Introduction

HIV is a serious epidemic among men who have sex with men (MSM) in China. In this key population, previous studies showed that the HIV prevalence exceeded 20% in a number of cities [1] and the HIV incidence was about five per 100 person-years [2,3]. In Hong Kong, the HIV prevalence was 4.31% in 2008 [4]. As a global strategy for the control of HIV, the World Health Organization (WHO) recommends health workers to increase case detection by promoting HIV antibody testing [5]. Previous studies have shown that HIV voluntary counseling and testing (VCT) is effective for both case detection and reduction of HIV-related risk behaviors [6,7]. It has been used a key measure of HIV prevention targeting MSM populations in China [8]. However, despite availability of free VCT services, the prevalence of life-time HIV antibody testing among MSM in mainland China ranged only from 18% to 47.9%, while it was 56.5% in Hong Kong in 2008 [9–12]. The proportion of MSM in China knowing about their HIV status (26%) is hence lower than those of the U.S. (56%) and Europe (73.7%) [13–16].

Unprotected anal sex (UAI) is prevalent among MSM [17,18], even among those who have ever taken up HIV antibody testing [12,19,20]; such ever-testers remain at high risk of HIV transmission. Case detection for ever-testers through regular HIV antibody testing is especially important as recent evidences show that with good adherence, the provision of earlier anti-retroviral therapy (ART) to HIV-infected individuals can reduce the risk of HIV transmission through sexual intercourse by up to 96% [21]. This effective treatment as prevention (TasP) approach, however, requires an efficient care cascade, which starts with HIV antibody testing and ends up with viral load suppression [22]. Low HIV antibody testing rate would largely diminish the potential effectiveness of using ART for prevention. The WHO guideline recommends MSM with high risk behaviors to take up HIV testing every six to twelve months [23], while the U. S. CDC recommends sexually active MSM to take up HIV testing every three to six months, in order to detect HIV infection and prevent ongoing transmission [24]. There is a dearth of studies investigating how well such guidelines have been followed by MSM.

A number of studies have identified factors associated with previous HIV antibody testing [12,20,25]. However, such studies included participants who had taken up HIV antibody testing only once or multiple times. It hence cannot inform health care workers on how to increase the likelihood of MSM returning for another HIV antibody testing in the future, as factors associated with HIV antibody testing in the past among all MSM may be different from those associated with intention to take up HIV antibody testing again in the future among ever-testers. Furthermore, according to the Trans-theoretical Model, an individual needs to go through five stages of change (pre-contemplation, contemplation, preparation, action and maintenance) before adopting a health-related behavior in the long term [26,27]. Those who had taken up HIV antibody testing only once are in the action stage, whilst those who had taken up HIV antibody testing multiple times are in the maintenance stage. It has been shown that different health promotion strategies are required for individuals at different stages of change [26–28]. Maintenance theory suggests that experience and satisfaction in performing a behavior are strong determinants of maintaining such a behavior [29]. Perceived discrimination exhibited by service providers is certainly a negative experience, while perceived empathy of service providers administering the HIV antibody testing is a satisfying experience of VCT among MSM. It is therefore warranted to understand associations between these two variables and behavioral intention for HIV retesting and their inter-relationship, as such factors are modifiable through interventions.

Perceived discrimination toward MSM is a hurdle against adoption of VCT among MSM [30]. As the Chinese culture does not approve of same-sex sexual behaviors among men [31,32], it is common for Chinese MSM to perceive discrimination against people like themselves [32,33], which has shown to be inversely associated with past HIV antibody testing behavior [12]. Furthermore, there are numerous cases reported that health service providers discriminated against MSM during their service utilization [34]; such acts would further increase perceived discrimination and hinder promotion of regular HIV antibody testing [35]. Perceived discrimination/stigma toward MSM is potentially modifiable [36]. It is warranted to reduce perceived discrimination, and to understand the mechanism (mediator) operating between perceived discrimination and behavioral intention for HIV retesting among MSM.

Perceived quality of service providers has found to be significantly associated with past HIV antibody testing behavior [25]. Empathy (defined as the ability to communicate an understanding of the user’s world and to act on that understanding in the clinical context) of health service providers is one of such important qualities [37,38]. It is associated with various types of health service utilization, such as specialty care, pain assessment and treatment, mental health service, services for child welfare and at-risk youths [39]. To our knowledge, there is however, no study investigating significance of association between perceived empathy of service providers and HIV antibody testing among MSM.

