ORIGINAL STUDY
Risk Factors for Syphilis Among Married Men Who Have Sex With Men in China Zhen Cao, MPH,* Juan Xu, MD, PhD,Þ Hongbo Zhang, MD, MS,* Dandan Song, MS,* Min She, MS,þ Jun Wang, MD,* Jing Wang, MD, PhD,* Yinguang Fan, MD,* Yehuan Sun, MD, PhD,* and Chengye Zhang, MD* Objective: The present study aimed to estimate the prevalence of syphilis among men who have sex with men (MSM) currently married with women in cities of China and examine the related factors for syphilis among them. Methods: ‘‘Snowballing’’ sampling was used to recruit participants in 4 cities from April 2008 to August 2009. Information of participants was collected anonymously and remained confidential. Blood samples were collected from all eligible participants for HIV and syphilis tests. Results: A total of 858 men participated in the study, and their average age was 38.3 years (ranged from 21 to 75 years). Fifty-three percent did not have residence cards, 37% accepted junior high school education or less, and 41% identified themselves as gay. The prevalence of HIV and syphilis was 8.0% and 17.9%, respectively. Older age, less education, homosexual orientation, the sex of the first sexual partner, residential places, and HIV infection were significantly associated with syphilis infection. Gay had higher proportions of some risk sexual behaviors than did nonYgay-identified participants, including the first insert sex before 18 years (17.9% vs. 13.0%), the first male sex partner (49.0% vs. 34.3%) anal sex in the last 6 months (88.0% vs. 83.0%), noncondom use in the last anal sex (35.9% vs. 28.0%), and never use condom in anal sex in the last 6 months (14.8% vs. 9.1%). NonYgay-identified participants had a higher proportion of having opposite sex than did gay participants (70.8% vs. 43.0%). Conclusions: Currently married MSM had a high prevalence of syphilis, and preventive interventions should be developed to control syphilis transmissions among currently married MSM via extromarital sex and intromarital opposite sex.
S
exually transmitted diseases (STDs) including syphilis were eliminated in China during 1960s,1 however, they resurged in
From the * School of Public Health, Anhui Medical University, Hefei, Anhui Province, People’s Republic of China; †National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China; and ‡Center for Disease Control and Prevention of Guiyang City, Guizhou Province, Guiyang, People’s Republic of China
Acknowledgments: This work was supported by National Natural Science Foundation. The authors thank the workers from the Center for Disease Control and Prevention of Beijing, Harbin, Zhengzhou, and Chengdu, as well as the men who have sex with men volunteers from 4 cities for their aid in the data collection and HIV testing during our research. Conflicts of interest and source of funding: None declared. This work was supported by the National Natural Science Foundation of China, Grant No. 30771850. Correspondence: Hongbo Zhang, MD, MS, School of Public Health, Anhui Medical University, 81 Meishan Rd, Hefei 230032, Anhui Province, People’s Republic of China. E-mail: [email protected]. Received for publication March 3, 2013, and accepted November 5, 2013. DOI: 10.1097/OLQ.0000000000000074 Copyright * 2014 American Sexually Transmitted Diseases Association All rights reserved.
98
the late 1970s. The first resurgent case of syphilis was recognized in China in 1979, and then the number increased rapidly to be one of the top 5 reportable diseases in China.2Y5 Between 1989 and 1999, syphilis increased 30-fold, from 0.2 to 6.5 cases per 100,000 people and a further 3-fold increase over the following decade up to 22 cases per 100,000 individuals.6Y8 Epidemiological studies have indicated a growing trend in the prevalence of syphilis among men who have sex with men (MSM). A cross-sectional study was conducted in 20 low HIV epidemic cities across 7 provinces in Western and Northern China of 4983 MSM. Results show that 9.8% of 4983 participants were infected with syphilis and that older age, less education, and inconsistent condom use during anal sex with men were the risk factors.9 A meta-analysis indicated that the syphilis prevalence of MSM increased from 6.8% in 2003 to 2004 to 10.4% in 2005 to 2006 and 13.5% in 2007 to 2008 in China.10 Another research, conducted in Guangzhou, capital of Guangdong province, found that prevalence of syphilis was 17.5% among MSM.11 In developed countries, there are few MSM who are married to women,12 whereas in China, it was frequently reported that MSM are married to women and engage in bisexual behaviors in terms of the traditional cultures.13,14 A meta-analysis of HIV risk behaviors indicated that 31.2% of MSM reported engaging in bisexual behavior in China.15 Feng et al.14 reported that 50.5% of unmarried MSM tended to marry women in Chengdu. However, few literatures have reported the STD prevalence of MSM who are married to women. The aims of this study were (1) to estimate the prevalence of syphilis of MSM who were currently married to women in 4 cities of China and (2) to examine the risk factors for syphilis among MSM. The findings would be helpful to better understand behaviors of MSM who were currently married with women and to develop syphilis prevention intervention strategies to target at this subpopulation of MSM in China.
METHODS Study Settings This study was conducted among MSM married to women in Beijing, Harbin, Zhengzhou, and Chengdu. Beijing is the capital of China, Harbin is the capital of Heilongjiang province located at the northeast of China, Zhengzhou is the capital of Henan province located at the middle of China, and Chengdu is the capital of Sichuan province located at the southwest of China.
Participants The cross-sectional study was conducted from April 2008 to August 2009, and a total of 858 eligible participants were recruited in the 4 cities by nongovernmental organizations of MSM community. Eligibility criteria were men who were 18 years or older, who had anal or oral sex with men in the past
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Risk Factors for Syphilis Among MSM in China
TABLE 1.
