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Maternal and pediatric nutrition

Maternal haemoglobin concentrations before and during pregnancy as determinants of the concentrations of children at 3–5 years of age: A large follow-up study

European Journal of Clinical Nutrition volume 73, pages 1102–1109 (2019)Cite this article

Subjects

Abstract

Objective

To examine the association between haemoglobin (Hb) concentrations in mothers before and during pregnancy and those in children at 3–5 years of age.

Methods

The study included 78,923 women who conceived during 1993–1996 and delivered a singleton live infant. Maternal Hb concentrations were measured at pre-pregnancy health check-up and first prenatal visit, and during the second and third trimester. Hb concentrations of children born to these women were measured at 3–5 years of age. Associations between Hb levels in mothers and children were examined. Unconditional logistic regression was used to explore the association between maternal Hb levels and risk for anaemia in children.

Results

Maternal Hb levels before and during pregnancy were positively associated with children’s Hb levels. Using maternal Hb ≥ 130 g/L as the referent, the risk for anaemia in children at 3–5 years of age was higher when maternal second trimester Hb concentrations were 70–99 g/L (odds ratio [OR] = 1.76, 95% confidence interval [CI] = 1.56–1.99), 100–109 g/L (OR = 1.45, 95% CI = 1.29–1.64), and 110–119 g/L (OR = 1.18, 95% CI = 1.04–1.33). Children were 1.52 and 1.23-times more likely to suffer from anaemia when maternal third trimester Hb concentrations were 70–99 and 100–109 g/L, respectively. A pre-pregnancy Hb concentration of 80–109 g/L and first prenatal visit Hb concentrations of 80–109 and 100–119 g/L were also associated with increased risks for childhood anaemia.

Conclusion

Low maternal Hb concentrations before or during pregnancy increase the risk for anaemia in children at 3–5 years of age.

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References

  1. Balarajan Y, Ramakrishnan U, Ozaltin E, Shankar AH, Subramanian SV. Anaemia in low-income and middle-income countries. Lancet. 2011;378:2123–35. https://doi.org/10.1016/s0140-6736(10)62304-5.

    Article  PubMed  Google Scholar 

  2. Hipgrave DB, Fu X, Zhou H, Jin Y, Wang X, Chang S, et al. Poor complementary feeding practices and high anaemia prevalence among infants and young children in rural central and western China. Eur J Clin Nutr. 2014;68:916–24. https://doi.org/10.1038/ejcn.2014.98.

    Article  CAS  PubMed  Google Scholar 

  3. Gao W, Yan H, Wang D, Dang S, Pei L. Severity of anemia among children under 36 months old in rural western China. PLoS ONE. 2013;8:e62883 https://doi.org/10.1371/journal.pone.0062883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Eneroth H, Persson LA, El Arifeen S, Ekstrom EC. Infant anaemia is associated with infection, low birthweight and iron deficiency in rural Bangladesh. Acta Paediatr. 2011;100:220–5. https://doi.org/10.1111/j.1651-2227.2010.02011.x.

    Article  CAS  PubMed  Google Scholar 

  5. Koura GK, Ouedraogo S, Le Port A, Watier L, Cottrell G, Guerra J, et al. Anaemia during pregnancy: impact on birth outcome and infant haemoglobin level during the first 18 months of life. Trop Med Int Health. 2012;17:283–91. https://doi.org/10.1111/j.1365-3156.2011.02932.x.

    Article  PubMed  Google Scholar 

  6. Kilbride J, Baker TG, Parapia LA, Khoury SA, Shuqaidef SW, Jerwood D. Anaemia during pregnancy as a risk factor for iron-deficiency anaemia in infancy: a case-control study in Jordan. Int J Epidemiol. 1999;28:461–8.

    Article  CAS  Google Scholar 

  7. Zhang Y, Jin L, Liu JM, Ye R, Ren A. Maternal hemoglobin concentration during gestation and risk of anemia in infancy: secondary analysis of a randomized controlled trial. J Pediatr. 2016;175:106. https://doi.org/10.1016/j.jpeds.2016.05.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Berry RJ, Li Z, Erickson JD, Li S, Moore CA, Wang H, et al. Prevention of neural-tube defects with folic acid in China. China–U.S. collaborative project for neural tube defect prevention. N Engl J Med. 1999;341:1485–90. https://doi.org/10.1056/nejm199911113412001.

