Intra-amniotic administration and dietary inulin affect the iron status and intestinal functionality of iron-deficient broiler chickens

Poultry Science

Volumn 91, Issue 6, 2012, Pages 1361-1370

  Tako, E ^a   Glahn, R P ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Bioavailability; Chicken; Intestine; Inulin; Iron

Indexed keywords

ANIMALIA; AVES; BACTERIA (MICROORGANISMS); CICHORIUM INTYBUS; GALLUS GALLUS; ZEA MAYS;

BACTERIAL DNA; FERRITIN; HEMOGLOBIN; INULIN; IRON; IRON BINDING PROTEIN; MESSENGER RNA; RNA 16S;

ANIMAL; ARTICLE; BLOOD; CECUM; CHEMISTRY; CHICK EMBRYO; CHICKEN; CLINICAL TRIAL; DRUG EFFECT; DUODENUM; GENE EXPRESSION PROFILING; LIVER; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; CECUM; CHICK EMBRYO; CHICKENS; DNA, BACTERIAL; DUODENUM; FERRITINS; GENE EXPRESSION PROFILING; HEMOGLOBINS; INULIN; IRON; IRON-BINDING PROTEINS; LIVER; MASS SPECTROMETRY; RNA, MESSENGER; RNA, RIBOSOMAL, 16S;

EID: 84930541592     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2011-01864     Document Type: Article

References (64)

