How heterogeneous are MSM from Brazilian cities? An analysis of sexual behavior and perceived risk and a description of trends in awareness and willingness to use PrEP

Background Brazil has the largest population of individuals living with HIV /AIDS in Latin America, with a disproportional prevalence of infection among gays, bisexuals and other men who have sex with men (MSM). Of relevance to prevention and treatment efforts, Brazilian MSM from different regions may differ in behaviors and risk perception related to HIV . Methods We report on MSM living in 29 different cities: 26 Brazilian state capitals, the Federal District and two large cities in São Paulo state assessed in three web-based surveys (2016-2018) advertised on Grindr, Hornet and Facebook. Using logistic regression models, we assessed factors associated with high-risk behavior and high HIV perceived risk. Results A total of 16,667 MSM completed the survey. Overall, MSM from the North and Northeast were younger, more black/mixed-black, of lower income and lower education compared to MSM from the South, Southeast and Central-west. Though 17% had never tested for HIV (with higher percentages in the North and Northeast), condomless receptive anal sex (previous 6 months) and high-risk behavior as per HIV Incidence Risk scale for MSM were observed for 41% and 64%, respectively. Sexual behaviors and HIV perceived risk had low variability by city. Younger age, being gay/homosexual , having a steady partner, binge drinking, report of STI and ever testing for HIV increased the odds of high-risk behavior. In contrast, younger age and having a steady partner decreased the odds of high HIV perceived risk, while report of STI most strongly increased the odds of high HIV perceived risk. All variables that serve as proxies for low socio-economic status (black/mixed-black race, low income and low education) were associated with increased odds of high HIV perceived risk. Awareness and willingness to use PrEP increased from 2016 to 2018 in most cities.

Conclusions Overall, MSM socio-demographic characteristics were heterogeneous among Brazilian cities, but similarities were noted among the cities from the same administrative region with a marked exception of the Federal District not following the patterns for the Central-West. The observed dissonance between sexual behavior and HIV perceived risk may be a barrier to effective PrEP implementation.

Background
Brazil is the largest country in Latin America and the fifth largest country by area and population, with more than 212 million inhabitants (1). Brazil is divided into five geographic regions: North (7 states), Northeast (9 states), Central-west (3 states and the Federal District), Southeast (4 states) and South (3 states). The Southeast, where São Paulo and Rio de Janeiro are located, is the most populous and industrialized region accounting for 42% of all Brazilians and almost 50% of the country's gross domestic product (GDP). Brazilian geographic regions have impressive disparities in terms of GDP per capita: the Northeast and North have the lowest values (USD 4,000-5,000) while GDP per capita in the Central-west, South and Southeast ranges from USD 9,000 to 10,000.
Furthermore, disparities exist within regions and cities, as a result of the dramatic inequalities in wealth and health. In Rio de Janeiro city, for example, the human development index (HDI) varies from very high to low in two neighbor areas: Gávea (0.970) and Rocinha (0.732) (2).
Brazil has the largest population of individuals living with HIV/AIDS in Latin America, with a disproportional prevalence of infection among men who have sex with men (MSM) (3,4).
A population-based study of HIV prevalence found that 18.4% of MSM in Brazil were living with HIV in 2016 (5), higher than the previous study conducted in 2009 (14.2%) (6). In 2017, approximately 60% of reported HIV infections among male were attributed to maleto-male sexual contact (7), even though a national survey has showed that approximately 3.5% (95% confidence interval [CI] 2.9%-4.3%) of the Brazilian men between 15-64 years old report sex with other men at the time of the survey (8). Unfortunately, new infections in this population continue to rise (9). To stop the HIV epidemic in Brazil, a continental, diverse and unequal country, it is necessary to understand and verify how heterogeneous are MSM from each region are in terms of sexual behavior and risk perception.
Since December 2017, pre-exposure prophylaxis (PrEP) with emtricitabine / tenofovir disoproxil fumarate (FTC/TDF) is offered free of charge through the Brazilian Public Health System (SUS) to populations at substantial risk for HIV infection including eligible MSM within the HIV prevention package (10). During 2018, the first year of PrEP provision in SUS, PrEP uptake among eligible MSM varied considerably from a maximum of 25% in Florianopolis (in the South) to a low of 1% in Belém (in the North) (4). One explanation for such a discrepancy could be a lack of perceived risk that differentially impacts PrEP uptake throughout the country. Data on sexual behavior, risk perception and willingness to use PrEP among MSM from each Brazilian region is essential to support the implementation and roll-out of the PrEP program.
This study provides an analysis of sexual behavior and perceived risk, as well as a description of socio-demographic characteristics and trends in awareness and willingness to use PrEP among MSM living in all Brazilian state capitals, the Federal District and two large cities from São Paulo state (Campinas and Santos).

