Extrinsic Labeling of Staple Food Crops with Isotopic Iron Does Not Consistently Result in Full Equilibration: Revisiting the Methodology

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 43, 2015, Pages 9621-9628

  Glahn, Raymond P ^a   Cheng, Zhiqiang ^b   Giri, Shree ^b  

^a ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

^b Stocking Hall ^*  (United States)

Author keywords

extrinsic iron labeling; iron bioavailability; isotopic exchange

Indexed keywords

BIOCHEMISTRY; CROPS; IRON;

BLACK BEANS; IN-VITRO DIGESTIONS; INTESTINAL ABSORPTION; IRON BIOAVAILABILITY; ISOTOPIC EXCHANGE; ISOTOPIC LABELING; SEED-COAT COLOR; STAPLE FOOD;

ISOTOPES;

IRON;

BIOLOGICAL MODEL; CACO 2 CELL LINE; CHEMISTRY; CROP; DIGESTION; EVALUATION STUDY; FOOD ANALYSIS; HUMAN; KINETICS; METABOLISM; PROCEDURES; STAINING;

CACO-2 CELLS; CROPS, AGRICULTURAL; DIGESTION; FOOD ANALYSIS; HUMANS; IRON ISOTOPES; KINETICS; MODELS, BIOLOGICAL; STAINING AND LABELING;

EID: 84946594260     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b03926     Document Type: Article

References (38)

