Effects of increased hemoglobin on child growth, development, and disease: a systematic review and meta-analysis

Annals of the New York Academy of Sciences

Volumn 1450, Issue 1, 2019, Pages 83-104

  Larson, Leila Margaret ^a   Kubes, Julianne Nicole ^b   Ramírez Luzuriaga, Maria J ^c   Khishen, Sarah ^d   H Shankar, Anuraj ^e,f   Prado, Elizabeth Leah ^g  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e EIJKMAN INSTITUTE FOR MOLECULAR BIOLOGY   (Indonesia)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

growth; hemoglobin; language development; mental development; motor development

Indexed keywords

HEMOGLOBIN;

CHILD DEVELOPMENT; HUMAN; META ANALYSIS; PHYSIOLOGY; PRESCHOOL CHILD;

CHILD DEVELOPMENT; CHILD, PRESCHOOL; HEMOGLOBINS; HUMANS;

EID: 85067050536     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.14105     Document Type: Review

References (112)

1. Stevens, G.A., M.M. Finucane, L.M. De-Regil, et al. 2013. Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995–2011: a systematic analysis of population-representative data. Lancet Glob. Health 1: e16–e25.
2. Petry, N., I. Olofin, R.F. Hurrell, et al. 2016. The proportion of anemia associated with iron deficiency in low, medium, and high human development index countries: a systematic analysis of national surveys. Nutrients 8. pii: E693.
3. Balarajan, Y., U. Ramakrishnan, E. Ozaltin, et al. 2011. Anaemia in low-income and middle-income countries. Lancet 378: 2123–2135.
4. Wang, M. 2016. Iron deficiency and other types of anemia in infants and children. Am. Fam. Physician. 93: 270–278.
5. WHO. 2011. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Accessed March 24 2015. http://www.who.int/vmnis/indicators/haemoglobin.pdf.
6. Grantham-McGregor, S. & C. Ani. 2001. A review of studies on the effect of iron deficiency on cognitive development in children. J. Nutr. 131: 649S–668S.
7. Walker, S.P., T.D. Wachs, J.M. Meeks-Gardner, et al. 2007. Child development: risk factors for adverse outcomes in developing countries. Lancet 369: 145–157.
8. Stoltzfus, R.J., L. Mullany & R.E. Black. 2004. Iron deficiency anaemia. In Comparative Quantification of Health Risks: Sexual and Reproductive Health. Vol. 2. M. Ezzati, A.D. Lopez, A. Rodgers, et al., Eds.: 163–210. Switzerland: World Health Organization.
9. Sherriff, A., A. Emond, J. Bell, et al. 2001. Should infants be screened for anaemia? A prospective study investigating the relation between haemoglobin at 8, 12, and 18 months and development at 18 months. Arch. Dis. Child. 84: 480–485.
10. WHO. 2016. World Malaria Report. WHO, Geneva. https://apps.who.int/iris/bitstream/handle/10665/252038/9789241511711-eng.pdf.
11. Jackson, N. & E. Waters. 2005. Criteria for the systematic review of health promotion and public health interventions. Health Promot. Int. 20: 367–374.
12. Stroup, D.F., J.A. Berlin, S.C. Morton, et al. 2000. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283: 2008–2012.
13. Wan, X., W. Wang, J. Liu, et al. 2014. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med. Res. Methodol. 14: 135.
14. Lozoff, B., I. De Andraca, M. Castillo, et al. 2003. Behavioral and developmental effects of preventing iron-deficiency anemia in healthy full-term infants. Pediatrics 112: 846–854.
15. Oski, F.A. & A.S. Honig. 1978. The effects of therapy on the developmental scores of iron-deficient infants. J. Pediatr. 92: 21–25.
16. Deinard, A.S., A. List, B. Lindgren, et al. 1986. Cognitive deficits in iron-deficient and iron-deficient anemic children. J. Pediatr. 108: 681–689.
