Abstract
Summary
Bisexual men (men who have sex with men and women) are potential epidemiological bridges responsible for the spread of HIV and other sexually transmitted infections from men who have sex with men only to the heterosexual population. We aimed to estimate the prevalence of syphilis and HIV and the factors associated with syphilis infection among men who have sex with men and women and men who have sex with men only from Shijiazhuang, China. In 2011–2013, a cross-sectional cohort of 427 men who have sex with men was recruited by a snowball sampling method and tested for syphilis and HIV. Chi square and logistic regression were performed to identify syphilis risk factors. Among the 427 men who have sex with men, 71 (16.6%) cases were syphilis-positive and 16 cases (3.7%) were HIV-positive. The proportions of men who have sex with men and women and men who have sex with men only in the total sample were 31.4% and 68.6%, respectively. Men who have sex with men and women exhibited double the syphilis prevalence of men who have sex with men only and were more likely to practice insertive anal sex. Higher education level, being married, having more male partners, and both receptive and insertive anal sex roles were associated with syphilis among men who have sex with men and women. Residing in suburban areas, being married, being HIV positive, and an absence of desire to change sexual orientation were associated with syphilis among men who have sex with men only. Therefore, men who have sex with men and women represent an important sub-group in the syphilis epidemic and further interventions should be developed to reduce risk among different sub-sets of men who have sex with men.
Keywords
Introduction
Men who have sex with men (MSM) are one of the groups at high risk of sexually transmitted infections (STIs), particularly syphilis and HIV. In China, MSM have a higher syphilis prevalence of 14.6% compared to other selected high-risk groups such as incarcerated female sex workers (12.5%) and drug users (6.8%). 1 Moreover, Chinese MSM exhibit an approximately 45-fold higher risk of acquiring HIV than other men in the heterosexual population. 2 Approximately 7.3%, 11.0%, 14.7%, and 17.4% of people with HIV/AIDS living in China were infected via unprotected man-to-man sexual transmission in 2005, 2007, 2009, and 2011, respectively; this finding reflects a rapid HIV expansion phase among MSM in recent years. 3 The percentage of new HIV infections attributed to MSM sex increased from 12.2% to 32.5% between 2007 and 2009. 4 In 2011, a meta-analysis of 71 studies targeting MSM in 24 provinces of China reviewed a pooled syphilis prevalence that increased from 6.8% during 2003–2004 to 10.4% during 2005–2006 and then to 13.5% during 2007–2008; in the same period, HIV prevalence also increased from 1.3% to 2.4% to 4.7%, respectively. 2 Therefore, factors associated with increasing incidence of syphilis and HIV among MSM in China should be elucidated.
In contrast to men who have sex with men only (MSM-only), men who have sex with men and women (MSMW) represent a specific target population in which to explore the spread of syphilis and HIV because of the inherent bridging aspect of their sexual behaviours. Approximately 95% of 5–10 million MSM in China have had at least one male sexual partner within a six month period. 5 Furthermore, MSM in China are generally married and have engaged in concurrent sexual relationships with men and women. In the United States, MSMW are five times more likely to be HIV positive than men who have sex with women exclusively; MSMW also practice unprotected sex with their female partner to a greater extent than with their male partners. 6 In a similar study on HIV risk behaviour in China, the rates of unprotected sex are significantly higher among married MSM than unmarried MSM. 7 Thus, MSMW who are unaware of their STI status may place their female partners at high risk. However, most studies on male same-sex behaviour have focused on MSM-only, and only few studies have targeted MSMW as a distinct sub-group in China.
Shijiazhuang, the capital city of Hebei Province in northern China, has a population size of 9.97 million. However, little is known about the prevalence of syphilis and HIV among MSMW in this city. In this study, a cross-sectional survey was conducted in Shijiazhuang to estimate the prevalence of syphilis and HIV infection. Related sexual behaviours were also dentified to evaluate the risk factors associated with syphilis and HIV infection among MSMW. Furthermore, a sub-group of MSM-only was evaluated for comparison.