Sociodemographic Characteristics and HIV/Syphilis Among Gay and NonYGay-Identified MSM Who Were Currently Married
Variables Overall age, y 21Y25 26Y35 36Y45 Q46 Have a residence card Yes No Education Junior high school or less High school or vocational College school or higher Monthly income (RMB) G1000 1001Y2000 2001Y3000 93000 HIV positive Syphilis positive
n (%)
Gay Identified (n = 351), n (%)
NonYGay Identified (n = 507), n (%)
W2
P
36 (4.2) 322 (37.5) 345 (40.2) 155 (18.1)
8 (2.3) 122 (34.8) 136 (38.7) 85 (24.2)
28 (5.5) 200 (39.4) 209 (41.2) 70 (13.8)
19.174
G0.001
400 (46.6) 458 (53.4)
164 (46.7) 187 (53.3)
236 (46.5) 271 (53.5)
0.003
0.960
315 (36.7) 319 (37.2) 224 (26.1)
130 (37.0) 132 (37.6) 89 (25.4)
185 (36.5) 187 (36.9) 135 (26.6)
0.174
0.916
192 (22.4) 358 (41.7) 163 (19.0) 145 (16.9) 69 (8.0) 154 (17.9)
90 (25.6) 151 (43.0) 59 (16.8) 51 (14.5) 32 (9.1) 76 (21.7)
102 (20.1) 207 (40.8) 104 (20.5) 94 (18.5) 37 (7.3) 78 (15.4)
6.537
0.088
0.928 5.533
0.335 0.019
12 months, who were currently married to women, who lived in 1 of the 4 cities, and who provided written informed consent. Owing to the hard-to-reach and hidden nature of the population, we used snowball sampling to recruit participants. Initial ‘‘seed’’ participants were identified by nongovernmental organization staff of MSM community. Each eligible initial seed was invited to participate in the study and then provided referrals to their MSM peers. After providing written informed consent, participants
completed a questionnaire of behavioral information by local Centers for Disease Control and Prevention (CDC) staff in a single private room. The data were collected anonymously.
Measures The questionnaire included sociodemographics, sexual behaviors, and condom use in the past 6 month, as well as HIVrelated knowledge. Sociodemographic characteristics included
TABLE 2.
Sexual Behaviors and Condom Use Among Gay and NonYGay Identified MSM Who Were Currently Married
Variables
Gay Identified (n = 351), n (%)
NonYGay Identified (n = 507), n (%)
63 (17.9) 288 (82.1)
Age of first insertive sexual encounter, y G18 918 The first sex of partner Men Women Had anal sex in past 6 mo Yes No Had vaginal intercourse in the past 6 mo Yes No Condom use in last anal sex Yes No Condom use in anal sex in past 6 mo Never Sometimes Always Condom use in last vaginal intercourse Yes No Condom use in vaginal intercourse in the past 6 mo Never Sometimes Always
Sexually Transmitted Diseases
&
W2
P
66 (13.0) 441 (87.0)
3.948
0.05
172 (49.0) 179 (51.0)
174 (34.3) 333 (65.7)
18.583
G0.01
309 (88.0) 42 (12.0)
421 (83.0) 86 (17.0)
4.080
0.04
151 (43.0) 200 (57.0)
359 (70.8) 148 (29.2)
66.434
G0.01
183 (52.1) 126 (35.9)
279 (55.0) 142 (28.0)
3.809
0.05
52 (14.8) 163 (46.4) 94 (26.8)
46 (9.1) 203 (40.0) 172 (33.9)
10.679
G0.01
50 (14.2) 101 (28.8)
141 (27.8) 218 (43.0)
1.724
0.189
74 (21.1) 48 (13.7) 29 (8.3)
180 (35.5) 91 (17.9) 88 (17.4)
2.950
0.229
Volume 41, Number 2, February 2014
99
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Cao et al.
TABLE 3.
Factors Associated With Syphilis Among Currently Married MSM (n = 858)
Variables Age, y 21Y25 26Y35 36Y45 Q46 Education College school or higher High school or vocational Junior high school or less City Zhengzhou Beijing Chengdu Harbin Gay-identified orientation No Yes Age of first insertive sexual encounter, y 918 G18 The first sex of partner Women Men No. sex partners in the past 6 mo 0Y5 Q6 Condom use in anal sex in the past 6 mo Always Sometimes Never No anal sex Condom use in vaginal intercourse in the past 6 mo Always Sometimes Never No vaginal intercourse Had commercial sex with men in the past 6 mo No Yes Score of HIV knowledge Q6 G6 HIV positive No Yes
n
Syphilis positive, n (%)
Univariate OR
95% CI
P
OR
90% CI
P
36 322 345 155
1 (2.8) Reference 39 (12.1) 7.823 74 (21.4) 13.907 40 (25.8) 12.311
0.988Y61.928 1.781Y108.575 1.548Y97.919
0.051 0.012 0.018
Reference 8.480 15.850 14.748
1.508Y47.682 2.851Y88.131 2.622Y82.947
0.042 0.008 0.010
224 319 315
30 (13.4) Reference 55 (17.2) 1.312 69 (21.9) 1.906
0.781Y2.203 1.127Y3.224
0.305 0.016
Reference 1.249 1.796
0.818Y1.907 1.186Y2.719
0.388 0.020
210 277 166 205
16 (7.6) Reference 62 (22.3) 3.737 17 (10.2) 1.240 59 (28.8) 5.421
1.995Y6.998 0.589Y2.611 2.844Y10.334
G0.001 0.572 G0.001
Reference 3.481 1.321 5.662
2.104Y5.761 0.714Y2.447 3.359Y9.543
G0.001 0.457 G0.001
507 351
78 (15.4) Reference 76 (21.7) 1.454
0.967Y2.186
0.072
Reference 1.543
1.116Y2.132
0.027
729 124 (17.0) Reference 129 30 (23.3) 1.180
0.700Y1.989
0.534
512 346
81 (15.8) Reference 73 (21.1) 1.385
0.930Y2.061
0.109
Reference 1.499
1.090Y2.061
0.037
602 256
91 (15.1) Reference 63 (24.6) 1.165
0.733Y1.853
0.519
266 366 98 128
43 (16.2) Reference 70 (19.1) 1.291 17 (17.3) 0.923 24 (18.8) 1.042
0.819Y2.034 0.471Y1.807 0.570Y1.904
0.272 0.814 0.894
117 142 254 345
22 (18.8) Reference 14 (9.9) 0.538 45 (17.7) 0.906 73 (21.2) 0.951
0.248Y1.167 0.489Y1.680 0.557Y1.864
0.117 0.754 0.951
823 148 (18.0) Reference 35 6 (17.1) 1.543
0.535Y4.456
0.422
772 133 (17.2) Reference 86 21 (24.4) 1.146
0.634Y2.073
0.652
789 135 (17.1) Reference 69 19 (27.5) 2.393
1.282Y4.465
0.006
Reference 2.537
1.517Y4.244
0.003
age, education, residency, and sexual orientation. Behavioral information collected included the age of the first insert sexual encounter, the sex of the first sexual partner, the condom use during anal and vaginal sex during past 6 months, and commercial sex behaviors (sex between men for gift or money). Based on the question, ‘‘which of the following conditions do you think yourself belong to?’’ we defined ‘‘homosexual’’ as gay identified and ‘‘bisexual, heterosexual, and unsure’’ as nonYgay identified. HIV/AIDS-related knowledge was measured using a validated 8-item measure (assessment of HIV/ AIDS-related knowledge from the Chinese CDC).16 ‘‘Do you think you can be infected with HIV by hugging or shaking hands with HIV-positive people?’’ and ‘‘Does using a
100
Multivariate
condom reduce the risk of HIV/STI? ’’ were 2 sample items, and response options consisted of ‘‘Yes,’’ ‘‘No,’’ and ‘‘I don’t know.’’ The questionnaire took approximately 15 minutes to complete.
