Older adults at high risk of HIV infection in China: a systematic review and meta-analysis of observational studies

Introduction

Human Immunodeficiency Virus (HIV) infection is a major public health challenge associated with high disease burden globally (Maartens, Celum & Lewin, 2014). In 2017, approximately 36.9 million people lived with HIV infection worldwide (UNAIDS, 2019). In China, the incidence of HIV was 4.1 per 100,000 individuals in 2018, which translates to approximately 56,993 newly infected persons (National Bureau of Statistics of China, 2018). Those who are at high risk of HIV infection include men who have sex with men (MSM) and younger adults (Knudson et al., 2018; Zhang et al., 2017b). In China, the highest HIV infection rate occurs in those aged between 20 and 40 years (Lu et al., 2008), but there has been an increasing prevalence in older adults recently, which is similar to trends in Western countries. For instance, around half of the people living with HIV were above 50 years old in the USA (High et al., 2012; Hosaka et al., 2019). In Europe, the number of adults aged 50 years or above living with HIV has been also growing (Seeley, 2017). A study in Chongqing, China found that the number of newly HIV infected persons aged over 50 years has increased six-fold from 1,091 in 2004 to 6,352 in 2015 (Zhang, Rongrong & Guohui, 2017a).

Epidemiological studies in China has found an increasing trend in the number and proportion of HIV infection among older adults (Xing et al., 2014). In the past decades, insufficient attention has been paid to older adults with HIV infection, with a lack of HIV risk reduction interventions (Cooperman, Arnsten & Klein, 2007; Crystal et al., 2003). Knowledge of safe sex activities and condom use are usually not addressed in older adults (Negin & Cumming, 2010), even though high risk sexual behaviors exist in this population (Crystal et al., 2003). In China, neglected sex education among older adults have been associated with unprotected sexual activities (Xing et al., 2014), which could increase the risk of HIV infection. On the other hand, the change in the age distribution of HIV infection in China could be partly due to the widespread use of free Highly Active Antiretroviral Therapy (HAART) in reducing transmission risk of HIV infection (Bhaskaran et al., 2008) among younger adults. Greater access to HIV clinics, free HAART treatment, and improved general healthcare service system in China have also increased their life expectancy therefore most are living to older adulthood (Greenbaum et al., 2008; Xing et al., 2014). These factors may also contribute to the growing proportion of older adults with HIV infection.

In order to develop appropriate strategies for HIV prevention and control, it is important to accurately determine the prevalence of HIV infection across different age groups. To date, no meta-analysis or systematic review of the prevalence of HIV infection in older Chinese adults has been published, which gave us impetus to conduct a meta-analysis to examine the prevalence and its associated factors in this population. In addition, we examined the association of demographic and clinical characteristics, such as sex and sexual orientation, with the prevalence of HIV infection in older adults using subgroup and meta-regression analyses. The target demographic and clinical characteristics were selected based on previous studies (Knudson et al., 2018; Zhang et al., 2017b).

Methods

Results

Literature search and study characteristics

A total of 3,641 publications were identified in the initial literature search. Finally, 46 studies with 363,399 subjects met the entry criteria and were included in the meta-analysis (Fig. 1); four studies were published in English (Chen et al., 2016; Feng et al., 2009; Ning et al., 2018; Xie et al., 2014), and the remaining were published in Chinese language. Table 1 shows the study characteristics. All studies were published between 2004 and 2018. Most studies (89%) used ≥ 50 years as cut-off age for older adults. Of the 46 studies, only one reported treatment information in HIV infected older adults, i.e., 53.75% of whom had HAART treatment (Ning et al., 2018).

Nine studies reported the HIV infection rate in all age groups (Chen et al., 2017; Chen et al., 2016; Chen et al., 2013; Du & Meng, 2016; Feng et al., 2009; Wang et al., 2018a; Zhao, Su & Jiang, 2015; Zhong et al., 2017; Zhu, Miu & Zhang, 2014), therefore only data in older adults were extracted for analyses; while five studies focused on older MSM adults. Thirteen studies reported transmission routes, while the remaining (71.7%) did not.

