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HIV-1 incidence among people seeking voluntary counseling and testing centers, including pregnant women, in Pernambuco State, Northeast Brazil

Incidência do HIV-1 em pessoas atendidas, incluindo gestantes, em um Centro de Testagem e Aconselhamento em Pernambuco, Nordeste do Brasil

Incidencia del VIH-1 en personas atendidas, incluidas las mujeres embarazadas, en un centro de pruebas y asesoramiento en Pernambuco, Noreste de Brasil

Abstracts

The HIV-1 epidemic in Brazil has displayed new characteristics over time, with an increase in heterosexual transmission and a decline in the male-to-female ratio in AIDS cases. HIV screening was offered to patients attending the Voluntary Counseling and Testing Center in Paulista, Greater Metropolitan Recife, Pernambuco State, in Northeast Brazil, to determine HIV-1 incidence. BED capture enzyme immunoassay (BED-CEIA) was used to measure HIV-1 incidence, comparing it to the AxSYM avidity index method (Ax-AI). From 2006 to 2009, 14,014 individuals were tested, and only 18 pregnant women were diagnosed with HIV infection, resulting in 0.15% annual incidence (95%CI: 0-0.33), significantly lower than in men (1.03; 95%CI: 0.45-1.61) and non-pregnant women (0.50; 95%CI: 0.11-0.89). Despite the low HIV-1 incidence in pregnant women, the high rate of recent infection detected during prenatal care emphasizes the need to increase measures to prevent vertical transmission.

HIV-1; Incidence; Infectious Disease Vertical Transmission


No Brasil, a epidemia do HIV-1 adquiriu novas características ao longo do tempo, como o aumento da transmissão heterossexual e um declínio da razão homens:mulheres em casos de AIDS. Foi oferecida triagem para a infecção pelo HIV a todos os pacientes atendidos no Centro de Testagem e Aconselhamento da cidade de Paulista, Região Metropolitana de Recife, Pernambuco, Nordeste do Brasil, com o objetivo de determinar a incidência do HIV-1. Foi usado o enzimaimunoensaio de captura BED (BED-CEIA) para determinar a incidência do HIV-1, comparando-o com o método de índice de avidez AxSYM (Ax-AI). No período analisado, 2006-2009, 14.014 pessoas foram testadas, e apenas 18 gestantes foram diagnosticadas para a infecção por HIV, resultando em uma incidência de 0,15% ao ano (IC95%: 0,00-0,33), significativamente menor do que os homens (1,03; IC95%: 0,45-1,61) e mulheres não-grávidas (0,50; IC95%: 0,11-0,89). Apesar da baixa incidência de HIV-1 entre as mulheres grávidas, a alta taxa de infecção recente reforça cuidados no pré-natal para esta infecção, para evitar a transmissão vertical.

HIV; Incidência; Transmissão Vertical de Doença Infecciosa


En Brasil, epidemia del VIH-1 adquiere nuevas características con tiempo, como el aumento de la transmisión heterosexual y disminución de la razón hombres:mujeres en los casos de SIDA. La detección de infección por VIH se ofrece a todos los pacientes que acuden al Centro de Asesoramiento y Pruebas (CTA) en la ciudad de Paulista, área metropolitana de Recife, noreste - Brasil, con objetivo de determinar la incidencia del VIH-1. BED inmunoensayo enzimático de captura (BED-CEIA) se utilizó para determinar la incidencia de VIH-1, comparándolo con el método del índice de avidez AxSYM (AX AI). En el período de 2006-2009, 14.014 personas se pusieron a prueba, 18 mujeres embarazadas fueron diagnosticados con infección por VIH, com incidencia de 0.15% anual (IC95%: 0-0.33), inferior a los hombres (1.03; IC95%: 0.45-1.61) y las mujeres no embarazadas (0.50; IC95%: 0.11-0.89). A pesar de la baja incidencia de VIH-1 en las mujeres embarazadas, alta tasa de infección reciente aumenta en la atención prenatal para esta infección para prevenir la transmisión vertical.

