Article Text

The incidence of syphilis, HIV and HCV and associated factors in a cohort of men who have sex with men in Nanjing, China
1. Chun Hao1,2,
2. Hongjing Yan3,
3. Haitao Yang3,
4. Xiping Huan3,
5. Wenhui Guan3,
6. Xiaoqin Xu3,
7. Min Zhang4,
8. Weiming Tang5,
9. Na Wang4,
10. Jing Gu2,6,
11. Joseph T F Lau1,2
1. 1Centre for Health Behaviours Research, School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong
2. 2Centre for Medical Anthropology and Behavioral Health, Sun Yat-sen University, PR China
3. 3Jiangsu Provincial Central for Disease Control and Prevention, Nanjing, Jiangsu, PR China
4. 4Nanjing Central for Disease Control and Prevention, Nanjing, Jiangsu, PR China
5. 5Nanjing Medical University, Nanjing, Jiangsu, PR China
6. 6School of Public Health, Sun Yat-sen University, PR China
1. Correspondence to Professor Joseph T F Lau, Centre for Health Behaviors Research, School of Public Health and Primary Care, Faculty of Medicine, The Chinese University of Hong Kong, 5/F, School of Public Health and Primary Care, Prince of Wales Hospital, Shatin, NT, Hong Kong Special Administrative Region, PR China; jlau{at}cuhk.edu.hk

## Abstract

Objective This study investigated the incidence of syphilis, HIV and hepatitis C virus (HCV), as well as factors associated with syphilis seroconversion among men who have sex with men (MSM) in Nanjing, China.

Methods A cohort of MSM was recruited by respondent-driven sampling methods. Those who were syphilis-, HIV- and HCV-seronegative at the baseline were invited to be retested at month 6. A Poisson regression analysis was performed.

Results Of the 416 participants in the study, 348 participants were HIV-, syphilis- and HCV-negative at the baseline, 250 (71.84%) of whom returned for retesting at month 6. Nine of these 250 participants had seroconverted to syphilis-positive (incidence=7.58 per 100 person-years (PY); 95% CI 2.63 to 12.53 per 100 PY), and five had seroconverted to HIV-positive (incidence=4.17 per 100 PY; 95% CI=0.52 to 7.83 per 100 PY). No HIV and syphilis coinfection and no HCV seroconversion were found. Multivariate analysis identified four statistically significant factors predicting syphilis seroconversion, including currently single marital status (RR=0.32, 95% CI 0.16 to 0.65, p<0.01), monthly income >US$300 (RR=2.68, 95% CI 1.28 to 5.61, p<0.01), self-reported homosexual orientation (RR=0.48, 95% CI 0.24 to 0.96, p<0.05) and recruitment of male sex partners mostly from gay saunas (RR=6.72, 95% CI 2.88 to 15.68, p<0.01). Conclusions The high incidence of syphilis and HIV reflects the seriousness and urgency of the HIV and sexually transmitted diseases (STD) epidemics among MSM in China. Effective interventions of syphilis treatment and prevention should target MSM with characteristics reflecting the aforementioned risk factors. • Sexually transmitted diseases • incidence • men who have sex with men • cohort study • China • gay men • STD ## Statistics from Altmetric.com ## Introduction A meta-analysis of 26 studies targeting men who have sex with men (MSM) in 12 Chinese cities reported a syphilis prevalence of 9.1%.1 Previous studies conducted in Nanjing, China showed that the prevalences of syphilis and hepatitis C virus (HCV) among MSM were respectively 26.7% and 1.0%,2 and positive syphilis status at the baseline was a significant predictor of HIV seroconversion.3 Only one Chinese study reported a syphilis incidence of 16.9 per 100 person-years (PY) among MSM in Beijing.4 This is the first study investigating factors predicting syphilis seroconversion among MSM in China. ## Methods This cohort study reports the incidence of HIV, syphilis and HCV among men (≥18 years old) having had anal or oral sex with a man in the past 12 months, who were recruited by respondent-driven sampling (RDS) in Nanjing, China. RDS was designed to recruit representative samples from hidden or hard-to-reach populations, such as MSM.5 6 RDS starts with an initial set of participants (called ‘seeds’).5 Nine seeds were recruited by a panel of researchers and peer educators. Each was given three coupons, with a unique serial number linking up the recruiter and the recruited, to recruit up to three of their MSM peers who were eligible to join the study. The recruited peers were in turn given three coupons to recruit their eligible peers to join the study. Further waves of recruitment were repeated by the recruited peers in a similar fashion until the target sample size was attained.5 Both the seeds and the recruited peers were given a phone card (worth about US$4) and a box of condoms as a token of appreciation.

The Rapid Plasma Regain Test (RPR; Beijing WanTai Biological Pharmacy Enterprise, Beijing, PR China) was used for syphilis screening, and the Treponema Pallidum Particle Agglutination Test (TPPA: Livzon Pharmaceutical Group, Zhuhai, PR China) was used for confirmation, while antibodies to HCV were tested by ELISA (Shanghai Kehua Bioengineering, Shanghai, PR China). The methodological designs, including details about HIV antibody testing, were documented in another paper investigating incidence and factors of HIV sero-conversion.3 The study was approved by the Ethics Committee of the Chinese Centre for Disease Control and Prevention. Poisson regression models were used for data analysis (SAS 9.1 for Windows).

