Introduction

Since the beginning of the epidemic, stigma and discrimination have been identified as major barriers to use HIV-related prevention services [1–3]. HIV/AIDS-related stigma and discrimination can adversely influence decisions to seek HIV testing [4, 5]. The effect of stigma and discrimination on people’s ability to access HIV testing, counseling, diagnosis, care, treatment, and prevention services varies from setting to setting, but when present, stigma and discrimination can create an environment where people may avoid HIV-related services. HIV continues to spread among men who have sex with men (MSM) globally [6]. HIV/AIDS-related stigma and discrimination as a perceived experience of HIV-infected individuals [7–9] or assessing the attitudes of the general population towards people living with HIV/AIDS [10–12] have been documented. HIV-related stigma/discrimination is common in the gay community [13, 14], however, limited data are available regarding prejudicial attitudes among gay men towards people living with HIV/AIDS (PLWHA). Unprotected sex between males continue to fuel the HIV epidemic in many western countries [15, 16] and China as well [17]. HIV testing and counseling plays a critical role in containing the epidemic, it may help reduce risk behaviors [18, 19], lead to early diagnosis and timely linkage to prevention and care programs [20, 21]. It is critical to investigate HIV/AIDS related stigma and discrimination among MSM and its impact on seeking HIV testing in containing the epidemic. This study assessed correlates for recent HIV testing and stigmatizing and discriminatory attitudes towards PLWHA among MSM in Beijing.

Methods

Study Participants

A cross-sectional study was conducted among MSM in September and October 2009 in an outpatient clinic affiliated with Beijing Center for Disease Control and Prevention (CDC). Individuals were eligible for the study if they (1) identified as male, (2) were 18 years of age or older, (3) reported living in Beijing, (4) reported oral, anal sex, or mutual masturbation with a man in the past 12 months, (5) had a valid study recruitment coupon, (6) had not previously participated in the survey, and (7) were able to provide written informed consent. Each study participant was screened for study eligibility prior to enrollment. The study was approved by the Committees for Human Research of the National Center for AIDS of the China CDC, Vanderbilt University and the University of California, San Francisco.

Recruitment

We employed respondent-driven sampling (RDS) to recruit study participants. RDS is a chain-referral recruitment approach for accessing and sampling hidden populations [22], it has been adopted widely for HIV prevalence and risk behavior surveillance among at-risk population [23]. With the support from formative research, we selected initial subjects to start recruitment chains. Seven seeds were selected from those attending bars, bathrooms, parks, Internets, grassroots organizations, and from peer referral. Seed selection criteria included the commitment to complete the survey, being identified as peer opinion leaders in their community, as well as representativeness of demographics, location of residency, and risk behaviors (sexual and drug use behaviors). Each seed received three recruitment coupons and was invited to recruit MSM peers from their network. The coupon included the project name, address and phone number of the interview site, study identification number, and expiration date. A unique serial number on each coupon linked each participant to their recruiter. The recruits of the seeds also received three coupons for additional recruitment.

Measures

After eligibility screening and giving informed consent, each participant completed a 20 min computer-assisted interview. The trained study staff, using the structured questionnaire, asked participants about general demographics, sexual and drug use behaviors, HIV testing history, and stigmatizing and discriminatory attitudes towards PLWHA.

Demographics, Sexual Risk Behaviors

Demographic questions included age, ethnicity, education, marital status, employment, sexual orientation, and Beijing residence status. Risk behavior measures included ever engaging in unprotected sexual intercourse, history of substance use (e.g., alcohol or drugs), disclosure of sexual orientation, and number of male and female sexual partners.

HIV Testing Behaviors

All participants were asked if they had ever tested for HIV and, if applicable, the number of prior tests, and the date and result of their most recent test. Recent testers were defined as participants who received a test for HIV in the past 12 months. Participants having ever received a test for HIV included those who had ever received the test in the past 12 months and more than 12 months.

HIV/AIDS-Related Stigma and Discrimination

Individual attitudes towards PLWHA were measured by asking participants about their agreement and disagreement (1 = ‘yes’, 2 = ‘no’) with 22 statements. The scale was adapted from two pilot investigations conducted in Thailand and Zimbabwe [24]. This scale measured three dimensions of HIV/AIDS-related stigma and discrimination: shame, blame, and social isolation; perceived discrimination; and equity. The scale included such questions 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, in which a higher score indicates a lower level of HIV/AIDS-related stigma and discrimination. Acceptable reliability was supported by a Cronbach’s alpha value of 0.83 in our study.

Laboratory Testing

Serum samples were screened for HIV-1 antibodies by enzyme-linked immunosorbent assay (ELISA; Vironostika HIV Uni-Form plus O, bioMerieux, Holland) and confirmed as positive by Western Blot test (HIV Blot 2.2 WBTM, Genelabs Diagnostics). Syphilis screening was performed by rapid plasma regain (RPR; Shanghai Rongsheng, Shanghai, China) and confirmed by Treponemapallidum particle assay test (TPPA; Fujirebioinc, Japan).

