Alcohol Use, Stigmatizing/Discriminatory Attitudes, and HIV High-Risk Sexual Behaviors among Men Who Have Sex with Men in China

Objective. This research was conducted to assess the correlates of alcohol consumption and HIV/AIDS-related stigmatizing and discriminatory attitudes among men who have sex with men (MSM) in Shandong province, China. Methods. A cross-sectional survey provided demographics, sexual behaviors, illicit drug use, alcohol consumptions, and service utilization. Results. Of 1,230 participants, 82.8% were single, 85.7% aged <35 years, 47.2% had college or higher education, and 11.7% drank alcohol >3 times per week in the past six months. The average total score of stigmatizing and discriminatory attitude was 37.4 ± 4.4. More frequent episodes of alcohol use were independently associated with higher levels of HIV/AIDS-related stigma and discrimination, unprotected anal sex, bisexual identity, multiple male sex partners, drug use, and lower levels of education. Expressing higher levels of HIV/AIDS-related stigmatizing and discriminatory attitudes was independently associated with alcohol use, unprotected male anal sex, bisexuals, more male sex partners, commercial sex with men, and non-receipt of peer education in the past year. Conclusion. HIV/AIDS-related stigmatizing and discriminatory attitudes are common and associated with alcohol use and unprotected sex among MSM. The finding highlights the needs to develop programs that would reduce HIV/AIDS-related stigmatizing and discriminatory attitudes and strengthen alcohol use prevention and risk reduction initiatives among MSM.


Introduction
The rapid rise in HIV prevalence among men who have sex with men (MSM) in many cities across the nation has drawn attention to the dynamics of the HIV epidemic in China [1][2][3]. It is estimated that about 2.2% of Chinese adult males had sex with another male [4]. According to the 2011 estimates for the HIV/AIDS epidemic in China,81.6% of 48,000 HIV new cases were infected through sexual contact, 29.4% of those infected from sexual contact were through homosexual contact [2]. Under the strong influence of Confucianism and collectivism, Chinese traditional culture emphasizes familial responsibilities; MSM behaviors are highly stigmatized and MSM face strong social pressure to hide their identity [5]. On the other hand, stigma surrounding HIV/AIDS has been shown to act as a barrier to HIV prevention, treatment, and care [6,7]. People who hold stigmatizing attitudes are also less likely to adopt preventive behaviors and more likely to have multiple sexual partners, a commercial sex partner, and some other HIV-related high-risk behaviors [8,9].
Alcohol consumption has increased considerably in China in the past three decades, accompanying a rapidly expanding economy, urbanization, and globalization [10]. The global literature suggests that alcohol consumption is associated with a number of sexual risk behaviors and outcomes, including premarital intercourse, multiple sexual partners, and unprotected sex [11,12]. As the most commonly used legal substance, drinking-related exposures to sexual risk behaviors and drinkers' increased biological susceptibility could lead to an increased risk of HIV and other sexually transmitted infections (STIs) [11]. Drink and HIV-related stigma/discrimination are common in the MSM community. Understanding the relationship between stigma, alcohol use, and sexual behavior among MSM has important intervention implications. The purpose of this study is to assess correlates for alcohol use and HIV/AIDS-related stigmatizing and discriminatory attitudes among MSM in Shandong province, China.

Study Participants.
A cross-sectional study was conducted among MSM to collect demographic, sexual behaviors, illicit drug use, alcohol consumptions, and health service utilization by local Center for Disease Control and Prevention (CDC) in three cities, Jinan, Qingdao, and Yantai, in Shandong province, China, from April to June in 2011. Prior to the recruitment of the participants, we conducted informative research including in-depth interviews with key informants to gather the background information among MSM, the venues to access them, and selection of the candidates of the first group for interview. Participants were recruited from gay-oriented venues such as bars, night clubs, tea houses, bathhouses, saunas, public parks and bathrooms, outdoor cruising areas, and HIV testing sites. After these initial participants were approached and interviewed by trained public health staff, we asked the participants to refer their peers to attend the study. A mixed recruitment method, including community outreach, venue-based recruitment, and internet advertisement, was also applied in the study. All potential participants were invited for eligibility assessments. The enrollment criteria included male, 18 years of age or older, self-reported ever having sex with another male in the past 12 months, and willing to complete the study. Survey information was collected anonymously and handled in a confidential manner. Verbal informed consent was obtained from all participants before the interview. Voluntary participation, anonymity, and confidentiality were ensured for all participants. The study was approved by the Institutional Review Board of Shandong Center for Disease Control and Prevention.