1. Amit-Romach, E., D. Sklan, and Z. Uni. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult. Sci. 83:1093-1098.
2. Aoyagi, S., and D. Baker. 1995. Iron requirement of chicks fed a semi purified diet based on casein and soy protein concentrate. Poult. Sci. 74:412-415.
3. Biggs, P., C. M. Parsons, and G. C. Fahey. 2007. The effects of several oligosaccharides on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. Poult. Sci. 86:2327-2336.
4. Bosscher, D., M. Van Caillie-Bertrand, R. Van Cauwenbergh, and H. Deelstra. 2003. Availabilities of calcium, iron, and zinc from dairy infant formulas is affected by soluble dietary fibers and modified starch fractions. Nutrition 19:641-645.
5. Bouglé, D., N. Vaghefi-Vaezzadeh, N. Roland, G. Bouvard, P. Ar-han, F. Bureau, D. Neuville, and J. L. Maubois. 2002. Influence of short-chain fatty acids on iron absorption by proximal colon. Scand. J. Gastroenterol. 37:1008-1011.
6. Bouhnik, Y., A. Attar, F. A. Joly, M. Riottot, F. Dyard, and B. Flourie. 2004a. Lactulose ingestion increases faecal bifidobacterial counts: A randomized double-blind study in healthy humans. Eur. J. Clin. Nutr. 58:462-466.
7. Bouhnik, Y., L. Raskine, G. Simoneau, E. Vicaut, C. Neut, B. Flourie, F. Brouns, and F. R. Bornet. 2004b. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: A double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. Am. J. Clin. Nutr. 80:1658-1664.
8. Collins, J. F., C. A. Franck, K. V. Kowdley, and F. K. Ghishan. 2005. Identification of differentially expressed genes in response to dietary iron deprivation in rat duodenum. Am. J. Physiol. Gastrointest. Liver Physiol. 288:G964-G971.
9. Conly, J. M., and K. Stein. 1992. The production of menaquinones (vitamin K2) by intestinal bacteria and their role in maintaining coagulation homeostasis. Prog. Food Nutr. Sci. 16:307-343.
10. Cummings, J. H., E. W. Pomare, W. J. Branch, C. P. Naylor, and G. T. Macfarlane. 1987. Short-chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221-1227.
11. Daly, K., M. A. Cuff, F. Fung, and S. P. Shirazi-Beechey. 2005. The importance of colonic butyrate transport to the regulation of genes associated with colonic tissue homoeostasis. Biochem. Soc. Trans. 33:733-735.
12. de Wiele, T. V., N. Boon, S. Possemiers, H. Jacobs, and W. Vers-traete. 2004. Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. FEMS Microbiol. Ecol. 51:143-153.
13. Delzenne, N., J. Aertssens, H. Verplaetse, M. Roccaro, and M. Rob-erfroid. 1995. Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci. 57:1579-1587.
14. Foye, O. T., P. R. Ferket, and Z. Uni. 2007. The effects of in ovo feeding arginine, β-hydroxy-β-methyl-butyrate, and protein on jejunal digestive and absorptive activity in embryonic and neonatal turkey poults. Poult. Sci. 86:2343-2349.
15. Foye, O. T., Z. Uni, and P. R. Ferket. 2006. Effect of in ovo feeding egg white protein, β-hydroxy-β-methylbutyrate, and carbohydrates on glycogen status and neonatal growth of turkeys. Poult. Sci. 85:1185-1192.
16. Frenkel, E. P., M. S. McCall, J. S. Reisch, and P. D. Minton. 1972. Analysis of methods for the prediction of normal erythrocyte mass. Am. J. Clin. Pathol. 58:260-271.
17. Gibson, G. R., E. R. Beatty, X. Wang, and J. H. Cummings. 1995. Selective stimulation of bifidobacteria in the human colon by oli-gofructose and inulin. Gastroenterology 108:975-982.
18. Haas, J. D., J. L. Beard, L. E. Murray-Kolb, A. M. del Mundo, A. Felix, and G. B. Gregorio. 2005. Iron-biofortified rice improves the iron stores of nonanemic Filipino women. J. Nutr. 135:2823-2830.
19. Hopkins, M. J., and G. T. Macfarlane. 2003. Nondigestible oligosac-charides enhance bacterial colonization resistance against Clos-tridium difficile in vitro. Appl. Environ. Microbiol. 69:1920-1927.
20. Høverstad, T., and A. Bjorneklett. 1984. Short-chain fatty acids and bowel functions in man. Scand. J. Gastroenterol. 19:1059-1065.
21. Høverstad, T., A. Bjorneklett, T. Midtvedt, O. Fausa, and T. Bohm-er. 1984a. Short-chain fatty acids in the proximal gastrointestinal tract of healthy subjects. Scand. J. Gastroenterol. 19:1053-1058.