VIH; Incidencia; Transmisión Vertical de Enfermedad Infecciosa


Estimates of HIV incidence rates are important for evaluating the epidemic’s dynamics, targeting the implementation of appropriate preventive measures, monitoring intervention strategies and highlighting the impact of the virus infectivity and its transmission 1Morgado MG, Bastos FI. Estimates of HIV-1 incidence based on serological methods: a brief methodological review. Cad Saúde Pública 2011; 27 Suppl 1:S7-18.. According to the Brazilian Ministry of Health 2Programa Nacional de DST-AIDS, Ministério da Saúde. Boletim Epidemiológico de AIDS e DST 2013; ano VII, nº 1., most cases of HIV-positive pregnant women were reported in the Southeast (43%) and South regions (32%), followed by the Northeast region (14%). An important point for the evaluation of HIV-positive pregnant women is the possibility of mother-to-child transmission 3Rodrigues R, Manenti S, Romao PR, de Paula Ferreira JL, Batista JP, Siqueira AF, et al. Young pregnant women living with HIV/AIDS in Criciuma, Southern Brazil, are infected almost exclusively with HIV type 1 clade C. AIDS Res Hum Retroviruses 2010; 26:352-7..

Surveillance of the epidemic through the counting of AIDS cases does not reflect the current epidemic dynamics. For this reason, we decided to apply for the first time in the Northeast of Brazil a methodology that uses laboratory assays for the identification of a period of recent seroconversion and estimates HIV-1 incidence, known as RITA (Recent Infection Testing Algorithm) 4UNAIDS Working Group on Global HIV/AIDS and STI Survaillance. When and how to use asssays for recent infection to estimate HIV incidence at a population level. Geneva: World Health Organization; 2011..

The study aimed to determine HIV-1 incidence through immunoassays among individuals attending at the Voluntary Counseling and Testing Center (VCT) in Paulista, city in the Metropolitan Region of Recife, Pernambuco State, Northeast Brazil, in the period from 2006 to 2009. The VCT treated a total of 14,014 individuals, including 5,949 pregnant women, 4,418 non-pregnant females and 4,092 male individuals in that period. Patients arrived at the VCT as a result of being sent by Primary Healthcare Units or through spontaneous demand.

HIV-1 diagnosis was performed according to the guidelines of the Brazilian Ministry of Health. To exclude the possibility of false recent infection results, the following were excluded: individuals who had previously used antiretroviral therapy (ART), those who reported mother-to-child transmission, and those with previous HIV-1 diagnosis detected more than six months from the date of collection of the research sample. These aspects were evaluated by observing the registration of individuals in HIV/AIDS healthcare programs or at medical records of the Central Public Health Laboratory of Pernambuco. Demographic characteristics data were retrieved from medical records at the VCT-Paulista.

A BED-capture enzyme immunoassay (BED-CEIA) was used for HIV-1 incidence (Calypte Biomedical Corporation, Portland, USA) 5Parekh BS, Kennedy MS, Dobbs T, Pau, C, Byers R, Green T, et al. Quantitative detection of increasing HIV type 1 antibodies after seroconversion: a simple assay for detection recent HIV infection and estimating incidence. AIDS Res Hum Retroviruses 2002; 18:295-307.. Incidence calculations and 95% confidence intervals were performed with the spreadsheet provided by the South African Centre for Epidemiological Modeling and Analysis (SACEMA; http://www.incidence-estimation.com/page/tools-for-incidence-from-biomarkers-for-recent-infection) 6Kassanjee R, McWalter TA, Bärnighausen T, Welte A. A new general biomarker-based incidence estimator. Epidemiology 2012; 23:721-8.. The incidence rate was estimated as 100 people per year and presented as a percentage. In addition, samples were tested for another recent HIV infection assay, the Avidity Index AxSYM method (Ax-AI), performed as described previously 7Suligoi B, Galli C, Massi M, Di Sora F, Sciandra M, Pezzotti P, et al. Precision and accuracy of a procedure for detecting recent human immunodeficiency virus infections by calculating the antibody avidity index by an automated immunoassay-based method. J Clin Microbiol 2002; 40:4015-20.. All samples were stored at minus 70ºC. We examined associations between groups using the Pearson’s chi-square test and kappa test to evaluate the degree of agreement between diagnostic assays. The study was approved by the Ethics Research Committee of Agamenon Magalhães Hospital, under registry number 429/2009, in accordance with Brazilian norms for research involving human subjects.

