Diets high in resistant starch and arabinoxylan modulate digestion processes and SCFA pool size in the large intestine and faecal microbial composition in pigs

British Journal of Nutrition

Volumn 112, Issue 11, 2014, Pages 1837-1849

  Nielsen, Tina S ^a   Lærke, Helle N ^a   Theil, Peter K ^a   Sørensen, Jens F ^b   Saarinen, Markku ^b   Forssten, Sofia ^b   Bach Knudsen, Knud E ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b DUPONT COMPANY   (United States)

Author keywords

Arabinoxylan; Microbial composition; Pigs; Resistant starch; SCFA

Indexed keywords

ARABINOSE; ARABINOXYLAN; BUTYRIC ACID; FAT; NON STARCH POLYSACCHARIDE; POLYSACCHARIDE; PROTEIN; RESISTANT STARCH; SHORT CHAIN FATTY ACID; STARCH; UNCLASSIFIED DRUG; XYLOSE; CARBOHYDRATE DIET; VOLATILE FATTY ACID; XYLAN;

ANIMAL EXPERIMENT; ARTICLE; ASCENDING COLON; BIFIDOBACTERIUM; BLAUTIA; BLAUTIA COCCOIDES; CECUM; CHEMICAL COMPOSITION; CONTROLLED STUDY; DESCENDING COLON; DIETARY FIBER; DIGESTION; EUBACTERIUM; EUBACTERIUM RECTALE; FAECALIBACTERIUM PRAUSNITZII; FECES MICROFLORA; FEMALE; HIGH FIBER DIET; INTESTINE TRANSIT TIME; LACTOBACILLUS; LIPID DIET; NONHUMAN; NUTRIENT UPTAKE; PARTICLE SIZE; ROSEBURIA INTESTINALIS; SPECIES COMPOSITION; SWINE; WESTERN DIET; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; ANIMAL; ANIMAL FOOD; ANIMAL MODEL; CARBOHYDRATE DIET; FECES; GASTROINTESTINAL TRANSIT; LARGE INTESTINE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PIG;

BIFIDOBACTERIUM; EUBACTERIUM RECTALE; FAECALIBACTERIUM PRAUSNITZII; LACTOBACILLUS; ROSEBURIA INTESTINALIS; SUIDAE;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET, WESTERN; DIETARY CARBOHYDRATES; DIETARY FIBER; DIGESTION; FATTY ACIDS, VOLATILE; FECES; FEMALE; GASTROINTESTINAL TRANSIT; INTESTINE, LARGE; MODELS, ANIMAL; STARCH; SUS SCROFA; XYLANS;

EID: 84925581144     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S000711451400302X     Document Type: Article

References (60)

