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Prevalence of unprotected anal intercourse and unprotected vaginal intercourse among HIV-positive men who have sex with men in China: a meta-analysis
  1. Qian He1,
  2. Wen-Jia Peng1,
  3. Jun-Qing Zhang2,
  4. Bing-Xiang Wang1,
  5. Jing Wang1
  1. 1Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, Hefei, China
  2. 2Center for Disease Control and Prevention of Hefei City, Hefei, China
  1. Correspondence to Dr Jing Wang, Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui, 230032, PR China; jwang2006{at}126.com

Abstract

This study aims at deriving a general description of the prevalence of unprotected anal intercourse among HIV-positive MSM in China using published epidemiological research. Comprehensively searching Wanfang, Weipu, China Biological Medicine (CBM), Chinese National Knowledge Infrastructure (CNKI) and Pubmed databases in the systematic review. Meta-analysis were conducted over a final set of nineteen studies (n=1603). The pooled prevalence of unprotected anal intercourse among HIV-positive MSM was 75.4% (95%CI: 67.5%∼82.5%) and unprotected vaginal intercourse was 68.0% (95%CI: 46.0%∼86.4%). The prevalence of unprotected anal intercourse differed significantly in sampling method, data collection method, sample size, location, recruitment setting and data collection period. Studies with the following features had a higher prevalence of unprotected anal intercourse: recruiting participants from 2005 to 2007, sample size being below 50, recruiting participants from MSM venues/internet, using convenience sampling, study location being Chongqing city, and using interviewer administered questionnaire. Findings from this meta-analysis indicate that a majority percentage of HIV-positive MSM engage in unprotected sexual behavior. So that place their sex partners at risk for infecting HIV and also place themselves at risk for other sexually transmitted diseases. An effective strategy for prevention and control is required for this specific population in China.

  • HIV
  • men who have sex with men
  • HIV seroprevalence
  • unprotected sex
  • China
  • behavioural interventions
  • meta-analysis

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Introduction

It is estimated that there are 740 000 people currently living with HIV in China and HIV prevalence in the whole population increased from 0.050% in 2005 to 0.057% in 2009.1 HIV prevalence among men who have sex with men (MSM) is increasing rapidly and MSM have become one of the most important groups in the HIV/AIDS epidemic.2 3 Sexual transmission is the main mode of HIV infection. Among reported HIV-positive and AIDS patients, 44.3% were infected through heterosexual transmission and 14.7% through homosexual transmission. The increase in the rate of homosexual transmission was much higher than that of heterosexual transmission from 2006 to 2009.4 Male homosexual transmission has become an important route of HIV transmission. High risk behaviours (eg, multiple sex partners, sexual intercourse without protection such as unprotected anal intercourse (UAI)) are most common among MSM.5 6

A large number of epidemiological studies have addressed HIV prevalence and sexual behaviour among MSM in China since 2001.7 Several studies also have examined the characteristics of sexual behaviour and influencing factors among HIV-positive MSM. In this meta-analysis, we expanded the scope of previous two systematic reviews7 8 by adding related literature from after 2008. More specifically, we examined the prevalence of UAI; analysed the prevalence of UAI stratified by study characteristics (sampling method, data collection method, data collection period, sample size and location) and type of UAI (insertive vs receptive), and assessed the prevalence of unprotected vaginal intercourse in the included studies.

Methods

Literature search

Studies investigating sexual behaviour among HIV-positive MSM in China were identified by searching the following databases: Wanfang, Weipu, China Biological Medicine, Chinese National Knowledge Infrastructure and PubMed, focusing on papers published from January 2008 to May 2011. Keywords used in the database search included (‘HIV’ OR ‘AIDS’) AND (‘MSM’ OR ‘gay’ OR ‘homosexual’) AND (‘sex behaviour’) AND ‘China’ to screen for potentially relevant studies. Only studies written in Chinese or English were considered. Additional studies were also identified using cross-referencing or personal contact with the authors of a study.

Study selection

Studies were included if they met the following criteria: conducted in mainland China; specifically targeted at HIV-positive MSM; examined sexual behaviour among HIV-positive MSM; reported at least one behavioural outcome: unprotected anal intercourse (UAI), insertive UAI or receptive UAI; UAI was viewed as not always insisting on condom use during anal intercourse; reported the number or prevalence of people who had UAI (insertive UAI or receptive UAI) among HIV-positive MSM. We excluded studies that were reviews or were reported in duplicate. Conference abstracts or dissertations were screened but not included, as they provided too few details for the study.

Data extraction

All data from original articles were independently extracted by two reviewers according to the selection criteria. The following data were extracted: first author, year of publication, location, data collection period, sampling method, sample size of HIV-positive participants, age of the participants, urban/rural, marital status, educational background, sexual orientation and results of the prevalence of UAI and unprotected vaginal intercourse. Discrepancies were reconciled by a third independent reviewer.

