Authors:
, , , , , , , , , , , , , , , , , and
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
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-
1.
McCoy DC, Peet ED, Ezzati M, Danaei G, Black MM, Sudfeld CR, Fawzi W, Fink G, 2016. Early childhood developmental status in low- and middle-income countries: National, regional, and global prevalence estimates using predictive modeling. PLoS Med 13: e1002034.
-
2.
Walker SP, Chang SM, Powell CA, Grantham-McGregor SM, 2005. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: Prospective cohort study. Lancet 366: 1804–1807.
-
3.
Mburu W, Conroy AL, Cusick SE, Bangirana P, Bond C, Zhao Y, Opoka RO, John CC, 2021. The impact of undernutrition on cognition in children with severe malaria and community children: A prospective 2-year cohort study. J Trop Pediatr 67: fmab091.
-
4.
Tau GZ, Peterson BS, 2010. Normal development of brain circuits. Neuropsychopharmacology 35: 147–168.
-
5.
Shonkoff JP, Garner AS, Siegel BS, Dobbins MI, Earls MF, Garner AS, McGuinn L, Pascoe J, Wood DL; The Committee on Psychosocial Aspects of Child and Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics, 2012. The lifelong effects of early childhood adversity and toxic stress. Pediatrics 129: e232–e246.
-
6.
Mireku MO, Boivin MJ, Davidson LL, Ouédraogo S, Koura GK, Alao MJ, Massougbodji A, Cot M, Bodeau-Livinec F, 2015. Impact of helminth infection during pregnancy on cognitive and motor functions of one-year-old children. PLoS Negl Trop Dis 9: e0003463.
-
7.
Chang S, Zeng L, Brouwer ID, Kok FJ, Yan H, 2013. Effect of iron deficiency anemia in pregnancy on child mental development in rural China. Pediatrics 131: e755–e763.
-
8.
Garrison A, Boivin MJ, Fiévet N, Zoumenou R, Alao JM, Massougbodji A, Cot M, Bodeau-Livinec F, 2021. The effects of malaria in pregnancy on neurocognitive development in children at one and six years of age in Benin: A prospective mother-child cohort. Clin Infect Dis 74: 766–775.
-
9.
Garrison A, Boivin M, Khoshnood B, Courtin D, Alao J, Mireku M, Ibikounle M, Massougbodji A, Cot M, Bodeau-Livinec F, 2021. Soil-transmitted helminth infection in pregnancy and long-term child neurocognitive and behavioral development: A prospective mother-child cohort in Benin. PLOS Negl Trop Dis 15: e0009260.
-
10.
Wiegersma AM, Dalman C, Lee BK, Karlsson H, Gardner RM, 2019. Association of prenatal maternal anemia with neurodevelopmental disorders. JAMA Psychiatry 76: 1294–1304.
-
11.
McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B, 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 12: 444–454.
-
12.
Churchill D, Nair M, Stanworth SJ, Knight M, 2019. The change in haemoglobin concentration between the first and third trimesters of pregnancy: A population study. BMC Pregnancy Childbirth 19: 359.
-
13.
Hutter D, Kingdom J, Jaeggi E, 2010. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: A review. Int J Pediatr 2010: e401323.
-
14.
Mireku MO, Davidson LL, Koura GK, Ouédraogo S, Boivin MJ, Xiong X, Accrombessi MMK, Massougbodji A, Cot M, Bodeau-Livinec F, 2015. Prenatal hemoglobin levels and early cognitive and motor functions of one-year-old children. Pediatrics 136: e76–e83.
-
15.
González R et al., 2014. Intermittent preventive treatment of malaria in pregnancy with mefloquine in HIV-negative women: A multicentre randomized controlled trial. PLoS Med 11: e1001733.
-
16.
Mireku MO, Davidson LL, Boivin MJ, Zoumenou R, Massougbodji A, Cot M, Bodeau-Livinec F, 2016. Prenatal iron deficiency, neonatal ferritin, and infant cognitive function. Pediatrics 138: e20161319.