17. Morley, R., R. Abbott, S. Fairweather-Tait, et al. 1999. Iron fortified follow on formula from 9 to 18 months improves iron status but not development or growth: a randomised trial. Arch. Dis. Child. 81: 247–252.
18. Friel, J.K., K. Aziz, W.L. Andrews, et al. 2003. A double-masked, randomized control trial of iron supplementation in early infancy in healthy term breast-fed infants. J. Pediatr. 143: 582–586.
19. Metallinos-Katsaras, E., E. Valassi-Adam, K.G. Dewey, et al. 2004. Effect of iron supplementation on cognition in Greek preschoolers. Eur. J. Clin. Nutr. 58: 1532–1542.
20. Domellof, M., R.J. Cohen, K.G. Dewey, et al. 2001. Iron supplementation of breast-fed Honduran and Swedish infants from 4 to 9 months of age. J. Pediatr. 138: 679–687.
21. Dewey, K.G., M. Domellöf, R.J. Cohen, et al. 2002. Iron supplementation affects growth and morbidity of breast-fed infants: results of a randomized trial in Sweden and Honduras. J. Nutr. 132: 3249–3255.
22. Akman, M., D. Cebeci, V. Okur, et al. 2004. The effects of iron deficiency on infants' developmental test performance. Acta Pædiatr. 93: 1391–1396.
23. Yalcin, S.S., K. Yurdakok, D. Acikgoz, et al. 2000. Short-term developmental outcome of iron prophylaxis in infants. Pediatr. Int. 42: 625–630.
24. Wasserman, G., J.H. Graziano, P. Factor-Litvak, et al. 1992. Independent effects of lead exposure and iron deficiency anemia on developmental outcome at age 2 years. J. Pediatr. 121: 695–703.
25. Wasserman, G.A., J.H. Graziano, P. Factor-Litvak, et al. 1994. Consequences of lead exposure and iron supplementation on childhood development at age 4 years. Neurotoxicol. Teratol. 16: 233–240.
26. Roy, A., H. Hu, D.C. Bellinger, et al. 2011. Hemoglobin, lead exposure, and intelligence quotient: effect modification by the DRD2 Taq IA polymorphism. Environ. Health Perspect. 119: 144–149.
27. Prado, E.L., S. Abbeddou, S. Adu-Afarwuah, et al. 2017. Predictors and pathways of language and motor development in four prospective cohorts of young children in Ghana, Malawi, and Burkina Faso. J. Child Psychol. Psychiatry. 58: 1264–1275.
28. Black, M.M., A.H. Baqui, K. Zaman, et al. 2004. Iron and zinc supplementation promote motor development and exploratory behavior among Bangladeshi infants. Am. J. Clin. Nutr. 80: 903–910.
29. Wachs, T.D., E. Pollitt, S. Cueto, et al. 2005. Relation of neonatal iron status to individual variability in neonatal temperament. Dev. Psychobiol. 46: 141–153.
30. Fahmida, U., J.S. Rumawas, B. Utomo, et al. 2007. Zinc-iron, but not zinc-alone supplementation, increased linear growth of stunted infants with low haemoglobin. Asia Pac. J. Clin. Nutr. 16: 301–309.
31. Gunnarsson, B.S., I. Thorsdottir, G. Palsson, et al. 2007. Iron status at 1 and 6 years versus developmental scores at 6 years in a well-nourished affluent population. Acta Pædiatr. 96: 391–395.
32. Ai, Y., S.R. Zhao, G. Zhou, et al. 2012. Hemoglobin status associated with performance IQ but not verbal IQ in Chinese preschool children. Pediatr. Int. 54: 669–675.
33. Aubuchon-Endsley, N.L., S.L. Grant, G. Berhanu, et al. 2011. Hemoglobin, growth, and attention of infants in southern Ethiopia. Child Dev. 82: 1238–1251.
