HIV and syphilis prevalence trends among men who have sex with men in Guangxi, China: yearly cross-sectional surveys, 2008–2012

The global HIV epidemic continues to expand disproportionately among men who have sex with men (MSM) [1]; the prevalence ranging from 3-25% [1, 2]. High HIV prevalence has been demonstrated among MSM in other regions of Asia [3], such as India (14.7%) and Thailand (24.6%). Sentinel surveillance in China in 2012 showed that the national HIV prevalence among MSM was 6.7% [4], fully 134 times higher than 0.05% in China’s general population [5]. Data from the 2011 surveillance system report indicate a much higher prevalence among MSM in some cities: 16.3% in Chengdu (Sichuan Province in the southwest), 12.5% in Zhengzhou (Henan Province in the center), and 10.3% in Harbin (Heilongjiang Province in the northwest) [6].

Although heterosexual transmission is mainly responsible for the spread of HIV in recent years in China, the prevalence of HIV among MSM is rising at an alarming rate [7] and the epidemic is in a rapid expansion phase [1]. Sentinel surveillance data in five provincial capitals in China showed that the percent of HIV-positive MSM had increased annually from 0.9% in 2003 to 6.3% in 2011 [6]. Of the newly reported HIV/AIDS cases nationwide, the proportion of MSM cases climbed from 15% in 2011 to 21.1% in 2012.

Syphilis likely increases the sexual transmission efficiency of HIV [1, 8–10]. In China, national surveillance data from 2005 through 2011 showed syphilis prevalence among MSM was around 10% [6] in some provincial capitals. The largest study [7] of MSM (n = 47,321) and HIV and syphilis prevalence in China showed a correlation between HIV and syphilis infection, similar to findings from Chinese cohort studies [11, 12]. There are a limited number of studies reporting HIV and syphilis prevalence trends among MSM in China, restricted to five other provincial capitals [6] or cities experiencing the highest HIV prevalence among the population [6, 13, 14].

Guangxi Province is located along a drug trafficking route, which originates from the Golden Triangle, passes through the northern provinces of Vietnam, and finally into Hong Kong and the rest of the world [15]. As the province with the second highest estimated number of people living with HIV/AIDS among 31 provinces in China in 2011 [5], Guangxi has been the focus of study for its heterosexual and needle sharing transmission routes [16]. In contrast, the HIV epidemic among MSM in Guangxi has not been well-studied though surveillance data suggest a growing contribution of MSM to the HIV epidemic. In this study, we analyzed five consecutive years’ of HIV and syphilis prevalence trends and risk factors among Guangxi MSM. The results of this study will assist in guiding HIV-related prevention and intervention efforts to effectively control the HIV epidemic in this province and beyond.

There were a number of statistically significant changes in demographic characteristics over the five-year period (Table 1). The year 2011 (the year with proportionately fewer internet-recruited men) had apparent anomalies for both HIV and syphilis prevalence, as well as some socio-demographic indicators. Linear trends over time were typical, with the exception of age and current marital status. A trend analysis of every other sample showed that most variables had similar P-values under both testing methods (results not shown).

MSM >25 years of age accounted for the largest subgroup in 2011 (71.4%) alone, but was near 60% in the other years. Also different in 2011 alone was the proportion of men who were currently married: 38.6% in 2011 compared to about 20% in the other years. Differences were also noted in the proportion of men who were officially registered Guangxi residents, varying from 83.5% in 2008, to 90.2% in 2011, and 87.8% in 2012. MSM having received education of senior high school or higher were fewer in earlier than in later years (Table 1).

Condoms were reported to be used more frequently in later years. Having sex with a male without a condom at the time of last sexual encounter in the past six months decreased from 41.9% in 2008 to 19.7% in 2011 and 23.2% in 2012. This salutary trend was also noted for MSM who never used a condom with a male in the past six months, decreasing from 15.6% in 2008 to 5.4% in 2012. MSM who had a sexual encounter with a female in the past six months accounted for 20-30% of the sample in all years except 2012 (14.6%). In the subset of MSM who also had sex with women, having sex without a condom at the time of last sexual encounter with a female in the past six months decreased slightly from 60.7% in 2008 to 53.7% in 2012, though the 2011 data was highly disparate (19.9%). Men who never used a condom with a female in the past six months decreased from 43.6% in 2008 to 36.0% in 2012, with an atypical nadir of 10.2% in 2011. In addition, condom use with men in the last sexual encounter in the subset of MSM >25 years of age increased from 52.3% in 2008 to 83.1% in 2011and 76.7 in 2012, while in younger subset increased modestly from 65.5% in 2008 to 71.1% in 2012 (not shown in tables).

History of ever abusing drugs remained at a very low level and decreased from 1.7% in 2008 to 0.2% in 2012. The percentage of participants receiving peer education in the past year increased consistently from 45.1% in 2008 to 66.6% in 2010, falling to 53.3% in 2012. MSM reporting having been tested for HIV in the past year increased from 30.8% in 2008 to 60.3% in 2011 and 54.3% in 2012.

In the subset of men who had sexual intercourse with a woman in the past six months, condom use with men was significantly associated with condom use with women. Fully 81.9% who used a condom in their last sexual encounter with a female also used a condom in their last sexual encounter with a male, while 88.6% who used condoms with females in the past six months also used condoms with males.

In this study, we found significantly rising trends of both HIV and syphilis prevalence among MSM in the four largest cities in Guangxi Province, China. Similar serial cross-sectional studies reported from China are few and often do not provide multi-year data [13, 14, 19]. Our finding of the rising prevalence exists in the context of increasing self-reported condom usage over time, similar to the finding of a recent meta analysis [20] of HIV risk reduction intervention studies among Chinese MSM. This is plausible because as background prevalence increases, MSM may have a higher risk of encountering an infectious partner, even if their own risk behaviors diminish somewhat; that is, the reported increased condom usage were not sufficient to offset the effects of elevated risk of infection [21].