Laboratory Testing Blood samples were collected from all eligible participants to test for HIV and syphilis. Two rapid antibody tests were used to screen HIV (RT-1 [Shanghai Kehua Biotechnology Co, Ltd, Shanghai, China] and RT-2 [Hangzhou ACON Biotechnology Co, Ltd, Hangzhou, China]). An enzyme-linked immunosorbent assay was used to retest individuals with HIV antibody positive (enzymelinked immunosorbent assay; Shanghai Kehua Biotechnology Co, Ltd) and a Western blot immune assay (Singapore MP
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Risk Factors for Syphilis Among MSM in China
Biomedical Asia Pacific Ltd, Singapore, Singapore) was used for HIV-1/2 confirmation. Syphilis was screened by rapid plasma regain (Shanghai Kehua Biotechnology Co, Ltd) and confirmed by Treponema pallidum particle agglutination assay (Singapore MP Biomedical Asia Pacific Ltd). Participants undergoing the tests received standard pretest and posttest counseling by local CDC staff. Participants with HIV-positive or syphilis infection were referred to an HIV/STD care clinic for services. This study was reviewed and approved by the institutional review board of Anhui Medical University.
Data Analysis EpiData 3.0 (The EpiData Association, Odense, Denmark) software was used to manage the original data, and Statistical Product and Service Solution 10.01 (SPSS Inc, Chicago, IL) was used to analyze the data. W2 Tests were used for comparing the demographic characteristics and the prevalence of HIV and syphilis between gay and nonYgay-identified married MSM. Univariate and multivariate logistic regression was used to examine the association of potential risk factors with syphilis among married MSM.
RESULTS A total of 858 currently married MSM were enrolled in this study, 210 participants in Zhengzhou, 277 in Beijing, 166 in Chengdu, and 205 in Harbin. The average age of participants was 38.3 years (ranged from 21 to 75 years). HIV and syphilis prevalences of all participants were 8.0% (69/858) and 17.9% (154/858), respectively. Of all participants, 77.7% were between 26 and 45 years, and 53.4% did not have a residence card that indicates that they were migrants. A total of 315 (36.7%) participants accepted a junior high school education or less, and 64.1% earned less than RMB 2000 Yuan (roughly US $323) monthly. Of 858 participants, 40.9% identified themselves as gay and 59.1% as nongay. As shown in Table 1, compared with nonYgay-identified married MSM, gay-identified married MSM were more likely to get syphilis (21.7% vs. 15.4%, P G 0.05). The proportions of some sexual behaviors in gayidentified participants were higher than those of nongay, including having the first insert sex before 18 years old (17.9% vs. 13.0%), the first sex with a man (49.0% vs. 34.3%), reported anal sex in the last 6 months (88.0% vs. 83.0%), noncondom use in the last anal sex (35.9% vs. 28.0%), and never use of condom in anal sex in the last 6 months (14.8% vs. 9.1%). Of nonYgayidentified participants, the proportion of reported having sex with women was significantly higher than that of gay (70.8% vs. 43.0%). There was no significant difference for condom use between gay and nongay participants during opposite sex in the last 6 months (Table 2). Table 3 shows the potential risk factors associated with syphilis among married MSM. Results of the univariate logistic regression analyses indicated that older age, lower education, study city, and HIV infection were associated with syphilis. The multiple logistic regression analyses also indicated that old age, low education, gay-identified orientation and sex of the first sexual partner, and HIV infection were associated with syphilis infection. Odds ratios (ORs) of Beijing versus Zhengzhou and Harbin versus Zhengzhou were 3.48 and 5.66.
DISCUSSION A study conducted in 9 cities in northeast (Harbin and Shenyang), middle (Zhengzhou and Wuhan), southwest (Chongqing Sexually Transmitted Diseases
&
and Chengdu), and east (Shanghai and Nanjing) of China shows that 17.7% of MSM participants reported sexual transmitted infection.17 Another study conducted in Beijing, Harbin, Zhengzhou, and Chengdu in 2008 reported that the prevalence of syphilis was 11.9% and 13.2% for MSM and men who have sex with men and women (MSMW), respectively. This study found that the prevalence of syphilis among MSM married to women was 17.9%, which was higher than that of MSM and that of MSMW in the same cities.18 This finding was consistent with that in other studies in Shenyang and Guangzhou, which reported that being married was a risky factor for syphilis among MSM,11,19 indicating that marriage might act as ‘‘a bridge’’ of spreading syphilis widely through intramarital sex between men and extramarital between opposite sex. Furthermore, this study shows that the prevalence of syphilis among married MSM was different between cities, the highest (28.8%) in Harbin, followed by Beijing (22.3%), Chengdu (10.2%), and Zhengzhou (7.6%). Proposed explanation may be that married MSM in different cities might have different risk of syphilis; for example, there were more gay bathhouses in Harbin and Beijing, where sex between men happened very frequently. Moreover, the prevalence of syphilis was increasing with the older age and lower education of married MSM, which was consistent with other studies among MSM.9,19Y21 Efforts of intervention are needed to address both on older age and less education of married MSM. In addition, this study found that HIV infection was a risk factor for syphilis, being parallel with other studies that found that syphilis increased the risk of HIV infection,19,20,22Y24 suggesting that HIV and syphilis are closely related to each other. For instance, in a community-based cross-sectional study conducted among MSM in Beijing from November 2006 to February 2007, syphilis infection was found to be independently associated with HIV infection.25 Therefore, married MSM act as a bridge between the MSM and heterosexual communities not only for syphilis but also for HIV and that the presence of syphilis can actually enhance the transmission of HIV. Hence, prevention intervention on syphilis would decrease the prevalence of HIV infection among married MSM. Finally, a great deal of evidence revealed that MSM who has heterosexual or married relationship played a significant role in sexually transmitted infection/HIV transmission in China. Among MSM in China, there is a considerably high prevalence of bisexual behaviors and relatively common unprotected vaginal sex. A meta-analysis of HIV risk behavior surveys in China estimated an overall prevalence of bisexual behavior of 31.2% among MSM in China.15 A survey conducted in Yunnan Province found that among 896 MSM, nearly one-third (31%) had engaged in bisexual behaviors in the past 6 months; of MSMW at the same time, 72% reported having unprotected vaginal sex with female partners in the past 6 months.26 Previous research has also revealed that in contrast with nonmarried MSM, married MSM report significantly higher rates of unprotected insertive anal, receptive anal, and vaginal sex.27 The inherent bridging aspect of MSMW associated with bisexual behaviors may accelerate transmission of HIV and other STDs in the general population. As in other cross-sectional studies, there are still some limitations in our study. First, the cross-sectional nature cannot prove the causative relationship between related factors and syphilis. Second, owing to the hard-to-reach nature of the population, the snowball sampling method used in the study might limit the representation of the targeting population and might lead to selective bias. Finally, the data were collected by self-reporting
Volume 41, Number 2, February 2014
101
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Cao et al.
