Prenatal zinc and Vitamin A reduce the benefit of iron on maternal hematologic and micronutrient status at delivery in Tanzania

Journal of Nutrition

Volumn 150, Issue 2, 2020, Pages 240-248

  Noor, Ramadhani A ^a   Abioye, Ajibola I ^a   Darling, Anne Marie ^a   Hertzmark, Ellen ^a   Aboud, Said ^b   Premji, Zulfiqarali ^b   Mugusi, Ferdinand M ^b   Duggan, Christopher ^a,c   Sudfeld, Christopher R ^a   Spiegelman, Donna ^a,d   Fawzi, Wafaie ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MUHIMBILI UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

^c HARVARD MEDICAL SCHOOL   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

Anemia; Iron; Micronutrients; Pregnancy; Vitamin A; Zinc

Indexed keywords

FERRITIN; FOLIC ACID; HEMOGLOBIN; IRON; RETINOL; ZINC; BIOLOGICAL MARKER; TRACE ELEMENT;

ADULT; ANEMIA; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE SEVERITY; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; FEMALE; FERRITIN BLOOD LEVEL; FIRST TRIMESTER PREGNANCY; HUMAN; IRON DEPLETION; MAJOR CLINICAL STUDY; MATERNAL NUTRITION; NUTRITIONAL STATUS; PREGNANT WOMAN; PRENATAL CARE; RANDOMIZED CONTROLLED TRIAL; RISK FACTOR; RISK REDUCTION; SECONDARY ANALYSIS; TANZANIA; WORLD HEALTH ORGANIZATION; YOUNG ADULT; ZINC BLOOD LEVEL; BLOOD EXAMINATION; METABOLISM; PREGNANCY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

ADULT; BIOMARKERS; FEMALE; HEMATOLOGIC TESTS; HEMOGLOBINS; HUMANS; IRON; MICRONUTRIENTS; PREGNANCY; PRENATAL CARE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TANZANIA; VITAMIN A; YOUNG ADULT; ZINC;

EID: 85079104302     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/nxz242     Document Type: Article

References (58)

