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Abstract
Objectives Pay-it-forward incentives effectively promote hepatitis B virus (HBV) and hepatitis C virus (HCV) testing among men who have sex with men (MSM) by offering free testing and donation opportunities. This study aims to explore the interaction between pay-it-forward incentives and recreational drug use on HBV and HCV testing uptake among Chinese MSM.
Methods We pooled data from two pay-it-forward studies that aimed to promote dual HBV and HCV testing among MSM in Jiangsu, China. We explored factors associated with hepatitis testing uptake in the two study groups and examined the interaction between pay-it-forward incentives and recreational drug use on hepatitis testing uptake.
Results Overall, 511 MSM participated in these two studies, with 265 participants in the pay-it-forward incentives group and 246 participants in the standard-of-care group. Among these participants, 59.3% in the pay-it-forward incentive group and 24.8% in the standard-of-care group received dual HBV and HCV testing, respectively. In the pay-it-forward incentives group, participants who used recreational drugs in the past 12 months (adjusted OR (AOR)=1.83, 95% CI 1.09 to 3.06) were more likely to receive dual HBV and HCV testing, compared with those who never used recreational drugs, whereas in the standard-of-care group, those who used recreational drugs were less likely to receive dual HBC and HCV testing (AOR=0.38, 95% CI 0.18 to 0.78). MSM with higher community connectedness (AOR=1.10, 95% CI 1.00 to 1.21) were also more likely to receive hepatitis testing with pay-it-forward incentives. There was a synergistic interaction on both the multiplicative (ratio of ORs=4.83, 95% CI 1.98 to 11.7) and additive scales (the relative excess risk of interaction=2.97, 95% CI 0.56 to 5.38) of pay-it-forward incentives and recreational drug use behaviours on dual HBV and HCV testing uptake among MSM.
Conclusion Pay-it-forward incentives may be particularly useful in promoting hepatitis testing among MSM who use recreational drugs.
- HEPATITIS
- Behavioral Sciences
- HEPATITIS B
- HEPATITIS C
- Homosexuality, Male
Data availability statement
Data are available upon reasonable request.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
Pay-it-forward incentives have demonstrated effectiveness in promoting dual hepatitis B virus (HBV) and hepatitis C virus (HCV) testing among men who have sex with men (MSM). However, the impact of the interaction between pay-it-forward incentives and recreational drug use on dual HBV and HCV testing behaviour remains unclear.
WHAT THIS STUDY ADDS
The synergistic interaction between pay-it-forward incentives and recreational drug use on MSM has both multiplicative and additive effects, affecting the uptake of dual HBV and HCV testing.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
These findings underscore the potential of this innovative incentive model in shaping health-seeking behaviours and highlight opportunities for targeted public health interventions.
Introduction
In 2016, the WHO established ambitious goals to eliminate hepatitis B virus (HBV) and hepatitis C virus (HCV) as a public health threat by 2030.1 Data from 2019 revealed a significant global burden of chronic HBV and hepatitis C virus (HCV infections, estimating approximately 295.9 million people worldwide living with chronic HBV and 57.8 million people living with chronic HCV.2 However, nearly 90% of people living with HBV and 80% of people living with HCV globally are estimated to remain undiagnosed.2 China bears a substantial burden, hosting about 87 million individuals living with HBV, representing one-third of the global HBV population, and approximately 9.5 million living with HCV, constituting one-sixth of the global HCV population.3 4 Despite these high prevalences, only 19% of those living with HBV and 18% living with HCV know their serostatus in China,5 reaching the HBV and HCV elimination goal becomes a challenging endeavour for the country.
Men who have sex with men (MSM) are a key population group for HBV and HCV infections.6 Studies, such as a multicity study in Brazil revealing a 10.1% HBV prevalence among MSM7 and a global meta-analysis showing an HCV prevalence 3.04 times higher among MSM than the general population,8 emphasise this vulnerability. In China, the estimated prevalence of HBV and HCV among MSM was 8.9% and 1.2%, respectively.9 Despite the pressing need to expand testing, rates remain dismally low in China,10 as evidenced by a recent national survey indicating that 62% of Chinese MSM had never been tested for HBV and 60% for HCV.11 Forty per cent not being tested underscores a critical impediment to achieving the WHO’s goal of eliminating HBV and HCV as major public health threats by 2030. To implement health promotion measures effectively, it is important to understand the correlates of hepatitis testing uptake among MSM. However, most of the published studies on MSM have focused on hepatitis infection, and the factors associated with their test uptake have not been well described.