and some questions related to personal privacy, which might result in reporting biases and social desirable bias and therefore might underestimate risks. In summary, the findings show that the prevalence of syphilis was high among currently married MSM in 4 cities in China, and preventive interventions should be developed for controlling syphilis spreading between same- and opposite-sex among currently married MSM. REFERENCES 1. 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): S223YS229. 2. Chinese Ministry of Health. Notifiable Diseases in China in 2004. Beijing: Ministry of Health, 2005. 3. Chinese Ministry of Health. Notifiable Diseases in China in 2005. Beijing: Ministry of Health, 2006. 4. Chinese Ministry of Health. Notifiable Diseases in China in 2006. Beijing: Ministry of Health, 2007. 5. Chinese Ministry of Health. Notifiable Diseases in China in 2010. Beijing: Ministry of Health, 2006. 6. Chen XS, Gong XD, Liang G, et al. Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138Y142. 7. Chen ZQ, Zhang GC, Gong XD, et al. Syphilis in China: Results of a national surveillance programme. Lancet 2007; 369:132Y138. 8. Tucker JD, Chen XS, Peeling RW. Syphilis and social upheaval in China. N Engl J Med 2010; 362:1658Y1661. 9. Xiao Y, Sun J, Li C, et al. 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):S66YS73. 10. Chow EP, Wilson DP, Zhang L. HIV and syphilis co-infection increasing among men who have sex with men in China: A systematic review and meta-analysis. PLoS One 2011; 6:e22768. 11. Zhong F, Lin P, Xu H, 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 2011; 15:1058Y1066. 12. Catania JA, Osmond D, Stall RD, et al. The continuing HIV epidemic among men who have sex with men. Am J Public Health 2001; 91:907Y914. 13. Zhang K, Li D, Li H, et al. Changing sexual attitudes and behaviour in China: Implications for the spread of HIV and other sexually transmitted diseases. AIDS Care 1999; 11:581Y589.
102
14. Feng Y, Wu Z, Detels R. Evolution of men who have sex with men community and experienced stigma among men who have sex with men in Chengdu, China. J Acquir Immune Defic Syndr 2010; 53(suppl 1):S98YS103. 15. Yun K, Xu JJ, Reilly KH, et al. Prevalence of bisexual behavior among bridge population of men who have sex with men in China: A meta-analysis of observational studies. Sex Transm Infect 2011; 87:563Y570. 16. National Center for AIDS/STD Control and Prevention, China CDC. China AIDS Monitoring and Evaluation Framework (for Trial Implementation). Beijing: People’s Medical Publishing House, 2007. 17. Li H, Zhang BC, Li XF, et al. Sexual partners and sexually transmitted infection incidence: A survey of 2250 men who have sex with men. Zhonghua Pi Fu Ke Za Zhi 2009; 10:665Y667. 18. She M, Zhang HB, Wang J, et al. Investigation of HIV and syphilis infection status and risk sexual behavior among men who have sex with men in four cities of China. Zhonghua Yu Fang Yi Xue Za Zhi 2012; 46:324Y328. 19. 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 in Shenyang, China. Sex Transm Dis 2010; 37:432Y439. 20. Li D, Jia Y, Ruan Y, et al. Correlates of incident infections for HIV, syphilis, and hepatitis B virus in a cohort of men who have sex with men in Beijing. AIDS Patient Care STDS 2010; 24:595Y602. 21. Champenois K, Cousien A, Ndiaye B, et al. Risk factors for syphilis infection in men who have sex with men: Results of a case-control study in Lille, France. Sex Transm Infect 2012. 22. Centers for Disease Control and Prevention, Syphilis & MSM (Men Who Have Sex With Men). CDC Fact Sheet, 2010, 9. Available at: URL: http://www.cdc.gov/std/syphilis/STDFact-MSM-Syphilis.htm 23. Li DL, Gao YJ, Yu MR, et al. Study on the incidence of HIV and associated risk factors through a prospective cohort among men who have sex with men in Beijing, China. Zhonghua Liu Xing Bing Xue Za Zhi 2012; 33:663Y666. 24. Yang H, Hao C, Huan X, et al. HIV incidence and associated factors in a cohort of men who have sex with men in Nanjing, China. Sex Transm Dis 2010; 37:208Y213. 25. Ruan Y, Luo F, Jia Y, et al. Risk factors for syphilis and prevalence of HIV, hepatitis B and C among men who have sex with men in Beijing, China: Implications for HIV prevention. AIDS Behav 2009; 13:663Y670. 26. Lau J, Wang M, Wong H, et al. Prevalence of bisexual behaviors among men who have sex with men (MSM) in China and associations between condom use in MSM and heterosexual behaviors. Sex Transm Dis 2008; 35:406Y413. 27. Xu J, Xu J, Guodong M, et al. Comparison of AIDS related sexual behaviors between married and unmarried MSM. Chin J Dis Control Prev 2010; 14:404Y407.