34. Aubuchon-Endsley, N.L., S.L. Grant, D.G. Thomas, et al. 2013. Infant responsiveness, alertness, haemoglobin and growth in rural Sidama, Ethiopia. Matern. Child Nutr. 9: 483–498.
35. Gerber, A.S., D.P. Green & D. Nickerson. 2001. Testing for publication bias in political science. Political Anal. 9: 385–392.
36. Gerber, A.S., N. Malhotra, C.M. Dowling, et al. 2010. Publication bias in two political behavior literatures. Am. Politics Res. 38: 591–613.
37. Simonsohn, U., L.D. Nelson & J.P. Simmons. 2014. P-curve: a key to the file-drawer. J. Exp. Psychol. Gen. 143: 534.
38. Muhsen, K., S. Goren & D. Cohen. 2015. Helicobacter pylori infection in early childhood and growth at school age. Helicobacter 20: 410–417.
39. Marasinghe, E., S. Chackrewarthy, C. Abeysena, et al. 2015. Micronutrient status and its relationship with nutritional status in preschool children in urban Sri Lanka. Asia Pac. J. Clin. Nutr. 24: 144–151.
40. Olney, D.K., P.K. Kariger, R.J. Stoltzfus, et al. 2009. Development of nutritionally at-risk young children is predicted by malaria, anemia, and stunting in Pemba, Zanzibar. J. Nutr. 139: 763–772.
41. Ahun, M.N., F.E. Aboud, R. Aryeetey, et al. 2018. Child development in rural Ghana: associations between cognitive/language milestones and indicators of nutrition and stimulation of children under two years of age. Can. J. Public Health 108: 578–585.
42. McCarthy, E.K., C. Chaoimh, L.C. Kenny, et al. 2018. Iron status, body size, and growth in the first 2 years of life. Matern. Child Nutr. 14. https://doi.org/10.1111/mcn.12458.
43. Mohammed, S.H. & A. Esmaillzadeh. 2017. The relationships among iron supplement use, Hb concentration and linear growth in young children: Ethiopian Demographic and Health Survey. Br. J. Nutr. 118: 730–736.
44. Olney, D.K., E. Pollitt, P.K. Kariger, et al. 2006. Combined iron and folic acid supplementation with or without zinc reduces time to walking unassisted among Zanzibari infants 5- to 11-mo old. J. Nutr. 136: 2427–2434.
45. Olney, D.K., E. Pollitt, P.K. Kariger, et al. 2007. Young Zanzibari children with iron deficiency, iron deficiency anemia, stunting, or malaria have lower motor activity scores and spend less time in locomotion. J. Nutr. 137: 2756–2762.
46. Gashu, D., B.J. Stoecker, K. Bougma, et al. 2016. Stunting, selenium deficiency and anemia are associated with poor cognitive performance in preschool children from rural Ethiopia. Nutr. J. 15: 38.
47. Khalifa, N., H. El-Massry, S. Awad, et al. 2009. Neurological assessment in a group of preschool children with iron deficiency anaemia. J. Appl. Sci. Res. 5: 103–108.
48. MAL-ED Network Investigators. 2018. Early childhood cognitive development is affected by interactions among illness, diet, enteropathogens and the home environment: findings from the MAL-ED birth cohort study. BMJ Glob. Health 3: e000752.
49. Wasserman, G., J. Graziano, P. Factor-Litvak, et al. 1992. Independent effects of lead exposure and iron deficiency anemia on developmental outcome at age 2 years. J. Pediatr. 121: 695–703.
50. Wasserman, G., J. Graziano, P. Factor-Litvak, et al. 1994. Consequences of lead exposure and iron supplementation on childhood development at age 4 years. Neurotoxicol. Teratol. 16: 233–240.
51. Palti, H., B. Pevsner & B. Adler. 1983. Does anemia in infancy affect achievement on developmental and intelligence tests? Hum. Biol. 55: 183–194.