Statistical analysis

For each relevant sexual behaviour, we calculated the prevalence and its corresponding weight. In estimating the prevalence across studies, we multiplied each estimate by its weight. Then we summed the weighted prevalence estimates and divided the sum of the weights, using the Freeman–Tukey double arcsine transformation method.9 10 Statistical heterogeneity was measured using the Q statistic test (p<0.05 was considered indicative of statistically significant heterogeneity). The χ2 test was used to assess the differences between the subgroups. Additionally, we conducted rank correlation of funnel plots to assess publication bias (p<0.05 was considered statistically significant). All analyses were conducted using R 2.12.0 software.

Results

Characteristics of included studies

Nineteen studies11–29 with a total of 1603 HIV-positive MSM met the inclusion criteria (figure 1). One study23 from which we failed to extract the prevalence of UAI was also included in our analysis. This was because it provided the prevalence of insertive UAI and receptive UAI among MSM living with HIV. A descriptive summary of each study is shown in online table 1. Eighteen studies (94.7%) reported the location of the study, and the commonly surveyed provinces and cities were Jiangsu, Beijing, Chongqing, Tianjin and Liaoning. Participants were mainly recruited from MSM venues, the internet and clinics. Seven studies (36.8%) collected the data from the 2005–2007 period, while ten studies (52.6%) covered the 2008–2009 period. The age of MSM living with HIV was over 16. Participants from 18 of the studies (94.7%) were from urban areas. The majority of the HIV-positive MSM were single or married. Fourteen studies (73.7%) collected information about education of the participants, and the majority have had over senior middle school education (the age range of junior middle school was from 12 to 16 years old in China and senior middle school is from 15 to 19 years old). Nine studies (47.4%) reported the status of sexual orientation among HIV-positive MSM, and the majority were homosexual or bisexual rather than predominantly heterosexual.

Figure 1

Selection process for study inclusion in this meta-analysis.

Study quality

The ability of the study sample to represent the population of HIV-positive MSM accurately (external validity) is of concern in all studies of this kind. The number of HIV-positive MSM in each study was from 10 to 872, with 11 studies (57.9%) having less than 50 participants, while seven studies (36.8%) had over 50 participants. Six studies adopted respondent-driven sampling, a new form of chain-referral sampling, to make accurate estimates about hidden populations and were designed to eliminate the bias caused by the non-random selection of the initial recruits.30 Other studies used convenience sampling (eg, MSM venues, internet-based, outreach staff and clinics recruitment). The method of administering the questionnaire (eg, interviewer administered vs self-administered) may introduce information bias. Nine studies used interviewers to administer the questionnaires and three studies used self-administered questionnaires.

Estimated prevalence of UAI and unprotected vaginal intercourse

The aggregated findings from 18 studies indicated that the prevalence of UAI was 75.4% (95% CI 67.5% to 82.5%). Figure 2 shows wide heterogeneity across studies (Q=144.6, p<0.0001). However, no obvious publication bias was observed (p=0.5542). The pooled prevalence of unprotected vaginal intercourse was 68.0% (95% CI 46.0% to 86.4%). There was no statistically significant publication bias (p=0.5249), but substantial heterogeneity among the included studies was noted (Q=103.8, p<0.0001) in figure 3.

Figure 2

Overall estimate of unprotected anal intercourse among HIV-positive MSM.

Figure 3

Overall estimate of unprotected vaginal intercourse among HIV-positive MSM.

Table 1 summarises the findings of stratified analyses. The pooled prevalence of insertive UAI was 46.5% (95% CI: 41.0% to 52.0%), while that of receptive UAI was 48.3% (95% CI 43.0% to 53.8%). The prevalence of UAI was significantly lower in studies that used respondent-driven sampling or snowball sampling (vs convenience sampling), those that recruited from clinics (vs MSM venues and the internet), those that used self-administered questionnaires (vs interviewer administered), those that collected data from 2008 to 2009 (vs from 2005 to 2007), those that investigated Beijing (vs Chongqing City or Jiangsu province) and sample size was over 50 (vs below 50).

Table 1

Prevalence estimates of unprotected anal intercourse by study features and sample characteristics among HIV-positive MSM.

Discussion

This meta-analysis provided the first quantitatively synthesised estimates of the prevalence of UAI among HIV-positive MSM in China. Nineteen eligible studies were included. The overall prevalence of UAI was 75.4% and it differed significantly depending on UAI mode, sampling method, recruitment setting, data collection method, sample size and data collection period.

The UAI prevalence in this meta-analysis was higher than the prevalence of UAI (43.0%) in the USA among MSM living with HIV.31 In addition, HIV-positive MSM showed a higher prevalence of receptive UAI compared to insertive UAI in our analysis. Other studies reported that HIV-positive MSM were more likely to use anal intercourse, especially receptive anal intercourse.32 33 MSM living with HIV may need more communication and education about HIV control and prevention, encouraging them to use condoms during anal intercourse and changing unsafe sexual behaviour in order to decrease the risk of HIV transmission.