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Risk Factors for Syphilis Among Married Men Who Have Sex With Men in China Zhen Cao, MPH,* Juan Xu, MD, PhD,Þ Hongbo Zhang, MD, MS,* Dandan Song, MS,* Min She, MS,þ Jun Wang, MD,* Jing Wang, MD, PhD,* Yinguang Fan, MD,* Yehuan Sun, MD, PhD,* and Chengye Zhang, MD* Objective: The present study aimed to estimate the prevalence of syphilis among men who have sex with men (MSM) currently married with women in cities of China and examine the related factors for syphilis among them. Methods: ‘‘Snowballing’’ sampling was used to recruit participants in 4 cities from April 2008 to August 2009. Information of participants was collected anonymously and remained confidential. Blood samples were collected from all eligible participants for HIV and syphilis tests. Results: A total of 858 men participated in the study, and their average age was 38.3 years (ranged from 21 to 75 years). Fifty-three percent did not have residence cards, 37% accepted junior high school education or less, and 41% identified themselves as gay. The prevalence of HIV and syphilis was 8.0% and 17.9%, respectively. Older age, less education, homosexual orientation, the sex of the first sexual partner, residential places, and HIV infection were significantly associated with syphilis infection. Gay had higher proportions of some risk sexual behaviors than did nonYgay-identified participants, including the first insert sex before 18 years (17.9% vs. 13.0%), the first male sex partner (49.0% vs. 34.3%) anal sex in the last 6 months (88.0% vs. 83.0%), noncondom use in the last anal sex (35.9% vs. 28.0%), and never use condom in anal sex in the last 6 months (14.8% vs. 9.1%). NonYgay-identified participants had a higher proportion of having opposite sex than did gay participants (70.8% vs. 43.0%). Conclusions: Currently married MSM had a high prevalence of syphilis, and preventive interventions should be developed to control syphilis transmissions among currently married MSM via extromarital sex and intromarital opposite sex.
S
exually transmitted diseases (STDs) including syphilis were eliminated in China during 1960s,1 however, they resurged in
From the * School of Public Health, Anhui Medical University, Hefei, Anhui Province, People’s Republic of China; †National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China; and ‡Center for Disease Control and Prevention of Guiyang City, Guizhou Province, Guiyang, People’s Republic of China
Acknowledgments: This work was supported by National Natural Science Foundation. The authors thank the workers from the Center for Disease Control and Prevention of Beijing, Harbin, Zhengzhou, and Chengdu, as well as the men who have sex with men volunteers from 4 cities for their aid in the data collection and HIV testing during our research. Conflicts of interest and source of funding: None declared. This work was supported by the National Natural Science Foundation of China, Grant No. 30771850. Correspondence: Hongbo Zhang, MD, MS, School of Public Health, Anhui Medical University, 81 Meishan Rd, Hefei 230032, Anhui Province, People’s Republic of China. E-mail: [email protected]. Received for publication March 3, 2013, and accepted November 5, 2013. DOI: 10.1097/OLQ.0000000000000074 Copyright * 2014 American Sexually Transmitted Diseases Association All rights reserved.
98
the late 1970s. The first resurgent case of syphilis was recognized in China in 1979, and then the number increased rapidly to be one of the top 5 reportable diseases in China.2Y5 Between 1989 and 1999, syphilis increased 30-fold, from 0.2 to 6.5 cases per 100,000 people and a further 3-fold increase over the following decade up to 22 cases per 100,000 individuals.6Y8 Epidemiological studies have indicated a growing trend in the prevalence of syphilis among men who have sex with men (MSM). A cross-sectional study was conducted in 20 low HIV epidemic cities across 7 provinces in Western and Northern China of 4983 MSM. Results show that 9.8% of 4983 participants were infected with syphilis and that older age, less education, and inconsistent condom use during anal sex with men were the risk factors.9 A meta-analysis indicated that the syphilis prevalence of MSM increased from 6.8% in 2003 to 2004 to 10.4% in 2005 to 2006 and 13.5% in 2007 to 2008 in China.10 Another research, conducted in Guangzhou, capital of Guangdong province, found that prevalence of syphilis was 17.5% among MSM.11 In developed countries, there are few MSM who are married to women,12 whereas in China, it was frequently reported that MSM are married to women and engage in bisexual behaviors in terms of the traditional cultures.13,14 A meta-analysis of HIV risk behaviors indicated that 31.2% of MSM reported engaging in bisexual behavior in China.15 Feng et al.14 reported that 50.5% of unmarried MSM tended to marry women in Chengdu. However, few literatures have reported the STD prevalence of MSM who are married to women. The aims of this study were (1) to estimate the prevalence of syphilis of MSM who were currently married to women in 4 cities of China and (2) to examine the risk factors for syphilis among MSM. The findings would be helpful to better understand behaviors of MSM who were currently married with women and to develop syphilis prevention intervention strategies to target at this subpopulation of MSM in China.
METHODS Study Settings This study was conducted among MSM married to women in Beijing, Harbin, Zhengzhou, and Chengdu. Beijing is the capital of China, Harbin is the capital of Heilongjiang province located at the northeast of China, Zhengzhou is the capital of Henan province located at the middle of China, and Chengdu is the capital of Sichuan province located at the southwest of China.
Participants The cross-sectional study was conducted from April 2008 to August 2009, and a total of 858 eligible participants were recruited in the 4 cities by nongovernmental organizations of MSM community. Eligibility criteria were men who were 18 years or older, who had anal or oral sex with men in the past
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Risk Factors for Syphilis Among MSM in China
TABLE 1.