A total of 14,014 individuals were tested serologically for HIV-1, most of whom were women (n = 9,912; 70.8%), and pregnant women comprised a total of 5,494 persons. In this study, 167 were diagnosed with HIV-1, among whom sociodemographic and behavioral characteristics were obtained for 159 of them (Table 1). Most HIV-positive individuals were male (54.1%) and heterosexual (78.6%).

Table 1
Epidemiological characteristics of individuals diagnosed with HIV infection in one Voluntary and Counseling Testing Center. Metropolitan Region of Recife, Pernambuco State, Northeast Brazil.

We observed a prevalence of 1.18% (95%CI: 1.01-1.37) and incidence of 0.50% per year (95%CI: 0.27-0.73) (Table 2). The prevalence for HIV-1 infection in pregnant women (0.33%; 95%CI: 0.19-0.52) was significantly lower than that observed in men (2.25%; 95%CI: 1.82-2.75) and non-pregnant women (1.29%; 95%CI: 0.98-1.67; p < 0.000001). Although the rate of recent infection was around 20% in all study groups, pregnant women had lower incidence rates (0.15% per year; 95%CI: 0.00-0.33) than non-pregnant women (0.50% per year; 95%CI: 0.11-0.89; p = 0.0015) and men (1.03% per year; 95% CI: 0.45-1.61, p < 0.000001). There are few HIV incidence estimates by serological methods in Brazil; however, it has been demonstrated that in the South and Southeast of the country there are usually higher rates, such as 2.86% (95%CI: 1.04-4.68) in the South 8Ferreira JLP, Thomaz M, Rodrigues R, Harrad D, Oliveira CM, Oliveira CAF, et al. Molecular characterisation of newly identified HIV-1 infections in Curitiba, Brazil: prepoderance of clade C among males with recente infections. Mem Inst Oswaldo Cruz 2008; 103:800-8. and between 1.2-2.7% for men and 0.6-1.2% for women in the Southeast 9Alves KA, Shafer KP, Caseiro M, Rutherford G, Falcao ME, Sucupira MC, et al. Risk factors for incident HIV infection among anonymous HIV testing site clients in Santos, Brazil: 1996-1999. J Acquir Immune Defic Syndr 2003; 32:551-9.,1010 Merçon M, Tuboi SH, Batista SM, Telles SRB, Grangeiro JR, Zaddenverg R, et al. Risk-based assessment does not distinguish between recent and chronic HIV-1 infection in Rio de Janeiro, Brasil. Braz J Infect Dis 2009; 13:272-5.. We should emphasize that we did not have enough data to determine HIV-1 incidence and prevalence among men who have sex with men (MSM), and as demonstrated by Merçon et al. 1010 Merçon M, Tuboi SH, Batista SM, Telles SRB, Grangeiro JR, Zaddenverg R, et al. Risk-based assessment does not distinguish between recent and chronic HIV-1 infection in Rio de Janeiro, Brasil. Braz J Infect Dis 2009; 13:272-5., in Rio de Janeiro, the incidence in this group was five times higher than in heterosexual men, supposing that the presence of MSM may have inflated HIV-1 incidence and prevalence estimates among males.

Table 2
Prevalence, recent infections and HIV-1 incidence estimated at Voluntary and Counseling Testing Center. Metropolitan Region of Recife, Pernambuco State, Northeast Brazil.

