Introduction

Sexual transmission by men that have sex with men (MSM) is the most commonly reported route of human immunodeficiency virus (HIV) transmission in Beijing and this group is disproportionately affected by HIV and accounts to 77.97% of the newly diagnosed cases [1]. During the initial years of the HIV epidemic, condom use was the only method available for preventing HIV transmission among MSM. However, a previous study demonstrated that the rate of consistent condom use during anal sex was relatively constant, without an obvious increase (approximately 60%–70%) for many years [2]. Therefore, the identification of new intervention methods to prevent the spread of HIV among MSM is of paramount importance.

The use of combined antiretroviral therapy (cART) has greatly improved the lives of people living with HIV/AIDS. More recently, considerable attention has been given to the use of cART as a strategy to prevent or control the spread of HIV transmission in several ways. It involves taking antiretroviral treatment to reduce the chances of HIV infection. In 2005, the United States Centers for Disease Control and Prevention (CDC) recommended a 28-day course of highly active antiretroviral therapy for individuals who experience nonoccupational exposure to blood, semen, or genital secretions from a known HIV-positive individual, provided they seek treatment within 72 h of exposure [3]. The cost-effectiveness of nonoccupational HIV post-exposure prophylaxis (nPEP) has been demonstrated, especially in high-risk groups [4].

Individuals who may require nPEP should be aware of its existence and be urged to request it immediately after high-risk exposure or condom failure. However, related studies in China are limited. Given that knowledge regarding nPEP is a prerequisite (although not sufficient) for acceptability, the current study sought to elucidate the behavioral, demographic, and social parameters correlating with nPEP. Identifying these parameters is essential in providing population-specific information. We aimed to study the factors associated with nPEP awareness among MSM. The results of our analysis will help policymakers conceptualize better strategies to increase the awareness and use of nPEP among MSM in Beijing.

Materials and methods

Sampling and recruitment

From April to August of 2018 and 2019, 13 and 11 MSM with different demographic characteristics were selected as survey seeds, respectively, and three recruitment cards were issued to each of them. They subsequently selected three other MSM from their friends to participate in the survey. The seeds had to meet the following inclusion criteria: a) be willing to recruit other MSM participants, b) have a wide range of contacts in the MSM community, and c) have a selection of seeds from across all types of demography. Seeds were selected mainly according to age, education level, and means of meeting partners, and they exhibited various types of these three aspects (Table 1). Each participant had to have a recruitment card to participate in the survey. After completing the survey, each participant received three recruitment cards. Recruitment continued until the number of participants reached approximately 600 per year.

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Table 1. Demographic composition of the study seeds in 2018 and 2019.

https://doi.org/10.1371/journal.pone.0255108.t001

After written informed consent was obtained from the participants, each subject underwent an anonymous interview to collect information. Participants were interviewed by skilled interviewers in a private room at the voluntary counseling and testing clinic of the Beijing CDC. Mobile phone numbers or email addresses were also provided by the participants for notification of laboratory testing results, when necessary. A cash reward of 50 Chinese Yuan (CNY) (approximately 7–8 United States dollars) was awarded for participation in the questionnaire survey. On recruiting three MSM, a participant would also receive a reward of 100 CNY. As a part of the national HIV sentinel surveillance program, this study was approved by the Institutional Review Board of the National Center for AIDS/STD Control and Prevention, China CDC, (IRB0000276 and FWA00002958).

Results

Population characteristics

Between 2018 and 2019, 1,202 MSM (602 and 600 in 2018 and 2019, respectively) were recruited. The average age of the MSM in our study was 39.4 years (SD±11.0). Table 2 demonstrates the characteristics of HIV-infection rate, demographics, condom use, HIV-testing history, and HIV knowledge among recruited MSM. Of these, 42.0% had a college degree or higher. Homosexual orientation was observed in 65.1% of the participants. Consistent condom use in sexual intercourse during the preceding 6 months was observed in 60.7% of our study population, and the self-reported history of contracting sexually transmitted infections (STIs) was 16.1%. Of the surveyed MSM, 66.4% were tested for HIV within the preceding 12 months. The HIV-infection rate was 7.8%. During the study, 79.8% of the MSM received peer-educator support. HIV knowledge was identified in 90.6% of the MSM in our study. The average stigma score was 3.7 (SD±1.2).