52. Wang, B., S. Zhan, T. Gong, et al. 2013. Iron therapy for improving psychomotor development and cognitive function in children under the age of three with iron deficiency anaemia. Cochrane Database Syst. Rev. CD001444. https://doi.org/10.1002/14651858.CD001444.pub2.
53. Thompson, J., B.A. Biggs & S.R. Pasricha. 2013. Effects of daily iron supplementation in 2- to 5-year-old children: systematic review and meta-analysis. Pediatrics 131: 739–753.
54. Pasricha, S.R., E. Hayes, K. Kalumba, et al. 2013. Effect of daily iron supplementation on health in children aged 4–23 months: a systematic review and meta-analysis of randomised controlled trials. Lancet Glob. Health 1: 70046–70049.
55. Larson, L.M. & A.K. Yousafzai. 2017. A meta-analysis of nutrition interventions on mental development of children under-two in low- and middle-income countries. Matern. Child Nutr. 13. https://doi.org/10.1111/mcn.12229.
56. Prado, E.L. & K.G. Dewey. 2014. Nutrition and brain development in early life. Nutr. Rev. 72: 267–284.
57. Georgieff, M.K. 2007. Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85: 614s–620s.
58. Bandhu, R., N. Shankar & O.P. Tandon. 2003. Effect of iron on growth in iron deficient anemic school going children. Indian J. Physiol. Pharmacol. 47: 59–66.
59. Sachdev, H., T. Gera & P. Nestel. 2006. Effect of iron supplementation on physical growth in children: systematic review of randomised controlled trials. Public Health Nutr. 9: 904–920.
60. Ramakrishnan, U., N. Aburto, G. McCabe, et al. 2004. Multimicronutrient interventions but not vitamin a or iron interventions alone improve child growth: results of 3 meta-analyses. J. Nutr. 134: 2592–2602.
61. Stoltzfus, R.J., J.D. Kvalsvig, H.M. Chwaya, et al. 2001. Effects of iron supplementation and anthelmintic treatment on motor and language development of preschool children in Zanzibar: double blind, placebo controlled study. BMJ 323: 1389–1393.
62. Gera, T., H.S. Sachdev & E. Boy. 2012. Effect of iron-fortified foods on hematologic and biological outcomes: systematic review of randomized controlled trials. Am. J. Clin. Nutr. 96: 309–324.
63. Gera, T., H.P. Sachdev, P. Nestel, et al. 2007. Effect of iron supplementation on haemoglobin response in children: systematic review of randomised controlled trials. J. Pediatr. Gastroenterol. Nutr. 44: 468–486.
64. Akman, M., D. Cebeci, V. Okur, et al. 2004. The effects of iron deficiency on infants' developmental test performance. Acta Paediatr. 93: 1391–1396.
65. Angeles, I.T., W.J. Schultink, P. Matulessi, et al. 1993. Decreased rate of stunting among anemic Indonesian preschool children through iron supplementation. Am. J. Clin. Nutr. 58: 339–342.
66. Attanasio, O.P., C. Fernandez, E.O. Fitzsimons, et al. 2014. Using the infrastructure of a conditional cash transfer program to deliver a scalable integrated early child development program in Colombia: cluster randomized controlled trial. BMJ 349: g5785.
67. Batra, P., N. Schlossman, I. Balan, et al. 2016. A randomized controlled trial offering higher- compared with lower-dairy second meals daily in preschools in Guinea-Bissau demonstrates an attendance-dependent increase in weight gain for both meal types and an increase in mid-upper arm circumference for the higher-dairy meal. J. Nutr. 146: 124–132.
68. Berger, J., N.X. Ninh, N.C. Khan, et al. 2006. Efficacy of combined iron and zinc supplementation on micronutrient status and growth in Vietnamese infants. Eur. J. Clin. Nutr. 60: 443–454.
