Background

Hepatitis C virus (HCV) infection remains a significant public health concern globally [1]. Untreated HCV infection contributes to a variety of severe complications such as liver cirrhosis and hepatocellular carcinoma [2]. According to the World Health Organization (WHO), at least 75 million people living with HCV, and 70,000 die each year from an HCV-related cause [3]. Men who have sex with men (MSM) are disproportionately affected by HCV infection, especially for MSM living with human immunodeficiency virus (HIV). In 2015, a global systematic review estimated that the HCV seroprevalence among MSM living with HIV was 6.3% (95% CI: 5.3–7.5) compared to 1.5% (95% CI: 1.0-2.1) in HIV-negative MSM worldwide [4]. In China, the estimated prevalence of HCV in general MSM was 0.67%, whereas the prevalence was about eight times higher among Chinese MSM who were HIV-positive (8.4%) [5].

The introduction of high effective direct-acting antiviral (DAA) therapy has significantly improved HCV treatment outcomes and reduced HCV transmission at the population level [6]. WHO recommends therapy for all HCV-infected individuals, regardless of disease stage [7]. However, MSM encounter barriers along the HCV continuum care, from early testing to achieve a sustained virologic response (SVR) [8]. Previous studies found that lack of HCV-related knowledge was the main reason among MSM [9, 10]. Negative attitudes, lack of self-efficacy, and social stigma also hindered the access and uptake of HCV healthcare services among MSM [10,11,12]. This situation could be worsen due to ongoing COVID-19 restrictions [13]. Numerous studies indicated that improving knowledge was effective in increasing uptake and adherence to antiretroviral therapy [14,15,16,17,18]. However, the studies regarding knowledge of HCV among MSM in China were limited.

This study aimed to explore and examine the knowledge and attitudes about HCV and their determinants among HIV-negative MSM and MSM living with HIV in China to provide effective basis for the development of tailored intervention program.

Methods

Study design and participants

This was a cross-sectional study of baseline data from two parallel randomized controlled trials (RCT), which aimed to evaluate the effectiveness of providing HCV self-testing to increase testing uptake among Chinese MSM: one among HIV-negative MSM and another among MSM living with HIV. Detailed information can be found in the protocol (Appendix p2-23. Study protocol). The baseline survey, was conducted online from December 2021 to January 2022 across seven provinces (Shandong, Guangdong, Liaoning, Qinghai, Hubei, Chongqing and Hebei) in China. Prospective participants were recruited in cooperation with seven local community-based organizations (CBOs). All the MSM living with HIV were recruited offline, whereas the recruitment ratio for HIV-negative MSM was half online and half offline. The offline recruitment was implemented at the MSM-led clinic sites. Staffs in the clinic sites provided information on the study to men who were seeking routine testing and care services, and enrolled HIV-negative men based on their test reports in the past three months and men living with HIV according to their HIV-positive test reports, and then send them links to access the online survey. For the online recruitment, study messages and a survey link were promoted through the chatting platforms or chat groups of the social media software by the CBOs staffs, and participants were required to upload a test result in the past three months to validate their HIV-negative status during the eligibility screening procedure. The survey was administered through Wenjuanxing (Changsha Haoxing Information Technology, China), a professional online questionnaire platform that can provide anonymous surveys.

All potential participants who clicked on the survey link were screened for eligibility after signing an electronic informed consent. Inclusion criteria included: born biologically as a male, aged 18 or over, engaged in anal sex with a man, had not been tested for HCV in the past year, and had at least one of the following risk factors in the past year (condomless anal sex or sexually transmitted infection (STI) diagnosed or injection drug use). Eligible participants must provide a working unique mobile phone number and WeChat account to be enrolled. All men who complete the survey received $3 as compensation for their time.

Measures

Socio-demographics characteristics

Sociodemographic information included: age, region of residence, marital status, educational attainment, employment status, annual income, sexual orientation, and sexual orientation disclosure to healthcare providers, family or friends.

Attitude towards HCV

Attitude towards HCV was measured by 13 items. For example, one item was “I would not want my child to attend school where one of the students had Hepatitis C.” Each item was 1 if participants agreed and 0 if they disagreed or neutral. The total score ranged from 0 to 13. A higher score indicated a more positive attitude towards people living with HCV. We categorized individuals’ attitudes into negative, neutral, and positive if they received scores of 0–3, 4–8, and 9–13, respectively [19].

