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Belief in Treatment As Prevention and Its Relationship to HIV Status and Behavioral Risk

Submitted Draft; Final Version in Journal of Acquired Immune Deficiency Syndrome

ABSTRACT

We evaluated attitudes towards Treatment as Prevention (TasP) among gay, bisexual, and other men who have sex with men (GBM) in Vancouver, Canada. Sexually-active GBM, aged >16, were recruited between 2012–2015 using respondent-driven sampling. At each six-month follow-up, participants completed a computer-administered questionnaire and nursing visit. Repeated measures latent class analysis (RMLCA), grouped by self-reported serostatus, identified patterns of TasP-endorsement by considering TasP-related awareness, attitudes, and behavior. Binary logistic regression identified covariates of class membership. Bivariate interactions with visit number identified factors associated with longitudinal changes in class membership. 774 men provided 2,590 observations. Of these, 698 enrolled in the cohort, 575 had at least 1 follow-up visit. Among these, the median follow-up time was 1.98 (Q1-Q2: 1.49–2.49) years. RMLCA identified three classes: “Unaware” (64.2% HIV-negative/unknown versus 29.2% of HIV-positive), “Skeptical” (29.7% versus 23.1%), and “Believing” (6.1% versus 47.7%). Membership in classes representing higher TasP-endorsement was associated with greater odds of condomless anal sex (CAS) and having more sexual partners. Age, sexual orientation, ethnicity, substance use, and social time spent with other GBM were also associated with class membership. Longitudinally, class membership was stable among HIV-positive men, but shifted towards greater TasP-endorsement among HIV-negative/unknown men. For HIV-negative/unknown men, increasing endorsement was positively associated with greater education, being employed, being in a relationship, and substance use, and inversely associated with recent serodiscordant CAS or STI diagnosis. Over time, disparities in TasP diffusion by HIV status have lessened, though continue to persist across other key social strata.

INTRODUCTION

Highly Active Antiretroviral therapies (HAART) are enabling people living with HIV to manage their viral load and achieve viral suppression.1,2 HAART has thus contributed to significant declines in HIV-related morbidity, mortality, and transmission,36 giving rise to a prevention strategy known as “Treatment as Prevention” (TasP).7 Under TasP programs, the expansion of HAART to all persons living with HIV has been associated with lower rates of forward transmission—demonstrating the effectiveness of using biomedical prevention strategies to reduce HIV incidence.712,

Yet, gay, bisexual, and other men who have sex with men (GBM) continue to be over-represented in the HIV epidemic.13 In British Columbia (BC), an increasing proportion of new HIV cases occur among GBM despite the number of new cases among GBM remaining relatively stable over the last decade.14 Given that biomedical prevention strategies, like TasP, have the potential to be highly effective,15 it is increasingly important that we understand their uptake and diffusion in at-risk social networks. Recent analyses of cross-sectional data collected between 2012–2014 demonstrate that while almost half of sampled GBM had heard of TasP, only 21% of HIV-positive men and 13% of HIV-negative men showed complete understanding of the concept.16 Other studies highlight a number of factors associated with TasP awareness among GBM, including HIV-status, socioeconomic indicators, social embeddedness, engagement in healthcare, and substance use.1618However, as most studies on TasP have been cross-sectional, it remains uncertain which factors are associated with the longitudinal development of TasP-related awareness, attitudes, and behavior.

In addition to providing insight into the potential obstacles to GBM’s knowledge of TasP, longitudinal research may also be relevant to understanding the emergence of PrEP, which has likewise been shown to be a highly effective risk reduction measure limited by restricted access and uptake.19,20,21,22 While we might not necessarily expect the diffusion of TasP and PrEP to be analogous,23 understanding factors which have shaped the diffusion of TasP may provide foresight for the eventual wide-spread rollout of PrEP.24 Indeed, based on Rogers’ Diffusion of Innovations theory,25 the spread of behavioral, ideological, and technological innovations may share common patterns of diffusion. For instance, one study reported that doctors who defer treatment for newly HIV-positive patients are also skeptical about PrEP.24 This demonstrates potential similarities in the diffusion of these biomedical prevention strategies, highlighting the need to examine how the diffusion of prevention attitudes within GBM’s social networks.

