World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control during Pregnancy in the African Region. AFR/MAL/04/01. Geneva, Switzerland: WHO.
Fleming AF, 1989. Tropical obstetrics and gynaecology. 1. Anemia in pregnancy in tropical Africa. Trans R Soc Trop Med Hyg 83: 441–448.
Bloland P, Slutsker L, Steketee RW, Wirima JJ, Heymann DL, Breman JG, 1996. Rates and risk factors for mortality during the first two years of life in rural Malawi. Am J Trop Med Hyg 55: 82–86.
Guyatt HL, Snow RW, 2004. Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa. Clin Microbiol Rev 17: 760–769.
McCormick MC, 1985. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med 312: 82–90.
Murphy SC, Breman JG, 2001. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57–67.
Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
Shulman CE, Marshall T, Dorman EK, Bulmer JN, Cutts F, Peshu N, Marsh K, 2001. Malaria in pregnancy: adverse effects on hemoglobin levels and birthweight in primigravidae and multigravidae. Trop Med Int Health 6: 770–778.
Steketee RW, Wirima JJ, Hightower AW, Slutsker L, Heymann DL, Breman JG, 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am J Trop Med Hyg 55: 33–41.
Cottrell G, Mary JY, Barro D, Cot M, 2007. The importance of the period of malarial infection during pregnancy on birth weight in tropical Africa. Am J Trop Med Hyg 76: 849–854.
Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR, 2010. The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Trans R Soc Trop Med Hyg 104: 416–422.
Taha Tel T, Gray RH, Mohamedani AA, 1993. Malaria and low birth weight in central Sudan. Am J Epidemiol 138: 318–325.
Kelly-Hope LA, McKenzie FE, 2009. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J 8: 19.
Ballard JL, Khoury JC, Wedig K, Wang L, Eilers-Walsman BL, Lipp R, 1991. New Ballard Score, expanded to include extremely premature infants. J Pediatr 119: 417–423.
Greenland S, Pearl J, Robins JM, 1999. Causal diagrams for epidemiologic research. Epidemiology 10: 37–48.
Hernan MA, Hernandez-Diaz S, Werler MM, Mitchell AA, 2002. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 155: 176–184.
van Buuren S, Boshuizen HC, Knook DL, 1999. Multiple imputation of missing blood pressure covariates in survival analysis. Stat Med 18: 681–694.
Brabin BJ, Johnson PM, 2005. Placental malaria and pre-eclampsia through the looking glass backwards? J Reprod Immunol 65: 1–15.
Rogerson SJ, Boeuf P, 2007. New approaches to pathogenesis of malaria in pregnancy. Parasitology 134: 1883–1893.
Menendez C, Fleming AF, Alonso PL, 2000. Malaria-related anemia. Parasitol Today 16: 469–476.
World Health Organization, 2009. Pregnancy, Childbirth, Postpartum and Newborn Care: A guide for Essential Practice. Geneva, Switzerland: WHO.
Kayentao K, Kodio M, Newman RD, Maiga H, Doumtabe D, Ongoiba A, Coulibaly D, Keita AS, Maiga B, Mungai M, Parise ME, Doumbo O, 2005. Comparison of intermittent preventive treatment with chemoprophylaxis for the prevention of malaria during pregnancy in Mali. J Infect Dis 191: 109–116.
Njagi JK, Magnussen P, Estambale B, Ouma J, Mugo B, 2003. Prevention of anemia in pregnancy using insecticide-treated bed nets and sulfadoxine-pyrimethamine in a highly malarious area of Kenya: a randomized controlled trial. Trans R Soc Trop Med Hyg 97: 277–282.
Schultz LJ, Steketee RW, Chitsulo L, Wirima JJ, 1995. Antimalarials during pregnancy: a cost-effectiveness analysis. Bull World Health Organ 73: 207–214.
Shulman CE, Dorman EK, Cutts F, Kawuondo K, Bulmer JN, Peshu N, Marsh K, 1999. Intermittent sulphadoxine-pyrimethamine to prevent severe anemia secondary to malaria in pregnancy: a randomised placebo-controlled trial. Lancet 353: 632–636.
