What is the potential for bisexual men in China to act as a bridge of HIV transmission to the female population? Behavioural evidence from a systematic review and meta-analysis

Although blood transfusions and injecting drug use had historically been the dominant risk factors associated with HIV infection in China, sexual transmission has become the main route of HIV transmission in recent years. Among the 48,000 (41,000-55,000) Chinese people newly diagnosed with HIV in 2009 [1], 42.2% and 32.5% were due to heterosexual and homosexual transmission respectively [1, 2]. Notably, HIV prevalence among men who have sex with men (MSM) in China had increased rapidly from 1.4% to 5.3% between 2001-2009 [3] and this increasing trend is likely to continue in coming years.

The rapid increase in HIV prevalence among Chinese MSM was probably due to many factors including the increasing numbers of men who engage in homosexual sex; multiple male partners; and high levels of unprotected anal intercourse. A recent systematic review and meta-analysis study showed that just over one-third of MSM report consistent condom use with their male sex partners in the last six months and only 20% consistently used condoms with their regular male partners [4]. It has also been reported that sexually active Chinese MSM report having an average of six to seven male sexual partners in the last six months and 18% of them had participated in group sex in the past 12 months [5].

Due to traditional cultural and family values, Chinese MSM often marry to conceal their homosexuality from family and friends. It was estimated that approximately 50-70% of MSM have had sex with females in their lifetime [6‐10] and 70-90% will eventually marry [11, 12]. This suggests that bisexual behaviours among Chinese MSM are common. As they are often the only son in their families, as a direct result of China's one-child policy, they also face their parents' expectation to have children to continue the family line.

Chinese MSM tend to have low rates of condom use with their female partners [13]. Given the rapid increase in HIV prevalence among Chinese MSM, their bisexual behaviours could potentially act as a bridge of HIV transmission to the general population [5, 9, 14‐16]. In this study we conducted a systematic review of studies on bisexual behaviours among Chinese MSM in both Chinese and English literature to examine the extent to which bisexual behaviour is common among Chinese MSM.

Our review, coupled with meta-analyses for specific questions, summarised evidence of bisexual behaviours of Chinese MSM. These included the age of MSM who are currently married; the percentage of Chinese MSM who had female sexual partners in last six months; the percentage of MSM who are currently married; and the condom usage rate among MSM with their female sexual partners at the last sex act or in the last six months. Different types of partnerships, including regular, non-commercial casual or commercial, were also distinguished in our review and analysis. In comparison with a recent published systematic review on behavioural studies among Chinese MSM [17], this study employed a meta-analysis approach with a strong focus on the condom use with different types of female partners. In addition, this study substantially extended the previous analysis to include both English and Chinese literature. Our study provides more detail insights and quantifiable results on the bisexual behaviours among MSM in China.

Our meta-analysis showed that approximately 17.0% of MSM are currently married to a female in China, which is consistent with another recent review which reported an average of 17.5% [17]. In contrast, the percentage of MSM who are married in most Western developed countries is much lower. Only 1.5-3.0% of MSM are currently married to a woman in the United States [31‐33] and 7.9% in Australia [34]; however, higher rates of marriage among MSM were observed in some other developing countries (for example, 35-42% in India [35, 36]). There is generally greater acceptance and legitimacy of gay identity, gay marriage or cohabitation relationships and less social stigma, discrimination and family pressure in developed countries. Previous studies showed that only 11-17% of Chinese MSM disclosed their homosexual sexual orientation to their wives [37, 38] and 1% of them disclosed to their children [37]. Due to the high prevalence of bisexual behaviours among MSM in China, this group is very likely to facilitate HIV transmission to the female population to a much greater extent than occurs in most countries where HIV predominantly affects MSM. Our review provides a timely synthesis of current evidence of bisexual behaviours among MSM in China, which could inform the implementation of effective intervention programs.

Previous available studies indicated that Chinese MSM had an average of 1-5 female sexual partners in the last six months [7, 8, 39, 40]. Additionally, we estimated that a higher proportion (83.9%) of married MSM have had female sexual partners than unmarried MSM (23.9%). However, only 16.2% and 28.5% of married and unmarried MSM have had consistent condom use with their female partners in the past six months, respectively [5]. Fifty-eight percent of married MSM had concurrent male and female sexual partners in last six months, hence putting their wives at a greater risk of HIV infection [41].

Partnership type had strong influences on condom use of MSM. In general, condom usage at last sex act between MSM and overall female sexual partners was estimated to be 41.4% (95% CI: 35.5-47.5%); but only 25.6% (95% CI: 23.0-28.4%) of MSM used condoms consistently in the last six months. A study in 2004 found that 31.8% of MSM had regular female sex partners, 6.0% had non-commercial casual female sex partners and 4.5% had commercial female sex partners [14]. Among three specific partnership types, consistent condom use was estimated to be the greatest in commercial partnerships (55.8%, 95% CI: 41.4-69.4%), followed by non-commercial casual partnerships (39.0%, 95% CI: 28.8-50.3%) and regular partnerships (23.3%, 95% CI: 11.2-42.1%). In general, reasons of low condom use with partners mainly included: emotional and physical sensation, availability of condoms, and loyalty and trust [5, 25]. In addition, sexual abuse was common in China. It was reported that 30% of wives were abused by their homosexual or bisexual husbands to relieve their mental pressure from social stigma and discrimination [42]. This indicated that regular sexual partners of Chinese MSM were often not empowered to negotiate for protected sexual intercourse with their male partners.