METHODS

Study Procedures

Since 1992, the distribution of HIV medications has been managed centrally by the British Columbia Centre for Excellence in HIV/AIDS and thereby made freely available to all persons living with HIV, regardless of CD4 count or viral load.26 In 2010, BC initiated a pilot program, known as STOP HIV/AIDS, to expand HIV testing and facilitate engagement in care and treatment for people living with HIV. The Momentum Health Study was established to investigate the effects of this expansion. Accordingly, data for this analyses were collected between 2012 and 2016. Prior to recruitment, formative research was undertaken to evaluate the social network structure of GBM in Metro Vancouver.27 Based on community maps, 134 initial participants, referred to as seeds, were recruited with the help of community partners and by advertising on popular geosocial networking applications tailored for GBM.28 Seeds, were then given six vouchers and asked to recruit other eligible participants (i.e., sexually active GBM, aged >16 years, living in Metro Vancouver, BC). Respondent-drive sampling (RDS) continued with each new recruit receiving up to six vouchers which they could provide to other GBM in their networks. Participants provided informed consent and were invited to enroll in a cohort with follow-up at six-month intervals.

At each study visit, participants completed a computer-assisted self-interview which assessed demographic, bio-behavioral, and psychosocial factors. Upon completion of the questionnaire, participants underwent clinical screenings during which a study nurse administered a point-of care HIV test or CD4 and viral load blood draws as appropriate, venipuncture for hepatitis C and syphilis testing, and optional screenings for gonorrhea and chlamydia. Upon completion of each study visit, participants received a $50 CAD honoraria which could be taken as cash or used to purchase $10 tickets for monthly and semi-annual drawings. Ethics approval was received from the research ethics boards at Simon Fraser University, the University of British Columbia, and the University of Victoria.

Statistical Analysis

All statistical analyses were conducted in SAS v. 9.4. TasP knowledge, attitudes, and behavior were characterized using RMLCA. Unconditional RMLCA models were constructed using the PROC LCA routine developed by Lanza and Collins.29 Considering the difference in treatment and HIV-awareness between HIV negative/unknown and positive groups,16 all analyses were stratified by self-reported HIV status, which was statistically supported as the assumption of measurement invariance restriction was rejected during RMLCA model specification. In specifying the number of classes in the RMLCA model, the adjusted Bayesian information criterion (aBIC) fit statistic was used, as it has been shown to perform well in LCA modeling.30 Ultimately, however, model selection was made with consideration of theoretical and conceptual appropriateness.A three class RMLCA solution was selected as it minimized the AIC, BIC, and ABIC for HIV-negative men and provided a class structure that was interpretable, parsimonious, and conceptually appropriate for both groups.

Bivariate odds ratios and 95% confidence intervals were generated using generalized equation modeling to identify the variables associated with class membership. Class membership was defined by posterior class membership probabilities, generated by the PROC LCA routine. Variables with a bivariate p-value <0.20 were included in a multivariable model for each class. While multinomial regression models are more common in latent class analysis, we constructed separate binary logistic models using generalized estimating equations for each class-by-class comparison; given a 3-class solution, this meant building 3 models, each with the same reference class. This modelling approach allowed the predictors of class membership to load independently for each class, providing independent and adjusted associations for each latent class rather than for the broad general construct. Each of these final models were constructed using a backwards elimination procedure to identify and adjust the independent covariates associated with TasP endorsement (RMLCA class membership). At each step, the variable with the lowest Type-III p-value was removed from the model until an optimal (minimized) Quasi-Akaike information criterion (QIC) value was achieved. As this study was longitudinal, additional bivariate analyses were undertaken to test for an interaction between TasP endorsement (LCA class membership) and visit number (time), allowing us to identify the factors associated with “slower” and “faster” uptake of TasP-related attitudes, knowledge, and behavior over time.