22. Høverstad, T., O. Fausa, A. Bjorneklett, and T. Bohmer. 1984b. Short-chain fatty acids in the normal human feces. Scand. J. Gastroenterol. 19:375-381.
23. Kolida, S., K. Tuohy, and G. R. Gibson. 2002. Prebiotic effects of inulin and oligofructose. Br. J. Nutr. 87(Suppl. 2):S193-S197.
24. Langendijk, P. S., F. Schut, G. J. Jansen, G. C. Raangs, G. R. Kam-phuis, M. H. Wilkinson, and G. W. Welling. 1995. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl. Environ. Microbiol. 61:3069-3075.
25. Leong, L. M., B. H. Tan, and K. K. Ho. 1992. A specific stain for the detection of nonheme iron proteins in polyacrylamide gels. Anal. Biochem. 207:317-320.
26. Lopez, H. W., C. Coudray, M. A. Levrat-Verny, C. Demigné, and C. Rémésy. 2000. Fructooligosaccharides enhance mineral apparent absorption and counteract the deleterious effects of phytic acid on mineral homeostasis in rats. J. Nutr. Biochem. 11:500-508.
27. Ludwiczek, S., I. Theurl, E. Artner-Dworzak, M. Chorney, and G. Weiss. 2004. Duodenal HFE expression and hepcidin levels determine body iron homeostasis: Modulation by genetic diversity and dietary iron availability. J. Mol. Med. 82:373-382.
28. Mentschel, J., and R. Claus. 2003. Increased butyrate formation in the pig colon by feeding raw potato starch leads to a reduction of colonocyte apoptosis and a shift to the stem cell compartment. Metabolism 52:1400-1405.
29. Mete, A., Y. R. Van Zeeland, A. B. Vaandrager, J. E. van Dijk, J. J. Marx, and G. M. Dorrestein. 2005. Partial purification and characterization of ferritin from the liver and intestinal mucosa of chickens, turtledoves and mynahs. Avian Pathol. 34:430-434.
30. NRC. 1994. Nutrition Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
31. Ohta, A., Y. Motohashi, K. Sakai, M. Hirayama, T. Adachi, and K. Sakuma. 1998. Dietary fructooligosaccharides increase calcium absorption and levels of mucosal calbindin-D9k in the large intestine of gastrectomized rats. Scand. J. Gastroenterol. 33:1062-1068.
32. Ortiz, L. T., M. L. Rodríguez, C. Alzueta, A. Rebolé, and J. Trevi-ño. 2009. Effect of inulin on growth performance, intestinal tract sizes, mineral retention and tibial bone mineralisation in broiler chickens. Br. Poult. Sci. 50:325-332.
33. Passaniti, A., and T. F. Roth. 1989. Purification of chicken liver fer-ritin by two novel methods and structural comparison with horse spleen ferritin. Biochem. J. 258:413-419.
34. Patterson, J. K., M. A. Rutzke, S. L. Fubini, R. P. Glahn, R. M. Welch, X. Lei, and D. D. Miller. 2009. Dietary inulin supplementation does not promote colonic iron absorption in a porcine model. J. Agric. Food Chem. 57:5250-5256.
35. Patterson, J. K., K. Yasuda, R. M. Welch, D. D. Miller, and X. Lei. 2010. Supplemental dietary inulin of variable chain lengths alters intestinal bacterial populations in young pigs. J. Nutr. 140:2158-2161.
36. Pietrangelo, A., G. Casalgrandi, D. Quaglino, R. Gualdi, D. Conte, S. Milani, G. Montosi, L. Cesarini, E. Ventura, and G. Cairo. 1995. Duodenal ferritin synthesis in genetic hemochromatosis. Gastroenterology 108:208-217.
37. Rebolé, A., L. T. Ortiz, M. L. Rodríguez, C. Alzueta, J. Treviño, and S. Velasco. 2010. Effects of inulin and enzyme complex, individually or in combination, on growth performance, intestinal microflora, cecal fermentation characteristics, and jejunal histo-morphology in broiler chickens fed a wheat- and barley-based diet. Poult. Sci. 89:276-286.
38. Rehman, H., C. Rosenkranz, J. Böhm, and J. Zentek. 2007. Dietary inulin affects the morphology but not the sodium-dependent glucose and glutamine transport in the jejunum of broilers. Poult. Sci. 86:118-122.
39. Roberfroid, M. B., J. A. Van Loo, and G. R. Gibson. 1998. The bifi-dogenic nature of chicory root inulin and its hysrolysis products. J. Nutr. 128:11-19.
40. Sáiz, M., M. Marti, M. Mitjavila, and J. Planas. 1993. Iron absorption by small intestine of chickens. Biol. Trace Elem. Res. 36:7-14.
41. Scholz-Ahrens, K. E., Y. Açil, and J. Schrezenmeir. 2002. Effect of oligofructose or dietary calcium on repeated calcium and phosphorus balances, bone mineralization and trabecular structure in ovariectomized rats. Br. J. Nutr. 88:365-377.
