Consumption of galacto-oligosaccharides increases iron absorption from a micronutrient powder containing ferrous fumarate and sodium iron EDTA: A stable-isotope study in Kenyan infants

American Journal of Clinical Nutrition

Volumn 106, Issue 4, 2017, Pages 1020-1031

  Paganini, Daniela ^a   Uyoga, Mary A ^b   Cercamondi, Colin I ^a   Moretti, Diego ^a   Mwasi, Edith ^c   Schwab, Clarissa ^a   Bechtler, Salome ^a   Mutuku, Francis M ^d   Galetti, Valeria ^a   Lacroix, Christophe ^a   Karanja, Simon ^b   Zimmermann, Michael B ^a  

^a ETH ZURICH   (Switzerland)

^b JOMO KENYATTA UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Kenya)

^c Msambweni County Referral Hospital   (Kenya)

^d TECHNICAL UNIVERSITY OF MOMBASA   (Kenya)

Author keywords

Anemia; Galacto oligosaccharides; GOS; Infants; Iron absorption; Iron deficiency; Kenya; Micronutrient powder; Prebiotics; Stable isotopes

Indexed keywords

EDETIC ACID; FERROUS FUMARATE; GALACTOSE OLIGOSACCHARIDE; STABLE ISOTOPE; FE(III)-EDTA; FERRIC ION; FERROUS ION; FERROUS SULFATE; GALACTOSE; IRON; IRON INTAKE; ISOTOPE; OLIGOSACCHARIDE; PREBIOTIC AGENT; TRACE ELEMENT;

ARTICLE; BIFIDOBACTERIUM; BIOAVAILABILITY; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; ERYTHROCYTE; FEMALE; FOOD INTAKE; HUMAN; HUMAN EXPERIMENT; INFANT; IRON ABSORPTION; KENYAN; LACTOBACILLUS; LEUCONOSTOC; MAIZE; MALE; PEDIOCOCCUS; PH; TEST MEAL; ANEMIA, IRON-DEFICIENCY; BACTERIUM; BLOOD; DIET; DRUG EFFECTS; FORTIFIED FOOD; GROWTH, DEVELOPMENT AND AGING; INTESTINE ABSORPTION; IRON INTAKE; KENYA; METABOLISM; PHARMACOKINETICS;

ANEMIA, IRON-DEFICIENCY; BACTERIA; BIOLOGICAL AVAILABILITY; DIET; EDETIC ACID; ERYTHROCYTES; FEMALE; FERRIC COMPOUNDS; FERROUS COMPOUNDS; FOOD, FORTIFIED; GALACTOSE; HUMANS; INFANT; INTESTINAL ABSORPTION; IRON; IRON, DIETARY; ISOTOPES; KENYA; MALE; MICRONUTRIENTS; OLIGOSACCHARIDES; PREBIOTICS; TRACE ELEMENTS; ZEA MAYS;

EID: 85031696240     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.116.145060     Document Type: Article

References (44)