Pay-it-forward (PIF), a community-led social innovation approach, can substantially improve HBV and HCV testing among MSM.12 This intervention aims to provide someone an opportunity to receive subsidised hepatitis testing and a subsequent opportunity to donate to encourage hepatitis testing among their peers.13 Our previous randomised controlled trial (RCT) indicated a significant 35.2% increase in HBV and HCV testing rates among MSM and a substantial 50.3% increase among MSM who used recreational drugs due to the implementation of PIF incentives.12 This suggests that the PIF incentives may be more effective in promoting HBV/HCV testing among MSM who are recreational drug users.
Recreational drug use among MSM is recognised as a pertinent factor affecting health behaviours.14 Among the MSM population, individuals who engage in drug use might encounter more severe or widespread hepatitis infections compared with other subgroups.8 Barriers such as lack of awareness, stigma, discrimination and fear of legal consequences related to drug use often deter MSM who use drugs from seeking routine medical care or participating in testing and treatment programmes or other health issues.15 Previous research has indicated that individuals engaged in drug use may demonstrate distinct behavioural patterns regarding healthcare-seeking practices,16 potentially impacting their response to interventions such as PIF incentives. Understanding how these factors interact can provide crucial insights into tailoring interventions effectively. Moreover, elucidating this interaction could unveil specific subgroups within the MSM community that may benefit most from tailored interventions, thereby enhancing the precision and impact of public health strategies aimed at promoting hepatitis testing among this population. However, it is unclear what is the interplay between the PIF incentives and previous recreational drug usage in affecting the HBV/HCV testing behaviours. Hence, this study aimed to identify the potential determinants of HBV and HCV testing uptake among Chinese MSM under different funding contexts and explore how past recreational drug usage interacts with PIF incentives in promoting HBV and HCV testing uptake.
Materials and methods
Study design and population
This study used data from a quasi-experimental study and an RCT (ChiCTR2100046140) evaluating the effectiveness of PIF incentives in promoting testing uptake among MSM in Jiangsu province, China.12The quasi-experimental study was conducted before this RCT for piloting and followed a similar intervention strategy without randomisation. The sample size of the RCT was calculated based on the superiority cluster randomised trial design. Given a superiority margin of 0.2 and an intraclass correlation coefficient of 0.02, as well as 80% power at the 5% significance level, the RCT calculated the need for 160 participants in each group. A detailed description of the RCT can be found elsewhere.12 From January 2021 to November 2021, both studies were conducted in Nanjing, Suzhou and Wuxi. In each city, participants were recruited by MSM-led community staff. During the study period, men who sought HIV or syphilis testing at the study sites and met the following criteria were invited to participate in the study: (1) 18 years old or above; (2) self-identified as MSM; (3) assigned a male gender at birth and (4) neither tested for hepatitis B surface antigen nor HCV antibody in the past 12 months. Men with a chronic HBV or HCV infection diagnosis and those who did not provide informed consent were excluded. Eligible participants either received PIF incentives (intervention group) or standard-of-care (SOC, control group). Participants in the PIF incentives group received free dual HBV and HCV testing donated by previous participants. Then, they were asked if they would like to donate any amount of money voluntarily to support HBV and HCV testing for subsequent participants. In contrast, participants in the SOC group had to pay RMB 50 (~$7.7) for HBV and HCV testing as is the standard at the clinic. In both groups, participants completed a brief, self-administered online questionnaire hosted on the Wenjuanxing online survey platform.
Measures
The main outcome of interest was the proportion of MSM tested for HBV and HCV in each group. Data on the uptake of dual HBV and HCV testing among MSM were collected from administration records at each community-led organisation.