Knowledge of HCV

Knowledge of HCV infection was measured by 14 items, which was adapted from the HCV knowledge scale developed and validated by Balfour et al. (2009) [20]. Item content areas included: knowledge about HCV transmission, prevention and treatments. Each of the 14 knowledge items was coded 0 for an incorrect answer and 1 for a correct answer, and the total score ranged from 0 to 14. A higher score indicated a better knowledge of HCV infection. We categorized individuals’ knowledge into poor, moderate and good if they received scores of 0–4, 5–9, and 10–14, respectively [19].

Sexual behaviors and testing history

Sexual behavioral variables included number of male sexual partners in the past 3 months, condomless sex with male partners in the last 6 months, group sex, and recreational substances use. Testing history included the following: HIV testing including either facility-based testing or self-testing, testing history for syphilis, Hepatitis B virus (HBV), chlamydia and gonorrhea.

Statistical analysis

Descriptive statistics were used to describe the distribution of the sample regarding socio-demographics, sexual behaviors, HCV-related knowledge, attitudes toward HCV. Chi-square tests were performed to compare differences in knowledge of and attitudes toward HCV across subgroups of respondents by socio-demographic and behavioral characteristics. Univariate and multivariable logistic regressions were conducted to explore the factors associated with knowledge and attitude about HCV. In the multivariable models, we adjusted for age, region of residence, education, marital status, and income. Statistical significance was defined as p < 0.05. All analyses were conducted using R (version 4.1.0).

Results

Overall, 410 people were approached for screening. Of whom, 1 did not complete the baseline survey and 230 did not meet eligibility requirements (7 were born biologically as a female, 7 were less than 18 years old, 40 reported no anal sex with other men, 87 was tested for HCV in the past year, 89 had no designated risk factors in the past year). A total of 179 individuals completed the online survey. Among them, 11 were further excluded, as they were unwilling to provide contact information (n = 10) and HIV-negative testing report (n = 1). In total, 168 participants (84 HIV-negative men and 84 men living with HIV) were included in this study. (Fig. 1)

Fig. 1
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Flowchart diagram of study population

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Socio-demographic characteristics

Most individuals reported never married (87.5%), employed (61.9%), had attained at least a junior college education (78.0%), had a moderate annual income (58.9% annual income between 5651 and 15,100 USD), and disclosed their sexual orientation to health provider, family or friends (69.6%). Key social-demographic were similar between individuals living with HIV and those who were HIV negative, except for the age and sexual orientation. (Table 1)

Table 1 Baseline social-demographic and behavioral characteristics of MSM in China
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Knowledge about HCV

Among HIV-negative men, the mean of correct answer rate for the 14 items on HCV knowledge was 53.9%. Only 39.3% (33/84) had a good level knowledge. (Table 2) The highest correct response (67.9%, 57/84) were obtained for two questions ‘The consumption of alcohol by people with HCV can damage the liver’ and ‘Using new, never used needles, syringes and other equipment reduces the risk of HCV infection’. The most frequently incorrect response (26.2%, 22/84) was for ‘The HCV vaccine can be used to prevent new infections with this virus’. (Table 3) Comparisons of knowledge level by socio-demographic and behavioral characteristics showed that only one variable was significantly different: employment status (p < 0.05). (Table 2)

Table 2 Participant characteristics by different levels of knowledge and factors correlated with knowledge among men who have sex with men in China
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Table 3 Knowledge related to HCV among MSM in China
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For men living with HIV, the mean rate was 55.6%. A total of 44.0% (37/84) had a good level of knowledge. (Table 2) The highest correct response (77.4%, 65/84) was obtained for the question ‘The consumption of alcohol by people with HCV can damage the liver’. The least correct response (10.7%, 9/84) was for ‘The HCV vaccine can be used to prevent new infections with this virus’. (Table 3) Comparisons of knowledge level by participants characteristics showed that four variables were significantly different in men living with HIV: the status of sexual orientation disclosure, number of sexual partners in the past 3 months, syphilis and HBV testing history (P < 0.05). (Table 2)

Comparing with MSM living with HIV, more HIV-negative men correctly reported that HCV cannot be prevented by vaccination (26.2% versus 10.7%, p < 0.05), but more incorrectly answered that HCV treatment did not eradicate the virus (35.7% versus 53.6%, p < 0.05). (Table 3)