Statistical Analyses

RDS Analysis Tool (RDSAT 5.6, Cornell University, Ithaca, NY, USA) was used to generate weighted point estimates and 95% confidence intervals (95%CI) [25]. Statistical Analysis Software (SAS 9.1 for Windows; SAS Institute Inc, Cary, NC) was used for all analyses. Univariate and multivariable analysis were conducted after assigning cases individual weights for recent HIV testing and HIV/AIDS-related stigma and discrimination exported from RDSAT. The factors associated with recent testing were assessed using univariate analysis and multivariable logistic regression analysis. Odds ratios (ORs) and 95%CIs were calculated in the multiple logistic regression analysis. Statistical significance was determined at p < 0.05 in the final model. The weighted mean scale scores of HIV-related stigma and discrimination were first calculated for each variable level. Subsequently, simple and multiple linear regression analysis were applied to determine which predictors (demographic factors, sexual behaviors, recent testing) were independently associated with total scale scores after controlling for all potential confounders.

Results

Characteristics of Participants

A total of 500 MSM eligible participants participated in the survey. RDS estimates suggest that among MSM in Beijing about half (50.4%) of MSM are younger than 30 years old, more than two-third (68.5%) have high school or higher levels of education, 79.9% are employed with a full time job, 61.7% self-identify as homosexual, 41.8% have ≥3male sex partners, 25.8% have female sexual partners, and 22.8% know the HIV status of their last male partner.

Sexual and Substance Use Behaviors

RDS adjusted estimates suggest that the rates of unprotected insertive and receptive anal sex with last male partners in the past 6 months were 34.8% and 40.5%, respectively. Of MSM in Beijing, 0.1% have used drugs in the past 12 months. Of the quarter of all MSM who have sex with females, 79.6% have unprotected sex with a female sexual partner in the past 6 months (Table 1).

Table 1 Recent HIV testing, stigmatizing and discriminatory attitudes towards people living with HIV/AIDS among men who have sex with men, Beijing, 2009
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HIV Testing and HIV/AIDS-related Stigma and Discrimination

Of MSM in Beijing, RDS estimates that 39.3% received a recent HIV test, almost half (48.6%) have never tested and the rest have tested more than 1 year in the past. The RDS weighted prevalence of HIV was 8.0% (95%CI: 4.7–12.0%) with 86.1% of those infected persons unaware of their infection. The weighted prevalence of syphilis was 22.0% (95%CI: 16.8–27.3%) (Table 1).

A comparison of stigma and discrimination scores for recent HIV testers and non-recent testers indicated that recent testers have significantly higher stigma and discrimination scores (p < 0.001), expressing as lower negative attitudes towards PLWHA, than non-recent testers (Fig. 1).

Fig. 1
figure 1

Comparison of stigmatizing and discriminatory attitudes towards people living with HIV/AIDS between participants who received (blue) and did not receive (red) a test for HIV in the past 12 months (Color figure online)

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Correlates for Recent HIV Testing

Multivariable logistic regression analysis indicated that recent HIV testing is associated with lower levels of HIV/AIDS-related stigma and discrimination (AOR=1.1, 95%CI: 1.0–1.2), having more male partners in the past 6 months (AOR=1.9, 95%CI: 1.1–3.3, ≥3 male partners), having no female sex partners in the past 6 months (AOR=3.0, 95%CI: 1.6–5.8), and knowing the HIV infection status of last male partners (AOR=3.6, 95%CI: 1.9–6.5) (Table 2).

Table 2 Correlates of recent HIV testing among men who have sex with men, Beijing, 2009
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Correlates for Stigmatizing and Discriminatory Attitudes towards PLWHA

Multivariable linear regression analysis suggest that MSM who have recent HIV testing (β = 0.7, p = 0.041) are younger (β = 1.8, p < 0.001), aware of the HIV infection status of their last male partner (β = 0.9, p = 0.022), and are more likely to express lower levels of stigmatizing and discriminatory attitudes towards PLWHA (Table 3).

Table 3 Correlates for HIV/AIDS-related stigmatizing and discriminatory attitudes among Beijing’s men who have sex with men
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Discussion

This is the first study in China which assesses stigmatizing and discriminatory attitudes towards PLWHA and its relationship with HIV testing among MSM in Beijing. This study suggests that stigmatizing and discriminatory attitudes against PLWHA are common and are inversely associated with recent HIV testing among MSM in Beijing. Confronting a rapid rise of HIV epidemic among MSM in China, common negative attitudes towards PLWHA, low levels of testing and high proportion of undiagnosed infections among this group have become emerging challenges in containing the epidemic. The negative attitudes towards PLWHA may be a critical barrier to expanding testing and reducing the proportion of HIV infected individuals who are unaware of their status. Studies have demonstrated that stigma and discrimination remains significant barriers to HIV testing in diverse settings[26, 27] and that lack of HIV testing was associated with greater negative attitudes towards PLWHA [5, 28]. The present study among MSM in Beijing highlights the imperative need to reduce stigmatizing and discriminatory attitudes towards PLWHA, expand HIV testing and reduce the proportion of undiagnosed HIV infections among this group.

