HIV and syphilis and sexual risk behaviours among men who have sex with men attending university in China: a systematic review and meta-analysis
Song Fan A B , Zuyao Yang C , Fengsu Hou A , Maohe Yu D , Zhenzhou Luo E , Meizhen Liao F , Yanhua Gong G , Xiaojun Meng H , Yong Cai I M * and Huachun Zou J K L M *
+ Author Affiliations
- Author Affiliations
A School of Public Health, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.
B School of Public Health, Southwest Medical University, Luzhou, Sichuan 646000, China.
C Division of Epidemiology, JC School of Public Health and Primary Care, Chinese University of Hong Kong, Hong Kong SAR 999077, China.
D Department of AIDS/STD Control and Prevention, Tianjin Center for Disease Control and Prevention, Tianjin 300011, China.
E Nanshan District Center for Chronic Disease Control, Shenzhen 518000, China.
F Shandong Center for Disease Control and Prevention, Jinan, Shandong 250014, China.
G Foshan Center for Disease Control and Prevention, Foshan, Guangdong 528051, China.
H Wuxi Center for Disease Control and Prevention, Wuxi, Jiangsu 214023, China.
I School of Public Health, Shanghai Jiao Tong University, Shanghai 200020, China.
J School of Public Health (Shenzhen), Sun Yat-sen University, Shenzhen, Guangdong 510006, China.
K Kirby Institute, UNSW Australia, Sydney, NSW 2052, Australia.
L Shenzhen Municipal Center for Disease Control and Prevention, Shenzhen 518055, China.
M Corresponding authors. Email: zouhuachun@mail.sysu.edu.cn; caiyong202028@163.com
Sexual Health 16(6) 554-565 https://doi.org/10.1071/SH18231
Submitted: 11 July 2018 Accepted: 16 April 2019 Published: 1 October 2019
Abstract
Background: This study was conducted to summarise the HIV epidemic, sexual behaviours and HIV testing among men who have sex with men (MSM) attending university in China. Methods: Five databases were searched for student MSM information in English and Chinese language publications. Meta-analyses were performed to calculate the pooled prevalence of HIV and syphilis, pooled mean age at first anal intercourse (AFAI) and the rate of other HIV-related behaviours among MSM attending university in China. Univariate meta-regression and subgroup analysis were conducted to explore potential sources of heterogeneity. Publication bias was measured using Egger’s test. Results: Thirty-three articles representing 31 studies were included in the analysis. The pooled HIV prevalence was 4.1% (95% CI 3.1–5.0%). The estimated AFAI was 18.7 years, but 37.5% of students had their first anal intercourse before 18 years of age. Most (88.2%) had their first sexual intercourse with a male partner. Of the MSM attending university, 4.2% of MSM engaged in commercial sex (either selling or buying sex), 10.3% had ever engaged in group sex, 13.1% had had sex with a female partner in the past month and 10.1% had ever used drugs. Most (77.7%) sought sex partners via geosocial networking gay apps or the Internet, and 42.9% had ever tested for HIV. There was a tendency for an increase in lifetime HIV testing rate from 32% in 2005–07 to 53% in 2014–16. Conclusions: This review found high HIV prevalence, early AFAI and a high prevalence of sexual risk behaviours among MSM attending university in China. Interventions aimed at increasing HIV testing and reducing sexual risk behaviours are urgently needed among this young population.
Additional keywords: HIV testing, student, youth.
References
[1] Wang L, Ding ZW, Yan RX, Li DM, Guo W, Ding GW, et al HIV/AIDS epidemic situation and data analysis among young students from 2006–2009 in China. Zhonghua Liu Xing Bing Xue Za Zhi 2010; 31 1017–21. [In Chinese]| 21162868PubMed |
[2] Wang LY, Qing QQ, Ding ZW, Cai C, Guo W, Li DM, et al Current situation of AIDS epidemic in China. Chin J AIDS STD 2017; 23 330–3. [In Chinese]
[3] Sohu News. Voice from the National People’s Congress and the Chinese People’s Political Consultative Conference 2017. 2017. Available online at: http://www.sohu.com/a/128715460_464387 [verified 29 November 2017].