Methods
Research participants were recruited from December 2011 to February 2013 by a non-governmental organisation by using the ‘snowballing’ method. To maximise the distribution of study information to the MSM community, we used multiple recruitment methods, including MSM-targeted website advertisement and distribution of flyers at MSM-frequented venues (e.g. MSM clubs, bars, parks and bathhouses). Inclusion criteria for eligibility in the survey included the following: at least 18 years old; had lived in Shijiazhuang for more than 12 months; identified as MSM-only or bisexual; and had performed anal or oral sex with another man in the past 6 months. 8 Participants completed an interviewer-administered questionnaire facilitated by a trained health professional in a single private room. The questionnaire included self-reported socio-demographic characteristics (age, education, habitat, marital status and sexual self-identity); sexual behaviour (any steady male partners, the number of male partners, condom use with male partners, usual anal sex position). Blood specimens were collected from participants and sent to the HIV/STI testing laboratory of Shijiazhuang CDC for serological tests for syphilis and HIV. 7 Referral services were provided to all HIV- or syphilis-positive cases. Analyses were conducted using SPSS 18.0 (SPSS Inc., Chicago, IL, USA). The association of demographic and behavioural characteristics with syphilis serostatus was evaluated using Pearson's Chi square test for categorical variables or Fisher's exact test when the expected values for these variables were ≤5. Covariates were included in the multivariate model based on theoretical and statistical considerations. Covariates were entered into logistic regression model if p value was ≤ 0.1 in the preliminary bivariate analyses.
Results
Characteristics and HIV/syphilis infection between men who have sex with men and women (MSMW) and men who have sex with men only (MSM-only).
Approximately 65% of MSMW and 53.3% of MSM-only reported that they lived with a steady male partner. A higher proportion of MSMW (76.9%) consistently used condoms with male partners than MSM-only. Among MSMW who had ever performed anal sex with men, 27.5%, 51.9%, and 20.6% reported that they took a receptive role, insertive role, and both receptive and insertive roles, respectively. Among MSM-only these percentages were 46.4%, 33.2%, and 20.4%, respectively. A higher proportion of MSM-only were likely to act as a receptive partner only than MSMW; by contrast, a higher proportion of MSMW were likely to act as an insertive partner only than MSM-only (Table 1).
Factors associated with infection among men who have sex with men and women (MSMW) and men who have sex with men only (MSM-only).
OR: odds ratio; CI: confidence interval.
p < 0.05.
p < 0.01.
Discussion
In this survey, the syphilis prevalence of the sample was 16.6%. This result is higher than the MSM prevalence observed in Indonesia (4.3%), India (7.4%), and the US (7.8%);9–11 by comparison, this result is very similar to the prevalence in several Chinese cities, including Beijing (19.9%), Guangzhou (17.5%), Shenzhen (21.1%), and Harbin (18.0%),8,12,13 with a high rate of syphilis infection. Furthermore, syphilis is a serious epidemic among MSM in China. Important interactions have also been observed between syphilis and HIV. This interaction is attributed to a biological mechanism in which mucosal integrity is disrupted because of syphilis-induced ulceration; the disrupted mucosal integrity then provides an entry point for the HIV virus. This ulceration may also result in the local influx of CD4 + lymphocytes, thereby increasing the number of HIV target cells. 10 In an investigation in San Francisco, 63% of MSM diagnosed with syphilis over a 2-year period were co-infected with HIV. 14 Therefore, our findings suggested that the relatively high prevalence of syphilis may increase HIV incidence among MSM in Shijiazhuang. Moreover, the obtained HIV prevalence in this survey (3.7%) is the lowest among other cities, such as Beijing (9.9%), Guangzhou (5.2%), Chongqing (12.5%), and Chengdu (39.3%).7,13,15