## Results

Of the 416 participants (including the nine seeds), 19 HIV cases (4.57%),3 53 syphilis (12.74%) cases and one HCV case (0.24%) were detected at the baseline. Four participants were HIV and syphilis coinfections (0.96%), and the HCV case was neither HIV- nor syphilis-positive. Out of the remaining 348 HIV and syphilis and HCV-negative participants, 250 (71.84%) returned and were retested for syphilis and HCV after 6 months. Retested participants were more likely than drop-outs to be local residents (RR=1.41) and having attained a postsecondary education level (RR=1.26). Nine of the 250 retested participants were found to be syphilis-positive (incidence of 7.58 per 100 PY; 95% CI=2.63 to 12.53 per 100 PY), and five participants had seroconverted HIV-positive (incidence=4.17 per 100 PY; 95% CI=0.52 to 7.83 per 100 PY); no syphilis and HIV coinfection and no HCV case were detected (95% CI for HCV incidence=−2.59 to 2.59 per 100 PY).

Being never married (RR=0.32, p<0.01), having a monthly income of >2000 RMB or around US\$ 300 (RR=2.68, p<0.01), self-identified homosexual orientation (RR=0.42, p<0.05) and recruitment of male sex partners mostly at saunas (RR=5.91, p<0.01) significantly predicted syphilis seroconversion. Adjusting for marital status, income, age and residence, self-identified homosexual orientation (ARR=0.48, p<0.05) and recruitment of male sex partners mostly at saunas (ARR=6.72, p<0.01) remained statistically significant (see table 1).

Table 1

Incidence of syphilis seroconversion and factors predicting syphilis seroconversion (Poisson regression model)

## Discussion

In this cohort, the incidence of syphilis was 7.58 per 100 PY and was higher than that of HIV (4.17 per 100 PY). Important risk factors such as marital status and sourcing sex partners from gay saunas were also identified. There was only one HCV-positive detected at the baseline, and no seroconversion was found. Fortunately, injecting-drug use was not prevalent among MSM in Nanjing.

This study has the strength of using RDS rather than inconvenience sampling methods for recruitment. This cohort study has, however, a number of limitations. The retention rate of 70% at month 6 is modest though comparable with other published studies. Second, the incidence was based on the HIV-negative sample and did not include those of the HIV-positive sample obtained from the baseline. Third, the sample size may be too small to detect HCV incidence, and a few of the independent variables had a p value of <0.1. Under those circumstances where 5–10% of the participants in the reference category of a risk factor were showing sero-conversion, the effective sample size of 250 would yield the smallest detectable relative risks ranging from 2.08 to 2.58 (α=0.05, power=0.8). The results may not be generalised to other parts of China. Moreover, intervention effects due to testing at the baseline might have reduced the observed syphilis incidence.

The obtained incidence was lower than that obtained from a Beijing cohort (16.9 per 100 PY)4; it was, however, comparable with that of a Peru cohort (8.4 per 100 PY),7 but was still much higher than those obtained from other cities such as Amsterdam (2.7 per 100 PY in 2003).8 The reported incidence is consistent with the high and increasing syphilis prevalence among MSM in China.2 9

Syphilis has become a very serious epidemic among MSM in China. In this cohort, the incidence of HIV or syphilis together approaches 12 per 100 PY. Our results warn policy makers about the pressing urgency of HIV/STD prevention among MSM in China. The high incidence of syphilis would also worsen the HIV situation among MSM in China, as syphilis is a strong risk factor for HIV transmission.10

The findings also have significant implications on HIV/STD prevention services. Voluntary counselling and testing targeting MSM in China should routinely include testing for HIV, syphilis and other STDs. Integrated low-cost syphilis treatment and prevention services should be offered to MSM in China, especially those who attend gay saunas or identify themselves as being homosexual, as these MSM tend to have high syphilis incidences. Such services may attract new users who do not participate in HIV programmes, hence enhancing the coverage of HIV/STD preventive services. Future studies should investigate the relationship between perceptions on syphilis and unprotected anal sex. Such data will facilitate the design of effective programmes for condom promotion, using an STD-based approach which may be complementary to those basing on HIV prevention. Randomised controlled trials of such STD-based interventions are warranted.

### Key messages

• The syphilis incidence was high (7.58 per 100 person-years) in this men-who-have-sex-with-men cohort in Nanjing, China; no HCV seroconversion occurred in this cohort.

• Recruitment of male sex partners, mostly from gay saunas, and non-homosexual orientation are predictors of syphilis seroconversion.

• Syphilis adds to the risk of HIV infection. Integration of syphilis and HIV treatment and prevention is hence greatly warranted and should take risk factors into account.

## Acknowledgments

The authors thank XG Wu, YX Zhu and Q Wei, ZQ Pu, Heizi, Zhuimeng, WJ Xu, JQ Ji, HX Guo and other staff of the Jiangsu CDC for implementing the testing and counselling parts of this project and members of the NGO, Jiangsu Tongtian, for their assistance.

## Footnotes

• Chun Hao and Hongjing Yan contributed equally to the preparation of the manuscript.

• Funding This cohort study is financially supported by Jiangsu Provincial Technologies Research Program, No BE2009685.

• Competing interests None.

• Patient consent Obtained.

• Ethics approval Ethics approval was provided by the The Chinese Centre for Disease Control and Prevention.

• Provenance and peer review Not commissioned; externally peer reviewed.

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