The questionnaire collected information on sociodemographics (including age, ethnicity, level of education, marital status, employment status, sexual orientation and monthly salary), condomless anal sexual behaviour and number of sexual partners in the past 3 months, previous history of recreational drug use, community engagement, community connectedness, social cohesion and gratitude (online supplemental data 1). Recreational drug use was measured by asking participants whether they had used the following substances for non-medical purposes in the past year: Cannabinoids (eg, Cannabis cigarettes, Hashish), Opioids (eg, Heroin, Methadone), Amphetamines (eg, MDMA, Methamphetamine), Hallucinogens (eg, Ketamine, LSD), Cocaine (eg, Coca leaf, Crack cocaine) and Aphrodisiacs (eg, Rush Popper, 5-Methoxy-diisopropyltryptamine). If the participant answered yes to either of the listed substances, they were categorised as having used recreational drugs.
Supplemental material
The level of community engagement was measured using an instrument used among MSM populations in China.17 The instrument consists of six binary items: (1) ever discussed online about MSM community-related issues, (2) aware of ongoing MSM community events, (3) ever encouraged someone to use MSM community resources, (4) ever attended community events, (5) ever donated to MSM-related causes and (6) ever volunteered for MSM-related causes. Each participant was categorised as having no, minimal, moderate or substantial engagement based on responses to the six items.17
Community connectedness refers to the desire of individuals to belong to a larger collective group.18 The adapted community connectedness scale assessed participants’ connectedness to the MSM community.18 Each item ranged from 0 to 3 (0=strongly disagree, 1=disagree, 2=agree and 3=strongly agree) and a computed aggregate score for each participant indicated the level of community connectedness. Higher scores indicate greater feelings of connectedness (Cronbach’s alpha=0.706).
Social cohesion was measured using a modified 7-item social cohesion scale ranging from 0 to 3 (0=strongly disagree, 1=disagree, 2=agree and 3=strongly agree), adapted from Swaziland.19 Items 6 and 7 were reverse-coded. The total score ranges from 0 to 21, and a higher score meant higher levels of social cohesion (Cronbach’s alpha=0.706).
Gratitude was assessed using the Gratitude Questionnaire (GQ-6), a six-item Likert scale ranging from 1 (strongly disagree) to 4 (strongly agree).20 Reverse scores for items 3 and 6 were aggregated with scores of items 1, 2, 4 and 5 to get the total score, which ranged between 6 and 24, with higher scores indicating a stronger sense of gratitude (Cronbach’s alpha=0.864).
Statistical analysis
Descriptive statistics were used to characterise the study population. The categorical variables were reported as numbers (%), continuous variables were expressed as mean±SD if they followed a normal distribution, and median (IQR, IQR) for skewed distributions. Univariable logistic regression was used to determine factors associated with dual HBV and HCV testing separately for the stand-of-care and PIF incentives groups. Variables including age, study site, education and marital status were recognised a priori as potential confounders. Subsequently, in multivariable logistic regression models, we adjusted for these preselected confounders to assess the factors associated with dual HBV and HCV testing uptake. The interaction between intervention and drug use behaviours on dual HBV and HCV testing uptake was formally examined on multiplicative and additive scales.21 The relative excess risk of interaction (RERI), attributable proportion (AP) of interaction and synergy index (SI) were used to evaluate the additive interaction. RERI quantifies the excess risk due to the interaction between two factors beyond the sum of their individual effects. A positive RERI suggests a positive interaction, indicating that the combined effect of the two factors is greater than the sum of their effects.22 AP represents the proportion of the combined effect of two factors attributable to their interaction, ranging from 0 (no interaction) to 1 (full interaction).22 SI measures the extent to which the combined effect of two factors is greater than the additive effect of each factor alone.22 If the CIs of RERI and AP include 0, and the CI of SI includes 1, there is no significant statistical interaction.22 SPSS V.26.0 and R V.4.1.1 statistical software were used to conduct all the analyses and p values ≤0.05 indicated statistical significance.
Results
Out of 627 MSM interested in participation, 116 participants were excluded because they had tested for HBV or HCV in the past 12 months and 511 were enrolled (322 RCT participants and 189 quasi-experimental study participants). Two hundred and sixty-five participants were in the PIF incentives group, and 246 were in the SOC group (online supplemental data 2).