1. De-Regil LM, Suchdev PS, Vist GE, Walleser S, Peña-Rosas JP. Home fortification of foods with multiple micronutrient powders for health and nutrition in children under two years of age. Evid Based Child Health 2013;8:112–201.
2. Jaeggi T, Moretti D, Kvalsvig J, Holding PA, Tjalsma H, Kortman GA, Joosten I, Mwangi A, Zimmermann MB. Iron status and systemic inflammation, but not gut inflammation, strongly predict gender-specific concentrations of serum hepcidin in infants in rural Kenya. PLoS One 2013;8:e57513.
3. Tondeur MC, Schauer CS, Christofides AL, Asante KP, Newton S, Serfass RE, Zlotkin SH. Determination of iron absorption from intrinsically labeled microencapsulated ferrous fumarate (sprinkles) in infants with different iron and hematologic status by using a dual-stable-isotope method. Am J Clin Nutr 2004;80:1436–44.
4. Jaeggi T, Kortman GA, Moretti D, Chassard C, Holding P, Dostal A, Boekhorst J, Timmerman HM, Swinkels DW, Tjalsma H, et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 2015;64:731–42.
5. Soofi S, Cousens S, Iqbal SP, Akhund T, Khan J, Ahmed I, Zaidi AK, Bhutta ZA. Effect of provision of daily zinc and iron with several micronutrients on growth and morbidity among young children in Pakistan: a cluster-randomised trial. Lancet 2013;382:29–40.
6. Troesch B, Egli I, Zeder C, Hurrell RF, de Pee S, Zimmermann MB. Optimization of a phytase-containing micronutrient powder with low amounts of highly bioavailable iron for in-home fortification of complementary foods. Am J Clin Nutr 2009;89:539–44.
7. Chavasit V, Porasuphatana S, Suthutvoravut U, Zeder C, Hurrell R. Iron bioavailability in 8-24-month-old Thai children from a micronutrient-fortified quick-cooking rice containing ferric ammonium citrate or a mixture of ferrous sulphate and ferric sodium ethylenediaminetetraacetic acid. Matern Child Nutr 2015;11 Suppl 4:179–87.
8. Bothwell TH, MacPhail AP. The potential role of NaFeEDTA as an iron fortificant. Int J Vitam Nutr Res 2004;74:421–34.
9. García-Casal MN, Layrisse M. The effect of change in pH on the solubility of iron bis-glycinate chelate and other iron compounds. Arch Latinoam Nutr 2001;51(1 Suppl 1):35–6.
10. Mason S. Some aspects of gastric function in the newborn. Arch Dis Child 1962;37:387–91.
11. Bertelsen RJ, Jensen ET, Ringel-Kulka T. Use of probiotics and prebiotics in infant feeding. Best Pract Res Clin Gastroenterol 2016;30: 39–48.
12. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, et al. Prebiotic effects: metabolic and health benefits. Br J Nutr 2010;104 Suppl 2:S1–63.
13. FDA. GRAS notification for halacto-oligosaccharides (GOS). GRN no. 236. United States Food and Drug Administration; 2007.
14. Paganini D, Uyoga MA, Kortman GAM, Cercamondi CI, Moretti D, Barth-Jaeggi T, Schwab C, Boekhorst J, Timmerman HM, Lacroix C, et al. Prebiotic galacto-oligosaccharides mitigate the adverse effects of iron fortification on the gut microbiome: a randomized controlled study in Kenyan infants. Gut 2017 Aug 3 (Epub ahead of print; DOI:10.1136/ gutjnl-2017-314418).
15. Scholz-Ahrens KE, Schaafsma G, van den Heuvel EG, Schrezenmeir J. Effects of prebiotics on mineral metabolism. Am J Clin Nutr 2001;73(2 Suppl):459S–64S.
16. Chernelch M, Fawwaz R, Sargent T, Winchell HS. Effect of phlebotomy and pH on iron absorption from the colon. J Nucl Med 1970;11: 25–7.
17. Campos MS, Gomez-Ayala AE, Lopez-Aliaga I, Pallarés I, Hariti S, Alférez MJM, Barrionuevo M, Rodriguez-Matas MC, Lisbona F. Role of the procimal colon in mineral absorption in rats with and without ferropenic anemia. Nutr Res 1996;16:1529–43.
18. Ohkawara Y, Bamba M, Nakai I, Kinka S, Masuda M. The absorption of iron from the human large intestine. Gastroenterology 1963;44: 611–4.
19. Erhardt JG, Estes JE, Pfeiffer CM, Biesalski HK, Craft NE. Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique. J Nutr 2004; 134:3127–32.
20. WHO/UNICEF/UNU. Iron deficiency anemia assessment, prevention, and control. Geneva (Switzerland): World Health Organization; 2001.
21. Walczyk T, Davidsson L, Zavaleta N, Hurrell RF. Stable isotope labels as a tool to determine the iron absorption by Peruvian school children from a breakfast meal. Fresenius J Anal Chem 1997;359:445–9.