[4] Ministry of Education. Ministry of education issues latest university list. 2017. Available online at: http://www.moe.edu.cn/jyb_xwfb/s5147/201706/t20170616_307075.html [verified 4 October 2017].
[5] Zhang PC, Chi XL, Wu MX, Wang SS, Wang J. Status and influencing factors of attitude toward LGBT among college students. Chin J Publ Health 2012; 28 921–3. [In Chinese]
[6] Ministry of Health. UNAIDS, WHO, HIV/AIDS epidemic estimation in China, 2011. Chin J AIDS STD 2012; 18 1–5. [In Chinese]
[7] Zhang XL, Chen JF, Li XT, Wu H, Ding JM, Jin J, et al Analysis of HIV/AIDS among college students in Hangzhou City. Yu FangYi Xue 2017; 29 161–4. [In Chinese]
[8] Cen P, Nong QX, Xu H, Xu XF, Deng XF. Epidemic characteristics of AIDS among students aged 6–25 years old in Nanning City from 2001–2015. Zhi Ye Yu Jian Kang 2017; 33 806–9. [In Chinese]
[9] Wang YM. The situation of sexual features and HIV influence factors among college students men who have sex with men. Master’s thesis, Kunming Medical University, Kunming, Yunnan, China; 2016. [In Chinese]
[10] Yang Z, Huang Z, Dong Z, Zhang S, Han J, Jin M. Prevalence of high-risky behaviors in transmission of HIV among high school and college student MSM in China: a meta-analysis. BMC Public Health 2015; 15 1272
| Prevalence of high-risky behaviors in transmission of HIV among high school and college student MSM in China: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 26690367PubMed |
[11] Li Y, Xu J, Reilly KH, Zhang J, Wei H, Jiang Y, et al Prevalence of HIV and syphilis infection among high school and college student MSM in China: a systematic review and meta-analysis. PLoS One 2013; 8 e69137
| Prevalence of HIV and syphilis infection among high school and college student MSM in China: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 24391964PubMed |
[12] Chang JF, Lu WQ. Knowledge attitudes and practices regarding HIV/AIDS among MSM college students in Guiyang City. Chinese Journal of School Health 2014; 35 500–2. [In Chinese]
[13] National Health and Family Planning Commission, Ministry of Education. Notice on establishing an epidemic notification system to strengthen AIDS prevention and control in schools. 2015. Available online at: http://www.moe.edu.cn/jyb_xxgk/moe_1777/moe_1779/201510/t20151019_214246.html [verified 6 November 2017].
[14] Ministry of Education. Guidelines of college health education. 2017. Available online at: http://www.moe.edu.cn/srcsite/A17/moe_943/moe_946/201707/t20170710_308998.html [verified 6 November 2017].
[15] Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6 e1000097
| Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.Crossref | GoogleScholarGoogle Scholar | 19753108PubMed |
[16] Rostom A, Dubé C, Cranney A, Saloojee N, Sy R, Garritty C, et al. Appendix D. Quality Assessment Forms. Rockville, MD: Agency for Healthcare Research and Quality; 2004. Available online at: https://www.ncbi.nlm.nih.gov/books/NBK35156/ [verified 7 June 2019].
[17] Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005; 5 13
| Estimating the mean and variance from the median, range, and the size of a sample.Crossref | GoogleScholarGoogle Scholar | 15840177PubMed |
[18] Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med 1997; 127 820–6.
| 9382404PubMed |
[19] Hu H. The distribution, regionalization and prospect of China’s population. Acta Geogr Sin 1990; 45 139–45.
| 12284413PubMed |
[20] Egger M, Smith GD, Schneider M, Minder CJB. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315 629–34.