69. Carrasco Quintero, M., L.O. Hernández, A. Chávez Villasana, et al. 2011. Impacto del consumo de harina de maíz con un bajo nivel de enriquecimiento en niños de zonas rurales. Nutrición Hospitalaria 26: 1097–1104.
70. Chen, K., T.Y. Li, L. Chen, et al. 2008. Effects of vitamin A, vitamin A plus iron and multiple micronutrient-fortified seasoning powder on preschool children in a suburb of Chongqing, China. J. Nutr. Sci. Vitaminol. (Tokyo) 54: 440–447.
71. de Almeida, C.A., J.E. Dutra-De-Oliveira, G.C. Crott, et al. 2005. Effect of fortification of drinking water with iron plus ascorbic acid or with ascorbic acid alone on hemoglobin values and anthropometric indicators in preschool children in day-care centers in Southeast Brazil. Food Nutr. Bull. 26: 259–265.
72. Dewey, K.G., M. Domellof, R.J. Cohen, et al. 2002. Iron supplementation affects growth and morbidity of breast-fed infants: results of a randomized trial in Sweden and Honduras. J. Nutr. 132: 3249–3255.
73. Dewey, K.G., M.K. Mridha, S.L. Matias, et al. 2017. Lipid-based nutrient supplementation in the first 1000 d improves child growth in Bangladesh: a cluster-randomized effectiveness trial. Am. J. Clin. Nutr. 105: 944–957.
74. Matias, S.L., M.K. Mridha, R.T. Young, et al. 2018. Prenatal and postnatal supplementation with lipid-based nutrient supplements reduces anemia and iron deficiency in 18-month-old Bangladeshi children: a cluster-randomized effectiveness trial. J. Nutr. 148: 1167–1176.
75. Dijkhuizen, M.A., P. Winichagoon, F.T. Wieringa, et al. 2008. Zinc supplementation improved length growth only in anemic infants in a multi-country trial of iron and zinc supplementation in South-East Asia. J. Nutr. 138: 1969–1975.
76. Dossa, R.A., E.A. Ategbo, F.L. de Koning, et al. 2001. Impact of iron supplementation and deworming on growth performance in preschool Beninese children. Eur. J. Clin. Nutr. 55: 223–228.
77. Faber, M., J.D. Kvalsvig, C.J. Lombard, et al. 2005. Effect of a fortified maize-meal porridge on anemia, micronutrient status, and motor development of infants. Am. J. Clin. Nutr. 82: 1032–1039.
78. Giovannini, M., D. Sala, M. Usuelli, et al. 2006. Double-blind, placebo-controlled trial comparing effects of supplementation with two different combinations of micronutrients delivered as sprinkles on growth, anemia, and iron deficiency in Cambodian infants. J. Pediatr. Gastroenterol. Nutr. 42: 306–312.
79. Heywood, A., S. Oppenheimer, P. Heywood, et al. 1989. Behavioral effects of iron supplementation in infants in Madang, Papua New Guinea. Am. J. Clin. Nutr. 50: 630–637; discussion 638–640.
80. Hop le, T. & J. Berger. 2005. Multiple micronutrient supplementation improves anemia, micronutrient nutrient status, and growth of Vietnamese infants: double-blind, randomized, placebo-controlled trial. J. Nutr. 135: 660s–665s.
81. Huybregts, L., F. Houngbe, C. Salpeteur, et al. 2012. The effect of adding ready-to-use supplementary food to a general food distribution on child nutritional status and morbidity: a cluster-randomized controlled trial. PLoS Med. 9: e1001313.
82. Idjradinata, P. & E. Pollitt. 1993. Reversal of developmental delays in iron-deficient anaemic infants treated with iron. Lancet 341: 1–4.
83. Inayati, D.A., V. Scherbaum, R.C. Purwestri, et al. 2012. Combined intensive nutrition education and micronutrient powder supplementation improved nutritional status of mildly wasted children on Nias Island, Indonesia. Asia Pac. J. Clin. Nutr. 21: 361–373.