We tested samples with Ax-AI assay for comparison with BED-CEIA. A higher correlation between the tests was observed in the group of pregnant women (kappa = 0.82), in which only 01/18 samples showed different results. The group of non-pregnant women showed a greater divergence between tests (kappa = 0.43), while for males a kappa of 0.69 was obtained.

One advantage of this work is data from two different methodologies for detection of recent HIV infection, the BED-CEIA and Ax-AI. These assays differ in the kinds of antigens and techniques, which increase the specificity for detecting recent infections. We demonstrate an excellent correlation between the results of the BED-CEIA and Ax-AI among pregnant women, therefore the changes in response to anti-HIV antibodies occurring during pregnancy are not sufficient to interfere with the results of these assays 1111 Laeyendecker O, Church JD, Oliver AE, Mwatha A, Owen SM, Donnell D, et al. Pregnancy does not affect HIV incidence test results obtained using the BED capture enzyme immunoassay or an antibody avidity assay. PLoS One 2010; 5:e13259.. Although serological assays have reasonable sensitivity to detect recent HIV infections, one disadvantage of the study is the absence of other laboratory markers for more accurate incidence estimates, such as the CD4+ T lymphocyte count, HIV-RNA detection and quantification of viral load, as well as data on the time interval between the last negative and the first positive HIV serological assay at multi-tested patients.

This is the first study reporting the HIV-1 incidence among pregnant women using a serological strategy in Northeast Brazil. We found an incidence rate of 0.15% per year in pregnant women, very similar to that determined in São Paulo (0.2% per year) 1212 Oliveira CAF, Ueda M, Yamashiro R, Rodrigues R, Sheppard HW, Brígido LFM. Rate and incidence estimates of recent human immunodeficiency virus type 1 infections among pregnant women In São Paulo, Brazil, from 1991 to 2002. J Clin Microbiol 2005; 43:1439-42.. Higher incidence estimates were observed in Rio de Janeiro (0.41%; 95%CI: 0.11-0.72) and Rio Grande do Sul (1.93%; 95%CI: 0.88-2.97) 1Morgado MG, Bastos FI. Estimates of HIV-1 incidence based on serological methods: a brief methodological review. Cad Saúde Pública 2011; 27 Suppl 1:S7-18.. A HIV-1 incidence estimate of 0.61 per 1,000 persons-years was found in Central Brazil, smaller than our estimates 1313 Costa ZB, Stefani MMA, Lima YAR, Souza WV, Filha NTS, Turchi MD, et al. Estimates incidence and genotypes of HIV-1 among pregnant women in Central Brazil. PLoS One 2013; 8:e79189..

HIV-1 prevalence was significantly higher among males. Although the HIV epidemic is concentrated in MSM in the Recife metropolitan area 1414 Cavalcanti AMS, Brito AM, Salustiano DM, Lima KO, Silva SP, Lacerda HR. Recent HIV infection rates among HIV positive patients seeking voluntary counseling and testing centers in the metropolitan region of Recife – PE, Brazil. Braz J Infect Dis 2012; 16:157-63., there is an increase in the rate of HIV infection in pregnant women since 2000 2Programa Nacional de DST-AIDS, Ministério da Saúde. Boletim Epidemiológico de AIDS e DST 2013; ano VII, nº 1.. An appropriate preventive or health intervention must be implemented to prevent the spread of the virus among pregnant women and their partners.

Paulista is part of the metropolitan region of Recife. Its proximity (17km) to the state capital, Recife, means there are significant population flows between the two cities. Data from incidence by serologic methods have been recommended for epidemiological studies because they provide real observations about the current epidemic. Our data demonstrate the large difference between the HIV-1 prevalence and incidence rates in different populations and the importance of serological testing for HIV during antenatal care, where we see a high rate of recent infection, so we assume that a significant proportion of pregnant women were infected at a time close to or during pregnancy.

Acknowledgements

We thank all the staff of VCT-Paulista.