Sociodemographic Characteristics and HIV/Syphilis Among Gay and NonYGay-Identified MSM Who Were Currently Married
Variables Overall age, y 21Y25 26Y35 36Y45 Q46 Have a residence card Yes No Education Junior high school or less High school or vocational College school or higher Monthly income (RMB) G1000 1001Y2000 2001Y3000 93000 HIV positive Syphilis positive
n (%)
Gay Identified (n = 351), n (%)
NonYGay Identified (n = 507), n (%)
W2
P
36 (4.2) 322 (37.5) 345 (40.2) 155 (18.1)
8 (2.3) 122 (34.8) 136 (38.7) 85 (24.2)
28 (5.5) 200 (39.4) 209 (41.2) 70 (13.8)
19.174
G0.001
400 (46.6) 458 (53.4)
164 (46.7) 187 (53.3)
236 (46.5) 271 (53.5)
0.003
0.960
315 (36.7) 319 (37.2) 224 (26.1)
130 (37.0) 132 (37.6) 89 (25.4)
185 (36.5) 187 (36.9) 135 (26.6)
0.174
0.916
192 (22.4) 358 (41.7) 163 (19.0) 145 (16.9) 69 (8.0) 154 (17.9)
90 (25.6) 151 (43.0) 59 (16.8) 51 (14.5) 32 (9.1) 76 (21.7)
102 (20.1) 207 (40.8) 104 (20.5) 94 (18.5) 37 (7.3) 78 (15.4)
6.537
0.088
0.928 5.533
0.335 0.019
12 months, who were currently married to women, who lived in 1 of the 4 cities, and who provided written informed consent. Owing to the hard-to-reach and hidden nature of the population, we used snowball sampling to recruit participants. Initial ‘‘seed’’ participants were identified by nongovernmental organization staff of MSM community. Each eligible initial seed was invited to participate in the study and then provided referrals to their MSM peers. After providing written informed consent, participants
completed a questionnaire of behavioral information by local Centers for Disease Control and Prevention (CDC) staff in a single private room. The data were collected anonymously.
Measures The questionnaire included sociodemographics, sexual behaviors, and condom use in the past 6 month, as well as HIVrelated knowledge. Sociodemographic characteristics included
TABLE 2.
Sexual Behaviors and Condom Use Among Gay and NonYGay Identified MSM Who Were Currently Married
Variables
Gay Identified (n = 351), n (%)
NonYGay Identified (n = 507), n (%)
63 (17.9) 288 (82.1)
Age of first insertive sexual encounter, y G18 918 The first sex of partner Men Women Had anal sex in past 6 mo Yes No Had vaginal intercourse in the past 6 mo Yes No Condom use in last anal sex Yes No Condom use in anal sex in past 6 mo Never Sometimes Always Condom use in last vaginal intercourse Yes No Condom use in vaginal intercourse in the past 6 mo Never Sometimes Always
Sexually Transmitted Diseases
&
W2
P
66 (13.0) 441 (87.0)
3.948
0.05
172 (49.0) 179 (51.0)
174 (34.3) 333 (65.7)
18.583
G0.01
309 (88.0) 42 (12.0)
421 (83.0) 86 (17.0)
4.080
0.04
151 (43.0) 200 (57.0)
359 (70.8) 148 (29.2)
66.434
G0.01
183 (52.1) 126 (35.9)
279 (55.0) 142 (28.0)
3.809
0.05
52 (14.8) 163 (46.4) 94 (26.8)
46 (9.1) 203 (40.0) 172 (33.9)
10.679
G0.01
50 (14.2) 101 (28.8)
141 (27.8) 218 (43.0)
1.724
0.189
74 (21.1) 48 (13.7) 29 (8.3)
180 (35.5) 91 (17.9) 88 (17.4)
2.950
0.229
Volume 41, Number 2, February 2014
99
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Cao et al.
TABLE 3.
Factors Associated With Syphilis Among Currently Married MSM (n = 858)
Variables Age, y 21Y25 26Y35 36Y45 Q46 Education College school or higher High school or vocational Junior high school or less City Zhengzhou Beijing Chengdu Harbin Gay-identified orientation No Yes Age of first insertive sexual encounter, y 918 G18 The first sex of partner Women Men No. sex partners in the past 6 mo 0Y5 Q6 Condom use in anal sex in the past 6 mo Always Sometimes Never No anal sex Condom use in vaginal intercourse in the past 6 mo Always Sometimes Never No vaginal intercourse Had commercial sex with men in the past 6 mo No Yes Score of HIV knowledge Q6 G6 HIV positive No Yes
n
Syphilis positive, n (%)
Univariate OR
95% CI
P
OR
90% CI
P
36 322 345 155
1 (2.8) Reference 39 (12.1) 7.823 74 (21.4) 13.907 40 (25.8) 12.311
0.988Y61.928 1.781Y108.575 1.548Y97.919
0.051 0.012 0.018
Reference 8.480 15.850 14.748
1.508Y47.682 2.851Y88.131 2.622Y82.947
0.042 0.008 0.010
224 319 315
30 (13.4) Reference 55 (17.2) 1.312 69 (21.9) 1.906
0.781Y2.203 1.127Y3.224
0.305 0.016
Reference 1.249 1.796
0.818Y1.907 1.186Y2.719
0.388 0.020
210 277 166 205
16 (7.6) Reference 62 (22.3) 3.737 17 (10.2) 1.240 59 (28.8) 5.421
1.995Y6.998 0.589Y2.611 2.844Y10.334
G0.001 0.572 G0.001
Reference 3.481 1.321 5.662
2.104Y5.761 0.714Y2.447 3.359Y9.543
G0.001 0.457 G0.001
507 351
78 (15.4) Reference 76 (21.7) 1.454
0.967Y2.186
0.072
Reference 1.543
1.116Y2.132
0.027
729 124 (17.0) Reference 129 30 (23.3) 1.180
0.700Y1.989
0.534
512 346
81 (15.8) Reference 73 (21.1) 1.385
0.930Y2.061
0.109
Reference 1.499
1.090Y2.061
0.037
602 256
91 (15.1) Reference 63 (24.6) 1.165
0.733Y1.853
0.519
266 366 98 128
43 (16.2) Reference 70 (19.1) 1.291 17 (17.3) 0.923 24 (18.8) 1.042
0.819Y2.034 0.471Y1.807 0.570Y1.904
0.272 0.814 0.894
117 142 254 345
22 (18.8) Reference 14 (9.9) 0.538 45 (17.7) 0.906 73 (21.2) 0.951
0.248Y1.167 0.489Y1.680 0.557Y1.864
0.117 0.754 0.951
823 148 (18.0) Reference 35 6 (17.1) 1.543
0.535Y4.456
0.422
772 133 (17.2) Reference 86 21 (24.4) 1.146
0.634Y2.073
0.652
789 135 (17.1) Reference 69 19 (27.5) 2.393
1.282Y4.465
0.006
Reference 2.537
1.517Y4.244
0.003
age, education, residency, and sexual orientation. Behavioral information collected included the age of the first insert sexual encounter, the sex of the first sexual partner, the condom use during anal and vaginal sex during past 6 months, and commercial sex behaviors (sex between men for gift or money). Based on the question, ‘‘which of the following conditions do you think yourself belong to?’’ we defined ‘‘homosexual’’ as gay identified and ‘‘bisexual, heterosexual, and unsure’’ as nonYgay identified. HIV/AIDS-related knowledge was measured using a validated 8-item measure (assessment of HIV/ AIDS-related knowledge from the Chinese CDC).16 ‘‘Do you think you can be infected with HIV by hugging or shaking hands with HIV-positive people?’’ and ‘‘Does using a
100
Multivariate
condom reduce the risk of HIV/STI? ’’ were 2 sample items, and response options consisted of ‘‘Yes,’’ ‘‘No,’’ and ‘‘I don’t know.’’ The questionnaire took approximately 15 minutes to complete.