Variables

Explanatory variables included participant demographics, sexual behavior, substance use, social behavior, and clinical outcomes. Demographic variables included age group, sexual orientation, race/ethnicity, education, annual income, and relationship status. Sexual behavior variables included recent (past 6 months, P6M) condomless anal sex (CAS), number of anal sex partners, and recent STI diagnosis, as well as whether participants reported “always using condoms.” Substance use variables included P6M use of cannabis, inhalants, stimulants, sedatives, opioids, poppers, erectile dysfunction drugs (EDD), party drugs (i.e., methamphetamines, ecstasy, ketamine, mushrooms, lysergic acid diethylamide (LSD), other hallucinogens, gamma-Hydroxybutyric acid), injection drugs (excluding steroids), and number of binge drinking events in the past month (defined by having more than 5 drinks on a single occasion). Social behavior variables included the amount of social time participants spent with other GBM and the number of GBM they reported knowing. Clinical variables included past year pharmacy refill adherence data, CD4 counts, and HIV viral load (<200, ≥200 copies/ml).

RESULTS

In total, 556 HIV-negative/unknown men provided 1,845 observations and 218 HIV-positive men provided 745 observations. Among participants with at least 1 follow-up visit (n=575) the median follow-up time was 1.98 (Q1-Q2: 1.49–2.49) years. At baseline, the median age of the sample was 34 years (Q1,Q3: 26,47) and the majority of the sample identified as gay (84.6%), were white (75.6%), had at least some post-secondary education (76.9%), and had annual incomes of <$30,000 CAD (62.7%). Over the P6M, 65.3% (n = 504/772) reported having CAS, the median number of anal sex partners was 3 (Q1,Q3: 1,8), and 10.6% reported being diagnosed with an STI. Of those reporting CAS, 60.9% (n = 307/504) reported CAS with at least one seroconcordant/unknown partner, 50.0% (n = 252/504) reported CAS with at least one unknown status partner, and 22.4% (n = 113/504) reported CAS with at least one serodiscordant partner. 

As described earlier, a three class RMLCA model was used to characterize the multidimensional patterns of TasP endorsement. In brief, the three resultant classes can be characterized as (i) those unaware of TasP, (ii) those who were skeptical of TasP, and (iii) those who were believingof TasP efficacy.

Class 1: Unaware

The majority (64.2%) of HIV-negative/unknown men and one-third (29.2%) of HIV-positive men belonged to the “Unaware” latent class. This class was characterized as not having heard of TasP, not engaging in viral load sorting, and being generally skeptical of the preventive benefits of TasP. For example, only 10.3% of HIV-negative/unknown men and 7.8% of HIV positive men in this class agreed that “a person with an undetectable viral load cannot pass on the virus.”

Class 2: Skeptical

The second latent class, described as the “Skeptical” class, represented 29.7% of HIV-negative/unknown men and 23.1% of HIV-positive men. The Skeptical class was characterized by greater awareness of TasP compared to the Unaware class, but also greater skepticism compared to the Believing class. For example, only 10.3% HIV-negative/unknown men and 53.9% of HIV-positive men in this class engaged in viral load sorting; 91.8% of Skeptical HIV-positive men also did not believe that an undetectable viral load was associated with an inability to transmit the virus; 37.3% of HIV-positive men and 37.0% HIV-negative/unknown men felt undetectable men still had to worry about transmitting HIV to their partners, and a significant proportion of both HIV-positive (31.9%) and HIV-negative/unknown (41.6%) men in this class felt that CAS was never safe regardless of viral load.

Class 3: Believing

The final latent class represented 47.7% of HIV-positive men, but only 6.1% of HIV-negative/unknown men. Men in the Believing class reported that TasP lowered HIV risk “a lot”, engaged in condomless viral load sorting with their serodiscordant partners, and agreed with statements regarding the preventive benefits of TasP. Despite this, 58% men in the Believing class believed that condomless sex is “never safe” regardless of viral load.