    Article  CAS  PubMed  Google Scholar 

  9. Li H, Ye R, Pei L, Ren A, Zheng X, Liu J. Caesarean delivery, caesarean delivery on maternal request and childhood overweight: a Chinese birth cohort study of 181 380 children. Pediatr Obes. 2014;9:10–16. https://doi.org/10.1111/j.2047-6310.2013.00151.x.

    Article  CAS  PubMed  Google Scholar 

  10. World Health Organisation. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: Vitamin and mineral nutrition information system (VMNIS); 2011. http://www.who.int/vmnis/indicators/haemoglobin.pdf. Accessed 4 Feb. 2018.

  11. De Pee S, Bloem MW, Sari M, Kiess L, Yip R, Kosen S. The high prevalence of low hemoglobin concentration among Indonesian infants aged 3-5 months is related to maternal anemia. J Nutr. 2002;132:2215–21.

    Article  Google Scholar 

  12. Blouin B, Penny ME, Maheu-Giroux M, Casapia M, Aguilar E, Silva H, et al. Timing of umbilical cord-clamping and infant anaemia: the role of maternal anaemia. Paediatr Int Child Health. 2013;33:79–85. https://doi.org/10.1179/2046905512y.0000000036.

    Article  PubMed  Google Scholar 

  13. Maketa V, Mavoko HM, da Luz RI, Zanga J, Lubiba J, Kalonji A, et al. The relationship between Plasmodium infection, anaemia and nutritional status in asymptomatic children aged under five years living in stable transmission zones in Kinshasa, Democratic Republic of Congo. Malar J. 2015;14:83 https://doi.org/10.1186/s12936-015-0595-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Rawat R, Saha KK, Kennedy A, Rohner F, Ruel M, Menon P. Anaemia in infancy in rural Bangladesh: contribution of iron deficiency, infections and poor feeding practices. Br J Nutr. 2014;111:172–81. https://doi.org/10.1017/s0007114513001852.

    Article  CAS  PubMed  Google Scholar 

  15. Gonzales GF. Hemoglobin and testosterone: importance on high altitude acclimatization and adaptation. Rev Peru De Med Exp y Salud Publica. 2011;28:92–100.

    Article  Google Scholar 

  16. Tran TD, Fisher J, Hanieh S, Tran T, Simpson JA, Tran H, et al. Antenatal iron supplementation regimens for pregnant women in rural Vietnam and subsequent haemoglobin concentration and anaemia among their infants. PLoS ONE. 2015;10:e0125740 https://doi.org/10.1371/journal.pone.0125740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Viteri FE. Iron endowment at birth: maternal iron status and other influences. Nutr Rev. 2011;69(Suppl 1):S3–16. https://doi.org/10.1111/j.1753-4887.2011.00449.x.

    Article  PubMed  Google Scholar 

  18. Braithwaite VS, Prentice A, Darboe MK, Prentice AM, Moore SE. The effects of maternal iron deficiency on infant fibroblast growth factor-23 and mineral metabolism. Bone. 2016;83:1–8. https://doi.org/10.1016/j.bone.2015.10.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dai AI, Demiryurek S, Aksoy SN, Perk P, Saygili O, Gungor K. Maternal iron deficiency anemia as a risk factor for the development of retinopathy of prematurity. Pediatr Neurol. 2015;53:146–50. https://doi.org/10.1016/j.pediatrneurol.2015.04.002.

    Article  PubMed  Google Scholar 

  20. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341:938–41.

    Article  CAS  Google Scholar 

  21. Harvey NC, Poole JR, Javaid MK, Dennison EM, Robinson S, Inskip HM, et al. Parental determinants of neonatal body composition. J Clin Endocrinol Metab. 2007;92:523–6. https://doi.org/10.1210/jc.2006-0456.

