A scoping review of prevalence, incidence and risk factors for HIV infection amongst young people in Brazil

Young people, especially young women, are considered a key population for HIV prevention interventions worldwide [1]. However, targeting interventions is difficult when information on HIV prevalence and risk factors is patchy or missing altogether. Several risk factors for sexually transmitted infections (STIs) are elevated amongst young people, such as being in the beginning of their sexual life, experimenting with high-risk behaviors and feeling invulnerable [2]. Although Brazil is world-renowned for its leadership in the fight against AIDS [3‐5], and even as AIDS rates are declining in many other places, Brazil is perceived to be facing a sharp increase in HIV infections among young people [6].

AIDS has been a reportable condition in Brazil throughout the epidemic. Over the past 10 years the AIDS detection rate has averaged 20.5 cases per 100,000 persons per year [7]. Between 2004 and 2013, reported AIDS cases in Brazil rose by 53.2% among those aged 15-19 and 10.3% among those aged 20-24 [8]. These increases were greater in men than in women: between 2005 and 2014 reported AIDS case rates per 100,000 persons per year rose from 2.1 to 6.7 for 15-19 year old males and from 3.4 to 4.2 among 15-19 year old females; for 20-24 year olds the rate rose from 16.0 to 30.3 among men but decreased from 15.3 to 12.0 among women [7]. These differences in case rate trends are reflected in the changing ratio of male to female AIDS notifications: among 13-19 year olds this ratio fell from 2.7:1 in 1990 to a low of 0.6:1 in 2005, before rebounding to reach 1.6:1 in 2014. Notably, these rising rates are in contrast to older ages: AIDS notification rates fell in all five-year age ranges from 30 to 49 years old between 2005 and 2014.

In contrast, HIV has not historically been a reportable condition. From 2007 to June 2015, 93,260 HIV infections were notified in Brazil [7], however, mandatory notification of HIV infection began only in June 2014. Additionally, health service providers can notify both newly-identified and existing known cases, which makes epidemiologic analysis of national HIV case reports difficult. In 2015, approximately 830,000 people were estimated to be living with HIV in Brazil, a prevalence of 0.40% [8]. Between 2007 and 2015, the proportion of HIV-positive individuals reported to be the age groups 10-14, 15-19 and 20-24 years old rose from 0.3%, 4.3% and 13.4% of all notifications to 0.3%, 6.1% and 18.2%, respectively. Across all ages, the male to female ratio of notified HIV infections increased slightly from 1.9 in 2007 to 2.2 in 2014.

Given these epidemiological patterns, a review of the literature on HIV in young people in Brazil seems timely. Past literature reviews have discussed specific aspects of HIV in adolescents and young people in Brazil. These studies have shown the difficulty of transitioning from childhood to adult life for adolescents living with AIDS [9], the efficacy of preventive interventions focusing on this population [10], the situation of orphans and vulnerable children [11] and the relationship between STIs, AIDS and abuse of psychoactive substances in adolescence [12]. In addition, several articles have analyzed risk behavior and HIV infection among adolescents in Brazil in specific populations, such as users of anonymous Counselling and Testing Centers (CTA), interns of the correctional system, pregnant women, men-who-have-sex-with-men (MSM) and others. However, there is no comprehensive literature review putting together the results of these studies amongst young people, and it is difficult to see trends over time in the adolescent HIV epidemic in Brazil.

The aim of this study is therefore to review all published evidence on HIV prevalence and incidence, and how they relate to risk behaviors among different populations of Brazilian adolescents between 1982 and 2015. Such information should help identify gaps in the literature, and provide a scientific basis for the development of preventive strategies for this age group.

We performed a systematic search on seven electronic databases – PubMed, Embase, PsycINFO, LILACS, Web of Science, Scopus and ProQuest – to identify potentially relevant analyses. The keywords we used for this search were the MeSH terms [“HIV” or “HIV infection”], “Adolescents” and “Brazil” or similar non-MeSH terms outside of PubMed. The search was conducted between March 25th and March 31st 2017. Reference lists were also analyzed for any potentially relevant articles not included in the original search. We included any conference proceedings (within Web of Science and Scopus) and dissertations (ProQuest) found in our database searches.