| 9310563PubMed |
[21] Bai JY, Yu MH, Liu ZQ, Xu P, Zhou N. Analysis of HIV infection status and its influencing factors among 730 MSM in Tianjin City. Chin J AIDS STD 2015; 21 1048–51. [In Chinese]
[22] Cheng GM, Lv JW, Fang YJ, He JG, Fan YG. Survey on the awareness of AIDS-related knowledge and behaviors among men who have sex with men in different colleges. Chin J Dis Control Prev 2010; 14 487–9. [In Chinese]
[23] Deng B, Jiang H, Wang WY, Lu C, Dickson S, Lai W, et al A cross-sectional survey of the HIV/STD related high-risk behavior in Chengdu’s men who have sex with men in college campus. Mod Prev Med 2010; 37 1543–6. [In Chinese]
[24] Du G, Jiang B. AIDS/HIV-related high risk sexual behavior and the infection of HIV among students of men who have sex with men (MSM). Chin J School Hlth 2011; 32 1312–3. [In Chinese]
[25] Feng LG, Ding XB, Lu RR, Xu SM, Guo XJ, Yang MF, et al Trend on prevalence of HIV and syphilis and estimated HIV incidence among young male students who have sex with men. Acta Academiae Medicinae Militaris Tertiae 2010; 32 2644–6. [In Chinese]
[26] Jin W, Cheng WB, Xu HF, Cai YS, Zhong F, Chen X, et al HIV-related risk behaviors among male students who have sex with men in Guangzhou China. Chin J AIDS STD 2017; 23 123–5. [In Chinese]
[27] Guo XJ, Ding XB, Feng LG, Xu SM, Zheng JQ, Yang MF, et al Sex behavior and HIV infection status of young MSM students in Chongqing. S China J Prev Med 2009; 35 36–7. [In Chinese]
[28] He QY, Wang XD, Yu F, Zhu CR, Wu XQ, Jiang WH, et al Sexual behavior characteristics and HIV infection risk factors among MSM college students. J Prev Med Inform 2011; 27 890–3. [In Chinese]
[29] Wei SS, Wei HD, Huang XH, Pan HP, Liu JH, Lv WJ, et al Utilization of AIDS voluntary counseling and testing among MSM college students in Guangxi. Chin J School Hlth 2017; 38 410–2. [In Chinese]
[30] Zhou C, Ding XB, Feng LG, Guo XJ, Xu SM, Ouyang L, et al Study of HIV infection status and its influencing factors among young student MSM. Chin J Prev Med 2010; 44 461–2. [In Chinese]
[31] Xu JJ, Reilly KH, Lu CM, Ma N, Zhang M, Chu ZX, et al A cross-sectional study of HIV and syphilis infections among male students who have sex with men (MSM) in northeast China: implications for implementing HIV screening and intervention programs. BMC Public Health 2011; 11 287
| A cross-sectional study of HIV and syphilis infections among male students who have sex with men (MSM) in northeast China: implications for implementing HIV screening and intervention programs.Crossref | GoogleScholarGoogle Scholar | 21554742PubMed |
[32] Zheng JD, Pang L, Xu J, Rou KM, Xiao D, Wu Z. Epidemiological study on the prevalence of HIV and syphilis and their correlates among male university students who have sex with men in Beijing, China. Chin J AIDS STD 2011; 17 358–9. [In Chinese]
[33] Zou H, Wu Z, Yu J, Li M, Ablimit M, Li F, et al Sexual risk behaviors and HIV infection among men who have sex with men who use the Internet in Beijing and Urumqi, China. J Acquir Immune Defic Syndr 2010; 53 S81–7.
