HIV Prevalence among Pregnant Women in Brazil: A National Survey

Abstract Background This study was conducted to determine the seroprevalence of HIV among pregnant women in Brazil and to describe HIV testing coverage and the uptake of antenatal care (ANC). Methods Between October 2010 and January 2012, a probability sample survey of parturient women aged 15–49 years who visited public hospital delivery services in Brazil was conducted. Data were collected from prenatal reports and hospital records. Dried blood spot (DNS) samples were collected and tested for HIV. We describe the age-specific prevalence of HIV infection and ANC uptake with respect to sociodemographic factors. Results Of the 36,713 included women, 35,444 (96.6%) were tested for HIV during delivery admission. The overall HIV prevalence was of 0.38% (95% confidence interval [CI]: 0.31–0.48), and it was highest in: the 30 to 39 year-old age group (0.60% [0.40–0.88]), in the Southern region of Brazil (0.79% [0.59–1.04]), among women who had not completed primary (0.63% [0.30–1.31]) or secondary (0.67% [0.49–0.97]) school education, and among women who self-reported as Asian (0.94% [0.28–3.10]). The HIV testing coverage during prenatal care was of 86.6% for one test and of 38.2% for two tests. Overall, 98.5% of women attended at least 1 ANC visit, 90.4% attended at least 4 visits, 71% attended at least 6 visits, and 51.7% received ANC during the 1st trimester. HIV testing coverage and ANC uptake indicators increased with increasing age and education level of education, and were highest in the Southern region. Conclusions Brazil presents an HIV prevalence of less than 1% and almost universal coverage of ANC. However, gaps in HIV testing and ANC during the first trimester challenge the prevention of the vertical transmission of HIV. More efforts are needed to address regional and social disparities.


Introduction
Brazil has an HIV/AIDS epidemic that is stable at the national level and concentrated in key populations. 1 Nevertheless, Brazil has the largest number of people living with HIV/AIDS in Latin America, with 798,366 recorded AIDS cases as of June 2015 and $ 40,600 new cases each year. 2 The AIDS mortality rate has decreased in Brazil over the last ten years, 3 and was of 5.7/100,000 inhabitants in 2014. 2 Despite recent efforts to expand antiretroviral treatment (ART), 4 ART coverage, at 74.6% in 2015, 1 requires further improvement.
Regarding HIV-infected pregnant women, 63.9% received ART to reduce mother-to-child transmission (MTCT) of HIV, 1 which is the main source of HIV infection in children in Brazil. In 2013, 14,352 children under 13 years were living with HIV in this country, 92.6% of whom had acquired HIV through MTCT. 5 Brazil issued the first recommendations on the prevention of mother-to-child transmission (PMTCT) of HIV in 1996. 6,7 These recommendations were revised in 2007 with the adoption of combination ART prophylaxis for women not eligible for lifelong ART. 8 In 2010, the guidelines were updated to offer lifelong ART to all HIV-infected pregnant women regardless of their CD4 count. 9 In 2011, the Stork Network Initiative was established to strengthen antenatal care (ANC) and to expand rapid testing for syphilis and HIV in ANC services. 10 The Brazilian government has conducted periodic and anonymous probability sample surveys to determine the HIV prevalence among parturient women utilizing public sector delivery clinics since the year 1996. [11][12][13][14][15] Data from these surveillance rounds have been used to monitor HIV infection among pregnant women. Moreover, the data have been used as a proxy to estimate the prevalence of HIV among adults in the general population, 16 to make projections about HIV incidence that are helpful for resource allocation, and to evaluate the effectiveness of the national surveillance system in identifying HIV cases among pregnant women. 17,18 In each survey, women were tested for HIV, 11,[13][14][15] except for the 2006 round, in which HIV prevalence was obtained from routinely collected data. 12 The study also monitors the coverage of HIV testing, knowledge of HIV status before giving birth, and participation in ANC.
The objective of this study was to determine HIV prevalence among pregnant women in Brazil. In addition, we describe the coverage of HIV testing and participation in ANC interventions.

Sample Size
The sample size was calculated based on the objective of estimating the prevalence of HIV among pregnant women in Brazil and its regions. Considering the prevalence of HIV among parturient women in 2006 (0.41%), 12 a 95% confidence interval (CI) with a margin of error no greater than 0.15%, a design effect of 1.1, and an estimated loss to followup of 10%, the required sample size was calculated to be at least of 40,000 parturient women (8,000 in each region).