-
17.
Bodeau-Livinec F, Davidson LL, Zoumenou R, Massougbodji A, Cot M, Boivin MJ, 2019. Neurocognitive testing in West African children 3–6 years of age: Challenges and implications for data analyses. Brain Res Bull 145: 129–135.
-
18.
World Health Organization, 2019. Bench Aids for the Diagnosis of Intestinal Parasites, Second Edition. Paris, France: WHO.
-
19.
Planche T, Krishna S, Kombila M, Engel K, Faucher JF, Ngou-Milama E, Kremsner PG, 2001. Comparison of methods for the rapid laboratory assessment of children with malaria. Am J Trop Med Hyg 65: 599–602.
-
20.
Ndam NT et al., 2017. Resisting and tolerating P. falciparum in pregnancy under different malaria transmission intensities. BMC Med 15: 130.
-
21.
Kaufman AS, Kaufman NL, 2014. Kaufman Assessment Battery for Children, Second Edition. Circle Pines, MN: American Guidance Service.
-
22.
Bruininks BD, Bruininks RH, 2005. Bruininks-Oseretsky Test of Motor Proficiency (BOT-2), Second Edition. Minneapolis, MN: Pearson Products, Inc.
-
23.
Mireku MO, Cot M, Massougbodji A, Bodeau-Livinec F, 2020. Relationship between stunting, wasting, underweight and geophagy and cognitive function of children. J Trop Pediatr 66: 517–527.
-
24.
Caldwell BM, Bradley RH, 2001. Home Inventory Administration Manual, Third Edition. Little Rock, AR: University of Arkansas for Medical Sciences.
-
25.
Cox JL, Holden JM, Sagovsky R, 1987. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. Br J Psychiatry 150: 782–786.
-
26.
Jones BL, Nagin DS, 2013. A note on a Stata plugin for estimating group-based trajectory models. Sociol Methods Res 42: 608–613.
-
27.
Sekhavat L, Davar R, Hosseinidezoki S, 2011. Relationship between maternal hemoglobin concentration and neonatal birth weight. Hematology 16: 373–376.
-
28.
Stephansson O, Dickman PW, Johansson A, Cnattingius S, 2000. Maternal hemoglobin concentration during pregnancy and risk of stillbirth. JAMA 284: 2611–2617.
-
29.
Liu D et al., 2022. Maternal hemoglobin concentrations and birth weight, low birth weight (LBW), and small for gestational age (SGA): Findings from a prospective study in Northwest China. Nutrients 14: 858.
-
30.
Randall DA, Patterson JA, Gallimore F, Morris JM, McGee TM, Ford JB; Obstetric Transfusion Steering Group, 2019. The association between haemoglobin levels in the first 20 weeks of pregnancy and pregnancy outcomes. PLoS One 14: e0225123.
-
31.
Young MF, Oaks BM, Rogers HP, Tandon S, Martorell R, Dewey KG, Wendt AS, 2023. Maternal low and high hemoglobin concentrations and associations with adverse maternal and infant health outcomes: An updated global systematic review and meta-analysis. BMC Pregnancy Childbirth 23: 264.
-
32.
Fararouei M, Robertson C, Whittaker J, Sovio U, Ruokonen A, Pouta A, Hartikainen A-L, Jarvelin M-R, Hyppönen E, 2010. Maternal Hb during pregnancy and offspring’s educational achievement: A prospective cohort study over 30 years. Br J Nutr 104: 1363–1368.
-
33.
Nampijja M, Mutua AM, Elliott AM, Muriuki JM, Abubakar A, Webb EL, Atkinson SH, 2022. Low hemoglobin levels are associated with reduced psychomotor and language abilities in young Ugandan children. Nutrients 14: 1452.
-
34.
Janbek J, Sarki M, Specht IO, Heitmann BL, 2019. A systematic literature review of the relation between iron status/anemia in pregnancy and offspring neurodevelopment. Eur J Clin Nutr 73: 1561–1578.
