Prenatal iron supplementation adjusted to maternal iron stores reduces behavioural problems in 4-year-old children.

behavioural problems child behaviour executive functioning iron supplementation pregnancy

Journal

Maternal & child nutrition
ISSN: 1740-8709
Titre abrégé: Matern Child Nutr
Pays: England
ID NLM: 101201025

Informations de publication

Date de publication:
02 Dec 2023
Historique:
revised: 07 11 2023
received: 14 07 2023
accepted: 08 11 2023
medline: 2 12 2023
pubmed: 2 12 2023
entrez: 2 12 2023
Statut: aheadofprint

Résumé

Prenatal iron supplementation improves children's health and cognitive performance, but few studies explore behavioural development. This study assessed the effects of adjusting prenatal iron supplementation to maternal iron stores during early pregnancy on children's behavioural problems. Randomized controlled trial conducted in Tarragona (Spain) involving 230 nonanaemic pregnant women and their children after a 4-year follow-up. Based on haemoglobin (Hb) levels before gestational week (GW) 12, women receive different iron doses: those with Hb = 110-130 g/L were randomized to receive 80 or 40 mg/day and those with Hb > 130 g/L were randomized to receive 20 or 40 mg/day. Maternal iron stores at GW12 were classified using serum ferritin (SF) as low (SF < 15 µg/L), normal (SF = 15-65 µg/L), and normal-high (SF > 65 µg/L). Children's behaviour was assessed by parents using the Child Behaviour Checklist for ages 1.5-5 years and the Behaviour Rating Inventory of Executive Function-Preschool Version, and by teachers using the Teacher's Report Form for ages 1.5-5 years. Multivariable regression models were performed. Taking 80 mg/day of iron improved child behaviour when women had low iron stores but worsened it when mothers had normal-high iron stores, except for depressive and attention/hyperactivity problems. Taking 20 mg/day of iron improved behaviour only in those children whose mothers had SF > 65 µg/L in early pregnancy. Additionally, executive functioning improved at high doses of prenatal iron when maternal baseline SF < 15 µg/L. Adjusting prenatal iron supplementation to both maternal baseline Hb levels and iron stores reduces behavioural problems in 4-year-old children.

Identifiants

pubmed: 38041537
doi: 10.1111/mcn.13595
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13595

Subventions

Organisme : Instituto de Salud Carlos III
ID : PI12/02777
Organisme : Instituto de Salud Carlos III
ID : PI17/01754

Informations de copyright

© 2023 The Authors. Maternal & Child Nutrition published by John Wiley & Sons Ltd.

