Abstract
Pre-exposure prophylaxis (PrEP) prevents HIV infection among men who have sex with men (MSM) and transgender women (TGW) who are the groups that presents the high incidence risk in Brazil. This cross-sectional secondary analysis describes possible risk compensation, attitudes, and beliefs regarding the use of PrEP among 723 MSM and TGW evaluated in the PrEP Brazil study pre-screening phase. Possible risk compensation was reported by 31.6% individuals. In the multivariate model, factors that increased the likelihood of possible risk compensation were: self-referring as white vs. Black (AOR 2.05; CI 1.09, 3.85), perceiving high likelihood of getting HIV in next 12 months (AOR 1.78; CI 1.23, 2.56), being less afraid of HIV infection if using PrEP (AOR 1.93; CI 1.19, 3.14), feeling liberated to have more partners if using PrEP (AOR 2.93; CI 1.92, 4.49), and believing closest friends would use PrEP (AOR 2.51; CI 1.1, 5.71). We found that possible risk compensation was more common among individuals who presented high-risk perception for HIV infection, probably reflecting they feel at risk and could benefit from PrEP use.
Keywords
Introduction
In Brazil, the HIV epidemic is concentrated among key populations, including men who have sex with men (MSM), with an estimated prevalence of 18.4%,1–4 and transgender women (TGW) for whom the chance or HIV infection is 50 times higher than for the general population.5,6 Thus, intensive prevention strategies, including pre-exposure prophylaxis (PrEP), targeting these populations, were implemented in the country in order to achieve the UNAIDS 90–90–90 goal. 3 PrEP is a biomedical prevention strategy based on the use of antiretroviral (ARV) drugs, as the use of tenofovir/emtricitabine. Its efficacy has been demonstrated among different populations including MSM and TGW,7–9 and it was found to be cost-effective in a Brazilian study. 10 PrEP was shown to be highly acceptable by MSM in low- and middle-income countries . 11 Specifically, in Brazil, willingness to use PrEP ranged from 52% 12 to 82.1%, while a study conducted in Peru (n = 45) found that PrEP acceptability was associated with out-of-pocket cost, perceived efficacy, and potential side effects. 13
Despite the high acceptability, uptake, and adherence showed in demonstration studies around the globe,11,13–17 questions remain on possible negative effects, such as antiretroviral resistance under PrEP users that are chronically infected by hepatitis B virus and risk compensation. 18 This last one may be understood as a behavior adjustment where PrEP users might decrease using condoms and thus become infected by other sexual transmitted infections (STIs). For instance, risk compensation has mostly been measured as increased prevalence rates of condomless sex 19 and/or increased incidence of STIs.7,20,21 Most studies found no evidence of risk compensation after using PrEP; among MSM (n = 2499), risk compensation was not observed, 7 and the Pre-exposure Prophylaxis Initiative (iPrEx study) and placebo-controlled trial of daily oral PrEP in HIV serodiscordant couples (Partners PrEP) showed that condom use increased and STI diagnosis decreased during the studies' follow-up periods. A study with 557 MSM using in-person interviews only and an other study (of 400 MSM) using a computer-assisted self-interview only 22 found fewer risky behaviors between baseline and follow-up. However, the prevalence of receptive condomless anal sex (CAS) increased in a cohort including 953 MSM in Chicago, 23 in a systematic review of 17 studies 24 and in other small studies.7,13,25,26
Beyond risk compensation, as PrEP availability increases, attitudes and beliefs regarding PrEP should be better understood in order to target individual and interpersonal barriers that may affect PrEP uptake and persistence. 12 Factors described to increase uptake/persistence include perceiving a high chance of HIV infection, having prior PrEP awareness, the type of PrEP provider, and presenting with high HIV risk-acquisition behavior.16,27 On the other hand, concerns about safety, adverse reactions, and cost were frequently reported as decreasing the willingness to use PrEP,13,28,29 followed by its effectiveness, places, and persons dispensing the drug. 13 Other potential barriers include stigma surrounding both HIV and ARV and low HIV infection risk perception.28,30 Some qualitative studies indicate that individuals who perceive PrEP to decrease anxiety regarding sex and HIV, 31 as well as those who perceive partners’ and peer’s support 28 were more likely to use it. To the best of our knowledge, there were no studies investigating how these attitudes and beliefs could affect risk compensation.