1. Lipkin M, Reddy B, Newmark H, et al. (1999) Dietary factors in human colorectal cancer. Annu Rev Nutr 19, 545-586.
2. Spooren CE, Pierik MJ, Zeegers MP, et al. (2013) Review Article: the association of diet with onset and relapse in patients with inflammatory bowel disease. Aliment Pharmacol Ther 38, 1172-1187.
3. Wong JM, de Souza R, Kendall CW, et al. (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40, 235-243.
4. Leonel AJ & Alvarez-Leite JI (2012) Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care 15, 474-479.
5. Perrin P, Pierre F, Patry Y, et al. (2001) Only fibres promoting a stable butyrate producing colonic ecosystem decrease the rate of aberrant crypt foci in rats. Gut 48, 53-61.
6. Toden S, Bird AR, Topping DL, et al. (2007) Dose-dependent reduction of dietary protein-induced colonocyte DNA damage by resistant starch in rats correlates more highly with caecal butyrate than with other short chain fatty acids. Cancer Biol Ther 6, 253-258.
7. Kovarik JJ, Tillinger W, Hofer J, et al. (2011) Impaired antiinflammatory efficacy of n-butyrate in patients with IBD. Eur J Clin Invest 41, 291-298.
8. Hamer HM, Jonkers DM, Bast A, et al. (2009) Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr 28, 88-93.
9. Clarke JM, Young GP, Topping DL, et al. (2012) Butyrate delivered by butyrylated starch increases distal colonic epithelial apoptosis in carcinogen-treated rats. Carcinogenesis 33, 197-202.
10. Canani RB, Di Costanzo M & Leone L (2012) The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics 4, 4.
11. Fung KY, Cosgrove L, Lockett T, et al. (2012) A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate. Br J Nutr 108, 820-831.
12. The European Commission (2008) EU and Codex Definitions of dietary fibre - text with comments by N.G. Asp and S. Bryngelsson. http://www.healthgrain.org/webfm-send/48 (accessed March 2014).
13. Bird AR, Conlon MA, Christophersen CT, et al. (2010) Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benef Microbes 1, 423-431.
14. Haenen D, Zhang J, Souza da Silva C, et al. (2013) A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. J Nutr 143, 274-283.
15. Hamer HM, Jonkers D, Venema K, et al. (2008) Review Article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27, 104-119.
16. Jackson-Thompson J, Ahmed F, German RR, et al. (2006) Descriptive epidemiology of colorectal cancer in the United States, 1998-2001. Cancer 107, 1103-1111.
17. Kolida S, Tuohy K & Gibson GR (2002) Prebiotic effects of inulin and oligofructose. Br J Nutr 87, Suppl. 2, S193-S197.
18. Izydorczyk MS & Biliaderis CG (1995) Cereal arabinoxylans: advances in structure and physicochemical properties. Carbohydr Polym 28, 33-48.
19. Glitso LV, Gruppen H, Schols HA, et al. (1999) Degradation of rye arabinoxylans in the large intestine of pigs. J Sci Food Agric 79, 961-969.
20. Nielsen KL, Hartvigsen ML, Hedemann MS, et al. (2014) Similar metabolic responses in pigs and humans to breads with different contents and compositions of dietary fibers: a metabolomics study. Am J Clin Nutr 99, 941-949.
21. Miller ER & Ullrey DE (1987) The pig as a model for human nutrition. Annu Rev Nutr 7, 361-382.
22. Damen B, Cloetens L, Broekaert WF, et al. (2012) Consumption of breads containing in situ-produced arabinoxylan oligosaccharides alters gastrointestinal effects in healthy volunteers. J Nutr 142, 470-477.
23. Bach Knudsen KE, Serena A, Kjaer AK, et al. (2005) Rye bread enhances the production and plasma concentration of butyrate but not the plasma concentrations of glucose and insulin in pigs. J Nutr 135, 1696-1704.
24. Choct M, Selby EAD, Cadogan DJ, et al. (2004) Effects of particle size, processing, and dry or liquid feeding on performance of piglets. Aust J Agric Res 55, 237-245.
25. Ingerslev AK, Theil PK, Hedemann MS, et al. (2014) Resistant starch and arabinoxylan augment SCFA absorption, but affect postprandial glucose and insulin responses differently. Br J Nutr 111, 1564-1576.
26. AOAC (1990) Official Methods of Analysis of AOAC International, 15th ed. Arlington, VA: AOAC International.
27. Hansen B (1989) Determination of nitrogen as elementary N, and alternative to Kjeldahl. Acta Agric Scand 39, 113-118.
28. Stoldt W (1952) Worslag zur verinheitlichung der fettbestimmung in lebensmitteln (Suggestion to standardise the determination of fat in foodstuffs). F Seif Anst 54, 206-207.
29. Larsson K & Bengtsson S (1983) Bestämning av lätttilgängeliga kolhydrater i växtmaterial (Determination of readily available carbohydrates in plant material). In National Laboratory of Agricultural Chemistry Methods Report no. 22, vol. 22, Uppsala: National Laboratory of Agricultural Chemistry.
30. Bach Knudsen KE (1997) Carbohydrate and lignin contents of plant materials used in animal feeding. Anim Feed Sci Technol 67, 319-338.
31. Kasprzak MM, Lærke HN & Bach Knudsen KE (2012) Effects of isolated and complex dietary fiber matrices in breads on carbohydrate digestibility and physiochemical properties of ileal effluent from pigs. J Agric Food Chem 60, 12469-12476.
