Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes bifidobacteria in pigs

Journal of Nutrition

Volumn 141, Issue 7, 2011, Pages 1273-1280

  Regmi, Prajwal R ^a   Metzler Zebeli, Barbara U ^a   Gänzle, Michael G ^a   van Kempen, Theo A T G ^b,c   Zijlstra, Ruurd T ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Provimi Research and Innovation Centre   (Netherlands)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOSE; BUTYRIC ACID; STARCH;

ARTICLE; BIFIDOBACTERIUM; CARBOHYDRATE DIET; DIGESTION; ENTEROBACTERIACEAE; FECES; FERMENTATION; GENE DOSAGE; IN VITRO STUDY; LACTOBACILLUS; NONHUMAN; SWINE;

AMYLOSE; ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BIFIDOBACTERIUM; BUTYRATES; DIGESTION; FERMENTATION; ILEUM; INTESTINAL ABSORPTION; METAGENOME; STARCH; SUS SCROFA;

BIFIDOBACTERIUM; ENTEROBACTERIACEAE; LACTOBACILLUS; SUIDAE;

EID: 79960319428     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.111.140509     Document Type: Article

References (62)

1. Topping DL, Gooden JM, Brown IL, Biebrick DA, McGrath L, Trimble RP, Choct M, Illman RJ. A high amylose (amylomaize) starch raises proximal large bowel starch and increases colon length in pigs. J Nutr. 1997;127:615-22.
2. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401-12.
3. Morita T, Tanabe H, Takahashi K, Sugiyama K. Ingestion of resistant starch protects endotoxin influx from the intestinal tract and reduces D-galactosamine-induced liver injury in rats. J Gastroenterol Hepatol. 2004;19:303-13.
4. Cummings JH, Englyst HN. Measurement of starch fermentation in the human large intestine. Can J Physiol Pharmacol. 1991;69:121-9.
5. Roediger WEW. The starved colon: diminished mucosal nurition, diminished absorption, and colitis. Dis Colon Rectum. 1990;33:858-62.
6. Scheppach W. Effects of short chain fatty acids on gut morphology and function. Gut. 1994;35:S35-8.
7. Bauer-Marinovic M, Florian S, Muller-Schmehl K, Glatt H, Jacobasch G. Dietary resistant starch type 3 prevents tumor induction by 1,2-dimethylhydrazine and alters proliferation, apoptosis and dedifferentiation in rat colon. Carcinogenesis. 2006;27:1849-59.
8. Scheppach W, Luehrs H, Menzel T. Beneficial health effects of lowdigestible carbohydrate consumption. Br J Nutr. 2001;85 Suppl 1:S23-30.
9. Bird AR, Vuaran M, Brown I, Topping DL. Two high-amylose maize starches with different amounts of resistant starch vary in their effects on fermentation, tissue and digesta mass accretion, and bacterial populations in the large bowel of pigs. Br J Nutr. 2007;97:134-44.
10. Brown I, Warhurst M, Arcot J, Playne M, Illman RJ, Topping DL. Fecal numbers of bifidobacteria are higher in pigs fed bifidobacterium longum with a high amylose cornstarch than with a low amylose cornstarch. J Nutr. 1997;127:1822-7.
11. Kleessen B, Stoof G, Proll J, Schmiedl D, Noack J, Blaut M. Feeding resistant starch affects fecal and cecal microflora and short-chain fatty acids in rats. J Anim Sci. 1997;75:2453-62.
12. Wang X, Brown IL, Khaled D, Mahoney MC, Evans AJ, Conway PL. Manipulation of colonic bacteria and volatile fatty acid production by dietary high amylose maize (amylomaize) starch granules. J Appl Microbiol. 2002;93:390-7.
13. Higgins JA. Resistant starch: metabolic effects and potential health benefits. J AOAC Int. 2004;87:761-8.
14. Englyst KN, Englyst HN. Carbohydrate bioavailability. Br J Nutr. 2005;94:1-11.
15. Singh J, Dartois A, Kaur L. Starch digestibility in food matrix: a review. Trends Food Sci Technol. 2010;21:168-80.
16. Regmi PR, van Kempen TA, Matte JJ, Zijlstra RT. Starch with high amylose and low in vitro digestibility increases short-chain fatty acid absorption, reduces peak insulin secretion, and modulates incretin secretion in pigs. J Nutr. 2011;141:398-405.