In contrast to discrimination, empathy shown by service providers, which is both cognitive and affectionate in nature, involves effective communication between the service provider and the client [40]. Such communication shares awareness, build up shared feelings and ultimately rapport, and requires an accurate understanding and acceptance of the clients’ feeling and expectation, professional integrity and warmth [41]. Previous studies have shown that perceived discrimination causes significant damages to effective communication between health service providers and their clients [42]. Empathy is also negatively associated with discrimination [42]. Therefore, MSM who perceived discrimination would be less likely than others to perceive empathy from health service providers. As empathy is a part of the communication process between health service providers and their clients [40], there are strong reasons to believe that there exists a mechanism that perceived discrimination would diminish perceived empathy, and in turn reduce behavioral intention to take up VCT among VCT ever-testers who are MSM. This mediation hypothesis was tested statistically in the present study (see Fig. 1). It is possible to increase empathy through training. If perceived empathy is shown to be a mediator, an increase in service providers’ empathy would be a potential means to alleviate negative impact of perceived discrimination onto maintenance of VCT behavior among MSM. It is also possible that perceived empathy of service providers moderates the association between perceived discrimination and behavioral intention for HIV retesting among MSM. Perceived empathy would then have additional protective effect in alleviating the magnitude of the negative effect of perceived discrimination onto HIV retesting. Also, such a moderation hypothesis has never been tested.

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Fig 1. Mediating effect of perceived empathy of service providers of the association between perceived discrimination toward MSM and behavioral intention to take up VCT in the next six months.

https://doi.org/10.1371/journal.pone.0117376.g001

This study hence investigated the prevalence of behavioral intention to take up HIV antibody testing in the next six months among Hong Kong MSM who were ever-testers. Behavioral intention is a strong predictor of future behavior according to literature [43–45] and it has been used in many HIV-related studies as the main outcome variable [17,46]. In addition, we investigated three types of associated factors of behavioral intention to take up HIV antibody testing in the next six months among MSM who were ever-testers, including: 1) background factors (e.g., education level, HIV-related knowledge, UAI with men), 2) perceived discrimination toward MSM in Hong Kong, and 3) perceived empathy of service providers administering the HIV antibody testing.

We hypothesized that ever-testers with higher education level, better HIV-related knowledge, UAI with men, low perceived discrimination toward MSM in Hong Kong, and high perceived empathy of service providers would be more likely than other ever-testers to show behavioral intention to take up HIV testing again in the next six months. Moreover, we tested the hypotheses that perceived empathy of service providers would mediate or moderate the association between perceived discrimination toward MSM in Hong Kong and behavioral intention to take up HIV antibody testing in the next six months.

Methods

Results

Background characteristics

Of the participants, 25% were 25 years old or younger (mean = 30.0 years, standard deviation (SD) = 8.5 years); 67.2% had attained at least senior high education; 73.9% were full-time employers; 93.5% were currently single and 94.1% were Hong Kong residents; 65.6% gave appropriate responses to all the three items on HIV-related knowledge (Table 1). Of those with RP (n = 166), NRP (n = 167) and either RP or NRP (n = 266), respectively 59.0%, 32.3% and 49.2% had UAI with such male sex partners.

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Table 1. Profiles of all participants (MSM who are ever-testers, n = 326).

https://doi.org/10.1371/journal.pone.0117376.t001

Perceived discrimination toward MSM and perceived empathy of service providers

Of the participants, 58.4% perceived that the Hong Kong public discriminated against MSM (no: 7.1%, little: 34.5%, noticeable: 42.9%, strong: 15.5%). Overall, 63.7% to 81% of the participants gave positive ratings (good, very good or excellent) to the individual items of the CARE Measure assessing perceived empathy of service providers (Table 2). We found that the mean CARE Measure score varied by the setting of testing (F = 7.86, df = 2, p<.001); the mean score of those who went to NGO for testing (33.8; SD = 9.3) was higher than those who went to governmental clinics (28.0; SD = 8.5) and those who went to other settings (30.2; SD = 8.9) for testing (p<.001 and p = .011); the latter two means (governmental clinics and other settings) were not statistically different (p = .172).

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Table 2. Item frequency distributions of the CARE Measure.^a

https://doi.org/10.1371/journal.pone.0117376.t002

Factors associated with behavioral intention to take up HIV antibody testing in the next six months

Table 3 shows that none of the background variables was significantly associated with strong behavioral intention to take up HIV antibody testing in the next six months, although two variables, current marital status (married/divorced/other marital status versus single marital status: OR = 2.44, p = .051), and UAI with NRP in the last six months (having had UAI versus absence of NRP: OR = 1.81, p = .066), showed marginal statistical significance (.05<p<.1). Non-significant independent variables with p>.2 included mode of recruitment, age, employment status, HIV-related knowledge, UAI with RP in the last six months, UAI with RP or NRP in the last six months, and the setting of the last episode of HIV antibody testing.

