From the *National Center for STD Control, Chinese Academy of Medical Science and Peking Union Medical College Institute of Dermatology, Nanjing, China; †Department of Health, Behavior and Society, at the Johns Hopkins School of Public Health, Baltimore, MD; and ‡Division of Infectious Disease, at the Massachusetts General Hospital, MA
Supported by the Mega Project of China National Science Research for the 11th Five-Year Plan, 2008ZX10001–005 (to B.X.W.); NIH/NRSA predoctoral training grant (to K.E.M.), NIH Fogarty Institute the Harvard Initiative for Global Health, and the American Society for Tropical Medicine and Hygiene (to J.D.T.).
Correspondence: Xiang-Sheng Chen, MD, PhD, National Center for STD Control, China CDC, 12 Jiangwangmiao St, Nanjing 210042, China. E-mail: email@example.com.
Received for publication December 15, 2009, and accepted December 19, 2009.
Since the first case of human immunodeficiency virus (HIV) among Chinese men who have sex with men (MSM) was discovered in 1989 in Beijing,1 a growing body of research has documented substantial and expanding epidemics of sexually transmitted diseases (STDs) and HIV within this group. In this issue of the journal, Xu et al report a disturbingly high incidence of HIV and syphilis infections among a 12-month MSM cohort in northern China.2 Their results are consistent with findings observed from other urban Chinese studies of MSM.3,4
Estimates of the total number of MSM in China vary widely, ranging from 2 to 10 million.5,6 While MSM account for 2% to 4% of the Chinese adult male population,7 they comprise an estimated 12.2% of all new HIV cases in 2007.8 Fewer than 15% of all Chinese MSM are covered by current health surveillance and education outreach efforts.4 Although disease monitoring has improved in the last 10 years, routine surveillance of MSM remains incomplete. A large population with high incidence of syphilis and HIV in the setting of limited clinic-based health services may fuel continued disease transmission within and beyond China's MSM population.
As Xu et al demonstrate using a prospective cohort study design (current issue),2 HIV and other sexually transmitted infections, especially syphilis, are spreading quickly among Chinese MSM. Coinfection with HIV and other STDs has also been documented in this population. In a Beijing study of 753 MSM recruited from a voluntary counseling and testing clinic, 94% of those with HIV infection also had one or more STD.9 Syphilis has been shown to increase the risk of HIV acquisition10 and transmission.11 This lethal synergy was also found in the study by Xu et al in which MSM with syphilis infection were 11.4 times more likely to HIV seroconvert during the 12-month study period.2 Although several other Chinese studies have measured syphilis and HIV prevalence among MSM, a recent meta-analysis suggests that coinfection studies are limited.12 This is a missed opportunity to gather critical information to improve efficiency of screening and prevention.
Sexual risk behaviors and dense sexual networks coupled with low condom use are driving these high transmission rates among MSM. A 2006 review of published HIV/STD studies among MSM in China (1990–2004) showed a low self-perceived risk for HIV/AIDS despite high prevalence of risk behaviors such as unprotected vaginal, anal and oral sex with men and women, casual sex, and commercial sex.6 The extent of injection drug use has not been assessed among the Chinese MSM community, however, small studies suggest that some MSM sell sex for drugs13,14 and other MSM increasingly use club drugs.15
Numerous studies from diverse geographic locations report high numbers of sex partners among some MSM and associations between number of partners and HIV/STD status.16–19 For example, in a Beijing study of 753 MSM, those who had 10 or more lifetime sex partners were significantly more likely to be HIV-positive.9 Similar to other Asian and Southeast Asian MSM groups, MSM in China often have both male and female sex partners.9,18 MSM also face considerable pressure from their families and society to marry and have a child.20–23 Because of the one-child policy enacted in 1979, many MSM are only-children and thus responsible for continuing the family line. A review of HIV/STD risk behaviors among MSM found that approximately one-third of all MSM reported being married,6 but this likely underestimates the true extent of married MSM in China since there is underreporting of MSM behaviors among married individuals. Wives are often unaware of their husbands' same-sex behaviors.22,23 Hence, HIV among MSM may spread not only to homosexual partners, but also to their wives and girlfriends. This phenomenon could play an important role in the heterosexual transmission of HIV infection in China.