| 20104115PubMed |
[34] Wei W. Survey on HIV/AIDS among 157 male homosexual in college students in Xinyang. Henan J Prev Med 2017; 28 355–7. [In Chinese]
[35] Zheng JD, Pang L, Xu J, Rou KM, Xiao D, Wu Z. Study on the characteristics of male-to-male sexual behaviors among male university students who have sex with men in Beijing, China. Disease Surveillance 2011; 26 450–3,7. [In Chinese]
[36] Cong L, Ono-Kihara M, Xu G, Ma Q, Pan X, Zhang D, et al The characterisation of sexual behaviour in Chinese male university students who have sex with other men: a cross-sectional study. BMC Public Health 2008; 8 250
| The characterisation of sexual behaviour in Chinese male university students who have sex with other men: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 18647381PubMed |
[37] Wang LX, Chen GZ, Zhang BC, Li Y, Li XF, Yu ZZ. Comparison of AIDS related high risk behavior between college students and the same age non-college students in men who have sex with men. Zhonghua Liu Xing Bing Xue Za Zhi 2010; 31 113–4. [In Chinese]
| 20302718PubMed |
[38] Zhang L, Ding X, Lu R, Feng L, Li X, Xiao Y, et al Predictors of HIV and syphilis among men who have sex with men in a Chinese metropolitan city: comparison of risks among students and non-students. PLoS One 2012; 7 e37211
| Predictors of HIV and syphilis among men who have sex with men in a Chinese metropolitan city: comparison of risks among students and non-students.Crossref | GoogleScholarGoogle Scholar | 23285080PubMed |
[39] Zou H, Xu J, Hu Q, Yu Y, Fu G, Wang Z, et al Decreasing age at first anal intercourse among men who have sex with men in China: a multicentre cross-sectional survey. J Int AIDS Soc 2016; 19 20792
| Decreasing age at first anal intercourse among men who have sex with men in China: a multicentre cross-sectional survey.Crossref | GoogleScholarGoogle Scholar | 27515018PubMed |
[40] Luo H, Zhao JS, Tan HZ, Hu SX, He J. HIV-testing behaviour and influencing factors among college student MSM, Changsha City. Mod Prev Med 2017; 13 2435–8. [In Chinese]
[41] Ruan Y, Li D, Li X, Qian HZ, Shi W, Zhang X, et al Relationship between syphilis and HIV infections among men who have sex with men in Beijing, China. Sex Transm Dis 2007; 34 592–7.
| 17325622PubMed |
[42] Zhang X, Wang C, Hengwei W, Li X, Li D, Ruan Y, 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 S53–7.
| Risk factors of HIV infection and prevalence of co-infections among men who have sex with men in Beijing, China.Crossref | GoogleScholarGoogle Scholar | 18172392PubMed |
[43] Zhu JL, Zhang HB, Wu HH. High risk sexual behavior and HIV/STD infection rate among 122 MSM from students. Chin J AIDS STD 2007; 13 350–2. [In Chinese]
[44] Zhou C, Ding XB, Liu F, Li P. Investigation on HIV/AIDS related knowledge and behavior among men who have sex with men of university students. Mod Prev Med 2010; 37 763–5. [In Chinese]
[45] Zhou ZH, Li SM, Liu YJ, Jiang SL, Zhang XX, Li QC, et al Study on the relationship between behavioral factors, psychological status and HIV infection among men who have sex with men in Beijing. Zhonghua Liu Xing Bing Xue Za Zhi 2010; 31 273–6. [In Chinese]
| 20510051PubMed |
[46] Xi QH, Li Q, Ruan SY, Zhou XJ. KAP survey on STD/AIDS among MSM students in universities in Nanchang City. Acta Acad Med Jiangxi 2011; 51 78–81. [In Chinese]
[47] Wei S, Zhang H, Wang J, Song D, Duan Y, Yu F, et al HIV and syphilis prevalence and associated factors among young men who have sex with men in 4 cities in China. AIDS Behav 2013; 17 1151–8.