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Table 3. Associations between background factors and behavioral intention to take up HIV antibody testing in the next six months.

https://doi.org/10.1371/journal.pone.0117376.t003

Adjusted for the four background variables with p<.2, perceived discrimination toward MSM (AOR = .60, 95% CI:. 36-.98) and the CARE Measure assessing perceived empathy of service providers (AOR = 1.05, 95% CI: 1.02–1.08) were both significantly associated with strong behavioral intention to take up HIV antibody testing in the next six months (see Model 1 and 2 of Table 4).

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Table 4. Testing associations and mediating effects of behavioral intention to take up HIV antibody testing in the next six months considering factors of perceived discrimination toward MSM and perceived empathy of service providers.

https://doi.org/10.1371/journal.pone.0117376.t004

Discussion

It is seen that only about one third of all the ever-testers expressed strong behavioral intention to take up HIV antibody testing in the next six months. Furthermore, only respectively 42.9% and 18.1% of those who had taken up HIV antibody testing for at least six and 13 months intended to do so again in the next six months. Discounting the discrepancy between behavioral intention and actual future behavior, the proportion of ever-testers who would actually take up HIV antibody testing would even be less. Assuming a discount rate of 40%, only about one-fifth of all ever-testers would eventually return for another HIV antibody testing within the next six months. Such situations are far from ideal and effective health promotion is greatly warranted.

Another published paper which was based on the same data showed that only 12.7% of the MSM who were had never taken up VCT (never-testers making up 44.0% of all sampled MSM) intended to take up VCT again in the next six months [19]. It is expected that prevalence of behavioral intention to take up VCT among ever-testers (this paper) was higher than that among never testers. However, piecing the two figures of the never-testers and ever-testers together, the picture reveals that despite recommendations made by international health authorities, only a minority of the MSM in Hong Kong intended to take up VCT in the next six months. It implies that only a small fraction of the HIV positive MSM in Hong Kong has been diagnosed, and potential early HIV treatment effect recommended by the WHO in lowering HIV transmission would largely be compromised. Increasing coverage of HIV testing is hence a priority of HIV prevention work targeting MSM.

Given the high prevalence of ever-testers having had UAI with NRP and/or RP, it implies that a high proportion of such MSM were at high risk of HIV transmission. The level of risk cannot be overlooked given the noticeably high prevalence of HIV among MSM in Hong Kong (close to 5%). It is important to point out those at risk of HIV transmission (e.g. having had UAI with RP/NRP) showed similarly low behavioral intention to take up HIV antibody testing in the next six months. Again, taking into account potential discount in behavioral intention without follow-up actions, the prevalence of HIV antibody retesting among at risk MSM who were ever-testers would fall short below that recommended by the U.S. CDC (sexually active MSM: every three to six months) or by the WHO (at risk MSM; every six to 12 months) [23,24].

As expected and in corroboration with the results of other reports, we found that perceived public discrimination toward MSM in Hong Kong was prevalent. In this study, perceived discrimination was found to be strongly associated with behavioral intention to take up HIV antibody testing in the next six months. It is warranted to reduce public discrimination and public stigma toward MSM, which require both structural changes (e.g. policies and legislation) and health promotion efforts. Factors associated with public discrimination toward MSM include knowledge, negative perception [55], and moral concerns [31–32], but such factors are modifiable [34]. Previous studies have shown that interventions could be effective in reducing public stigma toward MSM and/or people living with HIV [56–59]. However, health workers should be made aware of potential worry about layered stigma as those who are tested HIV positive would have to face double perceived discrimination, against his MSM status as well his new HIV positive status [60].

Besides, perceived discrimination is associated with self-stigma [61], which is prevalent among MSM [62–63]. According to some researchers, self-stigma results in concurrence with public stigma and decrement in self-esteem [64] and it is strongly associated with psychological problems [65]. Self-stigma may therefore be resulted from perceived discrimination, and may have both direct and indirect effects onto utilization of health services [65–66], including HIV antibody testing [67]. It is warranted to reduce self-stigma among MSM and a number of effective self-stigma reduction programs based on cognitive behavioral therapy have been reported, although such studies did not target MSM [66]. Research of the relationship between self-stigma and HIV antibody testing among MSM is warranted.

It is also warranted to unlock the association between perceived discrimination and HIV antibody testing. One direction is to investigate coping responses made by MSM under situations of perceived discrimination in order to reduce negative coping [68]. Another direction, which is supported by this study’s key result, is to increase perceived empathy of HIV testing service providers. The negative effect of perceived discrimination in decreasing perceived empathy could be offset by increase in perceived empathy resulted from effective interventions. In this study, perceived empathy was strongly associated with behavioral intention for HIV antibody testing. The finding is consistent with the maintenance theory that suggested that experience and satisfaction in performing a behavior are determinants of maintenance of the behavior [29]. Although the overall situation on perceived empathy of service providers was satisfactory (as two-third or more of the participants showed good responses to the items of the CARE Measures scale), there are still rooms for improvement. For instances, our data showed that slightly more than one third of the participants felt that service providers of HIV antibody testing were not interested to see them as a whole person, did not fully understand them and did not make a plan of action with them. In literature, there are effective interventions to increase empathy among health service providers [69–70]. Since the number of service providers involved HIV testing would be relatively small, training and incentives to improve the situation is highly feasible.