Références

Achenbach, T. M., & Rescorla, L. A. (2000). Manual for the ASEBA school-age makes & profiles. University von Vermont, Research Center for Children, Youth, & Families.
Aparicio, E., Jardí, C., Bedmar, C., Pallejà, M., Basora, J., & Arija, V. (2020). Nutrient intake during pregnancy and post-partum: ECLIPSES study. Nutrients, 12(5), 1325. https://doi.org/10.3390/NU12051325
Arija, V., Fargas, F., March, G., Abajo, S., Basora, J., Canals, J., Ribot, B., Aparicio, E., Serrat, N., Hernández-Martínez, C., & Aranda, N. (2014). Adapting iron dose supplementation in pregnancy for greater effectiveness on mother and child health: Protocol of the ECLIPSES randomized clinical trial. BMC Pregnancy and Childbirth, 14, 33. https://doi.org/10.1186/1471-2393-14-33
Arija, V., Hernández-Martínez, C., Tous, M., Canals, J., Guxens, M., Fernández-Barrés, S., Ibarluzea, J., Babarro, I., Soler-Blasco, R., Llop, S., Vioque, J., Sunyer, J., & Julvez, J. (2019). Association of iron status and intake during pregnancy with neuropsychological outcomes in children aged 7 years: The prospective birth cohort infancia y medio ambiente (INMA) study. Nutrients, 11(12), 2999. https://doi.org/10.3390/nu11122999
Barican, J. L. lou, Yung, D., Schwartz, C., Zheng, Y., Georgiades, K., & Waddell, C. (2022). Prevalence of childhood mental disorders in high-income countries: A systematic review and meta-analysis to inform policymaking. Evidence Based Mental Health, 25(1), 36-44. https://doi.org/10.1136/ebmental-2021-300277
Cusick, S. E., & Georgieff, M. K. (2016). The role of nutrition in brain development: The golden opportunity of the “First 1000 Days”. The Journal of Pediatrics, 175, 16-21. https://doi.org/10.1016/J.JPEDS.2016.05.013
Díaz-López, A., Canals-Sans, J., Julvez, J., Fernandez-Barrés, S., Llop, S., Rebagliato, M., Lertxundi, N., Santa-Marina, L., Guxens, M., Sunyer, J., & Arija, V. (2022). Maternal iron status during pregnancy and attention deficit/hyperactivity disorder symptoms in 7-year-old children: A prospective cohort study. Scientific Reports, 12(1), 20762. https://doi.org/10.1038/s41598-022-23432-1
DiPietro, J. A., Voegtline, K. M., Pater, H. A., & Costigan, K. A. (2018). Predicting child temperament and behavior from the fetus. Development and Psychopathology, 30(3), 855-870. https://doi.org/10.1017/S0954579418000482
Feldman, R. (2008). The intrauterine environment, temperament, and development: Including the biological foundations of individual differences in the study of psychopathology and wellness. Journal of the American Academy of Child and Adolescent Psychiatry, 47(3), 233-235. https://doi.org/10.1097/CHI.0b013e3181613a92
Gaillard, R., Eilers, P. H. C., Yassine, S., Hofman, A., Steegers, E. A. P., & Jaddoe, V. W. v (2014). Risk factors and consequences of maternal anaemia and elevated haemoglobin levels during pregnancy: A population-based prospective cohort study. Paediatric and Perinatal Epidemiology, 28(3), 213-226. https://doi.org/10.1111/ppe.12112
Georgieff, M. K. (2007). Nutrition and the developing brain: Nutrient priorities and measurement. The American Journal of Clinical Nutrition, 85(2), 614. https://doi.org/10.1093/ajcn/85.2.614S
Georgieff, M. K. (2008). The role of iron in neurodevelopment: Fetal iron deficiency and the developing hippocampus. Biochemical Society Transactions, 36(6), 1267-1271. https://doi.org/10.1042/BST0361267
Gioia, G. A., Espy, K. A., & Isquith, P. K. (2016). Evaluación conductual de la función ejecutiva (BRIEF-P). TEA.
Hanson, E. H. (2001). HFE gene and hereditary hemochromatosis: A HuGE review. American Journal of Epidemiology, 154, 193-206. https://doi.org/10.1093/aje/154.3.193
Hernández-Martínez, C., Canals, J., Aranda, N., Ribot, B., Escribano, J., & Arija, V. (2011). Effects of iron deficiency on neonatal behavior at different stages of pregnancy. Early Human Development, 87(3), 165-169. https://doi.org/10.1016/j.earlhumdev.2010.12.006
Iglesias, L., Canals, J., & Arija, V. (2017). Effects of prenatal iron status on child neurodevelopment and behavior: A systematic review. Critical Reviews in Food Science and Nutrition, 58(10), 1604-1614. https://doi.org/10.1080/10408398.2016.1274285