Compared with Unaware HIV-negative/unknown men, Skeptical HIV-negative/unknown men were more likely to identify their sexual orientation as “other”, to be white to report recent erectile dysfunction and party drug use, and to spend more social time with other gay men; they were also less likely to report “always using condoms.” Skeptical HIV-positive men were more likely than Unaware HIV-positive men to be aged 30–39 (vs. 16–29), to have CAS, and to spend more than three quarters of their social time with other gay men (vs. <25%); they were also less likely to always use condoms. Again, compared with the Unaware class, Believing HIV-negative/unknown men were more likely to identify as gay (vs. bisexual), engage in CAS, report recent erectile dysfunction and party drug use, and spend more than three quarters (vs. <25%) of their social time with other GBM; they were less likely to report “always using condoms.” Believing HIV-positive men were more likely than Unaware HIV-positive men to engage in serodiscordant or unknown CAS and to have more anal sex partners; they were less likely to binge drink.

Over time, TasP endorsement was relatively stable among HIV-positive men (p=0.20). However, HIV-negative/unknown men became increasingly aware of TasP (p<0.0001). The proportion of Unaware HIV-negative men dropped by 40.1%, while the Skeptical class increased 29.1%, and the Believing class increased 11.0%. For HIV-positive men, the proportion in the Unaware class dropped 4.3%, the proportion in the Skeptical class dropped 4.6%, and the proportion in Believing class increased 8.9%.

Using bivariate interaction terms we examined the relationship between TasP endorsement and time. Among HIV-negative/unknown men, we determined that having greater than a high school education (OR:1.16, 95%CI:[1.01,1.34]), being employed (OR:1.13, 95%CI:[1.01,1.26]), and having a regular partner (OR:1.14, 95%CI:[1.03,1.26]) were associated with a respective 16%, 13%, and 14% increase in odds of transitioning to a more-aware class, per visit (i.e, faster TasP endorsement). Conversely, among HIV-negative/unknown men, reporting recent CAS (OR:0.86. 95%CI:[0.76,0.98]) or STI diagnosis (OR:0.67. 95%CI:[0.50,0.89]) was associated with a respective 14% and 33% decrease in odds of transitioning to a more-aware class, per visit (i.e., slower TasP endorsement). For HIV-positive men, being ART naïve or recently starting treatment in the past 12 months (OR:1.45, 95%CI:[1.09,1.94]), being older (≥40 vs. 16–29; OR:2.13, 95%CI:[1.13,3.99]), and always using condoms (OR:1.24; 95%CI:[1.09,1.40]) were associated with a respective 113% and 24% increase in odds of transitioning to a more-aware class, per visit (i.e., faster TasP endorsement). Being Asian (vs. White; OR:0.72, 95%CI:[0.57,0.90]), use of inhalants (OR:0.49, 95%CI:[0.45,0.53]), sedatives (OR:0.81, 95%CI:[0.68,0.97]), and poppers (OR:0.86, 95%CI:[0.76,0.97]) was associated with a respective 28%, 51%, 19%, and 14% decrease in odds of transitioning to a more-aware class, per visit (i.e., slower TasP endorsement).

DISCUSSION

Using RMLCA we identified three classes representing a continuum of increasing TasP endorsement among 774 GBM recruited using RDS in Metro Vancouver: (i) those unaware of TasP, (ii) those who were aware though skeptical of TasP, and (iii) those who were believing of TasP efficacy. Interpreting our results within a Diffusion of Innovations framework,25 our study highlights that while some TasP concepts, such as the importance of knowing an HIV-positive partner’s viral load, have diffused within the observed socio-sexual networks, other concepts such as the preventive benefits of TasP have had a more limited impact. This is consistent with past research that has found that polarizing biomedical prevention strategies can have limited diffusion.18