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Table 2. Demographic and behavioral characteristics of MSM recruited in 2018 and 2019 in Beijing, China (N = 1202).

https://doi.org/10.1371/journal.pone.0255108.t002

Awareness, knowledge, and use of nPEP

Of the study participants, 42.5% reported having heard of nPEP. A total of 21 respondents (1.7%) reported previous nPEP use (Table 2). Table 3 shows the knowledge of nPEP among MSM. A total of 59.9% indicated that they would use nPEP in the future, if required. Of the MSM, 67.3% knew where to purchase nPEP medication. However, more than 60% of the MSM were not aware of the timing and duration of nPEP intake. The main reason for using nPEP was their involvement in high-risk sexual intercourse (85.7%).

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Table 3. Knowledge of nPEP among MSM recruited in 2018 and 2019 in Beijing, China (n = 511)^a.

https://doi.org/10.1371/journal.pone.0255108.t003

Factors related to nPEP awareness

Univariate and multivariate analyses were performed to explore the possible factors associated with nPEP awareness (Table 4). In the univariate analysis, we found the following factors to be associated with increased nPEP awareness: (1) age under 40 years (OR for 25–39 years of age was 3.493, 95% CI: 2.721–4.485, P<0.001, OR and that for age under 25 years 3.066, 95% CI: 1.849–5.085, P<0.001), (2) living in Beijing for over two years (OR: 1.893, 95% CI: 1.338–2.678, P<0.001), (3) attended college-level education and/or higher (OR: 9.483, 95% CI: 7.270–12.368, P<0.001), (4) higher monthly income (OR for income of 5,000–10,000 CNY was 2.982, 95% CI: 2.242–3.966, P<0.001, and OR that of 10,000 CNY and above 9.754, 95% CI: 6.955–13.680, P<0.001), (5) homosexual orientation versus bisexual (OR: 2.300, 95% CI: 1.788–2.959, P<0.001), (6) use of the Internet as the main way of meeting sexual partners (OR: 3.366, 95% CI: 2.615–4.334, P<0.001), (7) having good HIV knowledge (OR:8.776, 95%CI: 4.536–16.980, P<0.001), (8) use of rush poppers during the preceding 6 months (OR: 2.670, 95% CI: 2.071–3.442, P<0.001), (9) HIV-testing in the preceding 12 months (OR: 2.607, 95% CI: 2.014–3.375, P<0.001), (10) infection with an STI (OR: 1.793, 95% CI: 1.316–2.444, P<0.001), and (11) participation in peer-education programs on HIV prevention in the preceding 12 months (OR: 2.505, 95% CI: 1.830–3.428, P<0.001). MSM who were married/cohabitating and divorced/widowed were less likely to be aware of nPEP (OR: 0.264, 95% CI: 0.202–0.344, P<0.001, and OR: 0.310, 95% CI: 0.210–0.457, P<0.001, respectively). Those with HIV and syphilis infection (OR: 0.520, 95% CI: 0.327–0.825, P = 0.006, and OR: 0.538, 95% CI: 0.319–0.906, P = 0.020, respectively) and higher stigma score (OR: 0.637, 95% CI: 0.574–0.708, P<0.001) were also less likely to acquire nPEP knowledge.