Study design
We conducted three cross-sectional web-based studies targeting MSM in Brazil from 2016 to 2018, one per year. Individuals who met eligibility criteria (age ≥18 years, cisgender men, and HIV uninfected self-report) and who acknowledged reading the informed consent text were directed to the online questionnaire, which was programmed on SurveyGizmo®.

Survey instrument
The survey instrument was composed of five sections (25 questions) addressing: sociodemographic information, substance use, sexual behavior and history of sexually transmitted infections, HIV perceived risk and use of HIV testing as well as awareness and willingness to use PrEP. Though the instrument was not the same in the three surveys, the items used in this analysis were the present in all.

Socio-demographic
Age at the time of the survey was categorized in 4 brackets: 18 to 24; 25 to 29; 30 to 34 and ≥ 35 years; race was categorized in white/Asian, black and mix black/native; schooling was categorized in <10 years, 10-12 years, 13-16 years and >16 years. Family monthly income was grouped into the following strata: ≤ 1 >1-3, >3-10 and >10 minimum wages (Brazilian minimum wage was R$998 or US$268 in January 2019). Sexual orientation was dichotomized in gay or homosexual and other (bisexual, heterosexual or other). Steady partner (male or female) was dichotomized in yes/no. To infer the size of the MSM community in each city, we used the most recent nation-wide survey of sexual practices and behavior that estimated that 3.5% of men between 15-64 years had sex with other men (8).

Substance use
Binge drinking (14) was evaluated with the question "In the last 6 months, did you drink 5 or more drinks in a couple of hours?". Use of stimulants (cocaine, poppers, crack, or amphetamines) during the previous 6 months was dichotomized in yes/no. to screen individuals who should be evaluated for PrEP use (16). Scores <10 and ≥10 were considered as "low risk" and "high risk", respectively (15,16). Report of sexually transmitted infections (STI; syphilis, gonorrhea or rectal chlamydia) in the last six months were dichotomized in yes/no.

HIV Perceived risk and HIV testing
HIV perceived risk was assessed with the question "In your opinion, what is your risk of getting HIV in the next year?" with possible options grouped into "No risk", "Low risk" and "High risk" which was a combination of the options "High risk/50%" and "Certain/100%". This question included an "I don't know or I don't want to answer" option, which was considered as a missing value for the analysis. Individuals were asked about previous HIV tests (never or at least once in lifetime). Additionally, among those who reported never having tested, we accessed their reasons with the question "Why have you never tested for HIV?" with the following possible responses: "I am not at risk of getting infected", "I don't think it is practical to go to a health care center", "I am ashamed", "I am afraid of getting a positive result", "I am too lazy" and "Other reasons".