Laboratory Testing Blood samples were collected from all eligible participants to test for HIV and syphilis. Two rapid antibody tests were used to screen HIV (RT-1 [Shanghai Kehua Biotechnology Co, Ltd, Shanghai, China] and RT-2 [Hangzhou ACON Biotechnology Co, Ltd, Hangzhou, China]). An enzyme-linked immunosorbent assay was used to retest individuals with HIV antibody positive (enzymelinked immunosorbent assay; Shanghai Kehua Biotechnology Co, Ltd) and a Western blot immune assay (Singapore MP
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Risk Factors for Syphilis Among MSM in China
Biomedical Asia Pacific Ltd, Singapore, Singapore) was used for HIV-1/2 confirmation. Syphilis was screened by rapid plasma regain (Shanghai Kehua Biotechnology Co, Ltd) and confirmed by Treponema pallidum particle agglutination assay (Singapore MP Biomedical Asia Pacific Ltd). Participants undergoing the tests received standard pretest and posttest counseling by local CDC staff. Participants with HIV-positive or syphilis infection were referred to an HIV/STD care clinic for services. This study was reviewed and approved by the institutional review board of Anhui Medical University.
Data Analysis EpiData 3.0 (The EpiData Association, Odense, Denmark) software was used to manage the original data, and Statistical Product and Service Solution 10.01 (SPSS Inc, Chicago, IL) was used to analyze the data. W2 Tests were used for comparing the demographic characteristics and the prevalence of HIV and syphilis between gay and nonYgay-identified married MSM. Univariate and multivariate logistic regression was used to examine the association of potential risk factors with syphilis among married MSM.
RESULTS A total of 858 currently married MSM were enrolled in this study, 210 participants in Zhengzhou, 277 in Beijing, 166 in Chengdu, and 205 in Harbin. The average age of participants was 38.3 years (ranged from 21 to 75 years). HIV and syphilis prevalences of all participants were 8.0% (69/858) and 17.9% (154/858), respectively. Of all participants, 77.7% were between 26 and 45 years, and 53.4% did not have a residence card that indicates that they were migrants. A total of 315 (36.7%) participants accepted a junior high school education or less, and 64.1% earned less than RMB 2000 Yuan (roughly US $323) monthly. Of 858 participants, 40.9% identified themselves as gay and 59.1% as nongay. As shown in Table 1, compared with nonYgay-identified married MSM, gay-identified married MSM were more likely to get syphilis (21.7% vs. 15.4%, P G 0.05). The proportions of some sexual behaviors in gayidentified participants were higher than those of nongay, including having the first insert sex before 18 years old (17.9% vs. 13.0%), the first sex with a man (49.0% vs. 34.3%), reported anal sex in the last 6 months (88.0% vs. 83.0%), noncondom use in the last anal sex (35.9% vs. 28.0%), and never use of condom in anal sex in the last 6 months (14.8% vs. 9.1%). Of nonYgayidentified participants, the proportion of reported having sex with women was significantly higher than that of gay (70.8% vs. 43.0%). There was no significant difference for condom use between gay and nongay participants during opposite sex in the last 6 months (Table 2). Table 3 shows the potential risk factors associated with syphilis among married MSM. Results of the univariate logistic regression analyses indicated that older age, lower education, study city, and HIV infection were associated with syphilis. The multiple logistic regression analyses also indicated that old age, low education, gay-identified orientation and sex of the first sexual partner, and HIV infection were associated with syphilis infection. Odds ratios (ORs) of Beijing versus Zhengzhou and Harbin versus Zhengzhou were 3.48 and 5.66.
DISCUSSION A study conducted in 9 cities in northeast (Harbin and Shenyang), middle (Zhengzhou and Wuhan), southwest (Chongqing Sexually Transmitted Diseases
&
and Chengdu), and east (Shanghai and Nanjing) of China shows that 17.7% of MSM participants reported sexual transmitted infection.17 Another study conducted in Beijing, Harbin, Zhengzhou, and Chengdu in 2008 reported that the prevalence of syphilis was 11.9% and 13.2% for MSM and men who have sex with men and women (MSMW), respectively. This study found that the prevalence of syphilis among MSM married to women was 17.9%, which was higher than that of MSM and that of MSMW in the same cities.18 This finding was consistent with that in other studies in Shenyang and Guangzhou, which reported that being married was a risky factor for syphilis among MSM,11,19 indicating that marriage might act as ‘‘a bridge’’ of spreading syphilis widely through intramarital sex between men and extramarital between opposite sex. Furthermore, this study shows that the prevalence of syphilis among married MSM was different between cities, the highest (28.8%) in Harbin, followed by Beijing (22.3%), Chengdu (10.2%), and Zhengzhou (7.6%). Proposed explanation may be that married MSM in different cities might have different risk of syphilis; for example, there were more gay bathhouses in Harbin and Beijing, where sex between men happened very frequently. Moreover, the prevalence of syphilis was increasing with the older age and lower education of married MSM, which was consistent with other studies among MSM.9,19Y21 Efforts of intervention are needed to address both on older age and less education of married MSM. In addition, this study found that HIV infection was a risk factor for syphilis, being parallel with other studies that found that syphilis increased the risk of HIV infection,19,20,22Y24 suggesting that HIV and syphilis are closely related to each other. For instance, in a community-based cross-sectional study conducted among MSM in Beijing from November 2006 to February 2007, syphilis infection was found to be independently associated with HIV infection.25 Therefore, married MSM act as a bridge between the MSM and heterosexual communities not only for syphilis but also for HIV and that the presence of syphilis can actually enhance the transmission of HIV. Hence, prevention intervention on syphilis would decrease the prevalence of HIV infection among married MSM. Finally, a great deal of evidence revealed that MSM who has heterosexual or married relationship played a significant role in sexually transmitted infection/HIV transmission in China. Among MSM in China, there is a considerably high prevalence of bisexual behaviors and relatively common unprotected vaginal sex. A meta-analysis of HIV risk behavior surveys in China estimated an overall prevalence of bisexual behavior of 31.2% among MSM in China.15 A survey conducted in Yunnan Province found that among 896 MSM, nearly one-third (31%) had engaged in bisexual behaviors in the past 6 months; of MSMW at the same time, 72% reported having unprotected vaginal sex with female partners in the past 6 months.26 Previous research has also revealed that in contrast with nonmarried MSM, married MSM report significantly higher rates of unprotected insertive anal, receptive anal, and vaginal sex.27 The inherent bridging aspect of MSMW associated with bisexual behaviors may accelerate transmission of HIV and other STDs in the general population. As in other cross-sectional studies, there are still some limitations in our study. First, the cross-sectional nature cannot prove the causative relationship between related factors and syphilis. Second, owing to the hard-to-reach nature of the population, the snowball sampling method used in the study might limit the representation of the targeting population and might lead to selective bias. Finally, the data were collected by self-reporting
Volume 41, Number 2, February 2014
101
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Cao et al.