Among the total number of enrolled MSM, 31.4% identified themselves as MSMW; this number is higher than that observed in a 2013 MSM assessment in four cities in China (17.9%). 4 MSMW present a low rate of behaviours commonly associated with syphilis transmission risks, such as inconsistent condom use with male partners and frequent male partner change; however, syphilis prevalence among MSMW is approximately double that of MSM-only. In this study, the higher level of insertive anal sex by MSMW may be a contributor to this disparity. Moreover, having sex with women increases the likelihood of unprotected insertive anal intercourse with men; likewise, this condition likely enhances syphilis infection risk. 16 Chinese society, similar to many Asian cultures, emphasises the importance of marriage and traditional family structure. A study in Guangzhou and Chengdu in China revealed that more than half (59%) of 600 MSMW were married and 29% of these married MSMW had a girlfriend. 7 The insertive role in anal sex allows MSMW to exhibit a ‘masculine’ identity, which is equivalent to a heterosexual function. In addition, an investigation in four cities in China has shown that MSMW are more likely to act as insertive partners than MSM-only (33.7% versus 25.4%). 8 This discordance between behaviour and sexual orientation suggests that MSMW may be less likely to fully disclose their MSM behaviour to other people, including their female partners. 17 Thus, MSMW might serve as bridges enabling spread of syphilis from MSM to the heterosexual population. 18 For this reason, further research should evaluate whether sex with a bisexual man is a major risk factor for syphilis infection among women.
MSM-only are more likely to acquire HIV than MSMW, considering that the former engages in risk behaviour (unprotected receptive anal intercourse etc.) not performed by the latter.6,9 However, our stratified analysis results indicated that HIV prevalence was not significantly different between MSMW and MSM-only in Shijiazhuang. However, this result could be mainly attributed to our limited sample size.
Our results also demonstrate that the correlates of syphilis infection may differ between the two sub-groups. In MSMW, the correlates of syphilis infection were high education level and married status, which suggested that these demographic characteristics are protective factors against syphilis infection. The risk factors for syphilis infection included having more male partners within six months and performing both receptive and insertive anal sex with men. As such, interventions should be developed to decrease the number of male partners and promote condom use among MSMW. However, married status is a risk factor for syphilis infection in MSM-only. Similar to our results, the findings from a previous study of Chinese MSM showed that married status is a significant risk factor that increases the risks of syphilis infection by 50% compared with MSM who were never married. 12 Among MSM-only, residing in suburban areas is another risk factor for syphilis infection. Compared to an urban residence, the suburban area represents a lower socio-economic status, which has generally been linked to HIV and STIs at a macro level. Furthermore, HIV status, and an absence of desire to change sexual orientation (to one without the MSM component) are risk factors associated with syphilis infection among MSM-only. Therefore, these differences should be considered in developing effective interventions and strategies to control the spread of syphilis among MSM and from MSM to the general population. 8
This study is subject to a number of limitations that should be considered when interpreting our results. First, the recruited participants may not represent the general MSM population because of the limitation of sampling methods. Moreover, MSM in China remain highly stigmatised and inconspicuous; MSM may be unlikely to opt for public health services and undergo voluntary testing. 15 Therefore, a potential selection bias could not be excluded. Second, some bisexual men may have been misclassified as MSM-only. Approximately 29.8% of MSM-only reported that they were married. However, this study aimed to assess recent bisexual behaviour; hence, most sexual behavioural questions enquired about recent events. 17 Third, similar to information presented in other relevant studies, our data were self-reported by the participants; as a result, biases associated with accuracy or completeness of reporting might be present. However, these limitations can be minimised by using appropriately-worded questions, realistic recall timeframes, and appropriate selection of the target population. Finally, a cross-sectional study design exhibits inherent limitation that infers temporal association. As such, longitudinal studies should be conducted to further investigate syphilis-related risk behaviours among MSMW and MSM-only.
Footnotes
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by grant from the Hebei Provincial Technologies Research Program (Grant No. 14277709D).