Supplemental material
Sociodemographic characteristics of participants
The median age of participants was 30 years old (IQR, 25–37) in the SOC group and 29 years old (IQR, 25–39) in the PIF incentives group. Most participants were of Han ethnicity (97.5%), had a college and above level of education (80.4%), were unmarried (73.8%), employed (79.3%) and identified as gay (70.5%). Nearly half of the participants in the SOC group (48.9%) and more than one-third of the PIF incentives group (37.7%) earned between 801 and 1550 US$ monthly. More participants in the PIF incentives group (40.4%) had used recreational drugs in the past 12 months compared with the SOC group (31.3%). More participants in the PIF incentives group (48.3%) had condomless anal sex or more than two sexual partners in the past 3 months compared with the SOC group (37.8%) (table 1).
Descriptive statistics showing the sociodemographic characteristics of MSM participants, 2021 (N=511)
For community engagement, about two-fifths of participants reported minimal engagement in the SOC group (44.7%). In comparison, about one-third of participants in the PIF incentives group reported moderate engagement (34.3%). The median score on community connectedness was 12 (IQR: 11–17) in the SOC group and 13 (IQR: 11–16) in the PIF incentives group; the median score on social cohesion was 12 (IQR:10–14) in the SOC group and 12 (IQR: 10–14) in the PIF incentives group; the median score on the GQ-6 was 18 (IQR: 16–20) in the SOC group and 18 (IQR: 16–20) in the PIF incentives group (table 1).
Dual HBV and HCV test uptake
In the quasi-experimental study, 31.3% (20/84) of participants in the SOC group and 69.4% (62/105) in the PIF incentives group received dual HBV and HCV testing. In the RCT, 25.3% (41/162) of participants in the SOC group and 59.4% (95/160) in the PIF incentives group received dual HBV and HCV testing. Overall, 24.8% (61/246) of participants in the SOC group and 59.3% (157/265) in the PIF incentives group received dual HBV and HCV testing. The participants in the PIF incentives group were more likely to receive dual HBV and HCV testing compared with those in the SOC group (rate difference (RD)=34.5%, 95% CI 26.1 to 42.1).
In the SOC group, employed participants (adjusted OR (AOR)=0.46, 95% CI 0.23 to 0.94) and participants who used recreational drugs in the past 12 months (AOR=0.38, 95% CI 0.18 to 0.78) were less likely to receive dual HBV and HCV testing than those unemployed and those not using recreational drugs. Compared with gay MSM, participants who self-identified as bisexual were more likely to get dual HBV and HCV testing (AOR=2.07, 95% CI 1.06 to 4.05) (table 2).
Factors associated with HBV and HCV testing of MSM participants in the standard-of-care groups (N=246)
Different from the SOC group, in the PIF incentives group, participants who used recreational drugs in the past 12 months (AOR=1.83, 95% CI 1.09 to 3.06) were more likely to have dual HBV and HCV testing than those who did not use recreational drugs. MSM with higher levels of community connectedness were more likely to have dual HBV and HCV testing (AOR=1.10, 95% CI 1.00 to 1.21) (table 3).
Factors associated with HBV and HCV testing of MSM participants in the pay-it-forward groups (N=265)
Subgroup analyses of recreational drug types revealed that in the SOC group, MSM who had used aphrodisiacs in the past year were less likely to receive dual HBV and HCV testing (AOR=0.46, 95% CI 0.19 to 0.84) compared with those who had not. Conversely, in the PIF group, the association between aphrodisiac use and dual HBV and HCV testing did not demonstrate statistical significance (online supplemental data 3).
Supplemental material
Interaction between intervention and recreational drug use behaviours
After adjusting for age, study site, education and marital status, the results of the interaction analysis (table 4) indicated the interplay between PIF intervention and recreational drug use behaviour on dual HBV and HCV testing uptake.