42. Scholz-Ahrens, K. E., and J. Schrezenmeir. 2002. Inulin, oligofruc-tose and mineral metabolism-Experimental data and mechanism. Br. J. Nutr. 87(Suppl. 2):S179-186.
43. Smirnov, A., E. Tako, P. R. Ferket, and Z. Uni. 2006. Mucin gene expression and mucin content in the chicken intestinal goblet cells are affected by in ovo feeding of carbohydrates. Poult. Sci. 85:669-673.
44. Sturkie, P. 2000. Avian Physiology. Academic Press, San Diego, CA.
45. Tako, E., M. W. Blair, and R. P. Glahn. 2011. Biofortified red mottled beans (Phaseolus vulgaris L.) in a maize and bean diet provide more bioavailable iron than standard red mottled beans: Studies in poultry (Gallus gallus) and an in vitro digestion/Caco-2 model. Nutr. J. 10:113-123.
46. Tako, E., P. R. Ferket, and Z. Uni. 2004. Effects of in ovo feeding of carbohydrates and β-hydroxy-β-methylbutyrate on the development of chicken intestine. Poult. Sci. 83:2023-2028.
47. Tako, E., P. R. Ferket, and Z. Uni. 2005. Changes in chicken intestinal zinc exporter mRNA expression and small intestinal functionality following intra-amniotic zinc-methionine administration. J. Nutr. Biochem. 16:339-346.
48. Tako, E., and R. P. Glahn. 2010. White beans provide more bioavail-able iron than red beans: Studies in poultry (Gallus gallus) and an in vitro digestion/Caco-2 model. Int. J. Vitam. Nutr. Res. 80:416-429.
49. Tako, E., and R. P. Glahn. 2011. Iron status of the late term broiler (Gallus gallus). Embryo and hatchling. Int. J. Poult. Sci. 10:42-48.
50. Tako, E., R. P. Glahn, R. M. Welch, X. Lei, K. Yasuda, and D. D. Miller. 2008. Dietary inulin affects the expression of intestinal en-terocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Br. J. Nutr. 99:472-480.
51. Tako, E., J. M. Laparra, R. P. Glahn, R. M. Welch, X. Lei, S. Beebe, and D. D. Miller. 2009. Biofortified black beans in a maize and bean diet provide more bioavailable iron to piglets than standard black beans. J. Nutr. 139:305-309.
52. Tako, E., M. A. Rutzke, and R. P. Glahn. 2010. Using the domestic chicken (Gallus gallus) as an in vivo model for iron bioavailabil-ity. Poult. Sci. 89:514-521.
53. Tan, S. Y., C. K. Yeung, E. Tako, R. P. Glahn, R. M. Welch, X. Lei, and D. D. Miller. 2008. Iron bioavailability to piglets from red and white common beans (Phaseolus vulgaris). J. Agric. Food Chem. 56:5008-5014.
54. Tzortzis, G., A. K. Goulas, J. M. Gee, and G. R. Gibson. 2005. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J. Nutr. 135:1726-1731.
55. Uni, Z., P. R. Ferket, E. Tako, and O. Kedar. 2005. In ovo feeding improves energy status of late-term chicken embryos. Poult. Sci. 84:764-770.
56. Verdonk, J. M., S. B. Shim, P. van Leeuwen, and M. W. Verstegen. 2005. Application of inulin-type fructans in animal feed and pet food. Br. J. Nutr. 93(Suppl. 1):S125-S138.
57. Wang, R. F., W. W. Cao, and C. E. Cerniglia. 1996. PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl. Environ. Microbiol. 62:1242-1247.
58. Xu, Z. R., C. H. Hu, M. S. Xia, X. A. Zhan, and M. Q. Wang. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 82:1030-1036.
59. Yason, C. V., B. A. Summers, and K. A. Schat. 1987. Pathogenesis of rotavirus infection in various age groups of chickens and turkeys: Pathology. Am. J. Vet. Res. 48:927-938.
60. Yasuda, K., K. R. Roneker, D. D. Miller, R. M. Welch, and X. G. Lei. 2006. Supplemental dietary inulin affects bioavailability of iron present in corn and soybean meal to young pigs. J. Nutr. 136:3033-3038.
61. Yusrizal, G., and T. C. Chen. 2003. Effect of adding chicory fructans in feed on broiler growth performance, serum cholesterol and intestine length. Int. J. Poult. Sci. 2:188-194.
62. Zafar, T. A., C. M. Weaver, Y. Zhao, B. R. Martin, and M. E. Wastney. 2004. Nondigestible oligosaccharides increase calcium absorption and suppress bone resorption in ovariectomized rats. J. Nutr. 134:399-402.
63. Zduńczyk, Z., J. Juśkiewicz, J. Stańczuk, J. Jankowski, and B. Król. 2007. Effect of akestose and nystose preparation on growth performance and gastrointestinal tract function of turkeys. Poult. Sci. 86:1133-1139.
64. Zhu, X. Y., T. Zhong, Y. Pandya, and R. D. Joerger. 2002. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl. Environ. Microbiol. 68:124-137.