At the time the present study was conducted, PrEP was only available by demonstration study in Brazil. Since December 2017, PrEP is offered at no cost in the Brazilian public health system for men, women, or transgender people identified in high risk for HIV infection, determined by one or more of follow criteria in the last 6 months: condomless vaginal or anal sex and/or condomless vaginal or anal sex with an HIV-positive partner and/or recurring episodes of STD and/or recurrent PrEP use, as described in PrEP national guidelines. 32 Considering this, understanding motivations for PrEP use among potential users can be key for its success in changing the epidemic profile. Thus, this study aims to describe the prevalence of possible risk compensation, attitudes, and beliefs regarding PrEP use, as well as their associations, among MSM and TGW potentially eligible for PrEP.
Methods
This is a cross-sectional analysis benefiting from data obtained at the PrEP Brazil Study pre-screening visit. The PrEP Brazil Study was a demonstration study detailed elsewhere.14,16 Briefly, a total of 1270 participants were assessed for pre-screening at three Brazilian centers (Fundação Oswaldo Cruz-FIOCRUZ, Centro de Referência e Treinamento em DST/AIDS CRT-SP, and Universidade de São Paulo-USP) between 1 April 2014 and 28 July 2015. To be interviewed for pre-screening, individuals should be men at birth, 18 years of age or older, self-report HIV negative/unknown status, report anal sex intercourse with men/TGW in the prior 12 months, and live in Rio de Janeiro (RJ) or São Paulo (SP) states. These participants were assessed at the time of HIV testing, when looking for postexposure prophylaxis or when specifically looking for the study.
Participants
In the present analysis, we selected 753 individuals assessed at the pre-screening visit who were potentially eligible for PrEP use. Potentially eligible participants were those reporting sexual risky behavior in the last 12 months (i.e. two or more men CAS partners and/or ≥ 2 episodes of anal sex with an HIV-infected partner and/or history report of STI diagnosis) and having a negative rapid HIV test (ORAQUICK and DETERMINE). If the participants had a rapid HIV-positive test, they would be referred for treatment at the institution or place of referral.
14
Thirty individuals were excluded due to missing data. The final analysis sample comprised 723 MSM and TGW, as depicted in Figure 1.
Measures
Participants used tablets to self-answer a 15-minute long structured questionnaire regarding possible risk compensation, as well as PrEP attitudes and beliefs. Counselors were ready to help if participants had difficulty understanding or reading.
Outcome
Possible risk compensation was ascertained by the sentence: “I would stop using condoms if I used PrEP.” Answers were assessed using a 5-point Likert scale and dichotomized into “yes” (totally agree, partially agree, do not agree or disagree) and “no” (partially disagree and totally disagree) considering the answers’ distribution.
Variables
Sociodemographic variables included state (RJ or SP), self-reported color/race (white, mixed, and Black), and gender (male and TGW), age (18–24 years, 25–35 years, 36 years, or more), following previous categorizations of Brazilian HIV studies 33,34 and schooling (less than 12 years and 12 years or more).
Sexual risk behavior in the prior 12 months included: anal sex with an HIV-positive partner (yes, no, or do not know) and history of sexually transmitted infection—syphilis, rectal gonorrhea, or rectal chlamydia (yes or no).