-
35.
Wedderburn CJ et al., 2022. Association of maternal and child anemia with brain structure in early life in South Africa. JAMA Netw Open 5: e2244772.
-
36.
Ouédraogo S, Koura GK, Accrombessi MMK, Bodeau-Livinec F, Massougbodji A, Cot M, 2012. Maternal anemia at first antenatal visit: Prevalence and risk factors in a malaria-endemic area in Benin. Am J Trop Med Hyg 87: 418–424.
-
37.
Ouédraogo S, Koura GK, Bodeau-Livinec F, Accrombessi MMK, Massougbodji A, Cot M, 2013. Maternal anemia in pregnancy: Assessing the effect of routine preventive measures in a malaria-endemic area. Am J Trop Med Hyg 88: 292–300.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 619 | 619 | 216 |
| Full Text Views | 16 | 16 | 10 |
| PDF Downloads | 17 | 17 | 11 |
Prenatal Hemoglobin Concentration and Long-Term Child Neurocognitive Development
Michael O. Mireku
Michael O. Mireku
College of Health and Science, University of Lincoln, Lincoln, United Kingdom;
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Michael J. Boivin
Michael J. Boivin
Department of Psychiatry, Michigan State University, East Lansing, Michigan;
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Roméo Zoumenou
Roméo Zoumenou
UMR 261-MERIT, Institut de Recherche pour le Développement (IRD), Université Paris Cité, Paris, France;
Institute of Psychology, Laboratoire de Psychopathologie et Processus de Santé, Boulogne, France;
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Institute of Psychology, Laboratoire de Psychopathologie et Processus de Santé, Boulogne, France;
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Amanda Garrison
Amanda Garrison
Université Rennes, EHESP, Inserm, IRSET (Institut de Recherche en Santé, Environnement et Travail)–UMR_S 1085, Rennes, France;
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Michel Cot
Michel Cot
UMR 261-MERIT, Institut de Recherche pour le Développement (IRD), Université Paris Cité, Paris, France;
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Jules Alao
Jules Alao
Service de Pédiatrie, CHU de la Mère et de l’Enfant-Lagune de Cotonou, Cotonou, Benin;
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Nadine Fievet
Nadine Fievet
UMR 261-MERIT, Institut de Recherche pour le Développement (IRD), Université Paris Cité, Paris, France;
Institut de Recherche Clinique du Bénin (IRCB), Abomey-Calavi, Benin
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Institut de Recherche Clinique du Bénin (IRCB), Abomey-Calavi, Benin
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Achille Massougbodji
Achille Massougbodji
Institut de Recherche Clinique du Bénin (IRCB), Abomey-Calavi, Benin
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Florence Bodeau-Livinec
florence.bodeau-livinec@ehesp.fr
Florence Bodeau-Livinec
UMR 261-MERIT, Institut de Recherche pour le Développement (IRD), Université Paris Cité, Paris, France;
Université Rennes, EHESP, Inserm, IRSET (Institut de Recherche en Santé, Environnement et Travail)–UMR_S 1085, Rennes, France;
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ABSTRACT.
Anemia in pregnancy, defined by a hemoglobin level (Hb) of less than 110 g/L, contributes to infant mortality and morbidity in sub-Saharan Africa. Maternal Hb changes physiologically and pathologically during pregnancy. However, the impact of these changes on long-term child neurocognitive function is unknown. This study therefore investigates the association between Hb at specific antenatal care visits and prenatal Hb trajectories during pregnancy and long-term child neurocognitive function. We analyzed data from a prospective cohort study that included 6-year-old singleton children born to women enrolled before 29 weeks of gestation into an antimalarial drug clinical trial. Hemoglobin level was analyzed from venous blood collected at least twice during pregnancy and at delivery. We used group-based trajectory modeling to identify distinct prenatal Hb trajectories. In total, 478 children (75.1% of eligible children) had assessment of cognitive and motor functions at 6 years of age. Three distinct Hb trajectories were identified: persistently anemic (Hb <110 g/L throughout the second and third trimesters), anemic to nonanemic (Hb <110 g/L at second trimester with increasing Hb toward the third trimester to Hb ≥110 g/L), and persistently nonanemic (Hb ≥110 g/L throughout the second and third trimesters). Children of women in the persistently anemic and anemic-to-nonanemic groups had significantly lower neurocognitive scores than children of women in the persistently nonanemic group (β = −6.8, 95% CI: −11.7 to −1.8; and β = −6.3, 95% CI: −10.4 to −2.2, respectively). The study shows that maintaining an elevation of Hb at or above 110 g/L from the second to third trimester of pregnancy may be associated with optimal long-term child neurocognitive function.