Awareness and willingness to use PrEP
PrEP awareness was assessed with the question ''Have you ever heard of PrEP?'' (yes/no).
Willingness to use PrEP was defined as the ''High interest'' option on a four-point Likert scale with the question ''What level of interest would you have in using PrEP?". A brief explanation about PrEP was provided before these questions were asked. These questions have been previously used by our research team to describe PrEP awareness and willingness to use PrEP (11)(12)(13)17 Table 1). Considering the estimated MSM population of each city, Florianópolis was the city with the greatest proportion of responders (6.6%), followed by São Paulo (4.2%) and Rio de Janeiro (4.1%).
Overall, median age was 29 years (IQR: 24-36). The age distribution of the participants was shifted towards younger MSM (18-24 years) in most of cities in the North, Northeast and Central-west regions, representing almost half of responders from Manaus (46.5%) and Belém (43.1%), the two largest urban areas in the North. In large cities from the Southeast, South and Brasília the proportion of older MSM (35+ years) was higher (31% in São Paulo and Rio de Janeiro). Most responders from the North and Northeast self-declared mix black or native, and Salvador was the city with the greatest proportion of black MSM (30.7%). Conversely, more than half of responders from the Central-west, Southeast and Rio de Janeiro (18.7%). Having >12 years of schooling (equivalent to high school) was reported by more than half of the respondents in every city except for Manaus (45.8%).
Brasilia was the city with the greatest proportion of MSM with >16 years of schooling (36.3%).
Most participants self-declared as gay or homosexual (89.9%) ( Table 2). The proportion of MSM with a steady partner varied across the country, ranging in the largest urban areas from 19.5% in Belém to 28.2% in Brasília. Most MSM reported binge drinking (70.2%) with only slight variability by region and use of stimulants was more prevalent in the South and Southeast (~20%), the highest proportions were observed in the cities from São Paulo state (24.1% in São Paulo city), Brasília (23.1%) and Florianópolis (22.9%). Overall, 13.1% of participants reported an STI, Florianópolis (18.6%) had the highest proportion among the cities with >300 responders.
The proportion of MSM who reported never having tested for HIV was higher in the North and Northeast when compared to other regions: 26% in Manaus and Belém and 12% in Santos, Curitiba and Brasília. The main reason for never testing for HIV were, in order, "I am afraid of getting a positive result" (851; 32.4%), "I am ashamed" (559; 21.3%), "I am not at risk of getting infected" (459; 17.5%), "I am too lazy" (293; 11.2%), "I don't think it is practical to go to a health care center" (234; 8.9%) and others (227; 8.7%). This pattern was observed in all Brazilian regions except for the South where the response "I am not at risk of getting infected" was more frequent than "I am ashamed" (22% vs. 19%). In the North, more MSM reported "I am afraid of getting a positive result" (38%) in comparison to the other regions ( Figure 1). Overall, the number of responders who reported sex with more than five men was lower in Northern and Northeastern cities compared to the other regions, around 35%. In contrast, this proportion was higher in Southeastern cities, São Paulo (46.2%), Rio de Janeiro (45.4%), Brasília (44.8%) and in the Southern cities, ranging from 43.5% in Curitiba to 45.5% in Porto Alegre. Condomless receptive anal sex was reported by 6,865 participants (41.4%) with little heterogeneity by city. Most participants met criteria for "high risk" according to the HIRI-MSM (64.3%), indicating that PrEP should be recommended.
Conversely, only 28.0% of participants reported high HIV perceived risk, and this proportion was lower in Belém (23.5%) and Recife (24.9%). Table 3 shows that irrespective of the definition of high-risk behavior, overall, less than a half of those with high-risk behavior (as measured by a score >10 in the HIRI-MSM, condomless receptive anal sex, or >5 partners in the prior six months) perceived themselves at high risk. Among those reporting low-risk behavior, around one-fifth perceived themselves at high-risk (13.9% as measured by the HIRI-MSM, 19.7% who report condomless anal sex and 18.8% who had ≤5 partners). High-risk behavior increased the odds of perceiving oneself at high HIV perceived risk, a pattern also present when stratified by city (Table 4 and Table 5).
Overall, the association of socio-demographic and behavioral characteristics with high-risk behavior as measured by the HIRI-MSM was consistent across the cities (Table 6). Younger age, being gay or homosexual, having a steady partner, binge drinking, STI diagnosis and ever testing for HIV increased the odds of high-risk behavior. As participants from São Paulo and Rio de Janeiro make up the majority of the study population, the results of Brazil as a whole greatly reflect those for these two cities. One notable exception was the association of having a steady partner increasing the odds of high-risk behavior which is most strongly observed in Goiania. Similarly, the association of binge drinking with highrisk behavior is more pronounced in the North, Central-west, and South, and not apparent in the Northeast.
In contrast to the model for high-risk behavior described above, all variables were significantly associated with high perceived risk for HIV (Table 7). Notably, younger age and having a steady partner were associated with lower odds of perceiving oneself as being at high-risk. Having an STI most strongly increased the odds of high perceived risk while the association of ever testing for HIV increasing the odds of high perceived risk was much more subtle and not consistent across cities. Though of small magnitude, all variables that serve as proxies for low socio-economic status (black/mixed-black race, low income and low education) were associated with increased odds of high HIV perceived risk. When we stratify the study population by risk behavior as measured by the HIRI-MSM, model results change somewhat. Among those with high-risk behavior, the association of younger age and steady partner decreasing the odds of high perceived risk was stronger.
In contrast, among those with low-risk behavior, being black/mixed black or testing for HIV increased the odds of high perceived risk to a greater degree. Finally, in the two strata, having an STI increased the odds of high perceived risk consistently.
Overall, PrEP awareness increased overtime in Brazil from 58% in 2016 to 70% in 2018