Furthermore, Western categories for defining sexual identity may not appropriately or sufficiently fit the Chinese context. For example, although a man participates in same-sex behaviors, he may not necessarily self-identify as “gay,” “bisexual,” or “MSM,” complicating community and clinic-based interventions that target these groups. In addition, the commercial sex industry for MSM is comprised of numerous subgroups of men who sell sex to men, (called “money boys” or “MB”), and men who cross-dress or undergo various levels of gender reassignment surgery (unpublished data). As in other Asian and Southeast Asian contexts, these subgroups have their own range of self-identities and varying HIV/STD risk behaviors (UNAIDS, 2009).24
Access to HIV/STD testing among MSM is a significant issue, especially since many MSM do not consider themselves at risk for HIV infection. HIV test uptake among MSM remains low.6 A Sichuan study of 576 MSM found that 93% of men believed that there was no or little possibility that they could get HIV.25 Inquiring about anal sex and other MSM behaviors remains an uncommon practice in many Chinese STD clinics (unpublished data), increasing the need for improved sexual health services for MSM. In addition to the current HIV surveillance system's inefficiency in capturing data on the MSM population, the division of the HIV and STD surveillance systems in China presents an additional barrier, and missed opportunities for comprehensive screening.5
Some of the reported increases in prevalence may be an artifact of improved case-finding or the result of venue-based testing that leads to overrepresentation of disease (e.g., recruitment through STD clinics, bars, bathhouses, saunas). However, incidence studies such as Xu et al still show a high level of transmission in a closed cohort happening over a short period of time.2 In addition, cross-sectional studies with consistent sampling strategies show annual increases in HIV/STD prevalence,26–28 and a growing number of well-designed, respondent-driven sampling studies control for venue-based sampling biases.26–27,29 Furthermore, even if current studies are overrepresenting high-risk subgroups within the MSM population, frequent partner changing and concurrent partners could connect “high” and “low” risk partners within the broader Chinese MSM network. Several small sexual network studies have been done in China already,30,31 but further empirical work is needed to better understand the social and sexual relationships of MSM in China.
In recent years, the MSM population has become a priority population for HIV prevention and control for the Chinese government. Increases in national and international funding and a strong government commitment to focus on MSM are promising,5,24 but the efforts seem insufficient to stop the high incidence of HIV and syphilis as shown in the Xu et al study2 and similar studies3 in other areas in China. MSM peer networks and social ties are powerful, and may be utilized in HIV/STD programs. Internet sites, hotlines, and MSM-interest magazines link individuals across the country and MSM-focused NGOs make up a large portion of all existing NGOs. Programs should consider how to use existing MSM social networks in smart and sensitive ways. The internet is an entry point into the gay community for many Chinese MSM, a regular tool for finding commercial and noncommercial partners, and a resource for information (of varying quality) about sexuality and health. The continued incorporation of internet and cell phone technology is essential for MSM-focused programs. Since China's civil society is still emergent, the same NGO-focused community empowerment model that has been successful in other regions32 may be limited in the Chinese context. Although Chinese MSM nongovernmental organizations have been crucial in helping to organize HIV and syphilis studies,5 disappointingly few NGOs have focused on HIV/STD prevention as their primary goal.
Analysis of syphilis and HIV among MSM in China by Xu et al2 highlights the need for comprehensive MSM programs in China. Especially in light of the social factors related to stigma and sexual identity, creative ways to overcome these challenges are needed. Interventions and high quality sexual health services will be essential for responding to China's growing sexual HIV epidemic. STD services should be integrated with the planning and implementation of ongoing HIV programs for MSM in China in terms of testing, counseling, and interventions. STD clinics for MSM may be an entry point to encourage their clients to accept HIV counseling and testing, and interventions.
1. Zhang BC, Chu QS. MSM and HIV/AIDS in China. Cell Res 2005; 15:858–864.
2. Xu JJ, Zhang M, Brown K, et al. Syphilis and HIV seroconversion among a 12-month prospective cohort of men who have sex with men (MSM) in Shenyang, China. Sex Transm Dis. In press.
3. Ruan YH, Jia YJ, Zhang XX, et al. Incidence of HIV-1, syphilis, hepatitis B, and hepatitis C virus infections and predictors associated with retention in a 12-month follow-up study among men who have sex with men in Beijing, China. J Acquir Immun Defic Syndr 2009; 52:604–610.
5. Wong FY, Huang ZJ, Wang WB, et al. STIs and HIV among men having sex with men in China: A ticking time bomb? AIDS Educ Prev 2009; 21:430–446.
6. Liu H, Yang HM, Li XM, et al. Men who have sex with men and human immunodeficiency virus/sexually transmitted disease control in China. Sex Transm Dis 2006; 33:68–76.
7. Wei CY, Guadamuz TE, Stall R, et al. STD prevalence, risky sexual behaviors, and sex with women in a national sample of Chinese men who have sex with men. Am J Public Health 2009; 99:1978–1981.
8. State Council AIDS Working Committee Office, China Ministry of Health, UN Theme Group on HIV/AIDS in China. A joint assessment of HIV/AIDS prevention, treatment and care in China (2007). Beijing, China: State Council AIDS Working Committee Office, 2007. Available at: http://www.chinaids.org
. Accessed December 12, 2009.