Attitude towards HCV

For HIV-negative men, nearly one-third (32.1%, 27/84) had a positive attitude towards HCV. (Table 4) Half (50.0%, 42/84) disagreed with the statement that ‘I would not want to be friends with someone with HCV’, which obtained the highest positive attitude score. More than a quarter (27.3%, 23/84) agreed with the statement that ‘I would feel uncomfortable having a conversation with someone who had HCV’, which obtained the highest negative attitude score (Table 5). Comparisons of attitudes level by participant characteristics showed that two variables were significantly different in HIV-negative men: substances use status and number of sexual partners in the past 3 months (p < 0.05). (Table 4)

Table 4 Participant characteristics by different levels of attitudes and factors correlated with attitudes among men who have sex with men in China
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Table 5 Attitudes towards people living with HCV among MSM in China
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Among men living with HIV, a total of 41.7% (35/84) of the men reported a positive attitude towards people with HCV. (Table 4) Nearly two-thirds (65.5%, 55/84) disagreed with the statement that ‘I would feel uncomfortable having a conversation with someone who had HCV’, which obtained the highest positive attitude score. In addition, 34.5% (29/84) agreed with the statement that ‘I would not kiss someone with HCV’, and this statement showed the highest negative attitude score. (Table 5) Comparisons of attitudes level by participants characteristics showed that only two variables were significantly different in men living with HIV: recreational substances use status and education levels (p < 0.05). (Table 4)

Compared with HIV-negative men, men living with HIV significantly agreed more that they would feel pity for someone with HCV (59.5% versus 44.1%, p < 0.01). Moreover, men living with HIV significantly more often disagreed with two statements: ‘I would not want to go to a small neighborhood grocery store where the owner had HCV’ (62.0% versus 41.7%, p < 0.05), and ‘I would feel uncomfortable having a conversation with someone who had HCV’ (66.6% versus 50.0%, p < 0.05). (Table 5)

Sexual behaviors and STD testing history

Most participants reported having engaged in condomless anal intercourse in the past 6 months (73.1%, 98/134). Over half reported having two or more male anal sex partners in the past three months (58.9%, 99/168), having substance use before or during sex (53.6%, 90/168). In terms of other STD testing, about two-thirds (63.7%, 107/168) had tested for syphilis, roughly half (45.2%, 76/168) had ever tested for HBV, and a fifth tested for chlamydia (16.1%, 27/168) or gonorrhea (20.8%, 35/168). The sexual behavior and testing history characteristics of HIV-negative respondents were comparable to men living with HIV, except for the STI diagnosis experience. (Table 1)

Factors correlated with knowledge about HCV

In the multivariable ordinal logistic regression analyses adjusted for age, region of residence, education background, marital status, employment status, and monthly income, there was no factor significantly associated with the level of HCV knowledge in HIV-negative men.

For men who living with HIV, the odds of moving from a poor level of knowledge to a moderate or good level of knowledge among men who disclosed their sexual orientation were 7 times (aOR: 7.0, 95%CI: 1.9–26.0) greater than those did not. Two other factors were also positively associated with a higher odds of having a good level of knowledge: substances use before or during sex (aOR: 3.7, 95%CI: 1.1–13.1), and HBV testing history (aOR: 7.3, 95% CI: 1.6–32.7). The other factor of men who had multiple sexual partners was negatively associated with a higher likelihood of having a good level of knowledge (aOR: 0.2, 95% CI: 0.1-1.0). (Table 2).

Factors correlated with attitude towards HCV

For HIV-negative men, the odds of moving from negative attitude towards people living with HIV to neutral or positive attitude in men with multiple sexual partners were 5.8 times (aOR: 5.8, 95% CI: 1.9–18.1) greater than those with only one or no sexual partners. Another factor was also positively associated with a higher odds of having a positive attitudes: substances use before or during sex (aOR: 3.1, 95% CI: 1.0-9.4).

For men living with HIV, only one factor was positively associated with a higher odds of having a positive attitudes: substances use before or during sex (aOR: 3.1, 95% CI: 1.1-9.0). (Table 4)

Discussion

MSM are at high risk of HCV acquisition and transmission, especially for those living with HIV. Knowing about the knowledge and attitudes related to HCV among MSM are critical for designing tailored interventions to prevent and eliminate HCV. Our study is one of very limited studies evaluating the overall knowledge and attitudes about HCV infection among MSM in China. Findings in this study indicated that a much greater effort is needed to improve the knowledge and attitudes about HCV infection among Chinese MSM.

