What is the potential for bisexual men in China to act as a bridge of HIV transmission to the female population? Behavioural evidence from a systematic review and meta-analysis

BMC Infectious Diseases

Lei Zhang¹  David P Wilson²  Eric PF Chow² 

[1] CFI Building, Corner of West and Boundary Streets, Darlinghurst, Sydney NSW 2010, Australia;The Kirby Institute for infection and immunity in society, University of New South Wales, Sydney, Australia

关键词: condom use;    bisexual behaviour;    meta-analysis;    Men who have sex with men (MSM);   

Others  :  1175607
DOI  :  10.1186/1471-2334-11-242

 received in 2011-04-19, accepted in 2011-09-15,  发布年份 2011

【 摘 要 】

Background

HIV prevalence among men who have sex with men (MSM) in China has rapidly increased in recent years. It is suggested that MSM could be a potential bridge of HIV transmission to the general female population. We investigated the bisexual behaviour of MSM in China through systematic review and meta-analysis.

Methods

We conducted a systematic review and meta-analyses on published peer-reviewed Chinese and English literature during 2001-2010 according to the PRISMA guidelines. Marital status and sexual behavioural indicators of MSM were presented graphically using forest plots. The pooled effect rates with 95% confidence intervals were also calculated. Meta-regression analyses were performed to examine the factors associated with high heterogeneities across the studies.

Results

Forty-three eligible articles (11 in English and 32 in Chinese) were identified. Our results showed that 17.0% (95% CI: 15.1-19.1%) of MSM in China are currently married to a woman and 26.3% (95% CI: 23.6-29.1%) of MSM had female sexual partners in the last six months. The pooled estimates for condom use rate between MSM and female sex partners was 41.4% (95% CI: 35.5-47.5%) at the last sex act; and 25.6% (95% CI: 23.0-28.4%) in the last six months. The consistent condom use rates with regular, non-commercial, casual and commercial female sex partners in the last six months were 23.3% (95% CI: 11.25-42.1%), 39.0% (95% CI: 28.8-50.3%) and 55.8% (95% CI: 41.4-69.4%), respectively.

Conclusions

A substantial proportion of Chinese MSM is currently married or had sexual relations with a female in the past six months. In addition, low condom usage was common between married MSM and their wives, hence posing a higher risk of transmitting HIV. Harm-reduction programs targeting married MSM and their female partners are necessary to curb the further spread of HIV infection to the general female population.