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Table 4. Factors associated with the nPEP awareness among MSM recruited in 2018 and 2019 in Beijing, China.

https://doi.org/10.1371/journal.pone.0255108.t004

Multivariate logistic regression showed that MSM were two fold more likely to be aware of nPEP if they were younger (aOR for 25–39 years of age was 1.711, 95% CI: 1.246–2.351, p = 0.001, and that for age under 25 years was 2.343, 95% CI: 1.274–4.308, p = 0.006). MSM with high income were more likely to hear about nPEP (aOR: 1.471, 95% CI: 1.033–2.095, p = 0.032, and aOR: 2.801, 95% CI: 1.809–4.337, p<0.001). In addition, other factors, including having a college or higher degree (aOR: 4.011, 95% CI: 2.834–5.678, P<0.001), having used the Internet as their main way of meeting sexual partners (aOR: 2.016, 95% CI: 1.481–2.744, P<0.001), having good HIV knowledge (aOR: 3.817, 95% CI: 1.845–7.899, p<0.001), HIV testing in the preceding 12 months (aOR: 2.584, 95% CI: 1.874–3.563, p<0.001), and infection with STIs (aOR: 1.736, 95% CI: 1.174–2.569, P = 0.006) were found to be associated with increased nPEP awareness. MSM who had greater stigma score (aOR: 0.804, 95% CI: 0.713–0.906, P<0.001) were less likely to hear about nPEP.

Discussion

In the present study, 42.5% of MSM had heard about nPEP, and 1.7% had previously received nPEP. Knowledge of nPEP varies widely by geographical region; the rate of nPEP awareness among the present MSM was higher than that reported in Spain between 2009 and 2010 (34%) [6], San Juan between 2010 and 2012 (16%) [7], and New York from 2006 to 2007 (36%) [8]; however, it was similar to that reported in Pittsburgh between 2010 and 2012 (47%) [7] and lower than that reported in Boston between 2010 and 2012 (64%) [7], Italy in 2014 (82.3%) [9], New York in 2017 (80.2%) [10], and Africa in 2015 (71.1%) [11]. Although the awareness rate in some areas was lower than ours, most of these studies had small sample sizes or earlier survey times, rendering it difficult for their rates to be consistent with the current ones.

The prevalence of nPEP use was similar to that in Spain between 2009 and 2010 (2.6%) [6], Finland in 2010 (1.3%) [12], and the United States in 1999 (1.9%) [13]; however, it was lower than that in the United States (4.4%) in 2013 [14] and Canada between 2009 and 2012 (8.8–28.7%) [15]. In Beijing, the lack of an nPEP-promotion campaign, which had been undertaken only in recent years and is not widely available as nPEP is prescribed legally in only one Infectious Disease Hospital in Beijing. There has been no structured effort to broadcast its existence to the population. Previous studies have shown that these campaigns can promote the awareness and use of PEP in the future [6–8, 13].

In the analysis of the factors associated with nPEP awareness, we found that MSM with younger age, in general; a high level of education; and high income were more likely to be aware of nPEP probably due to superior knowledge regarding biomedical prevention. However, in similar studies in other countries, socioeconomic status was not a factor for nPEP awareness [10, 11]. This may be related to the unique national conditions and policies regarding the promotion of nPEP or a strong understanding and acceptance of new modalities; therefore, further research is warranted. Conditions associated with living in poverty, such as crowding, underemployment, financial and other stress, and exposure to violence, may increase HIV-risk behavior [16–20]. Therefore, targeting MSM of lower socioeconomic status understand and use nPEP is an issue that should be urgently addressed. A closer association with the MSM culture, such as having low levels of stigma related to sexual orientation, is also related to greater nPEP awareness [6]. Stigma can be perceived as a threat to social identity among MSM. The negative impact of stigma on nPEP awareness may be explained by social isolation and a lack of supportive networks. This corroborates the findings of other studies [9, 10, 21, 22]. Individuals living with high stigma were also less likely to have received nPEP or have had access to prescribers and providers of nPEP [21].