1. Engle-Stone, R.; Yeung, A.; Welch, R.; Glahn, R. Meat and ascorbic acid can promote Fe availability from Fe-phytate but not from Fe-tannic acid complexes J. Agric. Food Chem. 2005, 53, 10276-10284 10.1021/jf0518453
2. Wheby, M. S. Site of iron absorption in man Scand. J. Haematol. 1970, 7, 56-62 10.1111/j.1600-0609.1970.tb01869.x
3. Gardner, J. D.; Ciociola, A. A.; Robinson, M. Measurement of meal-stimulated gastric acid secretion by in vivo gastric autotitration J. Appl. Physiol. 2002, 92, 427-434 10.1152/japplphysiol.00956.2001
4. Tyssandier, V.; Reboul, E.; Dumas, J. F.; Bouteloup-Demange, C.; Armand, M.; Marcand, J.; Sallas, M.; Borel, P. Processing of vegetable-borne carotenoids in the human stomach and duodenum Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 284, G913-G923 10.1152/ajpgi.00410.2002
5. Hotz, C.; McClafferty, B. From harvest to health: challenges for developing biofortified staple foods and determining their impact on micronutrient status Food Nutr. Bull. 2007, 28 (2 Suppl.) S271-S279
6. Bailey, R. L.; West, K. P.; Black, R. E. The epidemiology of global micronutrient deficiencies Ann. Nutr. Metab. 2015, 66 (Suppl. 2) 22-33 10.1159/000371618
7. Welch, R. M. Biotechnology, biofortification, and global health Food Nutr. Bull. 2005, 26, 419-421
8. De Moura, F. F.; Palmer, A. C.; Finkelstein, J. L.; Haas, J. D.; Murray-Kolb, L. E.; Wenger, M. J.; Birol, E.; Boy, E.; Peña-Rosas, J. P. Are biofortified staple food crops improving vitamin A and iron status in women and children? New evidence from efficacy trials Adv. Nutr. 2014, 5, 568-570 10.3945/an.114.006627
9. Petry, N.; Egli, I.; Gahutu, J. B.; Tugirimana, P. L.; Boy, E.; Hurrell, R. Phytic acid concentration influences iron bioavailability from biofortified beans in Rwandese women with low iron status J. Nutr. 2014, 144, 1681-1687 10.3945/jn.114.192989
10. Sankaran, R. P.; Grusak, M. A. Whole shoot mineral partitioning and accumulation in pea (Pisum sativum) Front. Plant Sci. 2014, 23, 149 10.3389/fpls.2014.00149
11. Petry, N.; Egli, I.; Zeder, C.; Walczyk, T.; Hurrell, R. Polyphenols and phytic acid contribute to the low iron bioavailability from common beans in young women J. Nutr. 2010, 140, 1977-1982 10.3945/jn.110.125369
12. Glahn, R. P.; Lee, O. A.; Yeung, A.; Goldman, M. I.; Miller, D. D. Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model J. Nutr. 1998, 128, 1555-1561
13. Haas, J. D.; Villalpando, S.; Beebe, S.; Glahn, R. P.; Shamah, T.; Boy, E. The effect of consuming biofortified beans on the iron status of Mexican school children FASEB J. 2011, 25, 96.6
14. Haas, J. D.; Luna, S.; Lung'aho, M.; Ngabo, F.; Wenger, M.; Murray-Kolb, L.; Beebe, S.; Gahutu, J. B.; Egli, I. Iron biofortified beans improve iron status in Rwandan university women: results of a feeding trial. FASEB J. 2014, 28 (1), Suppl. 646.1.
15. Tako, E.; Hoekenga, O. A.; Kochian, L. V.; Glahn, R. P. High bioavailablilty iron maize (Zea mays L.) developed through molecular breeding provides more absorbable iron in vitro (Caco-2 model) and in vivo (Gallus gallus) Nutr. J. 2013, 12 (3) 3 10.1186/1475-2891-12-3
16. Petry, N.; Egli, I.; Gahutu, J. B.; Tugirimana, P. L.; Boy, E.; Hurrell, R. Stable iron isotope studies in Rwandese women indicate that the common bean has limited potential as a vehicle for iron biofortification J. Nutr. 2012, 142, 492-497 10.3945/jn.111.149286
17. Beiseigel, J. M.; Hunt, J. R.; Glahn, R. P.; Welch, R. M.; Menkir, A.; Maziya-Dixon, B. Iron bioavailability from maize and beans: a comparison of human measurements with Caco-2 cell and algorithm predictions Am. J. Clin. Nutr. 2007, 86, 388-396
18. Consaul, J. R.; Lee, K. Extrinsic tagging in iron bioavailability research J. Agric. Food Chem. 1983, 31, 684-689 10.1021/jf00118a002
19. Petry, N.; Egli, I.; Campion, B.; Nielsen, E.; Hurrell, R. Genetic reduction of phytate in common bean (Phaseolus vulgaris L.) seeds increases iron absorption in young women J. Nutr. 2013, 143, 1219-1224 10.3945/jn.113.175067