Several limitations of our study must be noted. First, the selected studies in this review recruited MSM participants predominantly from major urban Chinese cities. Bisexual behaviour such as MSM who have female sexual partners and condom usage may be significantly different between urban and rural regions. Second, based on our search criteria, we could not identify any studies on condom use at the last sex act in the South Central region or consistent condom use in the last six months in the Northwest region. Our pooled estimates of condom usage may not be representative for the entire MSM population in China. Third, very few studies reported bisexual behaviours stratified according to their marital status and partnership types. This substantially limited the strength of meta-analysis in these cases. Fourth, due to insufficient description of some studies, we were unable to classify whether the sexual contacts between MSM and female was penile-vaginal intercourse, penile-anal intercourse or oral sex. Male-to-female anal contacts often had a higher risk of HIV transmission than vaginal contact [43]. Due to reproductive reasons, MSM might not use condoms during vaginal sex but they may use condoms in anal sex. Since vaginal intercourse was more common than anal intercourse in male-female partnership, we assumed all condom usage estimates were associated with vaginal sexual intercourse. Fifth, due to limited number of studies available, we were unable to investigate the associations between the age of MSM and consistent condom use in different geographical locations and with different types of partnerships. For the same reason, the contribution of age to the heterogeneity of the studies could not be investigated. Sixth, our study only addressed the overall MSM population; specific populations such as male sex workers ('money boys') were not included in this study. In China, 'money boys' have become one of the emerging high-risk sub-populations in gay communities in recent years [44]. However, very few epidemiological and socio-behavioural studies have focused on this population to date. Limited studies indicated that Chinese 'money boys' are usually younger than the overall MSM population and unmarried [38, 45‐47]. An estimated 71% of Chinese money boys had 1-3 male clients and 11% had more than 10 clients per week [38]. Approximately 27% of money boys had female clients in last six months [48]. Unprotected sex with both male and female clients was very common (59.4% and 55.6%, respectively) [38]. A survey in 2007 found that 43% of the money boys had female sexual partners but only 36% reported consistent condom use in the last six months [45]. Money boys were more likely to move between major cities to earn extra income from the commercial sex industry and hence they may be a particularly important population for transmitting HIV in different geographical locations [49]. These characteristics may result in the population of money boys becoming the core group for HIV transmission among MSM and the general population [44, 45]. Further investigations are necessary to understand the behaviours of this sub-population in China.

Moderate to high heterogeneities were observed in the conducted meta-analyses. Given the limited details of study information, we only investigated five potential study characteristics associated with the heterogeneity in the meta-regression model. Recruitment method was found to be the major study characteristic associated with high heterogeneity in the stratified meta-analyses (associated with marital status, percent of MSM who had female sex partners and condom use at last sex act). Furthermore, we postulate that several other factors, including geographical Chinese regions, age of MSM and migrant status, may also be associated with the heterogeneity observed, although these factors could not be assessed by meta-regression due to limited data. Other study variables such as the quality of interviewers, questionnaire or marital status of MSM were not reported in the collated studies but may also contribute to the heterogeneities across studies.

MSM is a population highly susceptible to the emerging HIV epidemic in China [9, 50, 51]. Further studies on specific sub-populations of MSM, such as money boys, transgender MSM, MSM who inject drugs and bisexual MSM, are necessary to understand their sexual behaviours and contribution to the HIV transmission within and beyond the MSM population. Currently, there are no specific public health interventions targeting bisexual MSM in China. Our results indicate that MSM recruited at MSM venues were more likely to be currently married, had sex with females in last six months, and had unprotected sex with females. Harm-reduction interventions such as distribution of condoms and lubricants to bisexual MSM may be implemented at MSM venues and further expanded to the wider communities. Given the low condom usage between MSM and their regular female partners, public health intervention strategies should particularly target married MSM and their regular female partners. Sexual behaviour and condom use rates with different partnerships should be clearly identified in the future social-behavioural surveys in order to understand the bisexua behaviour among MSM and to curb the spread of HIV transmission from MSM to the overall female population.

Men who have sex with men are a population that is highly susceptible to the rapid spreading HIV infection in recent years. Our study shows that a substantial proportion of MSM is currently married or has had sex with a female in the past six months. Consistent condom use rates are low among partnerships with regular females. Our findings imply that the general female population, as regular partners of MSM, has a high risk of contracting HIV infection that are bridged from their bisexual male partners. Scale-up of the harm-reduction interventions and health educations for bisexual MSM and their female partners are necessary to halt the further spread of HIV into the general female population.