One author analyzed all articles found by title to select those that were potentially relevant, with a strong bias towards retention. The abstracts of all studies selected based on their titles were independently evaluated by two authors (IPS and GH) and any discrepancies were kept in the analysis. For all studies selected at the abstract stage, data were extracted using an instrument designed for this study, covering sociodemographic characteristics (gender, age group, location, race and social categories), methodology (study design, study population, data source, time period of data collection, baseline sample size and loss to follow up), and outcomes (HIV prevalence or HIV incidence, risk behaviors).

The final decision to include studies was made based on this data extraction and whether it met the inclusion/exclusion criteria, based on independent evaluation by two authors (IPH and GH), and a discussion of any discrepancies; the third author (HK) was available for consultation if agreement could not be reached. Our inclusion criteria were that studies: (i) contained either (a) HIV prevalence or incidence data or (b) analysis of risk factors for HIV infection; (ii) either focused on individuals aged between 10 and 25 years, or stratified their results by the age group of interest; (iii) included data on the Brazilian population. Conversely, our exclusion criteria were: (i) lack of stratification by age, if covering a broader age group than 10-25 years; (ii) lack of stratification by country, if a multinational study; (iii) lack of quantitative presentation of data on prevalence, incidence or risk factors; (iv) reporting only AIDS cases instead of HIV infections; (v) reporting only on HIV positive individuals.

Of the 2180 unique articles identified by database searches, 470 studies were selected as potentially relevant for this analysis based on their titles (Fig. 1). We retained 128 of these based on their abstracts, although we were unable to obtain the full text of four of these (all four were published before 1995). Sixty two studies that otherwise met our inclusion criteria were excluded because they did not stratify their results by age group so we could extract data specific to young people, and 14 other articles did not meet other inclusion criteria. This left 48 studies which reported either HIV prevalence or risk factors for our age group of interest and were published in English, Portuguese or French (note, we kept one study with an age range 15-26). Thirty-six of these 48 articles provided an age-specific HIV prevalence, but not HIV risk factors; we therefore report results separately for prevalence and risk exposures. We summarize all studies included in the final analyses in Table 1.

In this study, we reviewed all published evidence on HIV prevalence and risk factors for infection amongst 10-25 year olds in Brazil. A key finding of our review is the lack of comprehensive data regarding risk behaviors for HIV infection either through studies specifically amongst adolescents, or stratified for this age group. Most of the studies we identified covered a broad age range, from adolescence up to senior ages, and in most cases HIV prevalence, but not risk factors, were stratified by age group. In some cases, the stratification grouped young and middle-aged adults in the same age group (e.g. 20 to 40 years old), which limited their usefulness for understanding risks amongst young people. While analyses of wider age ranges and the conditions of already-infected individuals appear quite common, focused evidence of the extent, and predictors, of young Brazilians’ risk of HIV infection remains limited. As a result, we were not able to conduct a quantitative assessment of any outcome using meta-analysis.

Despite its limitations, some important themes can be seen in the literature reviewed. First, the geographic coverage of the literature was limited. Of the 48 articles included in the final analysis, 14 were conducted in the South region and 14 in the Southeast region, while ten were in the Northeast, four in the Center-West and one in the North region of Brazil (four were national and one covered cities in both the South and Northeast). According to the last HIV Epidemiological Bulletin released by the Brazilian Ministry of Health in 2015, AIDS cases are increasing in the Center-West, North, and Northeast regions in the general population, and two of the four states with the highest AIDS reporting rates (Amazonas and Roraima) are in the North [62]. At the municipal level, the state capitals with the second to fifth highest reported AIDS rates (Florianópolis SC, Manaus AM, São Luís MA and Belém PA) have no published studies regarding young people and HIV. The literature’s focus in the South is supported by two of the three states of this region having the second- and third-highest reported AIDS rates in the country, and by the fact that almost 75% of the AIDS cases identified in Brazil from 1980 until June of 2015 were in the South and Southeast regions [7]. While these higher reporting rates may reflect these regions wealth, and therefore ability to diagnose AIDS cases, it may also reflect that the body of literature reflects past history of the HIV epidemic, rather than the current situation. It is also notable that many studies were conducted in state capital cities, and even those studies conducted elsewhere were often conducted in university campus cities, such as Campos dos Goytacazes [17], Feira de Santana [27, 38], Londrina [32] or Campina Grande [33]. All these trends highlight a clear need for additional research in non-traditional risk areas of Brazil.