Discussion
In the present, we described the socio-demographic characteristics as well as sexual behavior and HIV perceived risk by city across all regions of Brazil. We noted significant heterogeneity with respect to some factors (i.e. socio-demographic characteristics, stimulant use and never testing for HIV) and a homogeneous profile for others (binge drinking and sexual behavior). Moreover, our results highlight which factors were most associated with high-risk behavior and high HIV perceived risk, by city and in the country as a whole.
One strength of this study was the inclusion of a large number of MSM living in Brazilian state capitals, in the Federal District and in two large cities from São Paulo state.
Considering the estimated population of MSM in each city, the highest proportions of MSM completing the questionnaire were from the South, Southeast and Central-west regions.
Compared to the North and Northeast, these regions are more developed likely providing greater access to and use of mobile phones and cell phone data services and/or public Wi-Fi services on a daily basis (18), thus facilitating participation. On the other hand, it could be that MSM from all regions had the same level of access to the survey but that a relatively lower fraction of men from the North and Northeast proceeded with participation due to increased stigma and discrimination and/or a lack of community belonging. São Paulo, Rio de Janeiro and Florianópolis, for instance, have large LGBTQI communities suggesting lower stigma and greater likelihood of participation in a research study addressing sexual behavior related to HIV aimed to enhance health policies. Lastly, differential participation among cities could result from differential use of apps for sexual encounters by the MSM community of each city.
We observed similarities among MSM from 1) the South, Southeast and Brasilia versus those from 2) the North and Northeast. Different from group 1), for group 2) a greater proportion of MSM were young, non-white, of lower income and lower schooling, which are characteristics of the population most vulnerable to HIV infection in Brazil (9). These group differences could be a reflection of the socio-demographic characteristics of the population from these regions according to national data (19), suggesting that our samples were representative of the region, though not representative of MSM with no mobile or internet connection. Despite large inequalities, Brazil has a large number of internet users in all social strata: 58% of individuals receiving one minimum wage per month (~US$260.00) have access to internet (18). According to estimates, 84% of Brazilians have a mobile phone (20) and 96% have access to internet/apps via mobile phones (21). This supports the use of apps and social media to broadcast information on sexual education and HIV/STI treatment and prevention.
MSM reporting high-risk behavior measured by the HIRI-MSM, condomless receptive anal sex and number of partners were more likely to perceive themselves at higher risk, which is consistent with a web-based study conducted among 800 MSM from the United States We found that some factors associated with high-risk behavior were also associated with high HIV perceived risk. MSM who self-declared gay or homosexual compared to other sexual orientations (bisexual, heterosexual or other), had greater odds of high-risk behavior and of high HIV perceived risk. Moreover, when stratifying by low vs high risk behavior, among those at high-risk, gay or homosexual sexual orientation had higher odds of high HIV perceived risk, while among those at low-risk, no association was found between sexual orientation and high HIV perceived risk. Although the proportion of nongay MSM in the sample was low and includes self-declared bisexual MSM, one could speculate that those who self-declared gay may be more engaged in gay communities and more aware of their risks. This could also indicate a gap in the framing of health messages which might be inadvertently excluding non-gay MSM (37), leading to a low HIV risk perception and knowledge of prevention technologies.
MSM who reported binge drinking were also found at higher odds of high-risk behavior and of high HIV perceived risk. Indeed, the positive association between binge drinking and high HIV perceived risk remained when stratifying men by risk behavior. Binge drinking is known to increase high-risk behaviors among MSM (38-40) and the loss of consciousness or self-control while under alcohol may explain the high-risk perception. In our study, binge drinking was highly prevalent across the cities (~70%), while more MSM from the Central-west, South and Southeast regions (~20%) reported use of stimulants (compared to ~10% in the North and Northeast). Alcohol is widely used, accepted and easy to access in Brazil (41). Stimulants, in contrast, are expensive and illegal; access may be easier in larger urban areas, what may explain these disparities (42).
Contrasting with the findings reported above is the association of age with sexual behavior and risk perception. We found that younger age was associated with an increased odds of high-risk behavior but a decreased odds of high perceived risk for HIV.
