et al. STD prevalence among high and low risk populations—Data from National Sexually Transmitted Disease Surveillance Program (1999). Chin J STD AIDS Prev Control 2001; 7:135–136.
31. Ministry of Health, National Center for AIDS/STD Control and Prevention, and the Collaboration Group for National HIV Sentinel Surveillance Program. National sentinel surveillance of HIV infection in China from 1995 to 1998. Chin J Epidemiol 2000; 21:7–9.
32. Choi KH, Diehl E, Guo Y, et al. High HIV risk but inadequate prevention services for men in China who have sex with men: An ethnographic study. AIDS Behav 2002; 6:255–266.
33. Wasserheit J. Epidemiological synergy: interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19:61–77.
34. Laga M, Manoka A, Kivuvu M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: Results from a cohort study. AIDS 1993; 7:93–102.
35. Fleming D, Wasserheit J. From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75:3–17.