Interaction between interventions and recreational drug use behaviour on the uptake of HBV and HCV testing
Compared with those in the SOC group that had not used recreational drugs in the past 12 months, participants in the PIF incentives group who had not used recreational drugs in the past 12 months showed significantly higher odds of receiving dual HBV and HCV testing (OR=2.84, 95% CI 1.79 to 4.49). The odds were even higher for individuals in the PIF incentives group who had used recreational drugs in the past 12 months (OR=5.18, 95% CI 3.05 to 8.80). Conversely, participants in the SOC group who had used recreational drugs were significantly less likely to receive testing (OR=0.38, 95% CI 0.18 to 0.78).
Further stratification analyses demonstrated that PIF incentives notably increased testing uptake in both subgroups, irrespective of recreational drug use behaviours. The effect was particularly pronounced in the subgroup with recreational drug use behaviours (OR=13.70, 95% CI 6.36 to 29.49) compared with the subgroup without drug use behaviours (OR=2.84, 95% CI 1.79 to 4.49).
The RERI was 2.97 (95% CI 1.98 to 11.76), meaning that there was some indication that the estimated joint effect on the additive scale of PIF incentives and recreational drug use behaviours together was greater than the sum of the estimated effects of pay-it-forward incentives alone and recreational drug use behaviours alone, so that there was positive interaction on the additive scale. Approximately 57% of hepatitis test uptake among MSM was attributed to the interaction of intervention and recreational drug use behaviours. The measure of interaction on a multiplicative scale, the ratio of ORs, was 4.83 (95% CI 1.98 to 11.76), meaning that there were some indications that the estimated joint effect on the OR scale of PIF incentives and recreational drug use behaviours together was greater than the product of the estimated effects of PIF incentives alone and recreational drug use behaviours alone, so that there was positive interaction on the multiplicative scale.
Discussion
HBV and HCV testing is the key initial step in the chronic viral hepatitis care continuum and is a crucial component of an effective hepatitis response.23 Our findings revealed noteworthy disparities in testing behaviours among participants in the PIF incentives group compared with the SOC group. Among those who had used recreational drugs in the past 12 months, individuals in the PIF incentives group exhibited a higher likelihood of receiving HBV and HCV testing. This finding is particularly striking when contrasted with the SOC group, where individuals who had used recreational drugs in the past 12 months exhibited lower odds of testing uptake. Notably, our study showed a synergistic interaction between PIF incentives and drug use behaviours on HBV and HCV testing among MSM. The findings from our study reveal contrasting testing behaviours among individuals with substance use tendencies in different intervention groups, indicating the potential influence of this innovative incentive model on health-seeking behaviours and presenting an innovative opportunity for tailored public health interventions.
Due to the high risks associated with sharing drug-use equipment and risky sexual behaviours, people who use drugs have a higher prevalence of HBV and HCV.24 25 However, many people who use drugs are not tested for HBV and HCV.26 Compounded barriers, including socioeconomic disadvantage,27 fear of diagnosis,28 the double stigma associated with drug use behaviours and hepatitis virus infections28 and mistrust of healthcare provider,26 contribute to the low test uptake rates among people who use drugs. The increased likelihood of HBV and HCV testing among MSM engaging in substance use within the PIF incentives group suggests that this incentive could counteract barriers associated with testing reluctance prevalent among this population. Individuals reporting drug use in our study tended to have lower monthly incomes, potentially influencing their testing behaviour. In the PIF incentives group, participants can receive free dual HBV and HCV testing regardless of donation, which seemed to significantly appeal to those using drugs due to reduced testing costs. Conversely, in the SOC group, participants need to pay out-of-pocket for the testing (about 1.3% of individual monthly income), which makes them less likely to receive the testing due to their financial constraints. This approach effectively addresses financial barriers, a crucial deterrent for testing uptake among individuals who use drugs. Second, understanding and leveraging the ‘recipient glow’ phenomenon within this context could be pivotal in encouraging acceptance of testing among marginalised populations. According to the ‘recipient glow’, theorised in the generalised reciprocity principle,29 beneficiaries of generous acts experience a ‘warm feeling’ that encourages them to be generous to others. In the context of PIF, the individual who receives the free test may feel obligated to accept testing as refusal may symbolise rejection of the donors’ generosity. Utilising this psychological aspect to counteract the stigma and fear associated with testing may facilitate a more positive attitude towards healthcare access.