20. Lin, L.-Z.; Harnly, J. M.; Pastor-Corrales, M. S.; Luthria, D. L. The polyphenolic profiles of common bean (Phaseolus vulgaris L.) Food Chem. 2008, 107, 399-410 10.1016/j.foodchem.2007.08.038
21. Hart, J. J.; Tako, E.; Kochian, L. V.; Glahn, R. P. Identification of black bean (Phaseolus vulgaris L.) polyphenols that inhibit and promote iron uptake by Caco-2 cells J. Agric. Food Chem. 2015, 63, 5950-5956 10.1021/acs.jafc.5b00531
22. Donangelo, C. M.; Woodhouse, L. R.; King, S. M.; Toffolo, G.; Shames, D. M.; Viteri, F. E.; Cheng, Z.; Welch, R. M.; King, J. C. Iron and zinc absorption from two bean (Phaseolus vulgaris L.) genotypes in young women J. Agric. Food Chem. 2003, 51, 5137-5143 10.1021/jf030151w
23. Petry, N.; Hurrell, R. Reply to R. P. Glahn J. Nutr. 2015, 145, 1026-1027 10.3945/jn.115.210658
24. Cook, J. D.; Layrisse, M.; Martinez-Torres, C.; Walker, R.; Monsen, E.; Finch, C. A. Food iron absorption measured by an extrinsic tag J. Clin. Invest. 1972, 51, 805-815 10.1172/JCI106875
25. Harnly, J. M.; Pastor-Corrales, M. A.; Luthria, D. L. Variance in the chemical composition of dry beans determined from UV spectral fingerprints J. Agric. Food Chem. 2009, 57, 8705-8710 10.1021/jf900852y
26. DellaValle, D. M.; Thavarajah, D.; Thavarajah, P.; Vandenberg, A.; Glahn, R. P. Lentil (Lens culinaris L.) as a candidate crop for iron biofortification: is there genetic potential for iron bioavailability? Field Crops Res. 2013, 144, 119-125 10.1016/j.fcr.2013.01.002
27. Miller, D. D.; Schricker, B. R.; Rasmussen, R. R.; Van Campen, D. An in vitro method for estimation of iron availability from meals Am. J. Clin. Nutr. 1981, 34, 2248-2256
28. Rao, N.; Prabhavathi, T. An in vitro method for predicting the bioavailability of iron from foods Am. J. Clin. Nutr. 1978, 31, 169-175
29. Jin, F.; Cheng, Z.; Rutzke, M. A.; Welch, R. M.; Glahn, R. P. Extrinsic labeling method may not accurately measure Fe absorption from cooked pinto beans (Phaseolus vulgaris): comparison of extrinsic and intrinsic labeling of beans J. Agric. Food Chem. 2008, 56, 6881-6885 10.1021/jf800658s
30. 13C breath tests: influence of age, sex and body mass index J. Gastroenterol. Hepatol. 2006, 21, 1832-1838 10.1111/j.1440-1746.2006.04449.x
31. Bornhorst, G. M.; Singh, P. R. Gastric digestion in vivo and in vitro: how the structural aspects of food influence the digestion process Annu. Rev. Food Sci. Technol. 2014, 5, 111-132 10.1146/annurev-food-030713-092346
32. Guerra, A.; Etienne-Mesmin, L.; Livrelli, V.; Denis, S.; Blanquet-Diot, S.; Alric, M. Relevance and challenges in modeling human gastric and small intestinal digestion Trends Biotechnol. 2012, 30, 591-600 10.1016/j.tibtech.2012.08.001
33. Hall, J. E. Chapter 66: Digestion and Absorption in the Gastrointestinal Tract. In Guyton and Hall Textbook of Medical Physiology, 13 th ed.; Elsevier: Philadelphia, PA, USA, 2015.
34. Bjorn-Rasmussen, E.; Hallberg, L.; Walker, R. B. Food iron absorption in man. Isotopic exchange of iron between labeled foods and between a food and an iron salt Am. J. Clin. Nutr. 1973, 26, 1311-1319
35. Tako, E.; Beebe, S. E.; Reed, S.; Hart, J. J.; Glahn, R. P. Polyphenolic compounds appear to limit the nutritional benefit of biofortified higher iron black bean (Phaseolus vulgaris L.) Nutr. J. 2014, 13, 28 10.1186/1475-2891-13-28
36. Finkelstein, J. L.; Mehta, S.; Udipi, S. A.; Ghugre, P. S.; Luna, S. V.; Wenger, M. J.; Murray-Kolb, L. E.; Przybyszewski, E. M.; Haas, J. D. A randomized trial of iron-biofortified pearl millet in school children in India J. Nutr. 2015, 145, 1576-1581 10.3945/jn.114.208009
37. Tako, E.; Reed, S. M.; Budiman, J.; Hart, J. J.; Glahn, R. P. Higher iron pearl millet (Pennisetum glaucum L.) provides more absorbable iron that is limited by increased polyphenolic content Nutr. J. 2015, 14, 11 10.1186/1475-2891-14-11
38. Tako, E.; Reed, S.; Anandaraman, A.; Beebe, S. E.; Hart, J. J.; Glahn, R. P. Studies of cream seeded carioca beans (Phaseolus vulgaris L.) from a Rwandan efficacy trial: in vitro and In vivo screening tools reflect human studies and predict beneficial results from iron biofortified beans PLoS One 2015, 10, e0138479 10.1371/journal.pone.0138479