【 授权许可】

   
2011 Chow et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Ministry of Health of the People's Republic of China: China 2010 UNGASS Country Progress Report. Beijing, China: Ministry of Health; 2010.
• [2]Ministry of Health People's Republic of China, Joint United Nations Programme on HIV/AIDS, World Health Organization: 2009 Estimates for the HIV/AIDS Epidemic in China. Beijing, China; 2010.
• [3]Chow EPF, Wilson DP, Zhang J, Jing J, Zhang L: Human Immunodeficiency Virus Prevalence Is Increasing Among Men Who Have Sex With Men in China: Findings From a Review and Meta-Analysis. Sexually Transmitted Diseases 2011, in press.
• [4]Chow EP, Wilson DP, Zhang L: Patterns of condom use among men who have sex with men in China: a systematic review and meta-analysis. AIDS and Behavior 2011, in press.
• [5]Zhang B, Li X, Chu Q, Wang n, Wang Z, Zhou S, Tong C, Zhang J, Guan W, Cui Z, et al.: [A survey of HIV/AIDS related behaviors among 2250 MSM in nine major cities of China]. Chinese Journal of AIDS & STD 2008, 14(6):541-547.
• [6]Hu Q, Lu FB, Gong JP, Li YC, Li GB, Liu JH, Chen H, Liao QH: [Knowledge, attitudes, and practice about STD/AIDS among the men who have sex with men in Nanchang City, Jiangxi Province]. Chinese Journal of Health Education 2006, 22(9):647-649.
• [7]Qu SQ, Zhang DP, Wu YH, Zhu H, Cui Y, Zhao DH, Zhang J: [A Survey of Knowledge, Attitude and Practice Related to HIV/AIDS among Men Who Have Sex with Men in a Northeast City of China]. Chin J STD/AIDS Prev Cont 2002, 8(6):338-340. 370
• [8]Yang HT, Ding JP, Chen GH, Li XF, Zhang BC, Guan WH: [Behavioral features of Men Who Have Sex with Men in Jiangsu]. Jiangsu Prev Med 2006, 17(1):1-4.
• [9]Choi KH, Gibson DR, Han L, Guo Y: 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(1):19-30.
• [10]Liu H, Liu Y, Xiao Y, Zhang Q, Shao Y, Zhen L, Li JH, Choi KH: [A survey of the knowledge, attitude, and behaviors on STD/AIDS in men who have sex with men in Beijing]. Chinese Journal of AIDS & STD 2005, 11(4):268-270.
• [11]Zhang B, Li X, Hu T, Liu D, Shi T: [HIV/AIDS interventions targeting men who have sex with men (MSM): theory and practice]. Chin J STD/AIDS Prev Cont 2000, 6(3):155-157.
• [12]Wang CH, Yang YH, Lu GJ, Yang XX, Ge LR, Zhao HR, Zhang YQ: [Intervent male male sexual contact AIDS high dangerous behavior and evaluate effection of intervention]. Chinese Journal of Health Laboratory Technology 2007, 17(12):2291-2292.
• [13]Feng L, Ding X, Lu R, Liu J, Sy A, Ouyang L, Pan C, Yi H, Liu H, Xu J, et al.: High HIV prevalence detected in 2006 and 2007 among men who have sex with men in China's largest municipality: an alarming epidemic in Chongqing, China. J Acquir Immune Defic Syndr 2009, 52(1):79-85.
• [14]He Q, Wang Y, Lin P, Liu Y, Yang F, Fu X, Li Y, Sun B, Li J, Zhao X, et al.: Potential bridges for HIV infection to men who have sex with men in Guangzhou, China. AIDS Behav 2006, 10(4 Suppl):S17-23.
• [15]Guo H, Wu ZY: [Review of study on marital status and sex behavior features of men who have sex with men]. Disease Surveillance 2010, 25(8):651-654.
• [16]Ruan S, Yang H, Zhu Y, Wang M, Ma Y, Zhao J, McFarland W, Raymond HF: Rising HIV prevalence among married and unmarried among men who have sex with men: Jinan, China. AIDS Behav 2009, 13(4):671-676.
• [17]Guo Y, Li X, Stanton B: HIV-Related Behavioral Studies of Men Who Have Sex with Men in China: A Systematic Review and Recommendations for Future Research. AIDS Behav 2010.
• [18]Moher D, Liberati A, Tetzlaff J, Altman DG, Grp P: Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. Plos Medicine 2009., 6(7)
• [19]Boyle MH: Guidelines for evaluating prevalence studies. Evidence-Based Mental Health 1998, 1(2):37-39.