It is interesting to see that the setting of HIV antibody testing (NGO, governmental and other settings) was associated with perceived empathy of service providers. We expected that the mean CARE Measure score would rank in the order of NGO, governmental and other settings. The results showed that the NGO group ranked the highest but those who visited governmental clinics and those did the testing in other settings (largely commercial settings as self-test is not common among MSM in Hong Kong) did not differ in this regard. Service providers of NGO are likely to be local peer MSM workers who would have better sensitivity for needs and culture of MSM. Improvement of governmental services is hence required. We suggest that process evaluation, including assessment of perceived empathy, to be included into regular evaluation of HIV antibody testing services offered by various institutions.

Our results further showed that perceived empathy mediated the association between perceived discrimination and HIV antibody testing as the significance of the association between perceived discrimination and HIV antibody testing disappeared after controlling for CARE Measures. Therefore, our study contributes to the field as we have identified a potential pathway of which perceived discrimination might operate to reduce behavioral intention to return for HIV antibody testing—ever-testers who felt MSM are being discriminated would perceive lower empathy of service providers and hence have lower intention for retesting. Perceived discrimination has therefore another potential negative effect of lowering perceived empathy, a topic that requires further investigation. The mediator of perceived empathy is specific and potentially modifiable [34]. An important insight on how to increase behavioral intention to return for another HIV testing by promotion of empathy therefore emerges. Intervention strategies based on improvement of empathy can be derived.

The non-significant moderation effect further clarifies the inter-relationship among perceived discrimination, perceived empathy of service providers and behavioral intention for HIV retesting. It implies that the negative impact of perceived public discrimination was the same for those perceiving and not perceiving empathy. Importance of structural intervention to remove public discrimination toward MSM is reinstated.

Return for HIV antibody testing among ever-testers is of utmost importance, as with such a low rate of retesting and hence a low rate of regular HIV antibody testing among at risk MSM, the care and treatment cascade would be highly inefficient [71], and the MSM population would not be able to obtain potential benefits derived from earlier anti-retroviral treatment and TasP approaches. Many of the HIV positive MSM in China did not know about their HIV status [72]. We contended that the low prevalence of retesting is one of the reasons why the HIV incidence among MSM in China was very high (5 to 7 per 100 person-years). To our knowledge, there is no previous study reporting prevalence of regular HIV antibody testing among MSM in Hong Kong and in mainland China.

This study has a number of limitations. First, it was based neither on probability sampling (which was not feasible) nor respondent-driven sampling methods. Since many HIV interventions targeting MSM are venue-based or internet-based [73–74], the venue-based and internet-based study design of this study has a practical implication that the promotion of HIV antibody testing may take place in such settings. Second, this is a cross-sectional study and no causal relationship could be established. Third, the outcome variable of this study is behavioral intention to take up HIV antibody testing and longitudinal studies investigating actual adoption of HIV antibody testing is warranted. Fourth, perceived discrimination toward MSM in Hong Kong was based on a single question and could not be validated. Lastly, data were self-reported and reporting bias may exist although anonymity would have reduced the bias. Reporting bias would favor intention to take up HIV antibody testing; the actual prevalence of intention to take up HIV antibody testing may hence be lower than that reported in this study. Lastly, the category of other settings for the last episode of HIV antibody testing did not distinguish commercial versus home-testing settings; prevalence of over-the-counter self-administrated HIV rapid testing (HICSRT) self-testing in Hong Kong was however, low (6% in 2010, unpublished data, n = 577).

In conclusion, performing HIV testing for once only or very infrequently, but not regularly, among at risk MSM would not effectively serve the purposes of case detection and inducement of behavioral changes. Low retesting rate is possibly one of the strongest obstacles compromising the effectiveness of existing HIV prevention among MSM. This study is among the first few ones inspecting problems of HIV antibody retesting and associated factors. We found that improvement in perceived empathy of service providers is a potentially useful strategy to counteract negative impact of perceived discrimination onto HIV antibody retesting among MSM. Randomized controlled trials to be conducted in different countries are required to establish evidence base for translation into services. Such research is urgently and greatly warranted.

Acknowledgments

The authors would like to thank all study respondents. Thanks are extended to all peer fieldworkers for their help in data collection.