In vitro assessment of iron availability from commercial Young Child Formulae supplemented with prebiotics

European Journal of Nutrition

Volumn 57, Issue 2, 2018, Pages 669-678

  Christides, Tatiana ^a   Ganis, Julia Clark ^a   Sharp, Paul Anthony ^b  

^a UNIVERSITY OF GREENWICH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Bioavailability; Caco 2; Iron; Prebiotics; Young Child Formulae; Young children

Indexed keywords

ASCORBIC ACID; FERRITIN; IRON; OLIGOSACCHARIDE; PREBIOTIC AGENT; 4'-GALACTOOLIGOSACCHARIDE; BIOLOGICAL MARKER; FRUCTOSE OLIGOSACCHARIDE; TRISACCHARIDE;

ARTICLE; ARTIFICIAL MILK; BIOAVAILABILITY; CACO-2 CELL LINE; CONTROLLED STUDY; IN VITRO STUDY; NUTRIENT AVAILABILITY; NUTRIENT CONCENTRATION; ADMINISTRATION AND DOSAGE; ANALYSIS; BIOSYNTHESIS; CHEMISTRY; CHILD NUTRITION; COMPARATIVE STUDY; DIGESTION; FOOD; HEAT; HUMAN; INFANT; INFANT NUTRITION; INTESTINE ABSORPTION; INTESTINE CELL; IRON INTAKE; METABOLISM; NUTRITIONAL VALUE; PRESCHOOL CHILD;

ASCORBIC ACID; BIOMARKERS; CACO-2 CELLS; CHILD NUTRITIONAL PHYSIOLOGICAL PHENOMENA; CHILD, PRESCHOOL; DIGESTION; ENTEROCYTES; FERRITINS; FOODS, SPECIALIZED; HOT TEMPERATURE; HUMANS; INFANT; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INTESTINAL ABSORPTION; IRON, DIETARY; NUTRITIVE VALUE; OLIGOSACCHARIDES; PREBIOTICS; TRISACCHARIDES;

EID: 85003875085     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-016-1353-3     Document Type: Article

References (56)