• [20]Higgins JPT, Thompson SG, Deeks JJ, Altman DG: Measuring inconsistency in meta-analyses. Brit Med J 2003, 327(7414):557-560.
• [21]Begg CB, Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics 1994, 50(4):1088-1101.
• [22]Thompson SG, Sharp SJ: Explaining heterogeneity in meta-analysis: A comparison of methods. Statistics in Medicine 1999, 18(20):2693-2708.
• [23]Fu LJ, Fang YR, Guo TY: [Investigation of the sexual behaviors among the MSM in Shaoxing City of Zhejiang Province]. Disease Surveillance 2007, 22(12):818-819.
• [24]Zhang M, Wang XD, Yang Y: [Prevalence oh HIV, anti-HCV, syphilis infection and AIDS knowledge among men who have sex with men (MSM) in Urumqi]. Chin J Public Health 2009, 25(9):1075-1076.
• [25]Chen SC, Luo Y, Cheng J, Ding JM, Dai YZ, Xu K, Chen KK, Chen WY, Shi SF: [Analysis on results of MSM behavioral surveillance on HIV/AIDS]. Disease Surveillance 2007, 22(3):175-177.
• [26]Cai GF, Ma QQ, Pan XH, Fu LJ, Xu WX, Shan XR, Yang Q: [HIV/AIDS Related Knowledge, Attitude, Practice and HIV/STD Infection among MSM in Two Cities of Zhejiang Province]. China Preventive Medicine 2008, 9(6):482-485.
• [27]Liao MZ, Liu XZ, Fu JH, Qian YS, Zhang XF: [Analysis of data of behavioral surveillance in men who have sex with men(MSM) in Shandong Province]. Chinese Journal of AIDS & STD 2006, 12(6):530-532.
• [28]Liu H, Wang N, Zhang Q, Shao Y, Wu T, Liu Y, Jiang HB, Song Y, Zhang L, Yin WY, et al.: [Study of HIV and syphilis infection situation and sexual behavioral characteristics among 416 MSM]. Chinese Journal of AIDS & STD 2007, 13(3):230-232. 234
• [29]Wang Y, Zhang HB, Gui ZG, Yang HW, Fan J, Zheng YJ, Liu L: [Analysis of behavior of MSM population and the biological monitoring result in Mianyang city]. Modern Preventive Medicine 2008, 35(19):3780-3783. 3789
• [30]Ruan Y, Li D, Li X, Qian HZ, Shi W, Zhang X, Yang Z, Wang C, Liu Y, Yu M, et al.: Relationship between syphilis and HIV infections among men who have sex with men in Beijing, China. Sex Transm Dis 2007, 34(8):592-597.
• [31]Catania JA, Osmond D, Stall RD, Pollack L, Paul JP, Blower S, Binson D, Canchola JA, Mills TC, Fisher L, et al.: The continuing HIV epidemic among men who have sex with men. American Journal of Public Health 2001, 91(6):907-914.
• [32]Jeffries WL: Sociodemographic, Sexual, and HIV and Other Sexually Transmitted Disease Risk Profiles of Nonhomosexual-Identified Men Who Have Sex With Men. American Journal of Public Health 2009, 99(6):1042-1045.
• [33]Weinhardt LS, Kelly JA, Brondino MJ, Rotheram-Borus MJ, Kirshenbaum SB, Chesney MA, Remien RH, Morin SF, Lightfoot M, Ehrhardt AA, et al.: HIV transmission risk behavior among men and women living with HIV in 4 cities in the United States. Jaids-J Acq Imm Def 2004, 36(5):1057-1066.
• [34]Prestage G, Hudson J, Bradley J, Down I, Sutherland R, Corrigan N, Gray B, Chalmers B, Batrouney C, Martin P, et al.: Three or More Study (TOMS). Sydney: National Centre in HIV Epidemiology and Clinical Research, The University of New South Wales; 2008.
• [35]Solomon SS, Srikrishnan AK, Sifakis F, Mehta SH, Vasudevan CK, Balakrishnan P, Mayer KH, Solomon S, Celentano DD: The Emerging HIV Epidemic among Men Who have Sex with Men in Tamil Nadu, India: Geographic Diffusion and Bisexual Concurrency. AIDS and Behavior 2010, 14(5):1001-1010.
• [36]Dandona L, Dandona R, Gutierrez JP, Kumar GA, McPherson S, Bertozzi SM, Team AFS: Sex behaviour of men who have sex with men and risk of HIV in Andhra Pradesh, India. AIDS 2005, 19(6):611-619.
• [37]Zhang B, Li X, Chu Q, Wang N, Wang Z, Zhou S, Tong C, Zhang J, Guan wh, Cui Z, et al.: [Correlation between AIDS and homosexuals: A study of 2046 male homosexuals in nine major cities of China]. The Chinese Journal of Human Sexuality 2008, 17(8):6-10.
