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The Hidden Burden of Plasmodium vivax Malaria in Pregnancy in the Amazon: An Observational Study in Northwestern Brazil

Anaclara PincelliDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil;

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Paulo A. R. NevesDepartment of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;

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Barbara H. LourençoDepartment of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;
Department of Preventive Medicine, Escola Paulista de Medicina, Federal University of São Paulo, São Paulo, Brazil;

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Rodrigo M. CorderDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil;

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Maíra B. MaltaDepartment of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;

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Juliana Sampaio-SilvaDepartment of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;

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Rodrigo M. de SouzaMultidisciplinary Center, Federal University of Acre, Cruzeiro do Sul, Brazil;

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Marly A. CardosoDepartment of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;

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Marcia C. CastroDepartment of Global Health and Population, Harvard T. H. Chan School of Public Health, Boston, Massachusetts

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Marcelo U. FerreiraDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil;

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for the MINA Brazil Working GroupDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil;
Department of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil;
Department of Preventive Medicine, Escola Paulista de Medicina, Federal University of São Paulo, São Paulo, Brazil;
Multidisciplinary Center, Federal University of Acre, Cruzeiro do Sul, Brazil;
Department of Global Health and Population, Harvard T. H. Chan School of Public Health, Boston, Massachusetts

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We measured the prevalence of malaria in pregnancy and estimated its impact on birth weight and length and maternal hemoglobin in 1,180 women from Juruá Valley, the main malaria hotspot in Brazil. Antenatal malaria episodes, 74.6% of them due to Plasmodium vivax, were microscopically diagnosed in 8.0% of the women and were associated with an average reduction in birth weight z-scores of 0.35 (95% confidence interval [CI] = 0.14–0.57) and in birth length z-scores of 0.31 (95% CI = 0.08–0.54), compared with malaria-free pregnancies. Affected mothers had a mean decrease in hemoglobin concentration at delivery of 0.33 g/100 mL (95% CI = 0.05–0.62 g/100 mL); 51.6% were anemic. The timing and frequency of antenatal infections influenced pregnancy outcomes and first- or second-trimester infections were not associated with decreased birth weight and length and maternal hemoglobin at delivery. Although repeated antenatal vivax infections were associated with poorer birth outcomes, even a single vivax malaria episode was associated with a significant reduction in birth weight and length and maternal hemoglobin. Overall, 7.5% women had the parasite’s DNA found in peripheral blood at delivery. Most (83.1%) of these 89 perinatal infections were due to P. vivax and only 7.9% of them progressed to symptomatic disease after delivery. Plasmodium vivax and Plasmodium falciparum DNA was found in 0.6% and 0.3% of 637 cord blood samples examined, respectively, but only one newborn developed clinical neonatal malaria. Our results further challenge the notion that vivax malaria is relatively benign during pregnancy and call for better strategies for its prevention.

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Author Notes

Address correspondence to Marcelo U. Ferreira, Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, Av. Prof. Lineu Prestes 1374, Cidade Universitária, 05508-900 São Paulo, Brazil. E-mail: muferrei@usp.br

Financial support: This study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil (FAPESP; grant 2016/00270-6 to MAC), the David Rockefeller Center for Latin American Studies (DRCLAS), Harvard University, Cambridge, MA, and the Fundação Maria Cecília Couto Vidigal, Brazil (to M. C. C.), the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil (CNPq; 407255/2013-3 to M. A. C.), and the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), USA (International Centers of Excellence in Malaria Research [ICEMR] program, grant U19 AI089681 to Joseph M. Vinetz). A. P., M. B. M., J. S-S., and M. C. C. receive or received scholarships from FAPESP. P. A. R. N., R. M. C., M. A. C., M. C. C., and M. U. F. receive or received scholarships from CNPq.

Authors’ addresses: Anaclara Pincelli, Rodrigo M. Corder, and Marcelo U. Ferreira, Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil, E-mails: anaclarapincelli@usp.br, rodrigo.corder@usp.br, and muferrei@usp.br. Paulo A. R. Neves, Maíra B. Malta, Juliana Sampaio-Silva, and Marly A. Cardoso, Department of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil, E-mails: paugustorn@gmail.com, mairamaltanutri@gmail.com, jukisbio@gmail.com, and marlyac@usp.br. Barbara H. Lourenço, Department of Nutrition, School of Public Health, University of São Paulo, São Paulo, Brazil, and Department of Preventive Medicine, Escola Paulista de Medicina, Federal University of São Paulo, São Paulo, Brazil, E-mail: barbara.lourenco@unifesp.br. Rodrigo M. de Souza, Multidisciplinary Center, Federal University of Acre, Campus da Floresta, Cruzeiro do Sul, Brazil, E-mail: rodrigo.souza@ufac.br. Marcia C. Castro, Department of Global Health and Population, Harvard T.H. Chan School of Public Health, Boston, MA, E-mail: mcastro@hsph.harvard.edu.

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