Sampling Strategy
A stratified two-stage cluster sampling design was used. In the initial stage of sample selection, 219 public hospital maternity services with at least 500 deliveries in 2007 were used as the primary sampling unit. Maternity services were stratified according to region (North, Northeast, Southeast, South, Central-West) and the population size of the municipality (< 50,000; 50,001 to 400,000; and ! 400,001 inhabitants) in which each service was located. In each stratum, 15 maternity services were selected by a probability proportional to the number of admissions for delivery in 2007. Finally, within each maternity service, 180 to 200 pregnant women were randomly selected upon admission for delivery.

Study Population and Procedures
Pregnant women admitted for delivery were included in the study if they were 15-49 years of age and had signed a written consent form to participate. Parental informed consent was not required for women younger than 18 years of age. In Brazil, according to law CFM n°1.865/96, HIV testing under 18 years of age is voluntary and consented to by the adolescent, without the need to obtain authorization or consent from their parents or their legal guardian. Trained health care workers completed a structured questionnaire that included sociodemographic variables, the date and number of ANC visits, and the date and results of HIV tests. Data were automatically recorded using the TeleForm 10.2 software (Cardiff Software Inc., Solana Beach, CA, USA).
Health professionals collected 8 drops of finger-prick blood using S&S 903 sample collection cards (Schleicher & Schuell BioScience, Keene, NH, USA). The dried blood spot (DBS) samples were sent, by mail, in ziplock plastic bags with desiccant silica to the HIV/AIDS Research Laboratory of Universidade de Caxias do Sul and stored at room temperature. Dried blood spot samples were tested using an enzymelinked immunosorbent assay (ELISA [Q-Preven HIV 1 þ 2 DBS, Symbiosis Diagnóstica, Leme, Brazil]). All positive results were confirmed with a second ELISA and Western blot analysis (DAVIH-BLOT, Laboratorios DAVIH, La Habana, Cuba). All women were informed of their tests results.

Data Analyses
HIV testing coverage during pregnancy was defined as the proportion of pregnant women among parturient women admitted for delivery who received ANC and who had an HIV test result documented in their prenatal reports. HIV testing participation during delivery admission was defined as the proportion of parturients who underwent an HIV test. HIV prevalence was defined as the number of women with positive HIV test results among parturient women admitted for delivery. Participation in ANC was classified as attending at least one, four, or six ANC visits, according to international indicators. The prevalence was calculated for the overall sample and stratified by age, region, and level of education. For women < 24 years of age, the HIV prevalence was analyzed by two-year age bands. We used the exact method to generate the confidence intervals of prevalence estimates. All analyses were conducted with the complex survey functions of Stata 11 (StataCorp LP, College Station, TX, USA) and incorporated weighting, clustering (because clinics with different sizes were included), and stratification of data.

Demographic Characteristics
Of the estimated sample size of 40,000 participants, 38,393 (96%) parturient women were included. Of those, 1,680 were excluded (4.4%) due to the lack of municipality information, which was important for the calibration of the sample, the absence of a signed informed consent form, or missing blood samples. Therefore, 36,713 pregnant women attending prenatal clinics across Brazil were included in the HIV prevalence survey. The proportion of women in the 15-19 year-old age group was 20.6%; 5.5% of participants had not completed primary school; 39.9% of participants lived in the Southeast region, and 51.2% of the participants self-reported as being of mixed race.