Iglesias-Vázquez, L., Voltas, N., Hernández-Martínez, C., Canals, J., Coronel, P., Gimeno, M., Basora, J., & Arija, V. (2023). Importance of maternal iron status on the improvement of cognitive function in children after prenatal iron supplementation. American Journal of Preventive Medicine, 65, 395-405.
Janbek, J., Sarki, M., Specht, I. O., & Heitmann, B. L. (2019). A systematic literature review of the relation between iron status/anemia in pregnancy and offspring neurodevelopment. European Journal of Clinical Nutrition, 73(12), 1561-1578. https://doi.org/10.1038/s41430-019-0400-6
Jayasinghe, C., Polson, R., van Woerden, H. C., & Wilson, P. (2018). The effect of universal maternal antenatal iron supplementation on neurodevelopment in offspring: A systematic review and meta-analysis. BMC Pediatrics, 18(1), 150. https://doi.org/10.1186/s12887-018-1118-7
Lavezzi, A. M., Mohorovic, L., Alfonsi, G., Corna, M. F., & Matturri, L. (2011). Brain iron accumulation in unexplained fetal and infant death victims with smoker mothers-The possible involvement of maternal methemoglobinemia. BMC Pediatrics, 11, 62. https://doi.org/10.1186/1471-2431-11-62
Martinsone, B., Supe, I., Stokenberga, I., Damberga, I., Cefai, C., Camilleri, L., Bartolo, P., O'riordan, M. R., & Grazzani, I. (2021). Social emotional competence, learning outcomes, emotional and behavioral difficulties of preschool children: Parent and teacher evaluations. Frontiers in Psychology, 12, 760782. https://doi.org/10.3389/fpsyg.2021.760782
McCann, S., Amadó, M. P., & Moore, S. E. (2020). The role of iron in brain development: A systematic review. Nutrients, 12(7):2001. https://doi.org/10.3390/NU12072001
McCarthy, E. K., Murray, D. M., Hourihane, J. O., Kenny, L. C., Irvine, A. D., & Kiely, M. E. (2021). Behavioral consequences at 5 y of neonatal iron deficiency in a low-risk maternal-infant cohort. The American Journal of Clinical Nutrition, 113(4), 1032-1041. https://doi.org/10.1093/ajcn/nqaa367
Niu, Y., Desmarais, T. L., Tong, Z., Yao, Y., & Costa, M. (2015). Oxidative stress alters global histone modification and DNA methylation. Free Radical Biology & Medicine, 82, 22-28. https://doi.org/10.1016/j.freeradbiomed.2015.01.028
de la Osa, N., Granero, R., Trepat, E., Domenech, J. M., & Ezpeleta, L. (2016). The discriminative capacity of CBCL/1½-5-DSM5 scales to identify disruptive and internalizing disorders in preschool children. European Child & Adolescent Psychiatry, 25(1), 17-23. https://doi.org/10.1007/s00787-015-0694-4
Parsons, A. G., Zhou, S. J., Spurrier, N. J., & Makrides, M. (2008). Effect of iron supplementation during pregnancy on the behaviour of children at early school age: Long-term follow-up of a randomised controlled trial. British Journal of Nutrition, 99, 1133-1139. https://doi.org/10.1017/S0007114507853359
Peña-Rosas, J. P., De-Regil, L. M., Garcia-Casal, M. N., & Dowswell, T. (2015). Daily oral iron supplementation during pregnancy. Cochrane Database of Systematic Reviews, 2015(7):CD004736. https://doi.org/10.1002/14651858.CD004736.pub5
Quezada-Pinedo, H. G., Cassel, F., Duijts, L., Muckenthaler, M. U., Gassmann, M., Jaddoe, V. W. V., Reiss, I. K. M., & Vermeulen, M. J. (2021). Maternal iron status in pregnancy and child health outcomes after birth: A systematic review and meta-analysis. Nutrients, 13(7):2221. https://doi.org/10.3390/NU13072221
Quezada-Pinedo, H. G., Cassel, F., Muckenthaler, M. U., Gassmann, M., Huicho, L., Reiss, I. K., Duijts, L., Gaillard, R., & Vermeulen, M. J. (2022). Ethnic differences in adverse iron status in early pregnancy: A cross-sectional population-based study. Journal of Nutritional Science, 11, e39. https://doi.org/10.1017/jns.2022.35
Radlowski, E. C., & Johnson, R. W. (2013). Perinatal iron deficiency and neurocognitive development. Frontiers in Human Neuroscience, 7, 585. https://doi.org/10.3389/fnhum.2013.00585
Rasmussen, S., Bergsjø, P., Jacobsen, G., Haram, K., & Bakketeig, L. S. (2005). Haemoglobin and serum ferritin in pregnancy - Correlation with smoking and body mass index. European Journal of Obstetrics & Gynecology and Reproductive Biology, 123(1), 27-34. https://doi.org/10.1016/j.ejogrb.2005.02.012
Rodríguez, I. T., Ballart, J. F., Pastor, G. C., Jordà, E. B., & Val, V. A. (2008). Validation of a short questionnaire on frequency of dietary intake: Reproducibility and validity. Nutrición Hospitalaria, 23(3), 242-252. http://scielo.isciii.es/scielo.php?script=sci_arttext&pid=S0212-16112008000300011
