High prevalence of HIV infection and unprotected anal intercourse among older men who have sex with men in China: a systematic review and meta-analysis

Human immunodeficiency virus (HIV) infection and other sexually transmitted infections (STIs) continue to disproportionately affect men who have sex with men (MSM) in China [1]. A study conducted in 61 cities in China between February 2008 to September 2009 found that 4.9% of MSM were infected with HIV [2]. According to a report from the Chinese Ministry of Health, it estimated that there were approximately 780,000 people living with HIV/ AIDS in 2011 in China [3], 17.4% of the estimated HIV/AIDS cases were attributable to male-to-male sexual contact. Sentinel surveillance data have shown an increasing trend of HIV infection among MSM, from 2.0% in 2007 to 6.3% in 2011 [4].

China has the largest number of the elderly in the world [5]. According to a report from the China National Committee on Ageing, there were an estimated 185 million elderly people (aged 60 years or older) in China by the end of 2011, and about half are men [6]. Chinese elderly people were generally not considered as a population at high-risk for HIV infection [7]. Whereas, among nationally reported HIV/AIDS cases, the proportion of total cases accounted for by the 50–64 age group increased from 1.6% to 13.8% in 2000 and 2011, respectively [4].

As the number of new HIV cases amongst the 50+ age group increased noticeably in recent years, there have been a few studies exploring the reasons in recent years, and shown that engaging in commercial sexual activities after their retirement is a major factor for the increased HIV epidemic among the older men [8, 9]. As MSM has become a major at-risk group, it is a concern about HIV among older MSM in China. However, studies on HIV prevalence and unprotected anal intercourse (UAI) among Chinese older MSM are relatively few and generally have small sample sizes [7, 10, 11]; it will be helpful for assessing the magnitude of HIV epidemic and risk behaviors in this age group through summarizing the findings from these studies. We performed Meta analysis of the prevalence of HIV, syphilis and unprotected anal sex (UAI) in the last 6 months among older MSM in China.

To our knowledge, this meta-analysis provides the first quantitatively synthesized estimates of the prevalence rates of HIV, syphilis and UAI among older MSM in China. The summarized estimates were HIV (11.6%; 95% CI: 8.0%-16.6%), syphilis (23.0%; 95% CI: 15.8%-32.3%) and UAI (79.5%; 95% CI: 72.7%-84.9%). Our meta-analysis also demonstrated that the trend of HIV prevalence among older MSM has substantially increased in the past decade. Besides, our analysis also provided evidence contradictory to a widely accepted assumption that young MSM was at higher HIV risk than older MSM [35, 36]. The overall and stratified estimates provide useful formation for epidemiologic modeling of HIV transmission among older MSM and for allocating resource for targeted prevention interventions.

HIV prevalence was higher among older MSM than their younger counterparts (11.6% vs. 5.2%), and is higher than average prevalence (4.9%) among nearly 50,000 MSM in a nationwide survey during 2008 and 2009 [2], and is also higher than the average prevalence among national sentinel sample (6.3% for HIV, and 10% for syphilis) [3]. Firstly, it is possible that older MSM had longer durations of exposure to HIV source. Secondly, HIV testing as increased HIV prevalence may be to some extent due to increase testing rate since HIV testing among Chinese MSM has been increasing over the decade [37], then antiretroviral treatment could also contribute to a higher prevalence among older MSM as they just age with their infection. In addition, UAI among older MSM was also more common than their younger counterparts, which might partly explain the higher HIV prevalence among older MSM. HIV prevalence among older MSM in China is higher than older MSM in European countries such as Sweden (3.8%) and Germany (2.6%), but was much lower than those in four major cities in the United States (19%) [38, 39].