Discussion

This was the first meta-analysis to examine the prevalence of HIV infection in older adults in China. The meta-analysis revealed that the pooled prevalence of HIV infection in older Chinese adults was 2.1%, which was substantially higher than the figure reported in the Chinese general population (0.05%) (National Bureau of Statistics of China, 2018). The high HIV infection rate could be due to several reasons. The life expectancy of HIV-infected adults has been significantly prolonged due to widespread use of HAART (Bhaskaran et al., 2008; Greenbaum et al., 2008; Xing et al., 2014); e.g., the National Free Antiretroviral Treatment Program (NFATP) has covered more than 97% of HIV-infected people in China (Zhang et al., 2009). The high HAART adherence rate in Chinese HIV patients, as confirmed by a recent meta-analysis (Wang et al., 2018b), would be expected to increase life expectancy and many patients are living into their older adulthood. Furthermore, many studies have indicated increasing transmission via commercial sexual activities among older Chinese men after retirement as a major reason for HIV infection (Wang et al., 2014; Zhou et al., 2014). It has been suggested that prevention of HIV transmission among older MSM should be an urgent priority in China’s HIV/AIDS strategy (Ning et al., 2018).

The high proportion of HIV infection in older adults is growing major public health challenge in China. Compared to younger adults, physical and psychiatric comorbidities, such as pneumonia, depression and insomnia, are usually more common in HIV-infected older adults (Ding et al., 2017), which could lead to heavy personal, family and economic burden. Therefore, appropriate allocation of healthcare resources and developing effective preventive strategies for HIV-infected older adults in China should be considered (Xing et al., 2014).

Consistent with previous findings on HIV prevalence in China (Zhang et al., 2013), we found in this meta-analysis that MSM was associated with a higher risk of HIV infection; the HIV prevalence in MSM older adults was 11.8%, which was the highest among all subgroups. Compared to community populations, hospital population samples were significantly associated with higher HIV infection rate, which is probably because older adults with HIV infection were more likely to receive HIV testing than those in the community. Compared to middle and eastern economic regions, HIV infection prevalence in older adults was significantly higher in the western region of China, being less developed than other parts of China. Therefore, the lack of access to HIV treatment and prevention measures in the western region could be associated with higher HIV infection rate. Due to degradation of traditional Chinese family structure and lack of family support, retired older men are also more likely to have engaged in commercial sex, particularly in under-developed western regions of China (Huang, Maman & Pan, 2012).

Unexpectedly, commercial sex as the transmission route was not significantly associated with higher HIV infection rate. This appears inconsistent with previous findings that commercial sex is a major route for HIV infection transmission among older Chinese men (Wang et al., 2014; Zhou et al., 2014). Studies published after 2014 were significantly associated with higher HIV infection rate, which we were unable to explain adequately. However, we found that higher study quality was significantly associated with higher HIV prevalence. Due to sigma and discrimination associated with HIV/AIDS, many sufferers, particularly older adults in China usually deny or conceal their diagnosis in order to avoid “loss of face”. High quality studies may identify patients more systematically, and obtain a more accurate and often higher rate HIV infection.

There were several limitations in this meta-analysis. First, similar to other meta-analyses of epidemiological studies (Liu et al., 2016; Long et al., 2014; Wang et al., 2018b; Winsper et al., 2013), there was substantial heterogeneity, although subgroup analyses were performed. The heterogeneity may be associated with different sampling methods, study designs, diagnostic criteria of HIV infection and demographic and clinical characteristics between studies. Second, most studies did not report the transmission route, therefore further sophisticated analyses could not be conducted. Third, due to the cross-sectional design of included studies, the causal relationship between HIV infection and related variables could not be explored.

In conclusion, this meta-analysis showed that the prevalence of HIV infection in older adult population is significantly higher than the general population in China. Attention should be given to this urgent public health issue, and effective HIV/AIDS preventive, screening and treatment measures are warranted in this population.

Supplemental Information