| HIV and syphilis prevalence and associated factors among young men who have sex with men in 4 cities in China.Crossref | GoogleScholarGoogle Scholar | 22198314PubMed |
[48] Xu J, An M, Han X, Jia M, Ma Y, Zhang M, et al Prospective cohort study of HIV incidence and molecular characteristics of HIV among men who have sex with men (MSM) in Yunnan Province, China. BMC Infect Dis 2013; 13 3
| Prospective cohort study of HIV incidence and molecular characteristics of HIV among men who have sex with men (MSM) in Yunnan Province, China.Crossref | GoogleScholarGoogle Scholar | 23286213PubMed |
[49] Dong Z, Xu J, Zhang H, Dou Z, Mi G, Ruan Y, et al HIV incidence and risk factors in Chinese young men who have sex with men–a prospective cohort study. PLoS One 2014; 9 e97527
| HIV incidence and risk factors in Chinese young men who have sex with men–a prospective cohort study.Crossref | GoogleScholarGoogle Scholar | 25541696PubMed |
[50] Cai Y, Qiao JG, Sun DW. Evaluation of intervention on AIDS high-risk sexual behavior among young students in Jilin MSM population. Acta Med Univ Sci Techn Huazhong 2017; 46 346–51. [In Chinese]
[51] Fan AP, Cheng L, Yang DF, Sun T, Zhang RQ. Prevalence of HIV and related sexual behaviors among male college students who have sex with men in Taian. Chin J School Hlth 2017; 38 819–22. [In Chinese]
[52] Wei SS, Xie PY, Li Y, Wu TY. Knowledge attitudes and practice regarding HIV/AIDS among men who have sex with men of college students in Guangxi. Mod Prev Med 2017; 44 1708–13. [In Chinese]
[53] Huang CY, Luo D, Liu B, Xiao Y, Xiao SY, Chen X. Utilization status of HIV voluntary counseling for MSM and its influencing factors. Chin Gen Pract 2014; 17 4220–4. [In Chinese]
[54] Zheng J, Wu Z, Poundstone KE, Pang L, Rou K. HIV, syphilis infection, and risky sexual behaviors among male university students who have sex with men in Beijing, China: a cross-sectional study. AIDS Educ Prev 2012; 24 78–88.
| HIV, syphilis infection, and risky sexual behaviors among male university students who have sex with men in Beijing, China: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 22339147PubMed |
[55] Shang H, Zhang L. MSM and HIV-1 infection in China. Natl Sci Rev 2015; 2 388–91.
| MSM and HIV-1 infection in China.Crossref | GoogleScholarGoogle Scholar |
[56] Gao L, Zhang L, Jin Q. Meta-analysis: prevalence of HIV infection and syphilis among MSM in China. Sex Transm Infect 2009; 85 354–8.
| Meta-analysis: prevalence of HIV infection and syphilis among MSM in China.Crossref | GoogleScholarGoogle Scholar | 19351623PubMed |
[57] Wang L, Norris J, Li D, Guo W, Ding Z, Wang N. HIV prevalence and influencing factors analysis of sentinel surveillance among men who have sex with men in China, 2003–2011. Chin Med J (Engl) 2012; 125 1857–61.
| 22884042PubMed |
[58] Li X, Lu H, Raymond HF, Sun Y, Jia Y, He X, et al Untested and undiagnosed: barriers to HIV testing among men who have sex with men, Beijing, China. Sex Transm Infect 2012; 88 187–93.
| Untested and undiagnosed: barriers to HIV testing among men who have sex with men, Beijing, China.Crossref | GoogleScholarGoogle Scholar | 22158932PubMed |
[59] Zhou L, Dong GY, Zhong L, Yuan BT. Study on the sexual behavior and its influencing factors among college students in Shenzhen, Guangdong. Chin J Soc Med 2008; 25 166–8. [In Chinese]
[60] Zou H, Tucker JD, Fan S, Xu J, Yu M, Luo Z, et al Learning about HIV the hard way: HIV among Chinese MSM attending university. Lancet Infect Dis 2018; 18 16–18.