1. Darnton-Hill I, Mkparu UC. Micronutrients in pregnancy in low- and middle-income countries. Nutrients 2015;7:1744-68.
2. Gernand AD, Schulze KJ, Stewart CP, West KP, Christian P. Micronutrient deficiencies in pregnancy worldwide: health effects and prevention. Nat Rev Endocrinol 2016;12(5):274-89.
3. Stevens GA, Finucane MM, De-Regil LM, Paciorek CJ, Flaxman SR, Branca F, Peña-Rosas JP, Bhutta ZA, Ezzati M. Nutrition Impact Model Study Group (Anaemia). 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 2013;1(1):16-25.
4. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J. Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 2008;371(9608):243-60.
5. Walker CF, Kordas K, Stoltzfus RJ, Black RE. Interactive effects of iron and zinc on biochemical and functional outcomes in supplementation trials. Am J Clin Nutr 2005;82:5-12.
6. Haider BA, Olofin I, Wang M, Spiegelman D, Ezzati M, Fawzi WW. Anaemia, prenatal iron use, and risk of adverse pregnancy outcomes: systematic review and meta-analysis. BMJ 2013;346:f3443.
7. Shankar AH, Prasad AS. Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr 1998;68(2 Suppl):447S-63S.
8. Shaw JG, Friedman JF. Iron deficiency anemia: focus on infectious diseases in lesser developed countries. Anemia 2011:260380.
9. Sandström B. Micronutrient interactions: effects on absorption and bioavailability. Br J Nutr 2001;85(Suppl 2):S181-5.
10. Solomons NW, Ruz M. Zinc and iron interaction: concepts and perspectives in the developing world. Nutr Res 1997;17(1):177-85.
11. Crofton RW, Gvozdanovic D, Gvozdanovic S, Khin CC, Brunt PW, Mowat NA, Aggett PJ. Inorganic zinc and the intestinal absorption of ferrous iron. Am J Clin Nutr 1989;50(1):141-4.
12. Olivares M, Pizarro F, Ruz M. Zinc inhibits nonheme iron bioavailability in humans. Biol Trace Elem Res 2007;117(1-3):7-14.
13. O'Brien KO, Zavaleta N, Caulfield LE, Yang DX, Abrams SA. Influence of prenatal iron and zinc supplements on supplemental iron absorption, red blood cell iron incorporation, and iron status in pregnant Peruvian women. Am J Clin Nutr 1999;69(3):509-15.
14. Cao C, O'Brien KO. Pregnancy and iron homeostasis: an update. Nutr Rev 2013;71(1):35-51.
15. Saaka M. Combined iron and zinc supplementation improves haematologic status of pregnant women in Upper West Region of Ghana. Ghana Med J 2012;46(4):225-33.
16. Christian P, Shrestha J, LeClerq SC, Khatry SK, Jiang T, Wagner T, Katz J, West KP, Jr. Supplementation with micronutrients in addition to iron and folic acid does not further improve the hematologic status of pregnant women in rural Nepal. J Nutr 2003;133(11):3492-8.
17. Hurrell R, Egli I. Iron bioavailability and dietary reference values. Am J Clin Nutr 2010;91(5):1461S-7S.
18. Mejia LA, Rucker RB, Hodges RE. Role of Vitamin A in the absorption, retention and distribution of iron in the rat. J Nutr 1979;109(1):129-37.
19. McCauley ME, van den Broek N, Dou L, Othman M. Vitamin A supplementation during pregnancy for maternal and newborn outcomes. Cochrane Database Syst Rev 2015;(10):CD008666.
20. de Sá Barreto da Cunha M, Campos Hankins NA, Arruda SF. Effect of Vitamin A supplementation on iron status in humans: a systematic review and meta-analysis. Crit Rev Food Sci Nutr 2019;59(11):1767-81.
21. Darling AM, Mugusi FM, Etheredge AJ, Gunaratna NS, Abioye AI, Aboud S, Duggan C, Mongi R, Spiegelman D, Roberts D, et al. Vitamin A and zinc supplementation among pregnant women to prevent placental malaria: a randomized, double-blind, placebo-controlled trial in Tanzania. Am J Trop Med Hyg 2017;96(4):826-34.
22. Etheredge AJ, Premji Z, Gunaratna NS, Abioye AI, Aboud S, Duggan C, Mongi R, Meloney L, Spiegelman D, Roberts D, et al. Iron supplementation in iron-replete and nonanemic pregnant women in Tanzania: a randomized clinical trial. JAMA Pediatr 2015;169(10):947-55.
23. Abioye AI, Aboud S, Premji Z, Etheredge AJ, Gunaratna NS, Sudfeld CR, Mongi R, Meloney L, Darling AM, Noor RA, et al. Iron supplementation affects hematologic biomarker concentrations and pregnancy outcomes among iron-deficient Tanzanian women. J Nutr 2016;146(6):1162-71.
24. DiRenzo GC, Spano F, Giardina I, Brillo E, Clerici G, Roura LC. Iron deficiency anemia in pregnancy. Womens Health (Lond) 2015;11(6):891-900.
25. WHO, Chan M. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva (Switzerland): World Health Organization; 2011. pp. 1-6.
26. Beard JL, Murray-Kolb LE, Rosales FJ, Solomons NW, Angelilli ML. Interpretation of serum ferritin concentrations as indicators of total-body iron stores in survey populations: the role of biomarkers for the acute phase response. Am J Clin Nutr 2006;84(6): 1498-505.
27. Castel R, Tax MGHM, Droogendijk J, Leers MPG, Beukers R, Levin MD, Sonneveld P, Berendes PB. The transferrin/log(ferritin) ratio: a new tool for the diagnosis of iron deficiency anemia. Clin Chem Lab Med 2012;50(8):1343-9.
28. Pasricha S-R, Drakesmith H, Black J, Hipgrave D, Biggs B-A. Control of iron deficiency anemia in low- and middle-income countries. Blood 2013;121(14):2607-17.
29. Spiegelman D, Hertzmark E. Easy SAS calculations for risk or prevalence ratios and differences. Am J Epidemiol 2005;162(3):199-200.