- Supplemental Materials (PDF 284.44 KB)
Author Notes
Financial support: This work was supported by the
Disclosures: All relevant data related to this study are within the manuscript and supporting supplemental documents. MiPPAD data cannot be shared publicly because of ethical restrictions. Access to MiPPAD study data may be available upon request through The MiPPAD Executive Committee (Raquel Gonzalez at +34-932-275-400 or raquel.gonzalez@cresib.cat).
We sought ethical approvals from the institutional ethical review boards of the Faculté des Sciences de la Santé and the Applied Biomedical Sciences Institute (CER-ISBA) in Benin, New York University in New York, New York, and the Research Institute for Development’s (IRD) Consultative Ethics Committee in France. We obtained informed consent from all mothers in accordance with the World Medical Association Declaration of Helsinki.
Authors’ contributions: M. O. Mireku, M. J. Boivin, M. Cot, and F. Bodeau-Livinec conceptualized the study. M. O. Mireku completed the literature review, performed the statistical analysis, and wrote the first draft of the manuscript. M. O. Mireku, R. Zoumenou, and A. Garrison performed data cleaning. All authors had full access to all the study findings, contributed to interpretation of the results and revision of the manuscript, and were responsible for the decision to submit the report for publication.
Current contact information: Michael O. Mireku, University of Lincoln, School of Psychology, Sarah Swift Building, Lincoln, United Kingdom, E-mail: Mmireku@lincoln.ac.uk. Michael J. Boivin, Department of Psychiatry, Michigan State University, East Lansing, Michigan, E-mails: boivin@msu.edu. Romeo Zoumenou, Laboratoire de Psychopathologie et Processus de Santé, Institute of Psychology, Boulogne, France, E-mail: zoumenour@yahoo.fr. Amanda Garrison, Université Rennes, EHESP, Rennes, France. E-mail: amanda.garrison@ehesp.fr. Michel Cot and Nadine Fievet, UMR 261 - MERIT, Institut de Recherche pour le Developpement (IRD), Universite Paris Cite, Paris, France, E-mails: michel.cot@ird.fr. and nadine.fievet@ird.fr. Jules Alao, Service de Pediatrie, CHU de la Mere et de l’Enfant-Lagune de Cotonou, Cotonou, Benin. E-mail: amomj@yahoo.fr. Achille Massougbodji, Institut de Recherche Clinique du Bénin, Abomey-Calavi, Benin, E-mail: massougbodjiachille@yahoo.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
McCoy DC, Peet ED, Ezzati M, Danaei G, Black MM, Sudfeld CR, Fawzi W, Fink G, 2016. Early childhood developmental status in low- and middle-income countries: National, regional, and global prevalence estimates using predictive modeling. PLoS Med 13: e1002034.
-
2.
Walker SP, Chang SM, Powell CA, Grantham-McGregor SM, 2005. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: Prospective cohort study. Lancet 366: 1804–1807.
-
3.
Mburu W, Conroy AL, Cusick SE, Bangirana P, Bond C, Zhao Y, Opoka RO, John CC, 2021. The impact of undernutrition on cognition in children with severe malaria and community children: A prospective 2-year cohort study. J Trop Pediatr 67: fmab091.
-
4.
Tau GZ, Peterson BS, 2010. Normal development of brain circuits. Neuropsychopharmacology 35: 147–168.