84. Kounnavong, S., T. Sunahara, C.G. Mascie-Taylor, et al. 2011. Effect of daily versus weekly home fortification with multiple micronutrient powder on haemoglobin concentration of young children in a rural area, Lao People's Democratic Republic: a randomised trial. Nutr. J. 10: 129.
85. Kuusipalo, H., K. Maleta, A. Briend, et al. 2006. Growth and change in blood haemoglobin concentration among underweight Malawian infants receiving fortified spreads for 12 weeks: a preliminary trial. J. Pediatr. Gastroenterol. Nutr. 43: 525–532.
86. Larson, L.M., M.F. Young, P.J. Bauer, et al. 2018. Effectiveness of a home fortification programme with multiple micronutrients on infant and young child development: a cluster-randomised trial in rural Bihar, India. Br. J. Nutr. 120: 176–187.
87. López de Romaña, G., S. Cusirramos, D. López de Romaña, et al. 2005. Efficacy of multiple micronutrient supplementation for improving anemia, micronutrient status, growth, and morbidity of peruvian infants. J. Nutr. 135: 646S–652S.
88. Lopez de Romana, D., S. Verona, O.A. Vivanco, et al. 2006. Protective effect of multimicronutrient supplementation against anemia among children, women, and adolescent girls in lower-income areas of Chiclayo, Peru. Food Nutr. Bull. 27: S143–S150.
89. Lopriore, C., Y. Guidoum, A. Briend, et al. 2004. Spread fortified with vitamins and minerals induces catch-up growth and eradicates severe anemia in stunted refugee children aged 3–6 y. Am. J. Clin. Nutr. 80: 973–981.
90. Lozoff, B., G.M. Brittenham, F.E. Viteri, et al. 1982. The effects of short-term oral iron therapy on developmental deficits in iron-deficient anemic infants. J. Pediatr. 100: 351–357.
91. Lozoff, B., Y. Jiang, X. Li, et al. 2016. Low-dose iron supplementation in infancy modestly increases infant iron status at 9 mo without decreasing growth or increasing illness in a randomized clinical trial in rural China. J. Nutr. 146: 612–621.
92. Luo, R., A. Yue, H. Zhou, et al. 2017. The effect of a micronutrient powder home fortification program on anemia and cognitive outcomes among young children in rural China: a cluster randomized trial. BMC Public Health 17: 738.
93. Lutter, C.K., A. Rodríguez, G. Fuenmayor, et al. 2008. Growth and micronutrient status in children receiving a fortified complementary food. J. Nutr. 138: 379–388.
94. Mangani, C., K. Maleta, J. Phuka, et al. 2015. Effect of complementary feeding with lipid-based nutrient supplements and corn-soy blend on the incidence of stunting and linear growth among 6- to 18-month-old infants and children in rural Malawi. Matern. Child Nutr. 11(Suppl. 4): 132–143.
95. Osei, A.K., P. Pandey, D. Spiro, et al. 2015. Adding multiple micronutrient powders to a homestead food production programme yields marginally significant benefit on anaemia reduction among young children in Nepal. Matern. Child Nutr. 11(Suppl. 4): 188–202.
96. Palupi, L., W. Schultink, E. Achadi, et al. 1997. Effective community intervention to improve hemoglobin status in preschoolers receiving once-weekly iron supplementation. Am. J. Clin. Nutr. 65: 1057–1061.
97. Penny, M.E., R.M. Marin, A. Duran, et al. 2004. Randomized controlled trial of the effect of daily supplementation with zinc or multiple micronutrients on the morbidity, growth, and micronutrient status of young Peruvian children. Am. J. Clin. Nutr. 79: 457–465.
98. Prado, E.L., S. Abbeddou, E. Yakes Jimenez, et al. 2016. Lipid-based nutrient supplements plus malaria and diarrhea treatment increase infant development scores in a cluster-randomized trial in Burkina Faso. J. Nutr. 146: 814–822.