In fact, when stratified by risk behavior, younger age was associated with an even lower Although there was no association of race, income or education with high-risk behavior (be it overall or by city except for 1 city), blacks/mixed-blacks, those with low income or low education had an increased odds of high HIV perceived risk. We interpret these findings as resulting from the persistent effects of stigma and discrimination, pervasive in our society (52), at the individual, interpersonal and structural levels that create a sense of selfstigma and low self-esteem (53). In addition, MSM populations may face different forms of stigma, including internalized, perceived, experienced and layered stigmas (54). This finding is even more pronounced for black/mixed-black race as even those with low-risk behavior had high-perceived risk for HIV (aOR 1.31 [1.12-1.54]). In a study conducted in Belo Horizonte, black individuals had over 50% higher odds of experiencing discrimination than whites, even after controlling for income, education, social status, and health problems (55). A systematic review showed a higher prevalence of mental health disorders in non-white Brazilians compared to their white counterparts (56), and this could be attributed to negative psychological stress response (57). According to Ribeiro, the place someone occupies in the society influences individual's experiences and perspectives and the multiplicity of speeches should be promoted in order to break the authoritarian and unique voice (mostly male, white and of higher income) supposed to be universal (58). In this regard, the inclusion of black/mixed-black individuals in the concept and accomplishment of educational campaigns is necessary to increase representativeness and to better understand the needs of this population. Use of simple media messages could benefit those with lower income and education.
Finally, having an STI and ever testing for HIV were both associated with an increased odds of high-risk behavior and with a high HIV perceived risk. In fact, the association between having an STI with high-risk behavior and with high HIV perceived risk was the largest in magnitude when compared to all other factors. In Brazil, STI diagnosis still relies extensively on syndromic management (59) suggesting that these infections were symptomatic which might explain its strong effect on perceived risk: an individuals' recognition of an STI could suggest his enhanced risk for other STIs, including HIV.
Corroborating these findings are those diametrically opposite where asymptomatic MSM with a rectal STI in England reported low or no perceived risk prior to diagnosis (60).
Furthermore, the interaction with health professionals at the time of STI diagnosis might have allowed for the provision of information on HIV risk thus increasing knowledge and awareness of one's risk. This highlights the importance of health care provides as source of information and sexual education. On the association of perceived HIV risk and testing behavior among MSM (30,61), results are not consistent across studies and depends on how HIV testing frequency was measured. In this study, we were conservative and captured information on testing at least once in lifetime.
Overall, almost 17% of the surveyed MSM reported never having tested for HIV (median age 29 years), which can be considered quite high as the CDC recommends that everyone aged 13-64 years should be tested at least once and that sexually active gay and bisexual men benefit from more frequent testing (e.g. every 3 to 6 months) (62). This proportion was even higher in the North and the Northeast. This may be related to limited access to health services in these regions, though only 7-10% of those who never tested reported that it was not practical to go to a health care center. The main reasons for not testing ("I am afraid of getting a positive result" and "I am ashamed") reflects the persistent HIV stigma in Brazil with fear of HIV stigma hindering HIV testing. In a study conducted in New York City, MSM and transgender women afraid of HIV stigma were less likely to get tested (63,64). In addition, some MSM already face stigma for being gay and a possible HIV diagnosis would represent a new stigma to bear. HIV testing is a key technology within the HIV prevention package, it is the necessary step to linkage to care and treatment for those with HIV infection and to prevention services for those with a negative result.
Information on the benefits of early HIV diagnosis and antiretroviral therapy initiation to decrease comorbidities related and not related to AIDS (65) and to decrease HIV transmission (50,66) are essential to decrease stigma, increase HIV testing and, as consequence, decrease new cases of HIV. HIV self-testing, which is available commercially in Brazil, can play in an important role in increasing testing, although awareness of this technology is still low in the country (12,13,67). A previous analysis verified that MSM willing to use PrEP were also willing to use HIV self-testing, indicating that both technologies could be offered in the same platform, which could be web-based (67). In this regard, it is encouraging that awareness and willingness to use PrEP increased overtime in This study has limitations. First, web-based studies are not probabilistic sampling strategies, precluding the generalization of the findings to all Brazilian MSM. Given the cross-sectional nature of the data, causality and the direction of association may not be inferred. All collected data were self-reported by participants and may be subject to bias.
However, individuals tend to be more open and honest through web-based surveys, thereby reducing the possibility of social desirability bias (69). Our data are subject to recall bias due to 6-month or 12-month recall periods. There is also a concern about participants taking the survey multiple times. To mitigate this bias, the first question of