Sans, J. C., Hidalgo, P. M., Castellví, J. R., Moreso, N. V., & Martínez, C. H. (2021). Prevalence and epidemiological characteristics of ADHD in pre-school and school age children in the Province of Tarragona, Spain. Journal of Attention Disorders, 25(13), 1818-1833. https://doi.org/10.1177/1087054720938866
Santa-Marina, L., Lertxundi, N., Andiarena, A., Irizar, A., Sunyer, J., Molinuevo, A., Llop, S., Julvez, J., Beneito, A., Ibarluzea, J., Imaz, L., & Ferrin, M. (2020). Maternal ferritin levels during pregnancy and ADHD symptoms in 4-year-old children: Results from the INMA-infancia y medio ambiente (environment and childhood) prospective birth cohort study. International Journal of Environmental Research and Public Health, 17(21), 7704. https://doi.org/10.3390/ijerph17217704
Schmidt, R. J., Tancredi, D. J., Krakowiak, P., Hansen, R. L., & Ozonoff, S. (2014). Maternal intake of supplemental iron and risk of autism spectrum disorder. American Journal of Epidemiology, 180(9), 890-900. https://doi.org/10.1093/aje/kwu208
Szajewska, H., Ruszczynski, M., & Chmielewska, A. (2010). Effects of iron supplementation in nonanemic pregnant women, infants, and young children on the mental performance and psychomotor development of children: A systematic review of randomized controlled trials. The American Journal of Clinical Nutrition, 91(6), 1684-1690. https://doi.org/10.3945/AJCN.2010.29191
Taeubert, M. J., de Prado-Bert, P., Geurtsen, M. L., Mancano, G., Vermeulen, M. J., Reiss, I. K. M., Caramaschi, D., Sunyer, J., Sharp, G. C., Julvez, J., Muckenthaler, M. U., & Felix, J. F. (2022). Maternal iron status in early pregnancy and DNA methylation in offspring: An epigenome-wide meta-analysis. Clinical Epigenetics, 14(1), 59. https://doi.org/10.1186/s13148-022-01276-w
Takegata, M., Matsunaga, A., Ohashi, Y., Toizumi, M., Yoshida, L. M., & Kitamura, T. (2021). Prenatal and intrapartum factors associated with infant temperament: A systematic review. Frontiers in Psychiatry, 12, 609020. https://doi.org/10.3389/fpsyt.2021.609020
Tearne, J. E., Allen, K. L., Herbison, C. E., Lawrence, D., Whitehouse, A. J. O., Sawyer, M. G., & Robinson, M. (2015). The association between prenatal environment and children's mental health trajectories from 2 to 14 years. European Child & Adolescent Psychiatry, 24(9), 1015-1024. https://doi.org/10.1007/s00787-014-0651-7
Vázquez, L. I., Arija, V., Aranda, N., Aparicio, E., Serrat, N., Fargas, F., Ruiz, F., Pallejà, M., Coronel, P., Gimeno, M., & Basora, J. (2019). The effectiveness of different doses of iron supplementation and the prenatal determinants of maternal iron status in pregnant spanish women: ECLIPSES study. Nutrients, 11, 2418. https://doi.org/10.3390/nu11102418
Voltas, N., Canals, J., Hernández-Martínez, C., Serrat, N., Basora, J., & Arija, V. (2020). Effect of vitamin d status during pregnancy on infant neurodevelopment: The eclipses study. Nutrients, 12(10), 3196. https://doi.org/10.3390/nu12103196
Wechsler, D. (1997). WAIS-III administration and scoring manual. The Psychological Corporation.
Wiegersma, A. M., Dalman, C., Lee, B. K., Karlsson, H., & Gardner, R. M. (2019). Association of prenatal maternal anemia with neurodevelopmental disorders. JAMA Psychiatry, 76(12), 1294. https://doi.org/10.1001/jamapsychiatry.2019.2309
Zerem, A., Ben-Sira, L., Vigdorovich, N., Leibovitz, Z., Fisher, Y., Schiffmann, R., Grishchuk, Y., Misko, A. L., Orenstein, N., Lev, D., Lerman-Sagie, T., & Kidron, D. (2021). White matter abnormalities and iron deposition in prenatal mucolipidosis IV- Fetal imaging and pathology. Metabolic Brain Disease, 36(7), 2155-2167. https://doi.org/10.1007/S11011-021-00742-3
Zhou, S. J., Gibson, R. A., Crowther, C. A., Baghurst, P., & Makrides, M. (2006). Effect of iron supplementation during pregnancy on the intelligence quotient and behavior of children at 4 y of age: Long-term follow-up of a randomized controlled trial. The American Journal of Clinical Nutrition, 83, 1112-1117.
Zou, R., el Marroun, H., Voortman, T., Hillegers, M., White, T., & Tiemeier, H. (2021). Maternal polyunsaturated fatty acids during pregnancy and offspring brain development in childhood. The American Journal of Clinical Nutrition, 114(1), 124-133. https://doi.org/10.1093/ajcn/nqab049