References

  • 1
    Morgado MG, Bastos FI. Estimates of HIV-1 incidence based on serological methods: a brief methodological review. Cad Saúde Pública 2011; 27 Suppl 1:S7-18.
  • 2
    Programa Nacional de DST-AIDS, Ministério da Saúde. Boletim Epidemiológico de AIDS e DST 2013; ano VII, nº 1.
  • 3
    Rodrigues R, Manenti S, Romao PR, de Paula Ferreira JL, Batista JP, Siqueira AF, et al. Young pregnant women living with HIV/AIDS in Criciuma, Southern Brazil, are infected almost exclusively with HIV type 1 clade C. AIDS Res Hum Retroviruses 2010; 26:352-7.
  • 4
    UNAIDS Working Group on Global HIV/AIDS and STI Survaillance. When and how to use asssays for recent infection to estimate HIV incidence at a population level. Geneva: World Health Organization; 2011.
  • 5
    Parekh BS, Kennedy MS, Dobbs T, Pau, C, Byers R, Green T, et al. Quantitative detection of increasing HIV type 1 antibodies after seroconversion: a simple assay for detection recent HIV infection and estimating incidence. AIDS Res Hum Retroviruses 2002; 18:295-307.
  • 6
    Kassanjee R, McWalter TA, Bärnighausen T, Welte A. A new general biomarker-based incidence estimator. Epidemiology 2012; 23:721-8.
  • 7
    Suligoi B, Galli C, Massi M, Di Sora F, Sciandra M, Pezzotti P, et al. Precision and accuracy of a procedure for detecting recent human immunodeficiency virus infections by calculating the antibody avidity index by an automated immunoassay-based method. J Clin Microbiol 2002; 40:4015-20.
  • 8
    Ferreira JLP, Thomaz M, Rodrigues R, Harrad D, Oliveira CM, Oliveira CAF, et al. Molecular characterisation of newly identified HIV-1 infections in Curitiba, Brazil: prepoderance of clade C among males with recente infections. Mem Inst Oswaldo Cruz 2008; 103:800-8.
  • 9
    Alves KA, Shafer KP, Caseiro M, Rutherford G, Falcao ME, Sucupira MC, et al. Risk factors for incident HIV infection among anonymous HIV testing site clients in Santos, Brazil: 1996-1999. J Acquir Immune Defic Syndr 2003; 32:551-9.
  • 10
    Merçon M, Tuboi SH, Batista SM, Telles SRB, Grangeiro JR, Zaddenverg R, et al. Risk-based assessment does not distinguish between recent and chronic HIV-1 infection in Rio de Janeiro, Brasil. Braz J Infect Dis 2009; 13:272-5.
  • 11
    Laeyendecker O, Church JD, Oliver AE, Mwatha A, Owen SM, Donnell D, et al. Pregnancy does not affect HIV incidence test results obtained using the BED capture enzyme immunoassay or an antibody avidity assay. PLoS One 2010; 5:e13259.
  • 12
    Oliveira CAF, Ueda M, Yamashiro R, Rodrigues R, Sheppard HW, Brígido LFM. Rate and incidence estimates of recent human immunodeficiency virus type 1 infections among pregnant women In São Paulo, Brazil, from 1991 to 2002. J Clin Microbiol 2005; 43:1439-42.
  • 13
    Costa ZB, Stefani MMA, Lima YAR, Souza WV, Filha NTS, Turchi MD, et al. Estimates incidence and genotypes of HIV-1 among pregnant women in Central Brazil. PLoS One 2013; 8:e79189.
  • 14
    Cavalcanti AMS, Brito AM, Salustiano DM, Lima KO, Silva SP, Lacerda HR. Recent HIV infection rates among HIV positive patients seeking voluntary counseling and testing centers in the metropolitan region of Recife – PE, Brazil. Braz J Infect Dis 2012; 16:157-63.

Publication Dates

  • Publication in this collection
    June 2015

History

  • Received
    31 Oct 2013
  • Reviewed
    24 Mar 2015
  • Accepted
    24 Apr 2015
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