Risk perception for HIV infection was evaluated by the question “What is your likelihood of getting HIV infection in the next 12 months?” Possible answers were dichotomized as 0–25% (none- 0% and little chance-25%) and 50–100% (some chance-50% and high chance and certainty-100%). HIV testing in the prior 12 months (yes/no) was also ascertained and considered a proxy of risk perception. 35
Attitudes and beliefs regarding PrEP were explored by the following sentences: “I would be less afraid to get HIV if I used PrEP,” “I would feel liberated to have more partners if I used PrEP,” “I would not take PrEP due to fear of side effects,” “I believe my closest friends would use PrEP,” “I would be ashamed if I used PrEP,” “I will never need PrEP,” “I believe I would be criticized or rejected if I used PrEP,” “If I use PrEP, I would like my partners to know,” and “I would be anxious/nervous if I used PrEP.”18,35,36
Possible drug diversion was explored by the sentences: “I would sell my pills to people who needed PrEP,” and “I would share my pills with people who needed PrEP.”18,36
Preferences for PrEP use included the sentences: “I would use PrEP even if regular testing was needed,” “I would take one tablet a day if it prevented me from HIV,” “I would use PrEP even if I had to pay for it,” “I would take a tablet before and after sex if it prevented HIV infection,” and “I would use PrEP even if not 100% effective.”18,35,36
The level of concordance with each one of the above sentences was measured using a 5-point Likert scale, and the answers “totally agree” and “partially agree” were categorized as “agree”; “I do not agree or disagree” means “do not know”; and “totally disagree” and “partially disagree” were categorized as “disagree.”
Finally, interest in using condoms was assessed by the sentence “What would be your degree of interest in using a condom if it was available in the SUS?” with possible answers dichotomized as “no” (“no interest,” “low interest,” and “some interest”) and “yes” (high interest).
Statistical analysis
Sociodemographic, sexual risk behavior, risk perception, attitudes and beliefs regarding PrEP, possible drug diversion, preferences for PrEP, and interest in using condoms were described by their absolute and relative frequencies, overall and by possible risk compensation. A Bivariate analysis was conducted to test their association with possible risk compensation using the chi-squared test (categorical variables) and the Mann–Whitney test (continuous variables with asymmetric distribution). A stepwise backwards logistic regression model was performed including variables that presented p-value <0.20 at the bivariate analysis. The variables age, schooling, and color were forced in this model. The crude and adjusted ORs were compared to verify effect modification and confusion variables. Final model included variables that remain statistically significant at p ≤ 0.05 or that were found to be confounders. Interactions between risk perception, feeling liberated to have more sexual partners, and feeling less afraid of getting HIV were tested. Data were analyzed using R Studio (Windows, version 3.3.3). 37
Ethical aspects
The PrEP Brazil Study was approved by Institutional Review Boards from INI FIOCRUZ (CAEE 08405912.9.1001.5262), USP, and CRT-SP.
Results
Sample characteristics by possible risk compensation. PrEP Brazil 2014–2015 (n = 723).
PrEP: pre-exposure prophylaxis; TGW: transgender women.
Attitudes, behaviors, and preferences for PrEP by possible risk compensation. PrEP Brazil 2014–2015 (n = 723).
PrEP: pre-exposure prophylaxis.
Possible risk compensation was reported by 31.6%. Almost half of the individuals (49.24%) totally disagreed with the sentence “I would stop using condoms if I used PrEP,” 19.23% partially disagreed, 15.21% did not agree or disagree, 4.29% partially agreed, and 12.03% totally agreed. (Figure 2). Frequency of possible risk compensation assessed by the sentence “I would stop using condoms if I used PrEP” (n = 723). PrEP Brazil (2014–2015).
Factors associated by possible risk compensation at the logistic regression model (n = 723). PrEP Brazil 2014–2015.
PrEP: pre-exposure prophylaxis.
At the bivariate analysis, factors that were statistically associated with possible risk compensation were: state, color/race, perceived likelihood of getting HIV in the next year, CAS in prior 12 months (Table 1), and the attitudes/beliefs “I would be less afraid to get HIV if I used PrEP,” “I would feel liberated to have more partners if I used PrEP,” “I would not take PrEP due to fear of side effects,” “I believe my closest friends would use PrEP,” “I would be ashamed if I used PrEP,” “I would use PrEP even if regular testing was needed,” “I would take one tablet a day if it prevented me from HIV,” and interest in using condoms (Table 2).