Auteurs

Lucía Iglesias-Vázquez (L)

Department of Basic Medical Sciences, Nutrition and Mental Health (NUTRISAM) Research Group, Universitat Rovira I Virgili, Reus, Spain.
Institut d'Investigació Sanitaria Pere Virgili (IISPV), Reus, Spain.

Josefa Canals (J)

Department of Basic Medical Sciences, Nutrition and Mental Health (NUTRISAM) Research Group, Universitat Rovira I Virgili, Reus, Spain.
Department of Psychology, Research Centre for Behavioral Assessment (CRAMC), Faculty of Education Sciences and Psychology, Universitat Rovira I Virgili, Tarragona, Spain.

Carmen Hernández-Martínez (C)

Department of Basic Medical Sciences, Nutrition and Mental Health (NUTRISAM) Research Group, Universitat Rovira I Virgili, Reus, Spain.
Department of Psychology, Research Centre for Behavioral Assessment (CRAMC), Faculty of Education Sciences and Psychology, Universitat Rovira I Virgili, Tarragona, Spain.

Núria Voltas (N)

Department of Basic Medical Sciences, Nutrition and Mental Health (NUTRISAM) Research Group, Universitat Rovira I Virgili, Reus, Spain.
Department of Psychology, Research Centre for Behavioral Assessment (CRAMC), Faculty of Education Sciences and Psychology, Universitat Rovira I Virgili, Tarragona, Spain.
Department of Psychology, Faculty of Education Sciences and Psychology, Serra Húnter Fellow, Universitat Rovira I Virgili, Tarragona, Spain.

Victoria Arija (V)

Department of Basic Medical Sciences, Nutrition and Mental Health (NUTRISAM) Research Group, Universitat Rovira I Virgili, Reus, Spain.
Institut d'Investigació Sanitaria Pere Virgili (IISPV), Reus, Spain.
Collaborative Research Group on Lifestyles, Nutrition, and Smoking (CENIT), Tarragona-Reus Research Support Unit, IDIAP Jordi Gol, Tarragona, Spain.

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