Measures.
Structured questionnaire-based interviews provided demographics (age, marital status, ethnicity, residency status and education, sexual, drug use, and alcohol drinking behaviors, access and utilization of HIV-related prevention services, and stigma and discriminatory attitudes towards People Living With HIV/AIDS (PLWHA)). The term "bisexual" was used for participants who were married or cohabiting with women or reported ever having sex with a woman in the past 6 months. Attitudes towards PLWHA were measured by asking participants about their agreement/disagreement (1 = "yes, " 2 = "no") with 22 statements [13]. The scale was adapted from two pilot investigations tested in Thailand and Zimbabwe and measured 3 dimensions of HIV/AIDS-related stigma and discrimination: shame, blame, and social isolation; perceived discrimination; and equity. The reliability (alpha) of the stigma measure was 0.83. The scale included questions such as "People living with HIV/AIDS should be ashamed"; "People living with HIV/AIDS face neglect from their family"; "People living with HIV/AIDS do not deserve any support. " Items were summed to create total scale scores, with a range of 22-44 where a higher score means lower stigma and lower score indicates a higher stigma. Frequency of alcohol use was determined directly from responses to a single questionnaire item in which respondents were asked how often they drank in the past six months. Responses included "about every day, " "5-6 days a week, " "3-4 days a week, " "1-2 days a week, " "2-3 days a month, " "less often than monthly, " and "never. " In the final analysis, the categories "About every day, " "5-6 days a week, " and "3-4 days a week" were collapsed into a single variable "more than 3 days per week, " because of the low frequencies of individual responses when the original categories were considered separately. Serum samples were screened for HIV-1 antibodies by enzyme-linked immunosorbent assay (ELISA; Vironostika HIV Uni-Form plus O, bioMerieux, Holland) and confirmed by Western Blot test (HIV Blot 2.2 WB, Genelabs Diagnostics). Syphilis screening was performed by rapid plasma regain (RPR; Shanghai Rongsheng, China) and confirmed by Treponema pallidum particle assay test (TPPA; Fujirebioinc, Japan). Pre-and posttesting counseling were provided by local CDC.

Statistical Analysis.
Survey data and blood testing results were recorded and assessed for congruency using EpiData software (EpiData 6.4 for Windows, the EpiData Association Odense, Denmark). The Statistical Program for Social Sciences software (SPSS software, Version 15.0; SPSS Inc., Chicago, IL, US) was utilized for all analyses. Univariate analyses were conducted for demographic, sexual, drug use, and drinking variables and related prevention services. Multivariable logistic regression analyses were conducted using a stepwise backward sequence. Variables with < 0.05 in multivariable analysis were determined as statistically significant. Multiple linear regression analysis was applied to determine which predictors were independently associated with total stigma scale scores after controlling for potential confounders.

Characteristics of Participants.
Of 1,230 eligible participants, 82.8% were single, 85.7% were between 18 and 35 years of age, nearly half (47.2%) had college or higher levels of education, 28.6% were married or cohabiting with women or reported ever having sex with women in the past 6 months. More than two-thirds of respondents (68.7%) identified themselves as homosexual, a quarter (26.3%) identified themselves as bisexual, and 1.4% identified themselves as heterosexual; 19.4% were non-Shandong province residents, and 2.0% belonged to a non-Han minority ethnic group (Table 1).

Sexual Behaviors and Prevalence Rates of HIV and
Syphilis. Approximately 91.4% of participants reported having had sex with men in the past six months, 54.3% had more than two male sex partners in the past week, 70.8% used a condom at last anal sex, and 31.3% consistently used condoms in the past 6 months with male partners. In addition, 27.2% of respondents admitted having had commercial sex with men, with only 29.8% reporting consistent condoms use in the past 6 months. Further, 21.5% of participants reported ever selling sex to another man, with only 31.1% of them reporting consistent condom use in the past 6 months. About one-quarter of respondents (23.4%) had sex with a female in the past 6 months, with one-third (32.5%) reporting consistent condom use over the same time period. Only 1.1% of participants reported ever using illicit drugs. Approximately half (50.7%) of participants received HIV testing in the past year, and three-quarters (75.2%) and 41.3% received condom promotion/HIV testing and counseling and peer education, respectively. Of all participants, 1.6% were HIV-infected and 6.8% were syphilis-infected (Table 2).