17. van Kempen TA, Regmi PR, Matte JJ, Zijlstra RT. In vitro starch digestion kinetics, corrected for estimated gastric emptying, predict portal glucose appearance in pigs. J Nutr. 2010;140:1227-33.
18. Canadian Council on Animal Care. Guide to the care and use of experimental animals. 2nd ed. 1st vol. Ottawa: Canadian Council on Animal Care; 1998.
19. de Lange CF, Sauer WC, Mosenthin R, Souffrant WB. The effect of feeding different protein-free diets on the recovery and amino acid composition of endogenous protein collected from the distal ileum and feces in pigs. J Anim Sci. 1989;67:746-54.
20. Sauer WC, Jørgensen H, Berzins R. A modified nylon bag technique for determining apparent digestibilities of protein in feedstuffs for pigs. Can J Anim Sci. 1983;63:233-7.
21. NRC. Nutrient requirements of swine. 10th rev. ed. Washington, DC: National Academies Press; 1998.
22. AOAC. Official methods of analysis of the association of official analytical chemists. 17th ed. Arlington (VA): AOAC; 2006.
23. Htoo JK, Araiza BA, Sauer WC, Rademacher M, Zhang Y, Cervantes M, Zijlstra RT. Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs. J Anim Sci. 2007;85:3303-12.
24. Metzler-Zebeli BU, Hooda S, Pieper R, Zijlstra RT, van Kessel AG, Mosenthin R, Gänzle MG. Non-starch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract. Appl Environ Microbiol. 010;76:3692-701.
25. Lee DH, Zo YG, Kim SJ. Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism. Appl Environ Microbiol. 1996;62:3112-20.
26. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol. 2001;67:2578-85.
27. Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol. 2002;68:114-23.
28. Rinttila 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.
29. Nubel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, LudwigW, Backhaus H. Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol. 1996;178:5636-43.
30. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998;64:3336-45.
31. Bartosch S, Fite A, Macfarlane GT, McMurdo ME. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol. 2004;70:3575-81.
32. Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70:7220-8.
33. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R. Development of 16S rRNA-gene-targeted groupspecific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol. 2002;68:5445-51.
34. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ. Restricted distribution of the butyrate kinase pathway among butyrateproducing bacteria from the human colon. J Bacteriol. 2004;186:2099-106.
35. Louis P, Flint HJ. Development of a semiquantitative degenerate realtime pcr-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Appl Environ Microbiol. 2007;73:2009-12.
36. Ketabi A, Dieleman LA, Gänzle MG. Influence of isomalto-oligosaccharides on intestinal microbiota in rats. J Appl Microbiol. 2011;110:1297-306.
37. Muyzer G, Smalla K. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek. 1998;73:127-41.
38. Pluske JR, Montagne L, Cavaney FS, Mullan BP, Pethick DW, Hampson DJ. Feeding different types of cooked white rice to piglets after weaning influences starch digestion, digesta and fermentation characteristics and the faecal shedding of b-haemolytic Escherichia coli. Br J Nutr. 2007; 97:298-306.
39. Pond WG, Lei XG. Of pigs and people. In: Lewis AJ, Southern LL, editors. Swine nutrition. 2nd ed. New York: CRC Press; 2001. p. 3-18.
40. Lee JE, Lee S, Sung J, Ko G. Analysis of human and animal fecal microbiota for microbial source tracking. ISME J. 2011;5:362-5.
41. Spurlock ME, Gabler NK. The development of porcine models of obesity and the metabolic syndrome. J Nutr. 2008;138:397-402.