1. Nyaradi A, Li J, Hickling S, Foster J, Oddy WH (2013) The role of nutrition in children’s neurocognitive development, from pregnancy through childhood. Front Hum Neurosci 7:97
2. Lozoff B, Jimenez E, Hagen J, Mollen E, Wolf AW (2000) Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics 105:E51
3. Domellof M, Braegger C, Campoy C, Colomb V, Decsi T, Fewtrell M et al (2014) Iron requirements of infants and toddlers. J Pediatr Gastroenterol Nutr 58:119–129
4. Paoletti G, Bogen DL, Ritchey AK (2014) Severe iron-deficiency anemia still an issue in toddlers. Clin Pediatr (Phila) 53:1352–1358
5. American Academy of Pediatrics Committee on Nutrition (1989) Iron-fortified infant formulas. Pediatrics 84:1114–1115
6. Scientific Advisory Committee on Nutrition (SACN) (2010) Iron and health. Department of Health, TSO, London
7. Brotanek JM, Gosz J, Weitzman M, Flores G (2008) Secular trends in the prevalence of iron deficiency among us toddlers, 1976-2002. Arch Pediatr Adolesc Med 162:374–381
8. Bates B, Lennox A, Prentice A, Bates C, Page P, Nicholson S, Swan G (2014) National diet and nutrition survey: results from years 1–4 (combined) of the rolling programme (2008/2009–2011/12): Executive summary. Department of Health, TSO, London
9. Ziegler EE (2011) Consumption of cow’s milk as a cause of iron deficiency in infants and toddlers. Nutr Rev 69(Suppl 1):S37–S42
10. Ghisolfi J, Fantino M, Turck D, de Courcy GP, Vidailhet M (2013) Nutrient intakes of children aged 1–2 years as a function of milk consumption, cows’ milk or growing-up milk. Public Health Nutr 16:524–534
11. McCarthy EK, Ni Chaoimh C, O′B Hourihane J, Kenny LC, Irvine AD, Murray DM, Kiely M (2016) Iron intakes and status of 2-year-old children in the Cork BASELINE Birth Cohort Study. Matern Child Nutr. doi:10.1111/mcn.12320
12. Lennox ASJ, Ong K, Henderson H, Allen R (2011) Diet and nutrition survey of infants and young children: executive summary. Department of Health, TSO, London
13. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412
14. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275
15. Yeung C, Glahn RP, Welch RM, Miller DD (2005) Prebiotics and iron bioavailability—is there a connection? J Food Sci 70:88–92
16. Braegger C, Chmielewska A, Decsi T, Kolacek S, Mihatsch W, Moreno L et al (2011) Supplementation of infant formula with probiotics and/or prebiotics: a systematic review and comment by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 52:238–250
17. Commission Directive 2006/141/EC of 22 December 2006 on infant formulae and follow-on formulae and amending Directive 1999/21/EC (Text with EEA relevance). Official Journal of the European Union. 30 December 2006. L401/1. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:401:0001:0033:EN:PDF. 11 Sept 2016
18. Krebs NF, Domellof M, Ziegler E (2015) Balancing benefits and risks of iron fortification in resource-rich countries. J Pediatr 167:S20–S25
19. Jaeggi T, Kortman GA, Moretti D, Chassard C, Holding P, Dostal A et al (2015) Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in kenyan infants. Gut 64:731–742
20. Zimmermann MB, Chassard C, Rohner F, N’Goran EK, Nindjin C, Dostal A et al (2010) The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Cote d’Ivoire. Am J Clin Nutr 92:1406–1415
21. Quinn EA (2014) Too much of a good thing: evolutionary perspectives on infant formula fortification in the United States and its effects on infant health. Am J Hum Biol 26:10–17
22. Singhal A, Morley R, Abbott R, Fairweather-Tait S, Stephenson T, Lucas A (2000) Clinical safety of iron-fortified formulas. Pediatrics 105:E38
23. Etcheverry P, Wallingford JC, Miller DD, Glahn RP (2004) Calcium, zinc, and iron bioavailabilities from a commercial human milk fortifier: a comparison study. J Dairy Sci 87:3629–3637
24. Viadel B, Perales S, Barbera R, Lagarda M, Farre R (2007) Ferritin synthesis by Caco-2 cells as an indicator of iron bioavailability: application to milk-based infant formulas. Food Chem 102:925–931
25. Laparra JM, Tako E, Glahn RP, Miller DD (2008) Supplemental inulin does not enhance iron bioavailability to Caco-2 cells from milk- or soy-based, probiotic-containing, yogurts but incubation at 37 degrees c does. Food Chem 109:122–128
26. Caro IBX, Rousset M, Meunier V, Bourrie M, Julian B, Joyeux H, Roques C, Berger Y, Zweibaum A, Fabre G (1995) Characterisation of a newly isolated Caco-2 clone (TC7), as a model of transport processes and biotransformation of drugs. Int J Pharm 116:147–158
27. Christides T, Sharp P (2013) Sugars increase non-heme iron bioavailability in human epithelial intestinal and liver cells. PLoS ONE 8:e83031
28. Christides T, Wray D, McBride R, Fairweather R, Sharp P (2014) Iron bioavailability from commercially available iron supplements. Eur J Nutr. doi:10.1007/s00394-014-0815-8
29. Johnson DM, Yamaji S, Tennant J, Srai SK, Sharp PA (2005) Regulation of divalent metal transporter expression in human intestinal epithelial cells following exposure to non-haem iron. FEBS Lett 579:1923–1929