and some questions related to personal privacy, which might result in reporting biases and social desirable bias and therefore might underestimate risks. In summary, the findings show that the prevalence of syphilis was high among currently married MSM in 4 cities in China, and preventive interventions should be developed for controlling syphilis spreading between same- and opposite-sex among currently married MSM. REFERENCES 1. 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): S223YS229. 2. Chinese Ministry of Health. Notifiable Diseases in China in 2004. Beijing: Ministry of Health, 2005. 3. Chinese Ministry of Health. Notifiable Diseases in China in 2005. Beijing: Ministry of Health, 2006. 4. Chinese Ministry of Health. Notifiable Diseases in China in 2006. Beijing: Ministry of Health, 2007. 5. Chinese Ministry of Health. Notifiable Diseases in China in 2010. Beijing: Ministry of Health, 2006. 6. Chen XS, Gong XD, Liang G, et al. Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138Y142. 7. Chen ZQ, Zhang GC, Gong XD, et al. Syphilis in China: Results of a national surveillance programme. Lancet 2007; 369:132Y138. 8. Tucker JD, Chen XS, Peeling RW. Syphilis and social upheaval in China. N Engl J Med 2010; 362:1658Y1661. 9. Xiao Y, Sun J, Li C, et al. 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):S66YS73. 10. Chow EP, Wilson DP, Zhang L. HIV and syphilis co-infection increasing among men who have sex with men in China: A systematic review and meta-analysis. PLoS One 2011; 6:e22768. 11. Zhong F, Lin P, Xu H, 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 2011; 15:1058Y1066. 12. Catania JA, Osmond D, Stall RD, et al. The continuing HIV epidemic among men who have sex with men. Am J Public Health 2001; 91:907Y914. 13. Zhang K, Li D, Li H, et al. Changing sexual attitudes and behaviour in China: Implications for the spread of HIV and other sexually transmitted diseases. AIDS Care 1999; 11:581Y589.
102
14. Feng Y, Wu Z, Detels R. Evolution of men who have sex with men community and experienced stigma among men who have sex with men in Chengdu, China. J Acquir Immune Defic Syndr 2010; 53(suppl 1):S98YS103. 15. Yun K, Xu JJ, Reilly KH, et al. Prevalence of bisexual behavior among bridge population of men who have sex with men in China: A meta-analysis of observational studies. Sex Transm Infect 2011; 87:563Y570. 16. National Center for AIDS/STD Control and Prevention, China CDC. China AIDS Monitoring and Evaluation Framework (for Trial Implementation). Beijing: People’s Medical Publishing House, 2007. 17. Li H, Zhang BC, Li XF, et al. Sexual partners and sexually transmitted infection incidence: A survey of 2250 men who have sex with men. Zhonghua Pi Fu Ke Za Zhi 2009; 10:665Y667. 18. She M, Zhang HB, Wang J, et al. Investigation of HIV and syphilis infection status and risk sexual behavior among men who have sex with men in four cities of China. Zhonghua Yu Fang Yi Xue Za Zhi 2012; 46:324Y328. 19. 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 in Shenyang, China. Sex Transm Dis 2010; 37:432Y439. 20. Li D, Jia Y, Ruan Y, et al. Correlates of incident infections for HIV, syphilis, and hepatitis B virus in a cohort of men who have sex with men in Beijing. AIDS Patient Care STDS 2010; 24:595Y602. 21. Champenois K, Cousien A, Ndiaye B, et al. Risk factors for syphilis infection in men who have sex with men: Results of a case-control study in Lille, France. Sex Transm Infect 2012. 22. Centers for Disease Control and Prevention, Syphilis & MSM (Men Who Have Sex With Men). CDC Fact Sheet, 2010, 9. Available at: URL: http://www.cdc.gov/std/syphilis/STDFact-MSM-Syphilis.htm 23. Li DL, Gao YJ, Yu MR, et al. Study on the incidence of HIV and associated risk factors through a prospective cohort among men who have sex with men in Beijing, China. Zhonghua Liu Xing Bing Xue Za Zhi 2012; 33:663Y666. 24. Yang H, Hao C, Huan X, et al. HIV incidence and associated factors in a cohort of men who have sex with men in Nanjing, China. Sex Transm Dis 2010; 37:208Y213. 25. Ruan Y, Luo F, Jia Y, et al. Risk factors for syphilis and prevalence of HIV, hepatitis B and C among men who have sex with men in Beijing, China: Implications for HIV prevention. AIDS Behav 2009; 13:663Y670. 26. Lau J, Wang M, Wong H, et al. Prevalence of bisexual behaviors among men who have sex with men (MSM) in China and associations between condom use in MSM and heterosexual behaviors. Sex Transm Dis 2008; 35:406Y413. 27. Xu J, Xu J, Guodong M, et al. Comparison of AIDS related sexual behaviors between married and unmarried MSM. Chin J Dis Control Prev 2010; 14:404Y407.
Sexually Transmitted Diseases
&
Volume 41, Number 2, February 2014
Copyright © 2014 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