32. Englyst HN & Cummings JH (1984) Simplified method for the measurement of total non-starch polysaccharides by gas-liquid-chromatography of constitute sugars as alditol acetate. Analyst 109, 937-942.
33. Theander O & A°man P (1979) Studies on dietary-fibers. 1. Analysis and chemical characterization of water-soluble and water-insoluble dietary-fibers. Swe J Agric Res 9, 97-106.
34. McCleary BV & Glennie-Holmes M (1985) Enzymatic quantification of (1 → 3)(1 → 4)-β-D-glucan in barley and malt. J Inst Brew 91, 285-295.
35. Schürch AF, Lloyd LE & Crampton EW (1950) The use of chromic oxide as an index for determining digestibility of a diet. J Nutr 41, 629-636.
36. Jensen MT, Cox RP & Jensen BB (1995) Microbial production of skatole in the hindgut of pigs given different diets and its relation to skatole deposition in the back fat. Anim Sci 61, 293-304.
37. Lahtinen SJ, Forssten S, Aakko J, et al. (2012) Probiotic cheese containing Lactobacillus rhamnosus HN001 and Lactobacillus acidophilus NCFM(R) modifies subpopulations of fecal lactobacilli and Clostridium difficile in the elderly. Age (Dordr) 34, 133-143.
38. Rinttila T, Kassinen A, Malinen E, et al. (2004) 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 97, 1166-1177.
39. Makivuokko H, Nurmi J, Nurminen P, et al. (2005) In vitro effects on polydextrose by colonic bacteria and caco-2 cell cyclooxygenase gene expression. Nutr Cancer 52, 94-104.
40. Russell WR, Hoyles L, Flint HJ, et al. (2013) Colonic bacterial metabolites and human health. Curr Opin Microbiol 16, 246-254.
41. Brahe LK, Astrup A & Larsen LH (2013) Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes Rev 14, 950-959.
42. Bach Knudsen KE & Lærke HN (2010) Rye arabinoxylans: molecular structure, physiochemical properties and physiological effects in the gastrointestinal tract. Cereal Chem 87, 353-362.
43. Annison G & Topping DL (1994) Nutritional role of resistant starch: chemical structure vs physiological function. Annu Rev Nutr 14, 297-320.
44. Glitso LV, Brunsgaard G, Hojsgaard S, et al. (1998) Intestinal degradation in pigs of rye dietary fibre with different structural characteristics. Br J Nutr 80, 457-468.
45. Rose DJ, Patterson JA & Hamaker BR (2010) Structural differences among alkali-soluble arabinoxylans from maize (Zea mays), rice (Oryza sativa), and wheat (Triticum aestivum) brans influence human fecal fermentation profiles. J Agric Food Chem 58, 493-499.
46. Higgins JA & Brown IL (2013) Resistant starch: a promising dietary agent for the prevention/treatment of inflammatory bowel disease and bowel cancer. Curr Opin Gastroenterol 29, 190-194.
47. Jonathan MC, Haenen D, Souza da Silva C, et al. (2013) Influence of a diet rich in resistant starch on the degradation of non-starch polysaccharides in the large intestine of pigs. Carbohydr Polym 93, 232-239.
48. Giuberti G, Gallo A, Moschini M, et al. (2013) In vitro production of short-chain fatty acids from resistant starch by pig faecal inoculum. Animal 7, 1446-1453.
49. McOrist AL, Miller RB, Bird AR, et al. (2011) Fecal butyrate levels vary widely among individuals but are usually increased by a diet high in resistant starch. J Nutr 141, 883-889.
50. Le Gall M, Serena A, Jorgensen H, et al. (2009) The role of whole-wheat grain and wheat and rye ingredients on the digestion and fermentation processes in the gut - a model experiment with pigs. Br J Nutr 102, 1590-1600.
51. Johnson IT (1992) The influence of dietary fibre on lipid digestion and absorption. In Dietary Fibre - A Component of Food. Nutritional Function in Health and Disease, pp. 167-180. New York, NY: Springer.
52. Neyrinck AM, Possemiers S, Druart C, et al. (2011) Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS ONE 6, e20944.
53. Regmi PR, Metzler-Zebeli BU, Ganzle MG, et al. (2011) Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes bifidobacteria in pigs. J Nutr 141, 1273-1280.
54. Theil PK, Jorgensen H, Serena A, et al. (2011) Products deriving from microbial fermentation are linked to insulinaemic response in pigs fed breads prepared from whole-wheat grain and wheat and rye ingredients. Br J Nutr 105, 373-383.
55. Bach Knudsen KE & Hansen I (1991) Gastrointestinal implications in pigs of wheat and oat fractions. 1. Digestibility and bulking properties of polysaccharides and other major constituents. Br J Nutr 65, 217-232.
56. Marsono Y, Illman RJ, Clarke JM, et al. (1993) Plasma lipids and large bowel volatile fatty acids in pigs fed on white rice, brown rice and rice bran. Br J Nutr 70, 503-513.
57. Govers MJ, Gannon NJ, Dunshea FR, et al. (1999) Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs. Gut 45, 840-847.
58. Yang J, Martinez I, Walter J, et al. (2013) In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe 23, 74-81.
59. Kaur A, Rose DJ, Rumpagaporn P, et al. (2011) In vitro batch fecal fermentation comparison of gas and short-chain fatty acid production using "slowly fermentable" dietary fibers. J Food Sci 76, H137-H142.
60. van den Abbeele P, Venema K, Van De Wiele T, et al. (2013) Different human gut models reveal the distinct fermentation patters of arabinoxylan versus inulin. J Agric Food Chem 61, 9819-9827.