Discussion
To the best of our knowledge, this is the first study from China that assesses HIV/AIDS-related stigmatizing and discriminatory attitudes and its relationship with alcohol consumption among MSM. This study revealed that HIV/AIDSrelated stigmatizing and discriminatory attitudes were common among MSM and associated with drinking behavior, unprotected anal sex, and commercial sex among MSM in Shandong province, China. Confronting a rapid rise of HIV incidence among MSM in China, common negative attitudes towards PLWHA, excessive alcohol use behaviors, and bisexual and unprotected sex among this group have become emerging challenges in containing the epidemic. Stigma is particularly relevant to prevention and treatment in the HIV/AIDS pandemic [14]. The negative attitudes towards persons living with HIV/AIDS (PLWHA) are often associated with self-imposed isolation that results from individuals' reluctance to access services due to fear that family and community members may shun them for their drinking and drug use behaviors [15,16]. On the other hand, Chinese cultural norms encourage social drinking. Alcohol is commonly consumed in social settings, particularly by men, as a normal part of their social life, to identify with new friends, maintain good relations, and celebrate events among friends. Other researchers have shown a consistent association between alcohol use and several sexual risk behaviors and HIV/STIs across both high-risk groups and general populations in China [17,18]. Hence, in confronting the rapid expansion of the HIV/AIDS epidemic among MSM in China, the findings of the present study underline the urgent need to reduce the stigmatizing and discriminatory attitudes towards PLWHA and call for the need for alcohol use prevention and risk reduction among MSM communities.
This study shows that self-identification as bisexual is independently associated with drinking behaviors and with more negative attitudes towards PLWHA. Shandong is the second most populous province in China and the home of Confucius. Under the strong influence of Confucianism and collectivism, MSM behaviors are stigmatized and MSM face strong social pressure [5,19]. Such social environments may lead MSM to hide their sexual orientation by unwillingly engaging in heterosexual relationships [20]. Many of them continue to be married and maintain sexual relationships with their wives while maintaining concurrent but hidden homosexual relationships. Nearly one-third of MSM are married in China, and an even higher proportion reported having had sex with women [21,22]. Our previous study showed approximately 40% of MSM being married or ever having had heterosexual behavior in Shandong province [23]. These bisexual and marital relationships have a strong impact on the HIV epidemic from MSM population to general population. Studies from different countries documented the high rate of unprotected sexual behaviors between spouses and/or regular heterosexual partners tends [22,24,25]. Therefore, bisexually active men in China could play a critical bridging role in spreading HIV and other STIs from their high-risk male sexual partners to low-risk female partners, for example, their wives [26,27]. Under social pressure, bisexual MSM may further reinforce the negative attitudes towards PLWHA and worsen drinking behaviors. While stigma is widely invoked as a major facilitator of the HIV epidemic [28], only few studies have demonstrated an association between stigma and increased risk behavior. This study showed that unprotected male anal sex in the past 6 months and ≥2 male sex partners in the past week are independently associated with drinking behavior and more negative attitudes towards PLWHA. Other studies that have demonstrated drinking behaviors will result in multiple sexual partners and unprotected sex [11,12]. A cross-sectional study of MSM in 5 cities in Jiangsu province showed that heavy alcohol consumption was linked to unprotected anal intercourse (OR = 2.32) compared with nondrinkers or light drinkers [29]. Alcohol consumption may directly impair judgment and cause social disinhibition, resulting in an increased likelihood of unprotected sexual encounters. The other explanation involves a social environment model, in which an association occurs because the social environment of drinking overlaps with an environment that facilitates meeting potential casual sexual partners. Stigma can have significant adverse effects on health and disease transmission by promoting delays in seeking care and reluctance to follow medical advice [28]. One study among Chinese migrants found that persons holding stigmatizing beliefs were more likely to have multiple sexual partners, a commercial sex partner, and a STI [30]. The findings of the present study suggest that common multiple sex partners and existing sexual network among this group could offer an intervention opportunity to reduce HIV/AIDS-related stigmatizing and discriminatory attitudes and strengthen alcohol use prevention and risk reduction initiatives among MSM.
This study also found that MSM who ever received peer education in the past year were more likely to express lower negative attitudes towards PLWHA. Peer education could relieve their social pressure, persuade MSM to receive HIV counseling and testing, and facilitate early diagnosis, timely prevention, and linkage to care and medical treatment.
Ti and Kerr showed that by creating peer-involved HIV testing clinics and pairing physicians with peers, high-risk groups may be more likely to use these services without fear of being discriminated by healthcare workers [31]. By shifting delivery of care from healthcare professionals to peers, or by incorporating peer workers into professionally led services, a reduction in stigma and discrimination in these settings may be achieved. The findings of the present study underline the effect of peer education and the need to deliver conventional HIV/AIDS services directly to MSM to reduce the stigmatization and discrimination among MSM communities.
These studies highlighted the importance of policy considerations for stigma, alcohol use, and its related sexual risk among MSM. This study is not without limitations. First, the stigma scale may provoke socially desirable answers from respondents. Participants may feel embarrassed to openly express stigmatizing and discriminatory attitudes towards PLWHA during face-to-face interviews. This study might therefore underestimate the true levels of negative attitudes and risk behavior. Second, the nature of the cross-sectional study design precluded identification of causal relationships. Third, since this study did not assess the cooccurrence of drinking behavior with inconsistent condom use or multiple sex partners, any inference on the causal relationship between these variables is impossible. Fourth, the variables used to characterize alcohol consumption are not a complete list and may miss some opportunities to capture all true relationships.
Despite its many limitations, this study provides important information for further research and suggests that MSM who experience stigmatizing and discriminatory attitudes towards PLWHA and exhibit patterns of excessive alcohol use may be at higher risk for increased numbers of sexual partners and for bisexual and unprotected sex. Common HIV/AIDS-related stigmatizing and discriminatory attitudes,