HIV testing among pregnant women in Brazil: rates and predictors

OBJECTIVE: To assess rates of offering and uptake of HIV testing and their predictors among women who attended prenatal care. METHODS: A population-based cross-sectional study was conducted among postpartum women (N=2,234) who attended at least one prenatal care visit in 12 cities. Independent and probabilistic samples were selected in the cities studied. Sociodemographic data, information about prenatal care and access to HIV prevention interventions during the current pregnancy were collected. Bivariate and multivariate analyses were carried out to assess independent effects of the covariates on offering and uptake of HIV testing. Data collection took place between November 1999 and April 2000. RESULTS: Overall, 77.5% of the women reported undergoing HIV testing during the current pregnancy. Offering of HIV testing was positively associated with: previous knowledge about prevention of mother-to-child transmission of HIV; higher number of prenatal care visits; higher level of education and being white. HIV testing acceptance rate was 92.5%. CONCLUSIONS: The study results indicate that dissemination of information about prevention of mother-to-child transmission among women may contribute to increasing HIV testing coverage during pregnancy. Non-white women with lower level of education should be prioritized. Strategies to increase attendance of vulnerable women to prenatal care and to raise awareness among health care workers are of utmost importance. DESCRIPTORS: Pregnant Women. HIV Infections, diagnosis. Acquired Immunodefi ciency Syndrome, prevention & control. Prenatal Care. Socioeconomic Factors. Cross-Sectional Studies. 860 HIV testing among pregnant women Veloso VG et al The availability of effective interventions to prevent mother-to-child transmission (PMTCT) of HIV infection makes the identifi cation of HIV-infected pregnant women a high priority.2 In 2000, it was estimated that 600,000 people were living with HIV/AIDS in Brazil with 0.4% prevalence among childbearing women.18 By mid 2006, 433,067 AIDS cases had been reported to the Brazilian Ministry of Health (30% in females).a Overall, three million deliveries occur each year in the country, 14,000 among HIV-infected women. Brazil was the fi rst developing country to implement a large scale PMTCT program.b Since 1997, the Brazilian Ministry of Health has adopted a policy of universal offering of HIV testing to pregnant women, coupled RESUMO OBJETIVO: Estimar as taxas de oferta e realização do teste anti-HIV e seus preditores entre mulheres que receberam atendimento pré-natal. MÉTODOS: Foi conduzido estudo transversal, de base populacional, com 2.234 puérperas em 12 cidades do Brasil. Amostras probabilísticas foram selecionadas independentemente por cidade, entre puérperas que compareceram a pelo menos uma visita pré-natal. Foram coletados dados sociodemográfi cos, informações sobre cuidado pré-natal e acesso a intervenções de prevenção do HIV durante a gravidez corrente, com a utilização de um questionário. Foram realizadas análises bivariadas e multivariadas para verifi car os efeitos independentes das covariáveis na oferta e realização do teste anti-HIV. Os dados foram coletados no período de novembro de 1999 a abril de 2000. RESULTADOS: A realização do teste na gravidez foi relatada por 77,5% das entrevistadas. A oferta do teste anti-HIV foi positivamente associada a: conhecimento prévio sobre a prevenção da transmissão materno-infantil do HIV; maior número de visitas pré-natal; maior nível de escolaridade e ter cor da pele branca. A taxa de aceitação do teste anti-HIV foi de 92,5%. CONCLUSÕES: Os resultados indicam que a disseminação da informação sobre prevenção da transmissão materno-infantil do HIV pode contribuir para aumentar a cobertura da testagem anti-HIV durante a gravidez. Mulheres nãobrancas com menores níveis educacionais devem ser priorizadas. Estratégias para aumentar a participação de populações vulneráveis ao cuidado pré-natal e a sensibilização de trabalhadores de saúde são de grande importância. DESCRITORES: Gestantes. Infecções por HIV, diagnóstico. Síndrome de Imunodefi ciência Adquirida, prevenção e controle. Cuidado PréNatal. Fatores Socioeconômicos. Estudos Transversais.

The availability of effective interventions to prevent mother-to-child transmission (PMTCT) of HIV infection makes the identifi cation of HIV-infected pregnant women a high priority. 2 2000, it was estimated that 600,000 people were living with HIV/AIDS in Brazil with 0.4% prevalence among childbearing women. 18By mid 2006, 433,067 AIDS cases had been reported to the Brazilian Ministry of Health (30% in females).a Overall, three million deliveries occur each year in the country, 14,000 among HIV-infected women.
Brazil was the fi rst developing country to implement a large scale PMTCT program.b Since 1997, the Brazilian Ministry of Health has adopted a policy of universal offering of HIV testing to pregnant women, coupled RESUMO OBJETIVO: Estimar as taxas de oferta e realização do teste anti-HIV e seus preditores entre mulheres que receberam atendimento pré-natal.