Consistent with previous research on the longitudinal trends of TasP awareness,31 our study found that TasP support was consistently higher among HIV-positive men than HIV-negative men throughout the study period. Accordingly, the largest class transitions were seen among HIV-negative men. There was a 40% decrease in the proportion of Unaware HIV-negative men, compared to a 4% decrease in Unaware HIV-positive men. However, most HIV-negative men transitioned from the Unaware class to the Skeptical class, and among both HIV-negative and HIV-positive men, the proportion of those transitioning into the Believing classes was only around 10%. These results can be considered in light of previous research which has reported skepticism among HIV-negative men about whether an undetectable viral load can prevent HIV transmission.32However, HIV-positive men in the Believing class were actually slightly less optimistic of TasP’s ability to eliminate transmission worries compared with HIV-negative men in the same class. Further, we observed that HIV-positive men who recently started treatment or who had never been on treatment increased in TasP support faster than those with sub-optimal adherence. This may suggest that HIV-positive men place greater weight on the potential limitations of TasP—perhaps owing to their greater exposure to medical professionals, sexual health information, and social norms which place a disproportionate responsibility on people living with HIV to prevent HIV transmission.

Our findings also present a nuanced view of the effect of TasP on sexual behaviours. We observed that greater TasP endorsement was associated with greater odds for engaging in any CAS and with the use of erectile dysfunction and party drugs. Further, membership in classes representing higher TasP endorsement was associated with lower odds of reporting “always using condoms.” These two key findings suggest that TasP endorsement is associated with increased CAS—and thus, in the absent of PrEP or TasP,6,20 greater risk for HIV. This finding generally agrees with previous studies examining the impact of TasP on CAS and subsequent acquisition of sexually transmitted infections (STI).3335 However, these findings should also be considered in light of research indicating that men willing to rely on TasP and other biomedical prevention strategies are already engaging in CAS.36 Indeed, TasP endorsement may not necessarily be the most salient predictor of condom use.37 It may be that TasP merely provides GBM with the knowledge and comfort to rely on other risk management options,38 such as viral-load sorting and PrEP—which a growing body of research suggests may eliminate the risk for HIV during CAS.6,20

Our findings support the view that TasP awareness may actually be an indicator of greater health literacy. For instance, we observed that faster TasP endorsement was associated with decreased odds for CAS and having a recent STI diagnosis among HIV-negative men. Likewise, “always using condoms” was associated with faster, not slower, TasP endorsement. These findings suggest that TasP has diffused more effectively among men who had been using condoms and effectively preventing STIs, but now employ TasP-related strategies as part of their risk management approach. With consideration to diffusions of innovation theory, this suggests that condoms may be increasingly viewed as a dated HIV prevention strategy by GBM who have adopted newer, preferred alternative risk management strategies, such as viral-load sorting and PrEP. With that said, we note that only about half of HIV-positive men in the Believing and Skeptical classes reported using their viral load status in determining when to use condoms with HIV-negative partners. Further, a higher proportion of HIV-positive and HIV-negative men in the Believingclasses agreed that condomless sex is “never safe” despite believing that people with undetectable viral loads “cannot pass on the virus” and “do not need to worry so much about infecting others with HIV.” These findings suggest that individuals well-informed of TasP, and especially HIV-positive persons, continue to weigh their sexual health and pleasure seeking behaviors carefully. Further, their agreement that CAS is “never safe” may indicate that they recognize the limitations of biomedical HIV preventions in addressing the risk for other STIs. However, given the independent diffusion of TasP principles, these findings provide an example of the potential benefits of educating GBM of both the benefits and limitations of TasP, allowing them to leverage evidence-driven knowledge to better manage their sexual health.

Implications

Considering that the diffusion of TasP differed across key subgroups of GBM which are regularly described as at-risk (e.g., socially isolated men, ethnic minorities, those with less formal education, those who are unemployed, and those who use sex and party drugs), ongoing and future biomedical interventions should be careful not to assume that the diffusion of prevention strategies will reach these communities. This is especially important given research which has found that differences in the sexual scripts and norms between subgroups can contribute to the breakdown of sexual negotiations which otherwise provide GBM with opportunities to protect themselves and their partners from unwanted risks.39 Programs designed to ensure that all GBM have a basic understanding of the benefits and limitations of biomedical prevention might also have the added benefit of addressing lagging negative attitudes towards HIV-positive men, thereby helping to establish realistic risk-perceptions for those who experience significant anxiety regarding their sexual behavior. Indeed, because disclosure of serostatus is an important precursor of several risk reductions strategies employed by GBM,4042 reducing stigma for HIV may enhance disclosure self-efficacy among HIV-positive men—making these strategies more effective for all GBM.43,44This is especially important for contexts where risk reduction measures not dependent on sero-disclosure, such as PrEP, are not yet widely available. Further, previous studies have also suggested that reduced stigma may facilitate better uptake of care—resulting ultimately in a higher proportion of HIV-positive men achieving undetectability.45,46 Among HIV-negative men, reduced HIV-stigma, brought about by increased TasP awareness, also has the potential to improve HIV-testing by reducing the fear associated with an HIV positive result.47 Research has also shown that increased TasP awareness is associated with taking post-exposure prophylaxis—reinforcing the idea that greater treatment awareness can contribute to risk-reduction strategies among GBM who are already engaging in high-risk sexual behaviors.31,36