The value of serial cross sectional surveys is apparent: HIV prevalence almost tripled over just five years, although absolute Guangxi rates for MSM were a bit lower than that estimated nationwide [5] from 5% in 2008 to 6.7% in 2012 or other selected cities [6, 9, 12] in China. The upward trend is similar to that seen in some other Chinese cities and nationwide in time periods proximate to those in our study [6, 13, 19]. The epidemic among MSM in Guangxi may be more serious than our findings indicate due to dual stigma of male-male sexual behavior and HIV infection. Additionally, HIV/AIDS prevention programs targeting MSM were only first carried out in Guangxi in 2006 which is later in comparison to other provinces or municipalities reporting a higher prevalence among MSM than Guangxi [20]. Over time, the MSM population in Guangxi may likely continue to disproportionally contribute to new HIV and syphilis cases if there remains a dearth in targeted prevention strategies. Guangxi has a significant opportunity to control the HIV epidemic among MSM before becoming more serious as in other areas in China.

In our study, MSM who reported no sex with women in the past six months were more likely to be HIV infected than those who had. This is similar to the finding reported in a study of southern African MSM engaging in heterosexual intercourse in the previous six months [22]. The men who report having sex with both men and women in Guangxi may play a role as a bridge of transmitting HIV to their female sex partners, but the risk is lower than among men who are exclusively having sex with men.

Our study found HIV prevalence to be much higher in MSM with current syphilis and syphilis was shown as a probable risk factor for HIV infection. That syphilis may facilitate HIV transmission among MSM is not surprising, and reinforces the need for aggressive public health measures to combat sexually transmitted infections [20, 23, 24].

The syphilis prevalence shown in our study was somewhat lower than that reported in previous Chinese studies: a meta-analysis [25] and the largest study [7] of HIV and syphilis infection among MSM in China reported syphilis prevalence of 9.1% and 11.8% respectively. However, syphilis prevalence increased year by year, notably among MSM who were older, married, officially registered local residents, less educated, and had a sexual encounter with a female in the past six months--all of which probably demonstrated an increasing risk of syphilis transmission from men having sex with both sexes to their female and male partners. Even though the probability of HIV transmission is much higher through unprotected receptive anal sex than unprotected vaginal sex [1], this finding suggests a possible increase in risk of HIV infection among the female sexual partners of the MSM. Therefore, to prevent further HIV transmission among MSM and their female sexual partners, timely treatment and prevention of syphilis warrants more attention. MSM >25 years are a key sub-population of concern for syphilis intervention [7].

Our finding that suboptimal MSM condom use was the rule with females was also demonstrated in a systematic review [26]. HIV interventions for MSM seldom promote condom use with their female sexual partners [27], accompanied by the traditional thinking that condoms with females were used mainly for contraception rather than an HIV/STD prevention strategy [28]. Loyalty and trust also facilitate sex without a condom [29]. Most MSM who used a condom with a female also used a condom with a male. HIV interventions among MSM should highlight the importance of condom use during any sexual encounters with either female or male partners.

The rising trend of condom use among the MSM population with male in the last sexual encounter in the five years of the study was more pronounced among MSM >25 years. This could indicate that MSM ≤25 years who are more sexually active are more likely to omit condom use or intentionally take risks, despite their knowledge about HIV transmission and prevention practices. This might indicate that the attitude toward HIV infection among the younger generation is changing: HIV is no longer viewed as a death sentence due to the knowledge of a long latent period and successful results with anti-retroviral treatment (ART). Also, to the young MSM, the desire for immediate gratification may be prioritized over health at the moment of sexual intercourse, especially if sex without any barriers is a replacement for lack of intimacy and emotion for them.

Demographic and behavioral characteristics in 2011 were significantly different from those of other years. Since there was a one year suspension of financing from the Global Fund [18] in 2011, less outreach was conducted by local CBOs among young MSM, particularly through the internet-based gay community where CDC staff have little access. That there was an asymmetry in recruiting in the 2011 year only suggests that trends may be distorted by alternative recruitment biases in that year.

HIV and syphilis prevalence increased significantly in the subcategory of MSM who had not tested for HIV in the previous year, while the trend was not substantial or did not exist in the subcategory of MSM who had tested for HIV in the previous year. HIV testing is a crucial strategy to effectively prevent HIV transmission among MSM [30] as early identification of infection enables timely treatment and increases knowledge of HIV status in order to prevent infecting others [31]. Large scale HIV testing also helps and contributes to increasing awareness of HIV prevention by promoting safe sexual behaviors including condom use, and it has shown to reduce HIV incidence rates among MSM [32–34]. Frequent HIV testing among MSM results in increased condom use and other protective sexual behaviors [35]. The testing rates in our study surpassed the national level in 2011 of 50.4% [36], but remain too low. This calls for more interventions to expand HIV testing and promote regular testing among the MSM population in the province.

Both the HIV and syphilis epidemics have expanded among MSM in Guangxi Province. Our study results illustrate the urgency for provincial HIV prevention and intervention strategies among this at risk population, including evidence-based policy decisions for program expansions. Comprehensive HIV prevention and intervention, supported and funded by local government, should include MSM-friendly HIV testing, syphilis treatment and prevention, peer education, CBO engagement and other HIV intervention measures for expanding HIV testing and condom use, and must be continuously strengthened for the MSM population in order to curb HIV epidemic in the province.