Syphilis infection is a good surrogate for high risk sexual behaviors. A high prevalence of syphilis (23.0%) among Chinese older MSM suggested that these men may have heavily engaged in unprotected sex, which could facilitate HIV spread in this group, and screening and treating syphilis could be an effective way prompting HIV detection [40]. Syphilis itself would also act as a cofactor for HIV acquisition [41–44]. Due to the mode of sexual transmission, single public health intervention campaign can be designed with the objectives of preventing HIV and preventing syphilis. Although UAI is common among older MSM, HIV has not yet reached the high level as syphilis. We interpret this as a significant opportunity to save lives through increasing public health intervention efforts [2].

We also found that a sizeable percentage (79.5%) of older MSM had engaged in UAI with male partners. This is an important public health concern, given the high prevalence of HIV and STIs among older MSM in China. The UAI prevalence was higher among older MSM than among their younger counterparts, which was generally consistent with several recent studies in China [11, 45], but it is contradictory to the studies in the United States [46].

Subgroup analysis showed the highest HIV infection rate in southwest China (16.4%), which was consistent with prior studies [47, 48].

Older MSM living with HIV may bring more medical challenges. The elders are more vulnerable to side effects of antiretroviral drugs [49]. Aged people are facing problems of diabetes and heart disease, whereas research suggests that antiretroviral drugs contribute to high cholesterol levels and hamper insulin production, thus increasing the risk of health problems [50]. Besides, significant HIV epidemic among older MSM is not only a medical issue but also a social problem. Due to traditional Chinese values, the majority was married, but they continued engaging in extramarital sex with their male partners. Studies have shown that they are less likely to take precautions [51], even though they know HIV risk from unprotected sex [52], because they have misconception that HIV/AIDS is a disease of young people [53]. What is worse, some of them hold opinion perception that the latent time from infection to development of AIDS could be up to ten years, and they may die of other diseases, so they do not even care about HIV/AIDS [54]. Little HIV prevention work has focused on older MSM, partly due to the widespread belief that older MSM are not sexually active [46]. Our analysis provides strong evidence of the need for interventions in this subgroup. Formative work is needed to determine appropriate approaches for this population. Some of the older MSM are likely to engage in bisexual behaviors, which may play a bridging role in the spread of HIV and other sexual transmitted diseases from this high-risk group to the general population [55]. Moreover, the alarming spread of HIV among older MSM is fuelled by an ongoing, persistent stigma against homosexuality in China [56]. This may lead to a result that older MSM hide their sexual identity, thereby increasing the difficulty of reaching them by prevention interventions. It is critical to reduce stigma against homosexuality and mitigating discrimination against homosexuals among the general population.

Our meta-analytic findings should be viewed within the context of the methodological limitations of the primary studies. Our findings are based on cross-sectional data, which provide snap shots of prevalence of HIV, syphilis, and UAI at the time of data collection. The included studies are heterogeneous in term of sample size; recruitment setting, sampling method, study year, and study location. For example, some studies recruited participants through RDS or snowball sampling rather than random sampling, and these sampling approaches may have selection bias [40]; More studies were conducted in east China, and few in west China. Therefore, the summary estimated may not represent the national sample. Small sample size may also restrict the statistical power in subgroup analyses, there are very small sample sizes of many studies and probably also bias in some studies. Though no major publication bias was indicated in the meta-analysis, the possibility of publication bias could not be fully excluded. In the stratified analyses, heterogeneity between studies was reduced, suggesting that the varied data collection method, recruitment setting, sample size, study time and study locations may account for the inconsistency among studies. A higher prevalence of HIV infection was found among studies with sample sizes ≤ 200 compared with sample sizes >200, and this may suggest the prevalence may be overestimated in the studies with a smaller sample size.

Our meta analysis provided important findings on HIV and syphilis epidemics and UAI among older MSM in China. These findings are contradictory to the widespread perception that young MSM are at the highest risk of HIV infection. Older MSM have been ignored in HIV/STI prevention intervention programs, and more focus should be given to this neglected and hard-to-reach subgroup in future HIV interventions. Further large-scale epidemiological investigations, with standard sampling methods and adequate power, should be conducted to gain a more precise estimate of the status of the HIV and other sexually transmitted infection epidemics among older MSM in China.