30. Glahn RP, Lee OA, Yeung A, Goldman MI, Miller DD (1998) Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. J Nutr 128:1555–1561
31. Jumarie C, Malo C (1991) Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J Cell Physiol 149:24–33
32. Bowles A, Keane J, Ernest T, Clapham D, Tuleu C (2010) Specific aspects of gastro-intestinal transit in children for drug delivery design. Int J Pharm 395:37–43
33. Davey MWMM, Inzé D, Sanmartin M, Kanellis A, Smirnoff N, Benzie IJ, Strain JJ, Favell D, Fletcher J (2000) Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860
34. Motulsky H (2010) Intuitive biostatistics, 2nd edn. Oxford University Press, Oxford
35. Allen L, de Benoist B, Dary O, Hurrell R (2006) In: Guidelines on food fortification with micronutrients. World Health Organization, Dept. of Nutrition for Health and Development
36. Lobo AR, Gaievski EH, De Carli E, Alvares EP, Colli C (2014) 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 112:1286–1295
37. Freitas Kde C, Amancio OM, de Morais MB (2012) High-performance inulin and oligofructose prebiotics increase the intestinal absorption of iron in rats with iron deficiency anaemia during the growth phase. Br J Nutr 108:1008–1016
38. Wang Y, Zeng T, Wang SE, Wang W, Wang Q, Yu HX (2010) Fructo-oligosaccharides enhance the mineral absorption and counteract the adverse effects of phytic acid in mice. Nutrition 26:305–311
39. Pérez-Conesa D, López G, Ros G (2007) Effect of probiotic, prebiotic and synbiotic follow-up infant formulas on iron bioavailability in rats. Food Sci Technol Int 13:69–77
40. Yasuda K, Roneker KR, Miller DD, Welch RM, Lei XG (2006) Supplemental dietary inulin affects the bioavailability of iron in corn and soybean meal to young pigs. J Nutr 136:3033–3038
41. Yasuda K, Dawson HD, Wasmuth EV, Roneker CA, Chen C, Urban JF et al (2009) Supplemental dietary inulin influences expression of iron and inflammation related genes in young pigs. J Nutr 139:2018–2023
42. Laparra JM, Glahn RP, Miller DD (2009) Assessing potential effects of inulin and probiotic bacteria on Fe availability from common beans (Phaseolus vulgaris L.) to Caco-2 cells. J Food Sci 74:H40–H46
43. Patterson JK, Yasuda K, Welch RM, Miller DD, Lei XG (2010) Supplemental dietary inulin of variable chain lengths alters intestinal bacterial populations in young pigs. J Nutr 140:2158–2161
44. Tako E, Glahn RP, Welch RM, Lei X, Yasuda K, Miller DD (2008) Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Br J Nutr 99:472–480
45. Marciano R, Santamarina AB, de Santana AA, Silva Mde L, Amancio OM, do Nascimento CM et al (2015) Effects of prebiotic supplementation on the expression of proteins regulating iron absorption in anaemic growing rats. Br J Nutr 113:901–908
46. Petry N, Egli I, Chassard C, Lacroix C, Hurrell R (2012) 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 96:325–331
47. van den Heuvel EG, Schaafsma G, Muys T, van Dokkum W (1998) Nondigestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. Am J Clin Nutr 67:445–451
48. Sazawal S, Dhingra U, Hiremath G, Sarkar A, Dhingra P, Dutta A et al (2010) Effects of Bifidobacterium lactis hn019 and prebiotic oligosaccharide added to milk on iron status, anemia, and growth among children 1 to 4 years old. J Pediatr Gastroenterol Nutr 51:341–346
49. Schaafsma G, Slavin JL (2015) Significance of inulin fructans in the human diet. Compr Rev Food Sci Food Saf 14:37–47
50. Laparra JM, Diez-Municio M, Herrero M, Moreno FJ (2014) Structural differences of prebiotic oligosaccharides influence their capability to enhance iron absorption in deficient rats. Food Funct 5:2430–2437
51. Vitali DRM, Cetina-Čižmek B, Dragojević Vedrina (2011) Caco-2 cell uptake of Ca, Mg and Fe from biscuits as affected by enrichment with pseudocereal/inulin mixtures. Acta Aliment 40:480–489
52. Klewicki R (2007) The stability of gal-polyols and oligosaccharides during pasteurization at a low pH. Food Sci Technol-LEB 40:1259–1265
53. Vega R, Zuniga-Hansen ME (2015) The effect of processing conditions on the stability of fructooligosaccharides in acidic food products. Food Chem 173:784–789
54. Walton J, Flynn A (2013) Nutritional adequacy of diets containing growing up milks or unfortified cow’s milk in irish children (aged 12–24 months). Food Nutr Res. doi:10.3402/fnr.v57i0.21836
55. Akkermans MD, van der Horst-Graat JM, Eussen SR, van Goudoever JB, Brus F (2016) Iron and vitamin D deficiency in healthy young children in Western Europe despite current nutritional recommendations. J Pediatr Gastroenterol Nutr 62:635–642
56. Fairweather-Tait S, Lynch S, Hotz C, Hurrell R, Abrahamse L, Beebe S et al (2005) The usefulness of in vitro models to predict the bioavailability of iron and zinc: a consensus statement from the harvestplus expert consultation. Int J Vitam Nutr Res 75:371–374