This study shows that having multiple sex partners is independently associated with HIV testing. This is consistent with other findings that MSM who have sex with multiple partners acknowledge their higher risk and undergo testing to determine whether this behavior has resulted in infection [29–31]. A survey in Baltimore which reported the highest HIV prevalence among MSM in U.S. suggested that young MSM with a greater number of lifetime male partners were more likely to receive HIV testing [32]. The present study suggests that addressing multiple sex partners and existing sexual networks may offer an intervention opportunity for expanding HIV testing among Beijing MSM.

This study also suggests that recent HIV testing is independently associated with the awareness of the HIV status of one’s last male partner. This is consistent with other reports from Australia and U.S. [29, 33]. Other studies on stigmatizing attitudes of the general population against PLWHA have shown that HIV/AIDS-related stigma are inversely related to discussion about HIV/AIDS [28, 34], disclosure of HIV status [35], and ever tested for HIV [5, 28]. Multiple sex partners, non-disclosure of HIV status, and negative attitudes towards PLWHA described in this study highlight the urgent need for focused efforts to encourage disclosure of HIV status between partners, promote HIV testing, and decrease stigmatizing and discriminatory attitudes towards PLWHA among MSM in Beijing.

This study suggests that nearly half of MSM have never tested for HIV, which is more than four times the level measured among MSM in 21 cities of U.S. in 2008 (10%) [36]. Men with undiagnosed HIV infection are also more likely to engage in unprotected anal sex and have unknown serostatus partners [37]. Men with undiagnosed HIV infection are also unaware of their most recent partner’s serostatus and hold higher negative attitudes towards safe sex practices. Recently community-based clinic trials results have provided proof of antiretroviral treatment as prevention [38–41]. The early initiation of antiretroviral therapy reduced rates of sexual transmission of HIV-1 and clinical events, indicating both personal and public health benefits from such therapy [41]. It is time to address various barriers in scaling up the effort to translate the best advancements in science to the needs of the community. It is critical to better understand stigmatizing and discrimination attitudes towards PLWHA when expanding HIV testing, prevention, care and treatment in controlling epidemic among this group.

This study also found that younger MSM are more likely to express lower negative attitudes towards PLWHA. The reasons for this could be that the younger MSM have higher levels of education, lower perceived social pressure towards HIV infections and homosexuality, and have greater access to HIV/AIDS message and health information. Studies on stigmatizing attitudes of the general population against PLWHA show that HIV/AIDS-related stigma are inversely related to knowledge about modes of HIV transmission [34], educational attainment [34, 42], and positively related to age [24]. The present study also found that bisexual MSM were inversely associated with HIV testing. A study among MSM in Shandong found that bisexual men are more likely to be older and have lower levels of HIV-related knowledge than men who have sex with men-only [43]. Bisexual practices described in the present study are consistent with previous studies and other reports in China [17, 43–47], it is more prevalent than reported in the West [48]. Chinese culture is still relatively conservative in discussing homosexuality as an open subject [49]. Stigma and discrimination towards MSM in Chinese societies may be still quite serious [50], and may explain partially the prevalence of bisexual behaviors [43]. Widespread stigmatizing and discriminatory attitudes against PLWHA and prevalent bisexual practices among MSM in Beijing highlight the challenges in effectively expanding HIV testing for this population.

This study highlights an important area that warrants HIV prevention and research work. We also recognize the limitations of this study. First, the stigma/discrimination scale may provoke socially desirable answers from respondents. Participants may feel embarrassed to be openly expressing stigmatizing and discriminatory attitudes towards PLWHA during the face-to-face interviews, thus, this study may have underestimated the true levels of negative attitudes and the risk behavior. Second, the nature of the cross-sectional study design precluded the ascertainment of causal relationship. Other limitations may stem from the monetary incentive having relatively stronger draw among persons of lower socio-economic status, as noted in other RDS surveys [51].

In conclusion, this study suggests that stigmatizing and discriminatory attitudes towards PLWHA are inversely associated with recent testing among MSM in Beijing. Widespread HIV/AIDS-related stigmatizing and discriminatory attitudes, low levels of testing, and a high proportion of undiagnosed infections among this group have become emerging challenges to containing the epidemic. Stigmatizing and discriminatory attitudes towards PLWHA may be a critical barrier to expanding testing and reducing the levels of undiagnosed HIV infections. The findings of this study highlight the imperative need to reduce HIV/AIDS related stigma and discrimination, encourage disclosure of HIV status, and expand HIV testing among MSM.