42. Kim WK, Chung MK, Kang NE, Kim MH, Park OJ. Effect of resistant starch from corn or rice on glucose control, colonic events, and blood lipid concentrations in streptozotocin-induced diabetic rats. J Nutr Biochem. 2003;14:166-72.
43. de Deckere EA, Kloots WJ, van Amelsvoort JM. Both raw and retrograded starch decrease serum triacylglycerol concentration and fat accretion in the rat. Br J Nutr. 1995;73:287-98.
44. Kishida T, Nogami H, Himeno S, Ebihara K. Heat moisture treatment of high amylose cornstarch increases its resistant starch content but not its physiologic effects in rats. J Nutr. 2001;131:2716-21.
45. de Deckere EA, Kloots WJ, van Amelsvoort JM. Resistant starch decreases serum total cholesterol and triacylglycerol concentrations in rats. J Nutr. 993;123:2142-51.
46. Verbeek MJ, De Deckere EA, Tijburg LB, Van Amelsvoort JM, Beynen AC. Influence of dietary retrograded starch on the metabolism of neutral steroids and bile acids in rats. Br J Nutr. 1995;74:807-20.
47. Phillips J, Muir JG, Birkett A, Lu ZX, Jones GP, O'Dea K, Young GP. Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. Am J Clin Nutr. 1995;62:121-30.
48. Saito K, Ito T, Kuribayashi T, Mochida K, Nakakuki T, Shibata M, Sugawara M. Effect of raw and heat-moisture treated high-amylose corn starch on fermentation by the rat cecal bacteria. Starch/Stä rke. 2001;53:424-30.
49. Bird AR, Vuaran M, Crittenden R, Hayakawa T, Playne MJ, Brown IL, Topping DL. Comparative effects of a high-amylose starch and a fructooligosaccharide on fecal bifidobacteria numbers and short-chain fatty acids in pigs fed Bifidobacterium animalis. Dig Dis Sci. 2009;54: 947-54.
50. Takeda H, Kiriyama S. Correlation between the physical properties of dietary fibers and their protective activity against amaranth toxicity in rats. J Nutr. 979;109:388-96.
51. Sun T, Lærke HN, Jørgensen H, Knudsen KEB. The effect of extrusion cooking of different starch sources on the in vitro and in vivo digestibility in growing pigs. Anim Feed Sci Technol. 2006;131:66-85.
52. Jenkins DJ, Vuksan V, Kendall CW, Wursch P, Jeffcoat R, Waring S, Mehling CC, Vidgen E, Augustin LS, et al. Physiological effects of resistant starches on fecal bulk, short chain fatty acids, blood lipids and glycemic index. J Am Coll Nutr. 1998;17:609-16.
53. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol. 1991;70: 443-59.
54. Sharp R, Macfarlane GT. Chemostat enrichments of human feces with resistant starch are selective for adherent butyrate-producing clostridia at high dilution rates. Appl Environ Microbiol. 2000;66:4212-21.
55. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol. 2000;66:1654-61.
56. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 007;102:1197-208.
57. Diez-Gonzalez F, Bond DR, Jennings E, Russell JB. Alternative schemes of butyrate production in Butyrivibrio fibrisolvens and their relationship to acetate utilization, lactate production, and phylogeny. Arch Microbiol. 1999;171:324-30.
58. Ryan SM, Fitzgerald GF, van Sinderen D. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl Environ Microbiol. 2006;72:5289-96.
59. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE. 2010;5:e15046.
60. de la Cal MA, Cerda' E, Abella A, Garcia-Hierro P. Classification of micro-organisms according to their pathogenicity. In: van Saene HKF, De La Cal MA, Silvestri L, editors. Topics in anaesthesia and critical care: infection control in the intensive care unit. 2nd ed. Milan: Springer; 2005. p. 49-60.
61. Schierack P, Walk N, Reiter K, Weyrauch KD, Wieler LH. Composition of intestinal Enterobacteriaceae populations of healthy domestic pigs. Microbiology. 2007;153:3830-7.
62. Baghurst PA, Baghurst KI, Record SJ. Dietary fibre, non-starch polysaccharides and resistant starch: a review. Food Aust. 1996;48:S3-35.