Second, a large proportion of infections amongst both adolescents and young people were recent: 9.6% of HIV-positive individuals aged under 25 in Santos [15]; 17.9% of HIV-positive 20-24 year olds attending antenatal care in Sao Paulo [31]; 18.8% and 19.4% of HIV-positive 18-24 year olds Recife and Curitiba respectively in 2013 [60]; 25% of HIV-positive 15-24 year olds in Sao Paulo CTAs [21]; and 44.4% of HIV-positive adolescents seeking care in Recife CTAs [26]. While unsurprising, given the briefer sexual history of younger people and the predominantly sexual transmission route for HIV in Brazil, these data highlight the importance of developing preventive strategies focusing this age group, based on the behavioral risk factors to which they are more susceptible.

Third, the literature highlights some groups of young people at increased risk of HIV infection. HIV infection rates are high among MSM, and are rising relative to the general population. Two nationwide studies of military conscripts in 2002 and 2007 reported HIV prevalence among MSM of 0.56% and 1.23% respectively, while the overall population prevalence remained stable [50, 52]. HIV prevalence was even higher amongst sex workers, with an HIV prevalence of 6.8% [55] and 5.3% [56] amongst sex workers aged under 26 in two studies in Santa Catarina state. Sex workers are well-recognized as being at higher risk of HIV infection; HIV prevention policies focused on younger sex workers may be particularly important. Finally, there may be a downward trend in decreasing the infection rates amongst pregnant women, at least in one setting: HIV prevalence among pregnant women aged between 10 and 20 in Paraná in 1996-98 was 1% [32], but had fallen to 0.3% among 14-19 year old pregnant women by 2010 [43].

Fourth, several behaviors were reported as predictors of HIV infection. Use of illicit drugs or attending drug-using/selling places was consistently associated with increased HIV risk [18, 27, 46, 61]. In addition, a history of STIs was also associated with HIV infection in more than one study [42, 46, 50]. Interestingly, being in a stable relationship was associated with HIV infection among women while being unmarried was associated with infection among men [27]. This may reflect the higher risk for HIV amongst MSM. Somewhat surprisingly, in no study was past condom use associated with infection rates; this may reflect low interest amongst researchers, inaccurate reporting by respondents (due to recall bias or intentional mis-reporting) or truly no association in the populations studied.

One topic of concern within Brazil in recent years has been the “feminization” of the HIV epidemic. This was reflected in research highlighting that the male to female ratio of reported AIDS cases among adolescents in Rio de Janeiro city fell from 4.7 in the period 1984-1989 to 0.5 in 2005-2009 [63], and from 24 to two nationally between 1985 and 1999 [64]. HIV prevalence rates amongst 14-20 year olds were reported to have equalized by 2002 [65]. This led to the launch of a national campaign to combat the feminization of the epidemic in 2007, particularly through combatting women’s vulnerabilities [66]. More recently the ratio of male to female AIDS cases has again risen [7], however, young women living with HIV appear to be particularly vulnerable, even amongst all women living with HIV [67].

Our review of the literature on HIV prevalence, incidence and risk factors in Brazil suggests that there is an unmet need for research into HIV risk patterns in the country. This is particularly true given suggestions in the literature that HIV prevalence may have been increasing among adolescents in recent years. The 2014 change in the law to require medical staff to notify the government of HIV infections may act as a spur to action for such research, by providing standardized nationwide data. However, given the relatively low national HIV prevalence, and thus relatively low HIV testing rates, amongst young Brazilians, the use of targeted, nationally representative surveys of young people using biological testing for HIV and STIs may well also be justified.