We found that many Chinese MSM did not have a good level of knowledge about the HCV irrespective of HIV infection status. The mean correct answer rates of HCV knowledge of HIV-negative men (53.9%) and men living with HIV (55.6%) in our study were lower than previously reported among HCV patients (77%) and HCV/HIV co-infected patients (76%) in Canada [20]. The low rates of knowledge suggests a relative lack of tailored HCV education campaigns for MSM. Most participants in our study maintained accurate knowledge on some aspect of HCV transmission, but some false beliefs that HCV is transmissible by sharing food or kitchenware with infected individuals still existed. In addition, over half of individuals in both subpopulations still harbored some misconceptions about HCV vaccination and reinfection, which may diminish threat perceived and lead to less implementation of preventive measures. Studies have shown that low self-perceived risk may contribute to increased incidence of HCV in marginalized populations [21, 22]. Therefore, a greater emphasis should be placed on health promotion and risk communication with MSM, as well as ongoing, comprehensive HCV educational programs should be available to address the knowledge differences.

Our study showed that negative attitudes towards HCV have been common in Chinese MSM, especially in HIV-negative MSM. These negative attitudes may be related to misconceptions and fear of HCV. HIV-negative men were more likely to socially exclude HCV patients compared with MSM living with HIV, which is consistent with a previous study conducted in Australian MSM [23]. Given the differences in attitudes between the two subpopulations, effective interventions for MSM should be tailored according to HIV status. Men living with HIV were more likely to feel pity for and socially accept HCV patients, demonstrating the possibility of developing interventions based on a common perception of vulnerability to HCV within this subpopulation. For HIV-negative MSM, eliminating misconceptions and reducing negative attitudes towards HCV should be the main focus of the strategy, placing particular emphasis on beneficial information in educational materials could be helpful, such as the curability of HCV and the safety of daily social contact with HCV patients.

In the present study, most HIV-negative MSM and MSM living with HIV have reported risky sexual practices such as condomless anal sex, multiple sexual partners and the use of mucosally administered recreational drugs. Sexual behaviors leading to mucosal trauma is the predominant route of HCV acquisition among MSM, especially in HIV-infected individuals [24, 25]. Meanwhile, we found that over one-third of both HIV-negative MSM and MSM living with HIV did not know that HCV can be transmitted through sexual contact. This misunderstanding may hinder the use of effective HCV risk reduction strategies and increase propensities for high-risk sexual behaviors, which may explain the higher HCV burden in the MSM population. These findings highlight that HCV prevention efforts targeting MSM should also be focused on activating behavioral changes. However, current behavioral interventions that have been shown to be effective in lowering risky acts still suffer from low uptake, [26, 27] and may be insufficient as a stand-alone prevention strategy in reducing HCV transmission and infection [28]. Thus, multicomponent packages of evidence-based behavioral, educational and structural interventions (e.g., decreasing stigma and discrimination related to being gay) must be assembled to be appropriate, acceptable, and deliverable to the MSM population, so as to improve dissemination and eventual uptake of HCV interventions among this marginalized population [29, 30].

There are several limitations in this study. First, as all collected data were self-reported, social desirability bias may be present. However, we anticipate that this bias to be minimal as the survey was anonymous. Second, online survey might cause selection bias in the study, since recruited participants were primarily MSM who were young and well educated [31]. Nevertheless, our empirical generalizability research suggested that the results were similar when the online survey was quantitatively generalized to a national, cross-sectional survey dataset on MSM in China [32]. Third, this study was cross-sectional, therefore there was no causal relationships can be inferred. Fourth, our study recruited participant with a relatively small sample size, this may limit the statistical inference and generalizations of the results. However, according to a previous study that when sample size is 10 times greater than the number of variables, the power of the result was enough [33].

In conclusion, many Chinese MSM did not have a good level of knowledge and positive attitudes about HCV irrespective of HIV infection status. Tailored public health campaigns are required to ensure that MSM possess adequate and accurate knowledge. Given the negative attitudes can contribute to stigma and isolation, more research is required to inform how best to address the negative attitudes.