Conclusions
Overall, MSM socio-demographic characteristics were heterogeneous among Brazilian cities, but similarities were noted among the cities from the same administrative region with a marked exception of the Federal District not following the patterns for the Central-West. Some behaviors were more homogeneous across the country, including high-risk sexual behavior, though never testing for HIV was notably higher in the least developed cities. Discordance between sexual behavior and HIV perceived risk may be a barrier to effective PrEP implementation, and prevention programs could evaluate the added role of assessing HIV risk perception.

Availability of data and materials
The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Consent for publication
Not applicable.

Competing interests
The authors declare that they have no competing interests.    In the next 12 months. with HIV-positive partner), age and use of stimulants, being stratified in low risk (< 10 points) and high risk (≥10 points; PrEP is recommended)."Unknown" answers scored 0 points on the HIRI-MSM; c During the previous 6 months. a measured by the HIRI-MSM, which was calculated based on sexual behavior in the previous six months (number of partners, condomless receptive anal intercourse, sex with HIV-positive partner), age and use of stimulants, being stratified in low risk (< 10 points) and high risk (≥10 points; PrEP is recommended); b HIV perceived risk (in the next 12 months) was dichotomized in low (no/low) and high risk. a During the previous 6 months; b HIV perceived risk (in the next 12 months) was dichotomized in low (no/low) and high risk.