22. Makower RU. Extraction and determination of phytic acid in beans (Phaseolus vulgaris). Cereal Chem 1970;47:288–95.
23. Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 2004;97:1166–77.
24. Furet JP, Firmesse O, Gourmelon M, Bridonneau C, Tap J, Mondot S, Dore J, Corthier G. Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 2009;68:351–62.
25. Brown E, Hopper J Jr., Hodges JL Jr., Bradley B, Wennesland R, Yamauchi H. Red cell, plasma, and blood volume in the healthy women measured by radiochromium cell-labeling and hematocrit. J Clin Invest 1962;41:2182–90.
26. Thurnham DI, McCabe LD, Haldar S, Wieringa FT, Northrop-Clewes CA, McCabe GP. Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: a meta-analysis. Am J Clin Nutr 2010;92:546–55.
27. Cook JD, Dassenko SA, Lynch SR. Assessment of the role of nonheme-iron availability in iron balance. Am J Clin Nutr 1991;54:717–22.
28. Cercamondi CI, Egli IM, Mitchikpe E, Tossou F, Hessou J, Zeder C, Hounhouigan JD, Hurrell RF. Iron bioavailability from a lipid-based complementary food fortificant mixed with millet porridge can be optimized by adding phytase and ascorbic acid but not by using a mixture of ferrous sulfate and sodium iron EDTA. J Nutr 2013;143: 1233–9.
29. Coudray C, Bellanger J, Castiglia-Delavaud C, Remesy C, Vermorel M, Rayssignuier Y. Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men. Eur J Clin Nutr 1997;51: 375–80.
30. van den Heuvel EG, Schaafsma G, Muys T, van Dokkum W. Non-digestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. Am J Clin Nutr 1998;67: 445–51.
31. Petry N, Egli I, Chassard C, Lacroix C, Hurrell R. Inulin modifies the bifidobacteria population, fecal lactate concentration, and fecal pH but does not influence iron absorption in women with low iron status. Am J Clin Nutr 2012;96:325–31.
32. Andersson HB, Ellegard LH, Bosaeus IG. Nondigestibility characteristics of inulin and oligofructose in humans. J Nutr 1999;129(7 Suppl):1428S–30S.
33. Hallberg L, Solvell L. Absorption of a single dose of iron in man. Acta Med Scand Suppl 1960;358:19–42.
34. Wheby MS, Crosby WH. The gastrointestinal tract and iron absorption. Blood 1963;22:416–28.
35. Marciano R, Santamarina AB, de Santana AA, Silva Mde L, Amancio OM, do Nascimento CM, Oyama LM, de Morais MB. Effects of prebiotic supplementation on the expression of proteins regulating iron absorption in anaemic growing rats. Br J Nutr 2015;113:901–8.
36. Lobo AR, Gaievski EH, De Carli E, Alvares EP, Colli C. Fructo-oligosaccharides and iron bioavailability in anaemic rats: the effects on iron species distribution, ferroportin-1 expression, crypt bifurcation and crypt cell proliferation in the caecum. Br J Nutr 2014;112:1286–95.
37. Yasuda K, Dawson HD, Wasmuth EV, Roneker CA, Chen C, Urban JF, Welch RM, Miller DD, Lei XG. Supplemental dietary inulin influences expression of iron and inflammation related genes in young pigs. J Nutr 2009;139:2018–23.
38. Laparra JM, Diez-Municio M, Herrero M, Moreno FJ. Structural differences of prebiotic oligosaccharides influence their capability to enhance iron absorption in deficient rats. Food Funct 2014;5:2430–7.
39. Institute of Medicine. Iron. In: Dietary Reference Intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Washington (DC): National Academy Press; 2001. p. 290–393.
40. Davidsson L, Walczyk T, Zavaleta N, Hurrell R. Improving iron absorption from a Peruvian school breakfast meal by adding ascorbic acid or Na2EDTA. Am J Clin Nutr 2001;73:283–7.
41. Chang S, Huang Z, Ma Y, Piao J, Yang X, Zeder C, Hurrell RF, Egli I. Mixture of ferric sodium ethylenediaminetetraacetate (NaFeEDTA) and ferrous sulfate: an effective iron fortificant for complementary foods for young Chinese children. Food Nutr Bull 2012;33:111–6.
42. Walter T, Pizarro F, Olivares M. Iron bioavailability in corn-masa tortillas is improved by the addition of disodium EDTA. J Nutr 2003;133: 3158–61.
43. Fidler MC, Davidsson L, Zeder C, Walczyk T, Hurrell RF. Iron absorption from ferrous fumarate in adult women is influenced by ascorbic acid but not by Na2EDTA. Br J Nutr 2003;90:1081–5.
44. Hurrell R. Use of ferrous fumarate to fortify foods for infants and young children. Nutr Rev 2010;68:522–30.