CONCLUSÕES:
Os resultados indicam que a disseminação da informação sobre prevenção da transmissão materno-infantil do HIV pode contribuir para aumentar a cobertura da testagem anti-HIV durante a gravidez.Mulheres nãobrancas com menores níveis educacionais devem ser priorizadas.Estratégias para aumentar a participação de populações vulneráveis ao cuidado pré-natal e a sensibilização de trabalhadores de saúde são de grande importância.with counseling.d Despite being crucial to the proper management of AIDS programs, evaluation of coverage of PMTCT interventions and outcomes are still limited in Brazil.The objective of the present study was to assess the rates of HIV testing offering and uptake and their predictors among women who attended prenatal care.

METHODS
A population-based cross-sectional study was conducted among postpartum women (≥18 years of age) who delivered under the coverage of the Sistema Único de Saúde (Brazilian Health System, SUS) and who attended at least one prenatal care visit and signed an informed consent form.According to Brazilian law, any woman younger than 18 years old, if not legally married or living with a partner, was only eligible for the study if their parents/guardians signed an informed consent form.Those women who had experienced an abortion, a stillbirth or any other clinical condition preventing an interview were excluded from the eligible population and from the study.
Every maternity hospital with at least one delivery per day comprised a selection stratum.The sample size of postpartum women for each city studied was determined to estimate the prevalence of HIV testing during prenatal care with a relative error varying from 0.1 to 0.3 (Table 1).The ratio of postpartum women sample size by mean daily deliveries covered by SUS in the city provided the number of survey days in a city.Each survey day corresponded to a cluster in which all women who delivered in the previous day, if eligible, were interviewed.After the number of clusters was de-termined, women were randomly selected from the set of days of the period of fi eldwork, with equiprobability and independently for each maternity hospital.
Since the number of 24-hour clusters was the same in all maternity hospitals in a given city, the sample size of women was proportionally allocated to the number of deliveries per hospital, which lead to a self-weighted sample by city.
Postpartum women were approached to participate in the study prior to being discharged from the maternity hospitals.
All eligible women were invited to participate.
Trained interviewers queried the women using a validated questionnaire.Sociodemographic data, information about prenatal care service utilization as well as access to HIV counseling, testing and prevention interventions during the current pregnancy were collected.Data was collected between November 1999 and April 2000.
Data entry and management were carried out using the Integrated Microcomputer Processing System, a statistical package developed by the United States Bureau of the Census.a In order to account for the effects of a complex sampling design, analyses were performed using SAS 13 version 8.2 and SUDAAN (SAS callable) version 8. 17 Descriptive statistics were generated for all study variables.Bivariate analyses were conducted to assess the relationship between offering and uptake of HIV testing and potential explanatory variables -age, race, level of education, formal employment, monthly income, previous knowledge about the importance of knowing one's HIV status and its potential benefi ts to the child ("previous knowledge"), primiparity (vs.previous birth[s]), trimester of fi rst prenatal visit, number of prenatal visits, and utilization of a public primary care unit for prenatal care.Moreover, there was a concern with capturing the effects of differences among the cities studied on the outcomes.Counseling and testing offering were considered in the explanation of testing uptake.
Multivariate logistic regression models were developed to assess the independent effects of the variables on HIV testing offering and uptake.
The National Research Ethics Committee approved the study protocol and all participating women signed an informed consent.

RESULTS
A total of 2,234 women were interviewed, 96.5% of the total sample size, who were selected from the study eligible population of 20,886 women.
Mean age was 25 years and half of the interviewees were non-white.Most reported 8 or less years of education and having received prenatal in a public primary care service.The large majority reported that the fi rst prenatal care visit occurred during the fi rst (66.5%) or the second trimester (27.6%) of pregnancy.Most of them reported they had attended at least six prenatal care visits.Knowledge about AIDS and awareness about the importance of HIV testing for PMTCT was reported by 92.6% and 85.2% of the women, respectively (Table 2).
Overall, 77.5% of the women reported undergoing HIV testing during the current pregnancy.Of them, 13.8% (1.2% -21.8%) reported they had been tested during routine prenatal screening tests without their prior knowledge or consent.
Among those who were offered HIV testing, 92.5% accepted it, but only 37.5% were informed they could choose not to take it.In addition, among those who received their HIV testing result, only 47.4% reported they were explained the meaning of the HIV testing result.
Regarding information about HIV prevention, only 50% of the women surveyed reported they had received it.A previous HIV testing at any point in lifetime before the current pregnancy was reported by 26.4%.The bivariate analyses showed that years of education, previous knowledge about HIV testing for PMTCT, number of prenatal care visits and cities were significantly associated with testing offering and uptake.In addition, testing uptake was also signifi cantly associated with race, monthly income, primiparity, trimester of fi rst prenatal care visit, counseling and testing offering.Table 3 shows the fi ndings of cross-analyses between testing offering and uptake and potential explanatory variables.
The multivariate logistic regression model for HIV testing offering is shown in Table 4. Offering of HIV testing was found to be positively associated with being white (borderline signifi cance, p=0.0655), having more years of formal education, having previous knowledge about the importance of HIV testing for the prevention of HIV vertical transmission, and having a higher number of prenatal care visits.The interaction effect of being white and having previous knowledge about the importance of HIV testing was found to be negative.The cities Duque de Caxias, Uruguaiana, and Curitiba did not differ signifi cantly from the city of Rio de Janeiro, which was the fi rst city to implement largescale PMTCT training of health care workers.For this reason, these cities were taken as the reference group in the analysis.In the cities São Paulo, Florianópolis, Porto Alegre, Campo Grande, and Brasília, testing offering was signifi cantly lower than in the reference group.The cities of Santos, Sorocaba, and Itajaí had a higher testing offering vis-à-vis all other cities.
We made several attempts to fi t a model for testing uptake but unsuccessfully.This is probably because 'testing offering' explained most of the variation in test uptake (OR=35.31)(Hosmer-Lemeshow test, p=0.2084).Nonetheless, the study data indicate that counseling and total number of prenatal care visits do had a positive effect on testing uptake.