People who use drugs often experience social isolation and stigmatisation, which have limited access to healthcare resources and opportunities for regular testing.30 Hence, when presented with an opportunity for free testing, people who use drugs may not only experience the recipient glow but also perceive it as a rare instance of goodwill extended to them within a society that frequently marginalises them. This experience of receiving such generosity in a PIF context may further reinforce their inclination to accept the test, as it represents a chance for healthcare access and positive interaction that counters their usual experiences of exclusion and neglect. Additionally, the involvement of local MSM-led community-based organisations in spearheading PIF interventions might mitigate stigma and overcome healthcare provider mistrust, common deterrents to seeking healthcare services among individuals with substance use behaviours. The application of tailored PIF incentives in HBV and HCV testing programmes, specifically targeted at substance-using populations, shows promise in addressing healthcare access disparities and enhancing public health outcomes. Future studies should focus on understanding the psychosocial factors influencing health-seeking behaviours in this context. Moreover, further research evaluating the scalability, sustainability and cost-effectiveness of integrating PIF incentives into public health initiatives is crucial for their widespread and enduring application in improving hepatitis testing rates among vulnerable populations.
In our study, we found that 32 (61.5%) of the unemployed participants in the PIF incentive group had dual HBV and HCV testing, which was higher than the employed participants (58.7%). This observation can be attributed to several factors. Unemployed participants typically have fewer financial resources and thus may be more receptive to free testing. PIF incentives reduce their financial burden by offering free testing, making them more willing to participate. Second, the unemployed may have more flexible schedules than those employed, making them more likely to participate in testing activities. Employed individuals often have less time due to work commitments, which can hinder their ability to attend testing sessions during standard hours. In contrast, unemployed individuals can more easily accommodate the timing of such activities. However, it is important to note that our univariable and multivariable logistic regression analyses did not find a significant association between employment status and HBV and HCV testing uptake.
Our study has several limitations. First, study participants were recruited at community-based HIV/syphilis testing sites, which may be subjected to selection bias and limit the generalisability of our study results to the larger MSM population. Second, due to the inclusion of sensitive questions in our survey (like finances, sexual behaviours and substance use), participants’ responses may have been subjected to social desirability. Third, our study assessed participants’ sexual behaviour and history of recreational drug use but did not specifically assess whether participants engaged in condomless sexual behaviour after recreational drug use. Future studies can build on our work by exploring this specific aspect in more detail. Additionally, PIF has only been implemented on a small scale in Jiangsu Province, thus limiting the study’s sample size. Implementation science is needed to better understand how the PIF strategy works and how to scale it up in diverse settings towards global health good.
Conclusion
The application of PIF incentives appears to hold significant promise in encouraging hepatitis testing, especially among MSM who use drugs and those exhibiting higher levels of community connectedness. Future studies should aim to delve deeper into the dynamics of PIF approaches, specifically targeting MSM who used drugs, to explore and optimise interventions that effectively promote hepatitis testing within this subgroup.
Abstract translation
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.Data availability statement
Data are available upon reasonable request.
Ethics statements
Patient consent for publication
Ethics approval
The original study was approved by the Jiangsu Center for Disease Prevention and Control (IRB number JSLK-2020-B014-2). Participants gave informed consent to participate in the study before taking part.
References
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
Handling editor Eric PF Chow
Contributors This manuscript is an original research paper that has not been published previously, nor is it under review with any other journal. WT conceived the idea and analysis plan. WA was responsible for data cleaning and data analysis and generated the final analysis outputs. YX, HL and TA provided advice for data analysis. WA wrote the first draft of the paper, and JDT, JO, DW, GM, YZ, HL, YX and WT contributed to the interpretation of the results and provided expert advice on the draft. WT is responsible for the overall content as guarantor. All co-authors provided constructive comments and approved the final draft of the submission.
Funding This work was supported by the Key Technologies Research and Development Program (2022YFC2304900-4 to WT), National Nature Science Foundation of China (81903371 to WT) and CRDF Global (G-202104-67775 to WT).
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer-reviewed.
Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.