• [38]Cai YM, Liu H, Pan P, Hong FC, Zhou H: [Survey of KABP on STD/AIDS among male sexual workers in Shenzhen City]. China Tropical Medicine 2007, 7(11):2131-2133.
• [39]Choi KH, Ning Z, Gregorich SE, Pan QC: 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 Immune Defic Syndr 2007, 45(1):77-84.
• [40]Li N, Wang Z, Sun GQ, Sun DY: [Analysis of HIV/AIDS sentinel surveillance among high risk population in Henan province in 2006]. Chinese Journal of AIDS & STD 2007, 13(5):427-429.
• [41]Xing JM, Zhang KL, Chen X, Zheng J: [Investigation on HIV/AIDS knowledge and sexual behaviors among men who have sex with men in Hunan province]. Chin J Prev Med 2007, 41(6):511-513.
• [42]Wives of Homosexual Men in China-A Disadvantaged Group [http:/ / www.chinadecoded.com/ 2010/ 12/ 02/ wives-of-homosexual-men-in-china-a- disadvantaged-group/ ] webcite
• [43]Varghese B, Maher JE, Peterman TA, Branson BM, Steketee RW: Reducing the risk of sexual HIV transmission-Quantifying the per-act risk for HIV on the basis of choice of partner, sex act, and condom use. Sexually Transmitted Diseases 2002, 29(1):38-43.
• [44]Jing J, Worth H: HIV in China: Understanding the Social Aspects of the Epidemic. Sydney: University of New South Wales Press; 2010.
• [45]Liu H, Cai Y, Rhodes AG, Hong F: Money boys, HIV risks, and the associations between norms and safer sex: a respondent-driven sampling study in Shenzhen, China. AIDS Behav 2009, 13(4):652-662.
• [46]Xi SJ, He YF, Zhou XH: [Analysis of influencing factors of risk behaviors associated with AIDS among money boys in Hangzhou, Zhejiang]. Disease Surveillance 2009, 24(11):839-842.
• [47]He N, Wong FY, Huang ZJ, Ding YY, Fu CW, Smith BD, Young D, Jiang QW: HIV risks among two types of male migrants in Shanghai, China: money boys vs. general male migrants. Aids 2007, 21:S73-S79.
• [48]Cao NX, Jiang J, Ge FQ: [Study on sexual safety among MSM sex workers]. Chinese Journal of AIDS/STD 2009, 15(6):583-585.
• [49]Hu LX, Chen YY, Li J, Du J, Zhao BL, Wang LT: [Effect evaluation of health education on prevention of HIV/AIDS among the migrant population]. Chinese Journal of Health Education 2007, 23(6):431-433.
• [50]Choi KH, Liu H, Guo Y, Han L, Mandel JS, Rutherford GW: Emerging HIV-1 epidemic in China in men who have sex with men. Lancet 2003, 361(9375):2125-2126.
• [51]Choi KH, Lui H, Guo Y, Han L, Mandel JS: Lack of HIV testing and awareness of HIV infection among men who have sex with men, Beijing, China. AIDS Educ Prev 2006, 18(1):33-43.
• [52]Wu J, Chen L, Fan HL, Ruan Y: [A survey on the prevalence of HIV-1 and syphilis infection and characteristics of sexual behaviors in MSM (men who have sex with men) living in Shanghai]. J Diagn Concepts Pract 2008, 7(3):296-299.
• [53]Zhu YW, Ruan SM, Yang H, Wang MH, Zhang CQ, Jia Z, Shi ZL, Zhang MY: [Investigation on AIDS Related Knowledge Risk Behavior and HIV Infection in MSM in Ji'nan City]. Preventive Medicine Tribune 2007, 13(6):490-492.
• [54]Gu Y, Qu P, Xu L, Luo M, Wang X, Gu J, Zhao L, Lu Y-h, Zhou B: [Survey of knowledge, attitude, behavior and practice related to STI/HIV among male homosexuality in Shenyang]. Chin J Public Health 2004, 20(5):573-574.
• [55]Liu LY: [Investigation on HIV/AIDS sexual behavior among men who have sex with men in 2006 in city of Mudanjiang]. Med Ani Prev 2008, 24(7):534-535.
• [56]Wang J, Luo C, Wen YC: [HIV infection and related risk behaviors among MSM in Harbin]. Chinese Journal of AIDS & STD 2008, 14(1):75.
• [57]Wang L, Jie Z, Liu F, Zhan Y, Wu YH: [A survey on general conditions and high risk behaviors among men who have sex with men in a city of Heilongjiang province]. Chinese Journal of AIDS & STD 2006, 12(4):339-340.