| Learning about HIV the hard way: HIV among Chinese MSM attending university.Crossref | GoogleScholarGoogle Scholar | 29303730PubMed |
[61] Yang SF, Li CC, Zhang JQ, Fan CN, Zhang JX. Present situation and influencing factors of university MSM students in search of sexual partner via MSM dating software in Chengdu. Chin J AIDS STD 2018; 24 66–9. [In Chinese]
[62] Tang WM, Ding JP, Yan HJ, Huan XP, Shan HT, Zhao JK. Sexual behaviors and HIV/syphilis infection among men who have sex with men: a meta analysis of data collected between 2001 and 2006 in the Chinese mainland. Chin J AIDS STD 2008; 5 015 . [In Chinese]
[63] Song Y, Ji CY, Xing Y, Hu PJ, Chen TJ, Zhang L. Association between age of early sexual debut and high-risk sexual behaviors among college students in China. Chin J School Hlth 2011; 32 538–40. [In Chinese]
[64] Burki T. Sex education in China leaves young vulnerable to infection. Lancet Infect Dis 2016; 16 26
| Sex education in China leaves young vulnerable to infection.Crossref | GoogleScholarGoogle Scholar | 26738835PubMed |
[65] Fan EL. HIV testing as prevention among MSM in China: the business of scaling-up. Glob Public Health 2014; 9 85–97.
| HIV testing as prevention among MSM in China: the business of scaling-up.Crossref | GoogleScholarGoogle Scholar | 24498955PubMed |
[66] Yang SF, Zhang JQ, Fan CN, Li CC, Zhang JX. Analysis of influencing factors of HIV test among university MSM students in Chengdu. Chin J School Hlth 2017; 38 1633–6. [In Chinese]
[67] Levy ME, Wilton L, Phillips G, Glick SN, Kuo I, Brewer RA, et al Understanding structural barriers to accessing HIV testing and prevention services among black men who have sex with men (BMSM) in the United States. AIDS Behav 2014; 18 972–96.
| Understanding structural barriers to accessing HIV testing and prevention services among black men who have sex with men (BMSM) in the United States.Crossref | GoogleScholarGoogle Scholar | 24531769PubMed |
[68] Jin X, Xiao D, Xiu XF, Ding ZW, Bao YG. Risk factors of men who have sex with men seeking for Internet based HIV self-testing. Chin J AIDS STD 2017; 23 1043–6. [In Chinese]
[69] Xinhua News. China strives to establish a perfect AIDS detection network. 2017. Available online at: http://www.sohu.com/a/207970235_166989 [verified 16 January 2018].
[70] Wang Z, Lau JTF, Ip M, Ho SPY, Mo PKH, Latkin C, et al A randomized controlled trial evaluating efficacy of promoting a home-based HIV self-testing with online counseling on increasing HIV testing among men who have sex with men. AIDS Behav 2018; 22 190–201.
| A randomized controlled trial evaluating efficacy of promoting a home-based HIV self-testing with online counseling on increasing HIV testing among men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 28831616PubMed |
[71] Jamil MS, Prestage G, Fairley CK, Grulich AE, Smith KS, Chen M, et al Effect of availability of HIV self-testing on HIV testing frequency in gay and bisexual men at high risk of infection (FORTH): a waiting-list randomised controlled trial. Lancet HIV 2017; 4 e241–50.
| Effect of availability of HIV self-testing on HIV testing frequency in gay and bisexual men at high risk of infection (FORTH): a waiting-list randomised controlled trial.Crossref | GoogleScholarGoogle Scholar | 28219619PubMed |
[72] Fu GF, Jiang N, Hu HY, Mahapatra T, Yin YP, Mahapatra S, et al The epidemic of HIV, syphilis, chlamydia and gonorrhea and the correlates of sexual transmitted infections among men who have sex with men in Jiangsu, China, 2009. PLoS One 2015; 10 e0118863
| The epidemic of HIV, syphilis, chlamydia and gonorrhea and the correlates of sexual transmitted infections among men who have sex with men in Jiangsu, China, 2009.Crossref | GoogleScholarGoogle Scholar | 25775451PubMed |
[73] Lu L, Xu D, Liu MB, Liu YT, Zhou XF. Study on HIV and five kinds of common STDs infection and its influencing factors among MSM in Nanchang City. Chin J Dis Control Prev 2014; 18 617–20. [In Chinese]
[74] Thornton A, Lee P. Publication bias in meta-analysis: its causes and consequences. J Clin Epidemiol 2000; 53 207–16.
| Publication bias in meta-analysis: its causes and consequences.Crossref | GoogleScholarGoogle Scholar | 10729693PubMed |