In the multivariate model (Table 3), factors that increased the likelihood of possible risk compensation were: self-referring as white compared to Black (AOR 2.05; CI 95% 1.09, 3.85), perceiving high likelihood of getting HIV in next 12 months (AOR 1.78; CI 95% 1.23, 2.56), being less afraid of HIV infection if using PrEP (AOR 1.93; CI 95% 1.19, 3.14), feeling liberate to have more partners if using PrEP (AO 2.93; CI 95% 1.92, 4.49), and believing closest friends would use PrEP (AOR 2.51; CI 95% 1.1, 5.71). On the other hand, interest in condom use and testing for HIV in prior 12 months decreased the odds of possible risk compensation (AOR 0.22; CI 95% 0.15, 0.33 and AOR 0.63; CI 95% 0.4, 0.98, respectively). We did not found evidence of interaction between risk perception, feeling liberated to have more sexual partners, and feeling less afraid of getting HIV (data not shown).
Discussion
Possible risk compensation was reported by 31% of participants, which is higher than found during the follow-up of heterosexual serodiscordant couples using PrEP in Partners PrEP study (13%), 8 PROUD (12–21%), 7 and higher than a cross-sectional survey among 19,457 MSM in Brazil, Peru, and Mexico (21.83%), 38 similar to CAS prevalence in the MSM study (8–25%), 39 lower than among US MSM (48–52%). 40 Additionally, a recent literature review showed in 16 relevant studies that there was no consistent evidence of a change in condom use after the start of PrEP use. 41 It is important to note that aforementioned studies have evaluated risk compensation measured by the prevalence of CAS during PrEP use, while we measure the intention of risk compensation in hypothetical PrEP use. Few other studies measuring the intention of risk compensation found that over 35% MSM from New York, 42 30% MSM from San Francisco and New York, 43 and 48% MSM 44 would decrease condom use if using PrEP.
Considering 75% of PrEP effectiveness, a mathematical model found that even with 100% reduction in condom use, 50% HIV risk reduction on PrEP would be possible. 45 We did not measure the frequency and consistency of condom use at the pre-screening, which precludes the evaluation of changes in condom use, but we found that individuals at greater risk for HIV infection were more prone to risk compensation. Forty percent of individuals referring CAS with more than two partners in prior 12 months reported possible risk compensation. Thus, these individuals would not be presenting a change in their risk behavior as they were not using condoms before the interview. Among Latino MSM, 1.6% of participants on PrEP and 15.8% not on PrEP reported CAS as a motivation to take PrEP. 29 Similar to observed in other studies including MSM,35,44,46 high-risk perception for HIV infection was associated with inconsistent condom use/no condom use intention. One hypothesis for this association would be that the participants identify they are at risk because they do not use condoms and, therefore, perceive the need of other prevention methods. This hypothesis is supported here by the fact that individuals who presented high risk (CAS and STI diagnosis in prior 12 months) also presented higher frequency of possible risk compensation. Longitudinal data are necessary to better disentangle this association.
Possible risk compensation was also associated with the feeling of release to have more partners and being less afraid of HIV infection if using PrEP. The same feelings were also found in other studies where MSM perceived PrEP as giving them a lot of hope for new possibilities in their lives (39.2%).18,36 A study with 224 MSM from Los Angeles showed a high intention to use PrEP was associated with “If I was taking PrEP, I would not worry about becoming infected with HIV when having sex with someone who is HIV positive (p = 0.003).” 47 Believing that closest friends would use PrEP was associated with possible risk compensation, as well as partner and peer support was a facilitator of PrEP in other analyses. 48 These findings may reflect an optimism around PrEP, that is, individuals would feel protected and no longer perceive the need for using condoms. No other studies evaluated attitudes and beliefs and possible risk compensation association in the context of PrEP use or intention to use it.
The interest in using condoms decreased the chance of possible risk compensation. It is possible that these individuals were satisfied using condoms as their prevention method and would not stop it if starting PrEP. This finding goes in the same direction of results from another study conducted by our research group where willing nwaa to use PrEP was associated with not willing to use condoms (AOR 1.16, 95% CI 1.00–1.33), suggesting a choice for one method between this options. 12 Having performed an HIV test in the prior 12 months also decreased the likelihood of possible risk compensation probably reflecting a protection attitude that would not change during PrEP use. Other studies have evaluated the perception on the impact of PrEP on condom use and showed that 22.2% of who performed HIV test between 3 and 6 months perceived possible risk compensation, 66.7% thought condom use would not change, and 11.1% thought condom use would increase. 44 However, an other study with 183 MSM in Seattle showed a decreased prevalence in condom use and a higher prevalence of STIs during PrEP use compared before PrEP initiation. 49
This study is not free of limitations. As other cross-sectional analyses, we may not infer on causality, and as the sample was not probabilistic, data should be generalized with caution. In addition, social desirability bias could not be ruled out, and the prevalence of possible risk compensation may be underestimated in the present study. We have not evaluated HIV risk among the 30 individuals excluded from the present analysis, but it is unlikely that final results would have changed considering they represent less than 1% of the total sample. Despite the limitations, the data presented reflect the context of a population being assessed for the first time to participate in the first demonstrative study of PrEP implementation in Brazil, and we believe that these data can contribute to the literature on the topic.