9. Zhang XX, Wang C, Wang HW, et al. Risk factors of HIV infection and prevalence of co-infections among men who have sex with men in Beijing, China. AIDS 2007; 21(suppl 8):S53–S58.
10. Reynolds SJ, Risbud AR, Shepherd ME, et al. High rates of syphilis among STI patients are contributing to the spread of HIV-1 in India. Sex Transm Infect 2006; 82:121–126.
11. Buchacz K, Patel P, Taylor M, et al. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS 2004; 18:2075–2079.
12. Gao L, Zhang L, Jin Q. Meta-analysis: Prevalence of HIV infection and syphilis among MSM in China. Sex Transm Infect 2009; 85:354–358.
13. Lau JT, Feng T, Lin X, et al. Needle sharing and sex-related risk behaviors among drug users in Shenzhen, a city in Guangdong, southern China. AIDS Care 2005; 17:166–181.
14. Gu J, Wang R, Chen H, et al. Prevalence of needle sharing, commercial sex behaviors and associated factors in Chinese male and female injecting drug user populations. AIDS Care 2009; 21:31–41.
15. He N, Wong FY, Huang ZJ, et al. HIV risks among two types of male migrants in Shanghai, China: Money boys vs. general male migrants. AIDS 2007; 21:S73–S80.
16. Gao MY, Wang S. Participatory communication and HIV/AIDS prevention in a Chinese marginalized (MSM) population. AIDS Care 2007; 19:799–810.
17. Liu H, Liu Y, Xiao Y. A survey on knowledge, attitude, belief and practice related to HIV/AIDS among MSM. J China AIDS/STD Prevent Control 2001; 7:289–291.
18. 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.
19. Qu S, Zhang D, Wu Y, et al. Seroprevalence of HIV and risk behaviors among men who have sex with man in a northeast city of China. J China AIDS/STD Prevent Control 2002; 8:145–147.
20. Wong WC, Zhang J, Wu SC, et al. The HIV related risks among men having sex with men in rural Yunnan, China: A qualitative study. Sex Transm Inf 2006; 82:127–130.
21. Wong WC, Kong TS. To determine factors in an initiation of a same-sex relationship in rural China: Using ethnographic decision model. AIDS Care 2007; 19:850–857.
22. Liu JX, Choi K. Experiences of social discrimination among men who have sex with men in Shanghai, China. AIDS Behav 2006; 10:S25–S33.
23. Zhou YR. Homosexuality, seropositivity, and family obligations: Perspectives of HIV-infected men who have sex with men in China. Cult Health Sex 2006; 8:487–500.
24. UNAIDS and the World Health Organization. AIDS Epidemic Update, 2009. Geneva, Switzerland: UNAIDS and the World Health Organization, 2009. Document ID: UNAIDS/09.36E/ JC1700E.
25. China-UK AIDS Care Project. Behavioral surveillance in MSM, Sichuan province. Presented at: Annual meeting of National STD/AIDS Detection and Surveillance; February 23–26, 2004; Nanchang, China.
26. Ruan SM, Yang H, Zhu YW, et al. Rising HIV prevalence among married and unmarried among men who have sex with men: Jinan, China. AIDS Behav 2009; 13:671–676.
27. Ma XY, Zhang QY, He X, et al. Trends in prevalence of HIV, syphilis, hepatitis C, hepatitis B, and sexual risk behavior among men who have sex with men: Results of 3 consecutive respondent-driven sampling surveys in Beijing, 2004 through 2006. J Acquir Immun Defic Syndr 2007; 45:581–587.
28. Zhang DP, Bi P, Lv F, et al. Changes in HIV prevalence and sexual behavior among men who have sex with men in a northern Chinese city: 2002 to 2006. J Infect 2007; 55:456–463.
29. Liu HJ, Liu H, Cai YM, et al. Money boys, HIV risks, and the associations between norms and safer sex: A respondent-driven sampling study in Shenzhen, China. AIDS Behav 2009; 13:652–662.
30. Choi KH, Ning Z, Gregorich SE, et al. The influence of social and sexual networks in the spread of HIV and syphilis among men who have sex with men in Shanghai, China. J Acquir Immun Defic Syndr 2007; 45:77–84.
31. Liu H, Feng T, Liu H, et al. Egocentric networks of Chinese men who have sex with men: Network components, condom use norms, and safer sex. AIDS Patient Care STDS 2009; 23:885–893.
32. Cassel JB, Ouellette S. A typology of AIDS volunteers. AIDS Educ Prev 1995; 7(suppl 5):80–90.