Sirima SB, Cotte AH, Konate A, Moran AC, Asamoa K, Bougouma EC, Diarra A, Ouedraogo A, Parise ME, Newman RD, 2006. Malaria prevention during pregnancy: assessing the disease burden one year after implementing a program of intermittent preventive treatment in Koupela District, Burkina Faso. Am J Trop Med Hyg 75: 205–211.
van Eijk AM, Ayisi JG, ter Kuile FO, Otieno JA, Misore AO, Odondi JO, Rosen DH, Kager PA, Steketee RW, Nahlen BL, 2004. Effectiveness of intermittent preventive treatment with sulphadoxine-pyrimethamine for control of malaria in pregnancy in western Kenya: a hospital-based study. Trop Med Int Health 9: 351–360.
Tuikue Ndam N, Deloron P, 2008. Towards a vaccine against pregnancy-associated malaria. Parasite 15: 515–521.
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Although consequences of malaria in pregnancy are well known, the period of pregnancy in which infection has the highest impact is still unclear. In Benin, we followed up a cohort of 1,037 women through pregnancy until delivery. The objective was to evaluate the relationship between the timing of infection and birth weight, and maternal anemia at delivery. At the beginning of pregnancy, peripheral infections were associated with a decrease in mean birth weight (−98.5 g; P = 0.03) and an increase in the risk of anemia at delivery (adjusted odds ratio [aOR] = 1.6; P = 0.03). Infections in late pregnancy were related to a higher risk of maternal anemia at delivery (aOR = 1.7; P = 0.001). To fully protect the women during the whole pregnancy, already implemented measures (insecticide-treated nets and intermittent preventive treatment) should be reinforced. In the future, a vaccine against pregnancy-associated malaria parasites could protect the women in early pregnancy, which seems to be a high-risk period.
Financial support: For their financial support, we thank Exxon Mobil and the GSK foundation (BTH funding).
Disclosure: This paper describes work undertaken in the context of the STOPPAM project, “Strategies To Prevent Pregnancy-Associated Malaria” (www.stoppam.org). STOPPAM is a Small and Medium Scale Collaborative Project supported by the European 7th Framework Programme, contract no.: 200889.
Authors' addresses: Bich-Tram Huynh, Nadine Fievet, Nicaise Tuikue Ndam, Philippe Deloron, and Michel Cot, Institut de Recherche pour le Développement (IRD), Mère et Enfant Face aux Infections Tropicales, Paris, France, and Faculté de Pharmacie, Université Paris Descartes, Paris, France, E-mails: bichtrambe@hotmail.com, fievet@ird.fr, nicaise.ndam@ird.fr, philippe.deloron@ird.fr, and michel.cot@ird.fr. Gildas Gbaguidi, Sébastien Dechavanne, and Sophie Borgella, Institut de Recherche pour le Développement (IRD), UMR216, Mère et Enfant Face aux Infections Tropicales, Paris, France, E-mails: gildas.gbaguidi@ird.fr, sebdechavanne@yahoo.fr, and sophie.borgella@ird.fr. Blaise Guézo Mévo, Hôpital de Comé, Comé, Bénin, E-mail: guemebla@yahoo.fr. Achille Massougbodji, Faculté des Sciences de la Santé (FSS), UER de Parasitologie, Université de Cotonou, Cotonou, Bénin, E-mail: massougbodjiachille@yahoo.fr.
World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control during Pregnancy in the African Region. AFR/MAL/04/01. Geneva, Switzerland: WHO.
Fleming AF, 1989. Tropical obstetrics and gynaecology. 1. Anemia in pregnancy in tropical Africa. Trans R Soc Trop Med Hyg 83: 441–448.
Bloland P, Slutsker L, Steketee RW, Wirima JJ, Heymann DL, Breman JG, 1996. Rates and risk factors for mortality during the first two years of life in rural Malawi. Am J Trop Med Hyg 55: 82–86.
Guyatt HL, Snow RW, 2004. Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa. Clin Microbiol Rev 17: 760–769.
McCormick MC, 1985. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med 312: 82–90.
Murphy SC, Breman JG, 2001. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57–67.
Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
Shulman CE, Marshall T, Dorman EK, Bulmer JN, Cutts F, Peshu N, Marsh K, 2001. Malaria in pregnancy: adverse effects on hemoglobin levels and birthweight in primigravidae and multigravidae. Trop Med Int Health 6: 770–778.
Steketee RW, Wirima JJ, Hightower AW, Slutsker L, Heymann DL, Breman JG, 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am J Trop Med Hyg 55: 33–41.
Cottrell G, Mary JY, Barro D, Cot M, 2007. The importance of the period of malarial infection during pregnancy on birth weight in tropical Africa. Am J Trop Med Hyg 76: 849–854.
Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR, 2010. The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Trans R Soc Trop Med Hyg 104: 416–422.
Taha Tel T, Gray RH, Mohamedani AA, 1993. Malaria and low birth weight in central Sudan. Am J Epidemiol 138: 318–325.
Kelly-Hope LA, McKenzie FE, 2009. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J 8: 19.
Ballard JL, Khoury JC, Wedig K, Wang L, Eilers-Walsman BL, Lipp R, 1991. New Ballard Score, expanded to include extremely premature infants. J Pediatr 119: 417–423.
Greenland S, Pearl J, Robins JM, 1999. Causal diagrams for epidemiologic research. Epidemiology 10: 37–48.
Hernan MA, Hernandez-Diaz S, Werler MM, Mitchell AA, 2002. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 155: 176–184.
van Buuren S, Boshuizen HC, Knook DL, 1999. Multiple imputation of missing blood pressure covariates in survival analysis. Stat Med 18: 681–694.
Brabin BJ, Johnson PM, 2005. Placental malaria and pre-eclampsia through the looking glass backwards? J Reprod Immunol 65: 1–15.
Rogerson SJ, Boeuf P, 2007. New approaches to pathogenesis of malaria in pregnancy. Parasitology 134: 1883–1893.
Menendez C, Fleming AF, Alonso PL, 2000. Malaria-related anemia. Parasitol Today 16: 469–476.
World Health Organization, 2009. Pregnancy, Childbirth, Postpartum and Newborn Care: A guide for Essential Practice. Geneva, Switzerland: WHO.
Kayentao K, Kodio M, Newman RD, Maiga H, Doumtabe D, Ongoiba A, Coulibaly D, Keita AS, Maiga B, Mungai M, Parise ME, Doumbo O, 2005. Comparison of intermittent preventive treatment with chemoprophylaxis for the prevention of malaria during pregnancy in Mali. J Infect Dis 191: 109–116.
Njagi JK, Magnussen P, Estambale B, Ouma J, Mugo B, 2003. Prevention of anemia in pregnancy using insecticide-treated bed nets and sulfadoxine-pyrimethamine in a highly malarious area of Kenya: a randomized controlled trial. Trans R Soc Trop Med Hyg 97: 277–282.
Schultz LJ, Steketee RW, Chitsulo L, Wirima JJ, 1995. Antimalarials during pregnancy: a cost-effectiveness analysis. Bull World Health Organ 73: 207–214.
Shulman CE, Dorman EK, Cutts F, Kawuondo K, Bulmer JN, Peshu N, Marsh K, 1999. Intermittent sulphadoxine-pyrimethamine to prevent severe anemia secondary to malaria in pregnancy: a randomised placebo-controlled trial. Lancet 353: 632–636.
Sirima SB, Cotte AH, Konate A, Moran AC, Asamoa K, Bougouma EC, Diarra A, Ouedraogo A, Parise ME, Newman RD, 2006. Malaria prevention during pregnancy: assessing the disease burden one year after implementing a program of intermittent preventive treatment in Koupela District, Burkina Faso. Am J Trop Med Hyg 75: 205–211.
van Eijk AM, Ayisi JG, ter Kuile FO, Otieno JA, Misore AO, Odondi JO, Rosen DH, Kager PA, Steketee RW, Nahlen BL, 2004. Effectiveness of intermittent preventive treatment with sulphadoxine-pyrimethamine for control of malaria in pregnancy in western Kenya: a hospital-based study. Trop Med Int Health 9: 351–360.
Tuikue Ndam N, Deloron P, 2008. Towards a vaccine against pregnancy-associated malaria. Parasite 15: 515–521.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
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