In conclusion, we found that possible risk compensation was more common among individuals who presented high-risk perceptions for HIV infection, probably reflecting they feel at risk and would be optimistic in having another prevention tool to add to their repertoire, as apparently they already did not use condoms. Prevalence and effects of risk compensation at population level should be monitored as PrEP availability is implemented in the real world to confirm or refute this hypothesis.
Supplemental Material
sj-pdf-1-std-10.1177_0956462421992157 – Supplemental Material for Possible risk compensation, attitudes, and beliefs among Brazilian individuals potentially eligible for pre-exposure prophylaxis
Supplemental Material, sj-pdf-1-std-10.1177_0956462421992157 for Possible risk compensation, attitudes, and beliefs among Brazilian individuals potentially eligible for pre-exposure prophylaxis by Larissa M Villela, Valdiléa G Veloso, Brenda Hoagland, Nilo M Fernandes, Esper G Kallas, Jose V Madruga, Ronaldo I Moreira, Beatriz Grinsztejn and Raquel B De Boni in International Journal of STD & AIDS
Footnotes
Acknowledgements
We are grateful to the study participants and the following individuals: Tania Krstic, Vinícius Pacheco, Mônica Derrico, Flávia Esper, Gelson Perim, and Denise Ribeiro Franqueira Pires. PrEP Brazil Study team includes Cristiane Regina V. de Castro, Daniel M. McMahon Waite, Desirée Vieira, José Roberto Granjeiro, Josias Freitas, Laylla Monteiro, Lucilene A. de Freitas, Marcus Vinícius M. da Costa, Maura L Gonzalez, Nélio Zuccaro, Rita de Cássia Elias Estrela, Sandra Wagner Cardoso, Sandro Nazer, Tiago Porto, Toni Araújo, Valéria Ribeiro (FIOCRUZ); Aline Tatiane Lumertz dos Anjos, Ana Paula Amaral, Arlene Augusta dos Santos, Camila Rodrigues, Camila Sunaitis Donini, Carlos Moreira, Celso Oliveira Tavares, Charlene Rocha, Claudia Satiko Tomiyama, Cristiane Bressani, Daniel Artur Bertevello, Denise Sales Mourão, Denivalda Araújo, Fatuma Odongo, Gisele N. Reis, Gladys Prado, Helena Tomiyama, Issler Moraes, Karine Milani da Silva Dias, Leandro Cocolato, Lilian Ferrari, Marcia Puerro, Maria Angelica Alcalá Neves, Maria Cândida de Souza Dantas, Mariana Sauer, Natália Barros Cerqueira, Rafael Salles, Raphaela Goulart, Renan Carvalho, Robério Alves Carneiro Jr., Rosângela Vitória Soares da Silva, Taís Sousa, Vinicius Vieira, Zelinda Bartolomei Nakagawa (USP); Priscilla de Lima e Menezes, Roberta Schiavon Nogueira, Valvina Madeira Adão, and Gustavo Mizuno (CRT-SP)
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was sponsored by the Brazilian Ministry of Health (#01/2013 BRA/K57), CNPq (#402004/2012-4, # 454931/2014-0) SVS (#281/2013), FAPERJ (#E-26/110.261/2014), and FAPESP (#2012/51743-0). BG acknowledge funding from the National Council of Technological and Scientific Development and the FAPERJ (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro. EGK acknowledges funding from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) RBDB acknowledges funding from the CNPq (grant # 76333/2013-0).
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References
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