-
5.
Shonkoff JP, Garner AS, Siegel BS, Dobbins MI, Earls MF, Garner AS, McGuinn L, Pascoe J, Wood DL; The Committee on Psychosocial Aspects of Child and Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics, 2012. The lifelong effects of early childhood adversity and toxic stress. Pediatrics 129: e232–e246.
-
6.
Mireku MO, Boivin MJ, Davidson LL, Ouédraogo S, Koura GK, Alao MJ, Massougbodji A, Cot M, Bodeau-Livinec F, 2015. Impact of helminth infection during pregnancy on cognitive and motor functions of one-year-old children. PLoS Negl Trop Dis 9: e0003463.
-
7.
Chang S, Zeng L, Brouwer ID, Kok FJ, Yan H, 2013. Effect of iron deficiency anemia in pregnancy on child mental development in rural China. Pediatrics 131: e755–e763.
-
8.
Garrison A, Boivin MJ, Fiévet N, Zoumenou R, Alao JM, Massougbodji A, Cot M, Bodeau-Livinec F, 2021. The effects of malaria in pregnancy on neurocognitive development in children at one and six years of age in Benin: A prospective mother-child cohort. Clin Infect Dis 74: 766–775.
-
9.
Garrison A, Boivin M, Khoshnood B, Courtin D, Alao J, Mireku M, Ibikounle M, Massougbodji A, Cot M, Bodeau-Livinec F, 2021. Soil-transmitted helminth infection in pregnancy and long-term child neurocognitive and behavioral development: A prospective mother-child cohort in Benin. PLOS Negl Trop Dis 15: e0009260.
-
10.
Wiegersma AM, Dalman C, Lee BK, Karlsson H, Gardner RM, 2019. Association of prenatal maternal anemia with neurodevelopmental disorders. JAMA Psychiatry 76: 1294–1304.
-
11.
McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B, 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 12: 444–454.
-
12.
Churchill D, Nair M, Stanworth SJ, Knight M, 2019. The change in haemoglobin concentration between the first and third trimesters of pregnancy: A population study. BMC Pregnancy Childbirth 19: 359.
-
13.
Hutter D, Kingdom J, Jaeggi E, 2010. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: A review. Int J Pediatr 2010: e401323.
-
14.
Mireku MO, Davidson LL, Koura GK, Ouédraogo S, Boivin MJ, Xiong X, Accrombessi MMK, Massougbodji A, Cot M, Bodeau-Livinec F, 2015. Prenatal hemoglobin levels and early cognitive and motor functions of one-year-old children. Pediatrics 136: e76–e83.
-
15.
González R et al., 2014. Intermittent preventive treatment of malaria in pregnancy with mefloquine in HIV-negative women: A multicentre randomized controlled trial. PLoS Med 11: e1001733.
-
16.
Mireku MO, Davidson LL, Boivin MJ, Zoumenou R, Massougbodji A, Cot M, Bodeau-Livinec F, 2016. Prenatal iron deficiency, neonatal ferritin, and infant cognitive function. Pediatrics 138: e20161319.
-
17.
Bodeau-Livinec F, Davidson LL, Zoumenou R, Massougbodji A, Cot M, Boivin MJ, 2019. Neurocognitive testing in West African children 3–6 years of age: Challenges and implications for data analyses. Brain Res Bull 145: 129–135.
-
18.
World Health Organization, 2019. Bench Aids for the Diagnosis of Intestinal Parasites, Second Edition. Paris, France: WHO.
-
19.
Planche T, Krishna S, Kombila M, Engel K, Faucher JF, Ngou-Milama E, Kremsner PG, 2001. Comparison of methods for the rapid laboratory assessment of children with malaria. Am J Trop Med Hyg 65: 599–602.
-
20.
Ndam NT et al., 2017. Resisting and tolerating P. falciparum in pregnancy under different malaria transmission intensities. BMC Med 15: 130.
-
21.