Limitations

There are several important limitations of this study. First, due to the nature of our questions, these data are vulnerable to favourable reporting. While computer-administered questionnaires may reduce some social pressures for favourable reporting, participants may be aware of the research implications of our work and therefore respond accordingly. Alternatively, some participants may not have fully recognized “Treatment as Prevention” as a descriptor for concepts they were in fact aware of – artificially reducing their endorsement of TasP. Second, by dichotomizing Likert-agreement scales for inclusion in the LCA, we may have masked over smaller transitions characterizing increasing TasP endorsement. Third, as the data are longitudinal, it is possible that increasing TasP awareness is attributable due to repeated measures. However, considering that faster TasP endorsement occurred primarily among HIV-negative men, repeated measures is not the best explanation for the observed changes. Fourth, as the data were distributed by visit number, rather than across time, our longitudinal estimates are subject to error. Finally, as we did not adjust for RDS structure in our analysis, the independence of observations cannot be assumed, and it is possible that the observed associations are biased along some unmeasured network characteristic inherent to the RDS sampling methodology we’ve employed. With that said, we found that equilibrium was achieved across several of the key indicators monitored during RDS recruitment (e.g., age, sexual orientation, ethnicity, citizenship, residence, student status, and income)—suggesting that with respect to these indicators our sample was not biased based on our initial recruits and was in fact likely representative of the social networks being studied in the present analysis.48 We should note, however, that HIV-positive men were deliberately over-sampled. However, because our sample is stratified by HIV-status, we would not expect this to impact our study results.

CONCLUSIONS

Despite these limitations, the present study highlights increasing TasP awareness among Vancouver GBM with significant increases among HIV-negative/unknown GBM. However, individuals in several key groups (e.g., substance users, those with low socioeconomic status, and those with lower attachment to other GBM) remain unaware of TasP and may therefore misunderstand how to safely negotiate sexual behavior in TasP environments. We conclude that it is likely that the diffusion of other HIV prevention strategies, such as PrEP, may likewise be hindered among these groups. Therefore, public health programs should seek to overcome the overall lack of health literacy among GBM with the aim of establishing broad, compatible safe-sex norms throughout at-risk social networks.

Acknowledgments

The authors would like to thank the Momentum Health Study participants, office staff and community advisory board, as well as our community partner agencies, Health Initiative for Men, YouthCO HIV & Hep C Society, and Positive Living Society of BC. Momentum is funded through the National Institute on Drug Abuse (R01DA031055-01A1) and the Canadian Institutes for Health Research (MOP-107544, 143342). NJL was supported by a CANFAR/CTN Postdoctoral Fellowship Award. DMM and NJL are supported by Scholar Awards from the Michael Smith Foundation for Health Research (#5209, #16863). JM is supported with grants paid to his institution by the British Columbia Ministry of Health and by the US National Institutes of Health (R01DA036307). JM has also received limited unrestricted funding, paid to his institution, from Abbvie, Bristol-Myers Squibb, Gilead Sciences, Janssen, Merck, and ViiV Healthcare. AC received support through a Doctoral Research Award from the CIHR HIV/AIDS Research Initiative and the Canadian Association for HIV Research (CAHR). HLA is supported by a Postdoctoral Fellowship Award from the Canadian Institutes of Health Research (Grant # MFE-152443).

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