Discussion
In our large and probabilistic antenatal care-based study, we found an HIV prevalence of 0.38%. This value classifies Brazil as having a concentrated epidemic (HIV prevalence < 1% in the general population), 19 but it hides regional variations.
HIV prevalence in the South region is twice that of the national estimate. This region has consistently presented the highest estimates in the country for HIV surveillance indicators. In 2012, the AIDS detection rate was reported at 30.9 cases/100,000 inhabitants, and the mortality rate was 7.7 deaths/100,000 inhabitants, which is higher than that of the country (20.2 cases/100,000 inhabitants and 5.5 deaths/ 100,000 inhabitants respectively). 1 The prevalence of HIV among young people (15-24 years of age) is one of the leading indicators of progress toward international goals, such as those set in the United Nations General Assembly Special Sessions (UNGASS) declaration on HIV/AIDS. 19 The HIV prevalence in this age group was of 0.31%, which is lower than the overall estimate for the country. The HIV prevalence in 15-24 year-olds is considered a reliable measurement to approximate HIV incidence because this population can be presumed to have recently become sexually active. 20,21 In our study, the 17-18 year-old age group presented a burden of potential HIV incidence of 0.40%, which is higher than the rate in pregnant women in the 15-24 year-old age group. HIV acquisition in this group reflects sexual initiation, which occurs at $ 16 years of age, 22 and is a concern if we assume that HIV transmission is highest during early and acute HIV infection. Changing the HIV epidemic burden in this group will require prevention and interventions targeted at teenagers.
We found an HIV prevalence similar to the prevalence of 0.41% estimated in 2006. 12 In that prior HIV survey, the HIV prevalence in childbearing women was estimated based on secondary data registered in prenatal reports or hospitalization records from public maternity hospitals. Although different methods were used in this prior survey and the current study (with values determined in 2006 based on routinely collected data, and in 2010-2012 based on testing women for HIV), similar results were obtained. These results indicate that HIV prevalence appears to be stable despite a continuing increase in ART coverage. The HIV detection rate among pregnant women in Brazil has exhibited an increasing trend during the preceding three years. 2  The HIV test coverage during pregnancy was of 86.6%, which is higher than the 74% estimated for Latin America and the Caribbean in 2013. 23 However, improvement is required to attain the coverage rate of 95% proposed by the Pan American Health Organization (PAHO) for the Latin American and Caribbean region for a vertical transmission control program. 24 Coverage of HIV testing has increased substantially since 2006 (62.3%). 12 The coverage improved in each region, but inequalities persist, with the North and Northeast regions presenting lower coverage estimates of 75.3% and 74.1% respectively. The geographical inequalities in testing coverage and in HIV prevalence are reflected in the MTCT rate for HIV, which varies across the country. The most recent estimates are higher for northern Brazil, ranging from 6.6% to 18.9%, [25][26][27] than for the south of the country, at 4.9%. 28 Only 38.2% of pregnant women underwent a second serological test for HIV. This second test is indicated in the third trimester, and was introduced in 2006 as part of a prenatal care routine. 29 The low coverage observed may be partly attributed to the fact that only 40.5% of women received ANC during the first trimester, which limits timely opportunities to perform a second test and to initiate strategies to prevent the vertical transmission of HIV.
Access to antenatal services in Brazil is high, with > 95% of pregnant women attending at least one ANC visit. While coverage of one ANC visit is practically universal, fewer women are covered when more meaningful and comprehensive ANC, consisting of four or more ANC visits or the national recommendation of six or more visits, is considered. The insufficient number of ANC consultations may be due to late presentation to ANC, issues with the quality of ANC, and/or failure to follow-up by the pregnant women. 23 The burden of HIV infection and lack of coverage of indicators, both for HIV testing and ANC visits, in women with lower educational levels and who are non-white, is concerning. Although Brazil has universal access to interventions to prevent the MTCT of HIV, it is failing to reach the lower social strata of society. Other studies have corroborated the association between socioeconomically and educationally disadvantaged women and lower levels of access to HIV prevention measures during pregnancy. [30][31][32] The study has several limitations. The extent to which pregnant women attending antenatal clinics are representative of all women is affected by attendance at private clinics, and is due to systematic differences among women who attend public ANC clinics, who have a lower socioeconomic status, and those who attend private clinics. In a national hospital-based study conducted on puerperal women in 2012, the HIV prevalence differed according to type of delivery service (0.10% in private hospitals and 0.58% in public hospitals). 30 In Brazil, more than 99% of deliveries occur in hospitals, and therefore non-attendance at ANC clinics might not have affected our estimates. 33 HIV in Brazil is prevalent among older women who experience lower fertility rates and thus are less likely to be represented among ANC clinic attendees. 34,35 Antiretroviral treatment may ameliorate HIV-related subfertility; 34 thus, with increasing high levels of ART coverage, HIV rates among older pregnant women may again become more similar to those of the general population. 36 Our study did not consider other factors that could influence the representativeness of HIV prevalence among ANC attendees, such as contraceptive use. 20,21,37 In conclusion, our results indicate that the prevalence of HIV in Brazil remains at less than 1% and similar to that of 2006, despite the expanded population level coverage of ART. The results from the youngest group (aged 15-24 years) are encouraging, given the large investment in the prevention of HIV. Access to ANC services is universal, but more efforts are needed to increase the proportion of women who successfully complete at least six ANC visits, as recommended by the Brazilian Ministry of Health. Coverage of HIV testing has greatly increased since 2006, and although it is > 80%, it is subject to improvement because universal and free access to HIV testing is provided at ANC services. This finding, coupled with the fact that only half of women receive ANC care in the first trimester, results in missed opportunities to prevent the MTCT of HIV. Regional and social disparities in access to ANC clinics and HIV testing show that actions to overcome barriers for these services are not reaching the populations with a higher burden of HIV infection. Programs might consider ways to make these services more targeted to the North region and to socially disadvantaged populations, who are most at risk for HIV.