30. Miettinen O. Theoretical epidemiology. New York (NY): John Wiley & Sons; 1985.
31. Zavaleta N, Caulfield LE, Garcia T. Changes in iron status during pregnancy in Peruvian women receiving prenatal iron and folic acid supplements with or without zinc. Am J Clin Nutr 2000;71(4): 956-61.
32. Christian P, Khatry SK, LeClerq SC, Ram Shrestha S, Kimbrough-Pradhan E, West KP. Iron and zinc interactions among pregnant Nepali women. Nutr Res 2001;21(1-2):141-8.
33. Nishiyama S, Kiwaki K, Miyazaki Y, Hasuda T. Zinc and IGF-I concentrations in pregnant women with anemia before and after supplementation with iron and/or zinc. J Am Coll Nutr 1999;18(3):261-7.
34. Nguyen P, Grajeda R, Melgar P, Marcinkevage J, Flores R, Ramakrishnan U, Martorell R. Effect of zinc on efficacy of iron supplementation in improving iron and zinc status in women. J Nutr Metab 2012:216179.
35. Donangelo CM, Woodhouse LR, King SM, Viteri FE, King JC. Supplemental zinc lowers measures of iron status in young women with low iron reserves. J Nutr 2002;132(7):1860-4.
36. Institute of Medicine, National Academies. Dietary Reference Intakes (DRIs) for Vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium and zinc. Washington (DC): National Academies Press; 2001. Available from: http://nap.edu/read/10026/chapter/1. [Accessed 2019 Oct 2].
37. Semba RD, Bloem MW. The anemia of Vitamin A deficiency: epidemiology and pathogenesis. Eur J Clin Nutr 2002;56:271-81.
38. Thorne-Lyman AL, Fawzi WW. Vitamin A and carotenoids during pregnancy and maternal, neonatal and infant health outcomes: a systematic review and meta-analysis. Paediatr Perinat Epidemiol 2012;26(Suppl 1):36-54.
39. García-Casal MN, Layrisse M, Solano L, Barón MA, Arguello F, Llovera D, Ramírez J, Leets I, Tropper E. Vitamin A and β-carotene can improve nonheme iron absorption from rice, wheat and corn by humans. J Nutr 1998;128(3):646-50.
40. Cusick SE, Tielsch JM, Ramsan M, Jape JK, Sazawal S, Black RE, Stoltzfus RJ. Short-term effects of Vitamin A and antimalarial treatment on erythropoiesis in severely anemic Zanzibari preschool children. Am J Clin Nutr 2005;82(2):406-12.
41. Smith ER, Muhihi A, Mshamu S, Sudfeld CR, Noor RA, Spiegelman D, Shapiro RL, Masanja H, Fawzi W. The effect of neonatal Vitamin A supplementation on morbidity and mortality at 12 months: a randomized trial. Int J Epidemiol 2016;45(6):2112-21.
42. Masanja H, Smith ER, Muhihi A, Briegleb C, Mshamu S, Ruben J, Noor RA, Khudyakov P, Yoshida S, Martines J, et al. Effect of neonatal Vitamin A supplementation on mortality in infants in Tanzania (Neovita): a randomised, double-blind, placebo-controlled trial. Lancet 2015;385(9975):1324-32.
43. Edmond KM, Newton S, Shannon C, O'Leary M, Hurt L, Thomas G, Amenga-Etego S, Tawiah-Agyemang C, Gram L, Hurt CN, et al. Effect of early neonatal Vitamin A supplementation on mortality during infancy in Ghana (Neovita): a randomised, double-blind, placebo-controlled trial. Lancet 2015;385(9975):1315-23.
44. WHO. WHO recommendations on antenatal care for a positive pregnancy experience. Geneva: WHO; 2016.
45. Gibson RS, King JC, Lowe N. A review of dietary zinc recommendations. Food Nutr Bull 2016;37(4):443-60.
46. de Benoist B, Darnton-Hill I, Davidsson L, Fontaine O, Hotz C. Conclusions of the joint WHO/UNICEF/IAEA/IZiNCG interagency meeting on zinc status indicators. Food Nutr Bull 2007;28(3 Suppl):480-4.
47. Pérès J-M, Bureau F, Neuville D, Arhan P, Bouglé D. Inhibition of zinc absorption by iron depends on their ratio. J Trace Elem Med Biol 2001;15:237-41.
48. O'Brien KO, Zavaleta N, Caulfield LE, Wen J, Abrams SA. Prenatal iron supplements impair zinc absorption in pregnant Peruvian women. J Nutr 2000;130(9):2251-5.
49. Simmer K, Iles CA, James C, Thompson RPH. Are iron-folate supplements harmful? Am J Clin Nutr 1987;45(1):122-5.
50. Ghishan FK, Said HM, Wilson PC, Murrell JE, Greene HL. Intestinal transport of zinc and folic acid: a mutual inhibitory effect. Am J Clin Nutr 1986;43(2):258-62.
51. Donangelo CM, King JC. Maternal zinc intakes and homeostatic adjustments during pregnancy and lactation. Nutrients 2012;4(7): 782-98.
52. Hambidge KM, Krebs NF, Jacobs MA, Favier A, Guyette L, Ikle DN. Zinc nutritional status during pregnancy: a longitudinal study. Am J Clin Nutr 1983;37:429-42.
53. Caulfield LE, Donangelo CM, Chen P, Junco J, Merialdi M, Zavaleta N. Red blood cell metallothionein as an indicator of zinc status during pregnancy. Nutrition 2008;24(11-12):1081-7.
54. King JC. Does zinc absorption reflect zinc status? Int J Vitam Nutr Res 2010;80(4-5):300-6.
55. WHO. Assessing the iron status of populations. 2nd ed. Geneva: WHO; 2007.
56. Mwangi MN, Maskey S, Andang'o PEA, Shinali NK, Roth JM, Trijsburg L, Mwangi AM, Zuilhof H, van Lagen B, Savelkoul HF, et al. Diagnostic utility of zinc protoporphyrin to detect iron deficiency in Kenyan pregnant women. BMC Med 2014;12(1): 229.
57. Mwangi MN, Prentice AM, Verhoef H. Safety and benefits of antenatal oral iron supplementation in low-income countries: a review. Br J Haematol 2017;177:884-95.
58. World Health Organization. Guideline: daily iron and folic acid supplementation in pregnant women. Geneva: WHO; 2012.