MSM constitute a hidden population, and it is difficult to disseminate health-related information through mass media. LGBTQ-related or institutional websites have become the main channels of awareness. Since 2018, the China CDC has implemented programs and mobilized funding to support the Beijing Health Department and nongovernmental organizations in nPEP implementation. They have also provided extensive nPEP information online, which can be an effective resource for education/outreach programs. It is possible that MSM who use the Internet as their main way of meeting sexual partners may also frequent LGBTQ-related or institutional websites where information regarding preventive measures exists. The use of the Internet for meeting partners was certainly associated with greater nPEP awareness in the present study, and this finding has also been reported by other authors [6, 8].

Survey participants who had undergone HIV-testing in the previous year had, therefore, received a certain degree of HIV-related counseling, which ideally should include education regarding prevention. nPEP awareness among MSM who have been tested is 2.584 times that among those untested. Consistent with previous studies, previous HIV testing could be a marker for higher awareness for HIV risky behavior or reflect previous counselling [8]. Similarly, previous STD infection can also increase the awareness of nPEP, which indicates nPEP knowledge received during healthcare consultation. However, approximately 50% of the MSM who had been tested for STIs or HIV infection remained unaware of nPEP, highlighting a missed opportunity for targeted counseling.

Previous studies have indicated that the links between sexual behavior and nPEP awareness are contradictory and inconclusive [6, 8]. In our study, compared with self-assessed individuals at lower risk of HIV infection, MSM who are at high risk do not have better knowledge regarding nPEP. Further, nPEP awareness did not increase with the number of partners and/or non-association with condom or aphrodisiac use during sexual behavior. Therefore, high-risk groups in need of greater nPEP protection do not have the relevant requisite knowledge.

Therefore, nPEP awareness remains suboptimal and is probably not reaching MSM most likely to benefit from nPEP. To resolve this issue, the following should be considered: First, in the current era of universal HIV testing, providers should also integrate the sexual history of all patients, as understanding patients’ sexual practices can facilitate the appropriate targeting and delivery of HIV prevention and counseling. Second, in our study, peer education did not play an effective role in the dissemination of nPEP knowledge. As shown in other studies, well-trained peer educators are critical in terms of delivering accurate knowledge on HIV [23] and promoting harm-reduction interventions (e.g., condom use, encouraging regular HIV testing, and psychological support) through outreach activities [23, 24]. Therefore, as nPEP is a relatively novel HIV prevention method, health departments should target counseling providers and peer educators for training on nPEP education and referral resources. This may help improve awareness of and access to nPEP for at-risk MSM.

One encouraging finding is that nPEP seems to be very appealing to MSM. Sixty percent of MSM who knew about nPEP indicated that they would likely use nPEP in the future, demonstrating consistency between knowledge, willingness, and actions. It also suggests that lack of awareness is a primary barrier. Unfortunately, more than 30% of MSM do not know where to purchase nPEP medicine, and more than 60% do not know the correct timing for initiating and concluding nPEP therapy. Low rates of nPEP utilization suggest that, even if MSM are aware of nPEP, they may still find it difficult to either recognize the high risk underlying their behavior or identify sources of nPEP medication, since nPEP entails self-identification of a high-risk exposure and healthcare-seeking behavior within 72 h for optimal chemoprotection. This indicates that basic medication information should be included in the nPEP promotion program [14].

Our study had certain limitations. First, due to the cross-sectional design, we could only evaluate the association and not the causality of the risk factors for nPEP awareness. Second, it was difficult to implement randomization. Generally, we applied a convenience sampling method; hence, our results might not have been representative of the entire MSM population in Beijing. Third, in our study, behavioral information relied on self-reporting, which might have been influenced by recall and social-desirability bias.

In conclusion, we found suboptimal awareness and low utilization of nPEP in Beijing. Most MSM were willing to use nPEP in the future, if necessary. It is critical to strengthen the training of healthcare providers and peer educators to improve the dissemination of nPEP knowledge.

Supporting information

Acknowledgments

We would like to express our gratitude to Haijun Yue, Xingang Fan, and our partner organization (Na Mo community) for their assistance in recruiting participants as well as to all the members of the research team. We would also like to thank Editage (www.editage.cn) for English language editing.