• [58]Zhang D, Bi P, Lv F, Zhang J, Hiller JE: Changes in HIV prevalence and sexual behavior among men who have sex with men in a northern Chinese city: 2002-2006. Journal of Infectection 2007, 55(5):456-463.
• [59]Zhao H, Wang G, Liu H: [The Investigation Report of Male-to-male Contact During the Voluntary Consulation in Daolin District of Harebin]. Guide of China Medicine 2009, 7(10):181-183.
• [60]Guo W, Song AJ, Meng HD, Pang L, Rou KM, Wu ZY: [Survey on AIDS/STD risk behaviors and prevalence among men who have sex with men in Langfang, Hebei]. Chinese Journal of Epidemiology 2008, 29(6):545-547.
• [61]Liu H, Liu Y, Xiao Y: [A Survey on Knowledge, Attitude, Belief and Practice related to HIV/AIDS among MSM]. Chin J STD/AIDS Prev Cont 2001, 7(5):289-291.
• [62]Ma J, Guo J: [Internet survey of high risk sexual behaviors and sexually transmitted diseases among male homosexuals in Tianjin]. Modern Preventive Medicine 2007, 34(20):3928-3931.
• [63]Qu L, Yang JY, Zhang XG, Yang YR, Bao ZQ: [Study on HIV and syphilis infections among men who have sex with men in selected cities of Inner Mongolia]. Chin J Epidemiol 2009, 30(10):1089-1090.
• [64]Zhong F, Lin P, Xu H, Wang Y, Wang M, He Q, Fan L, Li Y, Wen F, Liang Y, et al.: Possible Increase in HIV and Syphilis Prevalence Among Men Who Have Sex with Men in Guangzhou, China: Results from a Respondent-Driven Sampling Survey. AIDS Behav 2009.
• [65]Cai YM, Liu H, Pan P, Hong FC, Feng TJ: [Survey of HIV/AIDS related knowledge and high risk behavior among men who have sex with men in Shenzhen using respondent-driven sampling]. South China J Prev Med 2009, 35(1):4-7.
• [66]He Q, Wang Y, Lin P, Zhang Z-b, Zhao X-x, Xu H-f: [KAP study on AIDS among men who have sex with men in Guangzhou, Guangdong province]. Chinese Journal of Disease Control & Prevention 2005, 9(2):106-108.
• [67]Xu YF, Zhou J, Chen SH, Zhou FH, Mo JC, Zhu JJ: [Investigation of HIV Knowledge and High-risk Behavior Among Men Who Have Sex With Men in Nanning]. Journal of Preventive Medicine Information 2008, 24(10):753-755.
• [68]Miao ZF, Li J, Lei LM, Han X, Zhang XP: [Survey of AIDS-related Knowledge and Behavior in 312 MSM]. Journal of Ningxia Medical University 2009, 31(6):761-762.
• [69]Feng Y, Wu Z, Detels R, Qin G, Liu L, Wang X, Wang J, Zhang L: HIV/STD prevalence among men who have sex with men in Chengdu, China and associated risk factors for HIV infection. J Acquir Immune Defic Syndr 2010, 53(Suppl 1):S74-80.
• [70]Lau JT, Wang M, Tse YK, Gu J, Tsui HY, Zhang Y, Wang N, Cheng F: HIV-related behaviors among men who have sex with men in China: 2005-2006. AIDS Educ Prev 2009, 21(4):325-339.
• [71]Xiao Y, Ding X, Li C, Liu J, Sun J, Jia Y: Prevalence and correlates of HIV and syphilis infections among men who have sex with men in Chongqing Municipality, China. Sex Transm Dis 2009, 36(10):647-656.
• [72]Zhou J, Zhu JJ, Bin H, Zhang L, Yao M, Zhang W, Zhang W, Zhong JY, You QY, Gao L: [A survey of HIV/STD, HBV and HCV infections and risk behaviors among MSM in two central districts of Guiyang city]. Chinese Journal of AIDS & STD 2008, 14(1):47-48, 51.
• [73]Xiao Y, Sun J, Li C, Lu F, Allen KL, Vermund SH, Jia Y: Prevalence and correlates of HIV and syphilis infections among men who have sex with men in seven provinces in China with historically low HIV prevalence. J Acquir Immune Defic Syndr 2010, 53(Suppl 1):S66-73.
• [74]Zhang BC, Zeng Y, Xu H, Li XF, Zhou SJ, Li H, Liao LM, Zhang XM: [Study on 1389 men who have sex with men regarding their HIV high-risk behaviors and associated factors in mainland China in 2004]. Zhonghua Liu Xing Bing Xue Za Zhi 2007, 28(1):32-36.