99. Rosado, J.L., P. Lopez, E. Munoz, et al. 1997. Zinc supplementation reduced morbidity, but neither zinc nor iron supplementation affected growth or body composition of Mexican preschoolers. Am. J. Clin. Nutr. 65: 13–19.
100. Rosado, J.L., P. Lopez, O.P. Garcia, et al. 2011. Effectiveness of the nutritional supplement used in the Mexican Oportunidades programme on growth, anaemia, morbidity and cognitive development in children aged 12–24 months. Public Health Nutr. 14: 931–937.
101. Schumann, K., P. Longfils, D. Monchy, et al. 2009. Efficacy and safety of twice-weekly administration of three RDAs of iron and folic acid with and without complement of 14 essential micronutrients at one or two RDAs: a placebo-controlled intervention trial in anemic Cambodian infants 6 to 24 months of age. Eur. J. Clin. Nutr. 63: 355–368.
102. Singla, D.R., S. Shafique, S.H. Zlotkin, et al. 2014. A 22-element micronutrient powder benefits language but not cognition in Bangladeshi full-term low-birth-weight children. J. Nutr. 144: 1803–1810.
103. Shafique, S., D.W. Sellen, W. Lou, et al. 2016. Mineral- and vitamin-enhanced micronutrient powder reduces stunting in full-term low-birth-weight infants receiving nutrition, health, and hygiene education: a 2 × 2 factorial, cluster-randomized trial in Bangladesh. Am. J. Clin. Nutr. 103: 1357–1369.
104. Siegel, E.H., K. Kordas, R.J. Stoltzfus, et al. 2011. Inconsistent effects of iron-folic acid and/or zinc supplementation on the cognitive development of infants. J Health Popul. Nutr. 29: 593–604.
105. Smuts, C.M., M.A. Dhansay, M. Faber, et al. 2005. Efficacy of multiple micronutrient supplementation for improving anemia, micronutrient status, and growth in South African infants. J. Nutr. 135: 653S–659S.
106. Thakwalakwa, C., P. Ashorn, J. Phuka, et al. 2010. A lipid-based nutrient supplement but not corn-soy blend modestly increases weight gain among 6- to 18-month-old moderately underweight children in rural Malawi. J. Nutr. 140: 2008–2013.
107. Thu, B.D., W. Schultink, D. Dillon, et al. 1999. Effect of daily and weekly micronutrient supplementation on micronutrient deficiencies and growth in young Vietnamese children. Am. J. Clin. Nutr. 69: 80–86.
108. Untoro, J., E. Karyadi, L. Wibowo, et al. 2005. Multiple micronutrient supplements improve micronutrient status and anemia but not growth and morbidity of Indonesian infants: a randomized, double-blind, placebo-controlled trial. J. Nutr. 135: 639s–645s.
109. Wasantwisut, E., P. Winichagoon, C. Chitchumroonchokchai, et al. 2006. Iron and zinc supplementation improved iron and zinc status, but not physical growth, of apparently healthy, breast-fed infants in rural communities of northeast Thailand. J. Nutr. 136: 2405–2411.
110. Palti, H., B. Pevsner & B. Adler. 1983. Does anemia in infancy affect achievement on developmental and intelligence tests? Hum. Biol. 55: 183–194.
111. Cardoso, M.A., R.A. Augusto, G.A. Bortolini, et al. 2016. Effect of providing multiple micronutrients in powder through primary healthcare on anemia in young Brazilian children: a multicentre pragmatic controlled trial. PloS One 11: e0151097.
112. Rosado, J.L., P. Lopez, E. Muñoz, et al. 1997. Zinc supplementation reduced morbidity, but neither zinc nor iron supplementation affected growth or body composition of Mexican preschoolers. Am. J. Clin. Nutr. 65: 13–19.