DISCUSSION
The results showed that, in spite of receiving prenatal care, almost one-fourth of the women went through pregnancy without being tested.Unaware of their status, these women were unable to benefi t from interventions available in Brazil to reduce mother-to-child HIV transmission.
Several studies have already demonstrated that minority populations have more diffi cult access to health care, even when it is free. 1,20,21This seems to be the case of HIV counseling and testing during pregnancy in Brazil.
It was found a lower rate of HIV testing offering among non-white women, those with lower level of education and those attending fewer prenatal care visits when compared to white women, those with intermediate or higher level of education, and those attending a higher number of prenatal care visits.This is a matter of concern, since in Brazil the HIV/AIDS epidemic has primarily affected the poor, especially those with lower education and belonging to the Black population. 5Education and prenatal care were found to be determinants for being tested in several studies conducted in developed and developing countries, including Brazil. 10,16 developed countries, the lack of testing offering is known to be one of the main reasons for pregnant women not to receive HIV testing. 10Although most obstetricians support HIV testing in prenatal care, they often rely on their perceptions about women's risk. 19Insuffi cient time and training and the sensitive nature of discussing issues related to HIV infection may also prevent providers from offering HIV testing to pregnant women. 3nce there are now available effective interventions to reduce HIV transmission from mother to child to below 2%, failure to offering HIV testing to pregnant women and appropriate interventions for those infected should be considered negligence.
The fi nding of 92.5% of HIV testing acceptance is reassuring.Similar rates of acceptance were also found in other studies conducted in Brazil, including when HIV testing was offered during labor. 6,9,12The wide availability of free HIV prevention and care services in Brazil, which includes highly potent antiretroviral therapy and HIV testing, as well as the policy of universal offering of HIV testing to pregnant women would be among the several factors contributing to the high rate of HIV testing acceptance seen in the present study.
The high proportion of women (14%) who reported they were HIV tested as part of prenatal care routine tests whithout being informed raises concern.In addition, among those women to whom HIV testing was offered, less than two-thirds were informed they had the right to refuse it.This practice can explain a higher number of women tested for HIV than the number of women offered testing in the cities of São Paulo, Sorocaba, Curitiba, and Porto Alegre.A large study conducted in Porto Alegre for one year during the same period covered by the present study also found a high proportion of unawareness of being tested/compulsory HIV testing. 9The literature review we carried out did not fi nd any study in the other three cities adressing the issue of compulsory HIV testing.In a study performed in Spain to compare self-reporting with medical record information regarding HIV testing, unawareness of having been tested was found in 10.7% of the study population.
Although it is unquestionable that HIV testing would be benefi cial to all pregnant women, they must not be tested without their knowledge and have the right to be informed to make decisions about their health.postpartum women allowed to gathering data about interventions received during the entire prenatal care period.In Brazil, births take place predominantly in hospitals.In the year 2000, only 1.4% of the deliveries occurred outside hospitals, and home delivery is uncommon in the cities included in the study. 7ong limitations of the study, HIV testing data were based on self-reports.However, while recall bias cannot be excluded, it is unlikely that patients would not recall their testing and counseling experiences related to the current pregnancy.Also, it cannot be excluded that some women assumed they were tested for HIV, when they were not.Another point to consider is that women under 18 years of age were not adequately represented in the study population, as the Brazilian law does not allow them to be enrolled in such studies.
In conclusion, Brazil continues to face a huge challenge to prevent mother-to-child transmission of HIV infection.In spite of the high rate of HIV testing acceptance among pregnant women, one-fourth of the women attending prenatal care has not been tested for HIV or even have been offered it.The study data indicate that dissemination of information about prevention of mother-to-child transmission among women may contribute to increase HIV testing coverage during pregnancy.Non-white women with lower education should be prioritized.In addition, strategies to increase attendance rates of vulnerable populations to prenatal care visits as well as to sensitize and train health care workers to systematically offer HIV testing in prenatal care are of utmost importance to overcome the barriers to prevent HIV infection among children.
* Based on data from 1997, excluding maternity hospitals that discontinued their services and those funded after 1997.** The calculated number of clusters is the number of study days in each hospital and was calculated as the ratio of the calculated sample size of postpartum women by the number of daily deliveries in a city, without adjusting for the expected prevalence of prenatal care coverage rate.

Table 2 .
Sociodemographic data and knowledge about prevention of mother-to-child transmission by city.Brazil, 1999-2000.