Our meta-analysis also revealed that the pooled prevalence of unprotected vaginal intercourse was 68.0%. Gorbach PM et al pointed out that men who have sex with men and women reported little condom use with female partners, especially during vaginal intercourse.34 Additionally, due to social pressures and traditional family values, a majority of Chinese MSM will eventually get married.35 36 It is reported that 74.0% of married MSM had sex with women in the last 6 months and about 84.0% of them had unprotected sex with women.35 Sexual intercourse without protection among MSM have made this population become a potential bridge for HIV infection, and play a role in spreading HIV in female, gay and other populations.37–40

The prevalence of UAI was significantly higher in studies of participants recruited from MSM venues or via the internet compared with studies of participants recruited from clinics, which is consistent with an earlier meta-analysis.31 This suggests that samples which are recruited from venues or internet are more likely to engage in unprotected sexual intercourse. Sadler KE and colleagues also showed that individuals who were selected through MSM venues or the internet were more likely to transmit HIV infection.41 In China, many medical institutions have been providing voluntary HIV counselling and testing services. The participants from medical settings (eg, clinics) may obtain knowledge about the prevention and control of HIV and thus tend to pay more attention to their sexual behaviour and have a lower prevalence of UAI. The UAI prevalence was also significantly lower in studies that used respondent-driven and snowballing sampling compared with studies that used convenience sampling. One explanation is that convenience samples might have selected participants from more high-risk MSM populations. Self-reported sexual behaviours may have social desirability biases. HIV-positive MSM may have under-reported socially undesirable behaviours when the questionnaire was administered by an interviewer.31 However, our study revealed that UAI was significantly lower in studies using self-administered questionnaires than in studies using interviewer administration. This may be due to an inadequate number of studies; in our analysis, only three studies used self-administered questionnaires.

Our results also showed a higher prevalence of UAI in studies with a sample size below 50. The prevalence may be overestimated by the studies with small sample sizes and excluding studies of insufficient size may help in decreasing heterogeneity across studies. However, due to limited studies being available, we also included studies with sample sizes below 50. A significant difference in the the prevalence of UAI was found among different locations, with Chongqing ranking top. Chongqing is the largest municipality in southwest China and has a higher HIV prevalence than the national average.42 A survey of MSM demonstrated that major cities in southwest China, such as Chongqing, Chengdu and Guiyang, had a higher percentage of patients diagnosed as being HIV-positive than other cities in China.4 Regions with a higher rate of HIV might reflect a higher incidence of unprotected sexual intercourse and increased UAI prevalence.

All the included studies were conducted in urban area of China, but not in rural areas. Thus, the estimated prevalence of UAI may not be representative of the entire population of MSM living with HIV. Our findings are likely to overestimate the prevalence of UAI among HIV-positive MSM. People in rural areas often migrate to a city for a temporary job and this population may play an important role in spreading HIV between rural and urban areas.43 Therefore, it will be important to survey and understand the state of MSM living with HIV in rural areas.

Our meta-analytical findings should be read within the context of several limitations. First, although no indication of publication bias was found in the analysis, publication bias could not be ignored, as positive results are more likely to be published. Second, some studies indicated that unprotected sexual intercourse was closely linked with HIV-positive sex partners, injecting drug users, highly active antiretroviral therapy and intimacy with sexual partners.44–46 However, these were not included in our analysis since few studies provided information in these areas.

In conclusion, our analysis revealed that HIV-positive MSM had a high prevalence of UAI and unprotected vaginal intercourse. In China, related health education and prevention measures targeting MSM started in 1991. At present, some homosexual organisations and medical departments are providing hot-line consultation, peer education, and information, communication and education materials. Given the higher UAI prevalence, much more effort is needed to promote health education and behavioural interventions for HIV-positive MSM to reduce high-risk sexual behaviour. To ensure a precise estimate of the status of sexual behaviours among HIV-positive MSM in China, more large-scale epidemiological studies with adequate standard sampling methods may be essential in the future. Meanwhile, concerted efforts to establish and maintain positive programs may be needed to reduce HIV transmission to other general populations from MSM living with HIV in China.

Key messages

  • This study is the first meta-analysis on the prevalence of unprotected anal intercourse and unprotected vaginal intercourse among HIV-positive MSM in China.

  • Our analyses demonstrate a high prevalence of UAI among HIV-positive MSM, and an effective strategy for prevention and control is needed for this population.

  • HIV-positive MSM engaged in sexual intercourse without protection and their sexual partners are at risk of acquiring HIV.

References

Footnotes

  • Funding This work was supported by the grants from the Academic Leader Foundation and Doctor's Scientific Research Foundation of Anhui Medical University (code: XJ200907).

  • Competing interests None.

  • Provenance and peer review Not commissioned; externally peer reviewed.