    Article  CAS  PubMed  Google Scholar 

  22. Entringer S, Kumsta R, Nelson EL, Hellhammer DH, Wadhwa PD, Wust S. Influence of prenatal psychosocial stress on cytokine production in adult women. Dev Psychobiol. 2008;50:579–87. https://doi.org/10.1002/dev.20316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Entringer S, Wust S, Kumsta R, Layes IM, Nelson EL, Hellhammer DH, et al. Prenatal psychosocial stress exposure is associated with insulin resistance in young adults. Am J Obstet Gynecol. 2008;199:498.e491–497. https://doi.org/10.1016/j.ajog.2008.03.006.

    Article  CAS  Google Scholar 

  24. Zerfu TA, Umeta M, Baye K. Dietary diversity during pregnancy is associated with reduced risk of maternal anemia, preterm delivery, and low birth weight in a prospective cohort study in rural Ethiopia. Am J Clin Nutr. 2016;103:1482–8. https://doi.org/10.3945/ajcn.115.116798.

    Article  CAS  PubMed  Google Scholar 

  25. Backstrand JR, Allen LH, Black AK, de Mata M, Pelto GH. Diet and iron status of nonpregnant women in rural Central Mexico. Am J Clin Nutr. 2002;76:156–64.

    Article  CAS  Google Scholar 

  26. Zimmermann MB, Chaouki N, Hurrell RF. Iron deficiency due to consumption of a habitual diet low in bioavailable iron: a longitudinal cohort study in Moroccan children. Am J Clin Nutr. 2005;81:115–21.

    Article  CAS  Google Scholar 

  27. Horton S. The economics of food fortification. J Nutr. 2006;136:1068–71.

    Article  CAS  Google Scholar 

  28. Wilunda C, Tanaka S, Esamai F, Kawakami K. Prenatal anemia control and anemia in children aged 6–23 months in sub-Saharan Africa. Matern Child Nutr. 2016. https://doi.org/10.1111/mcn.12375

    Article  Google Scholar 

  29. Martorell R, Ascencio M, Tacsan L, Alfaro T, Young MF, Addo OY, et al. Effectiveness evaluation of the food fortification program of Costa Rica: impact on anemia prevalence and hemoglobin concentrations in women and children. Am J Clin Nutr. 2015;101:210–7. https://doi.org/10.3945/ajcn.114.097709.

    Article  CAS  PubMed  Google Scholar 

  30. Zhang CM, Zhao WY, Gao AX, Su TT, Wang YK, Zhang YQ, et al. How could agronomic biofortification of rice be an alternative strategy with higher cost-effectiveness for human iron and zinc deficiency in China? Food Nutr Bull. 2017. doi:https://doi.org/10.1177/0379572117745661.

    Article  Google Scholar 

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Acknowledgements

All authors read and approved the final manuscript. The original project was supported by a cooperative agreement between the US Centers for Disease Control and Prevention and Peking University (grant No. U01 DD000293).

Author contributions

AR conceived the study and revised the manuscript; YZ analysed the data and wrote the first draft; LJ provided critical comments on the first draft; JL and RY supervised the follow-up study. No honorarium, grant, or other form of payment was given to anyone to produce the manuscript. AR takes primary responsibility for the final content.

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Authors and Affiliations

  1. Health Care Department, Haidian Maternal and Child Health Hospital, Beijing, 100080, China

    Yiting Zhang

  2. Institute of Reproductive and Child Health/Ministry of Health Key Laboratory of Reproductive Health, Peking University, Beijing, 100191, China

    Yiting Zhang, Lei Jin, Jian-meng Liu, Rongwei Ye & Aiguo Ren

  3. Department of Epidemiology and Biostatistics, School of Public Health, Peking University, Beijing, 100191, China

    Lei Jin, Jian-meng Liu, Rongwei Ye & Aiguo Ren

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Correspondence to Aiguo Ren.

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Zhang, Y., Jin, L., Liu, Jm. et al. Maternal haemoglobin concentrations before and during pregnancy as determinants of the concentrations of children at 3–5 years of age: A large follow-up study. Eur J Clin Nutr 73, 1102–1109 (2019). https://doi.org/10.1038/s41430-018-0284-x

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