Kaufman AS, Kaufman NL, 2014. Kaufman Assessment Battery for Children, Second Edition. Circle Pines, MN: American Guidance Service.
-
22.
Bruininks BD, Bruininks RH, 2005. Bruininks-Oseretsky Test of Motor Proficiency (BOT-2), Second Edition. Minneapolis, MN: Pearson Products, Inc.
-
23.
Mireku MO, Cot M, Massougbodji A, Bodeau-Livinec F, 2020. Relationship between stunting, wasting, underweight and geophagy and cognitive function of children. J Trop Pediatr 66: 517–527.
-
24.
Caldwell BM, Bradley RH, 2001. Home Inventory Administration Manual, Third Edition. Little Rock, AR: University of Arkansas for Medical Sciences.
-
25.
Cox JL, Holden JM, Sagovsky R, 1987. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. Br J Psychiatry 150: 782–786.
-
26.
Jones BL, Nagin DS, 2013. A note on a Stata plugin for estimating group-based trajectory models. Sociol Methods Res 42: 608–613.
-
27.
Sekhavat L, Davar R, Hosseinidezoki S, 2011. Relationship between maternal hemoglobin concentration and neonatal birth weight. Hematology 16: 373–376.
-
28.
Stephansson O, Dickman PW, Johansson A, Cnattingius S, 2000. Maternal hemoglobin concentration during pregnancy and risk of stillbirth. JAMA 284: 2611–2617.
-
29.
Liu D et al., 2022. Maternal hemoglobin concentrations and birth weight, low birth weight (LBW), and small for gestational age (SGA): Findings from a prospective study in Northwest China. Nutrients 14: 858.
-
30.
Randall DA, Patterson JA, Gallimore F, Morris JM, McGee TM, Ford JB; Obstetric Transfusion Steering Group, 2019. The association between haemoglobin levels in the first 20 weeks of pregnancy and pregnancy outcomes. PLoS One 14: e0225123.
-
31.
Young MF, Oaks BM, Rogers HP, Tandon S, Martorell R, Dewey KG, Wendt AS, 2023. Maternal low and high hemoglobin concentrations and associations with adverse maternal and infant health outcomes: An updated global systematic review and meta-analysis. BMC Pregnancy Childbirth 23: 264.
-
32.
Fararouei M, Robertson C, Whittaker J, Sovio U, Ruokonen A, Pouta A, Hartikainen A-L, Jarvelin M-R, Hyppönen E, 2010. Maternal Hb during pregnancy and offspring’s educational achievement: A prospective cohort study over 30 years. Br J Nutr 104: 1363–1368.
-
33.
Nampijja M, Mutua AM, Elliott AM, Muriuki JM, Abubakar A, Webb EL, Atkinson SH, 2022. Low hemoglobin levels are associated with reduced psychomotor and language abilities in young Ugandan children. Nutrients 14: 1452.
-
34.
Janbek J, Sarki M, Specht IO, Heitmann BL, 2019. A systematic literature review of the relation between iron status/anemia in pregnancy and offspring neurodevelopment. Eur J Clin Nutr 73: 1561–1578.
-
35.
Wedderburn CJ et al., 2022. Association of maternal and child anemia with brain structure in early life in South Africa. JAMA Netw Open 5: e2244772.
-
36.
Ouédraogo S, Koura GK, Accrombessi MMK, Bodeau-Livinec F, Massougbodji A, Cot M, 2012. Maternal anemia at first antenatal visit: Prevalence and risk factors in a malaria-endemic area in Benin. Am J Trop Med Hyg 87: 418–424.
-
37.
Ouédraogo S, Koura GK, Bodeau-Livinec F, Accrombessi MMK, Massougbodji A, Cot M, 2013. Maternal anemia in pregnancy: Assessing the effect of routine preventive measures in a malaria-endemic area. Am J Trop Med Hyg 88: 292–300.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 619 | 619 | 216 |
| Full Text Views | 16 | 16 | 10 |
| PDF Downloads | 17 | 17 | 11 |