A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine1-3

Journal of Nutrition

Volumn 143, Issue 3, 2013, Pages 274-283

  Haenen, Daniëlle ^a   Zhang, Jing ^a   da Silva, Carol Souza ^a   Bosch, Guido ^a   van der Meer, Ingrid M ^a   van Arkel, Jeroen ^a   van den Borne, Joost J G C ^a   Gutiérrez, Odette Pérez ^a   Smidt, Hauke ^a   Kemp, Bas ^a   Müller, Michael ^a   Hooiveld, Guido J E J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; GLUCAGON; MONOCARBOXYLATE TRANSPORTER 1; RESISTANT STARCH; SHORT CHAIN FATTY ACID; STARCH; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CARBOHYDRATE DIET; CONTROLLED STUDY; ESCHERICHIA COLI; EXPERIMENTAL PIG; FAECALIBACTERIUM PRAUSNITZII; FEMALE; GENE EXPRESSION; MICROFLORA; NONHUMAN; PILOT STUDY; PSEUDOMONAS; SATIETY;

ANIMALS; BACTERIA; CECUM; COLON; DIET; DIETARY CARBOHYDRATES; FATTY ACIDS, VOLATILE; FEMALE; GENE EXPRESSION; GLUCAGON; INTESTINAL MUCOSA; INTESTINE, LARGE; LIPID METABOLISM; METAGENOME; MONOCARBOXYLIC ACID TRANSPORTERS; STARCH; SWINE;

EID: 84874710218     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.112.169672     Document Type: Article

References (63)

1. Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. 2010;303:235-41.
2. Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999-2006. Diabetes Care. 2011;34:216-9.
3. Amine E, Baba N, Belhadj M, Deurenberg-Yap M, Djazayery A, Forrester T, Galuska D, Herman S, James W, Buyamba J, et al. Diet, nutrition and the prevention of chronic diseases. Geneva: World Health Organization; 2003. Report No.: 0512-3054.
4. Feldeisen SE, Tucker KL. Nutritional strategies in the prevention and treatment of metabolic syndrome. Appl Physiol Nutr Metab. 2007;32: 46-60.
5. Lattimer JM, Haub MD. Effects of dietary fiber and its components on metabolic health. Nutrients. 2010;2:1266-89.
6. Keenan MJ, Zhou J, McCutcheon KL, Raggio AM, Bateman HG, Todd E, Jones CK, Tulley RT, Melton S, Martin RJ, et al. Effects of resistant starch, a non-digestible fermentable fiber, on reducing body fat. Obesity (Silver Spring). 2006;14:1523-34.
7. So PW, Yu WS, Kuo YT, Wasserfall C, Goldstone AP, Bell JD, Frost G. Impact of resistant starch on body fat patterning and central appetite regulation. PLoS ONE. 2007;2:e1309.
8. Robertson MD, Bickerton AS, Dennis AL, Vidal H, Frayn KN. Insulinsensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am J Clin Nutr. 2005;82:559-67.
9. Weickert MO, Mohlig M, Schofl C, Arafat AM, Otto B, Viehoff H, Koebnick C, Kohl A, Spranger J, Pfeiffer AF. Cereal fiber improves whole-body insulin sensitivity in overweight and obese women. Diabetes Care. 2006;29:775-80.
10. Wanders AJ, van den Borne JJ, de Graaf C, Hulshof T, Jonathan MC, Kristensen M, Mars M, Schols HA, Feskens EJ. Effects of dietary fibre on subjective appetite, energy intake and body weight: a systematic review of randomized controlled trials. Obes Rev. 2011.
11. Nugent AP. Health properties of resistant starch. Nutr Bull. 2005;30:27-54.
12. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81:1031-64.
13. 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.
14. Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch. 2004;447:619-28.
15. Roy CC, Kien CL, Bouthillier L, Levy E. Short-chain fatty acids: ready for prime time? Nutr Clin Pract. 2006;21:351-66.
16. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27:104-19.
17. Hosseini E, Grootaert C, Verstraete W, Van de Wiele T. Propionate as a health-promoting microbial metabolite in the human gut. Nutr Rev. 2011;69:245-58.
18. Sleeth ML, Thompson EL, Ford HE, Zac-Varghese SE, Frost G. Free fatty acid receptor 2 and nutrient sensing: a proposed role for fibre, fermentable carbohydrates and short-chain fatty acids in appetite regulation. Nutr Res Rev. 2010;23:135-45.
19. Zhou J, Hegsted M, McCutcheon KL, Keenan MJ, Xi X, Raggio AM, Martin RJ. Peptide YYand proglucagon mRNA expression patterns and regulation in the gut. Obesity (Silver Spring). 2006;14:683-9.
20. Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, Danna SC, Tripathy S, Hegsted M, Keenan MJ. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 2008;295:E1160-6.
21. Cherbut C, Ferrier L, Roze C, Anini Y, Blottiere H, Lecannu G, Galmiche JP. Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. Am J Physiol. 1998;275: G1415-22.
22. Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA. 2008;105:16767-72.
23. Miyauchi S, Hirasawa A, Ichimura A, Hara T, Tsujimoto G. New frontiers in gut nutrient sensor research: free fatty acid sensing in the gastrointestinal tract. J Pharmacol Sci. 2010;112:19-24.
24. Miller ER, Ullrey DE. The pig as a model for human nutrition. Annu Rev Nutr. 1987;7:361-82.
25. Guilloteau P, Zabielski R, Hammon HM, Metges CC. Nutritional programming of gastrointestinal tract development: is the pig a good model for man? Nutr Res Rev. 2010;23:4-22.
26. da Silva CS, van den Borne JJ, Gerrits WJ, Kemp B, Bolhuis JE. Effects of dietary fibers with different physicochemical properties on feeding motivation in adult female pigs. Physiol Behav. 2012;107:218-30.
27. Serena A, Jorgensen H, Bach Knudsen KE. Absorption of carbohydratederived nutrients in sows as influenced by types and contents of dietary fiber. J Anim Sci. 2009;87:136-47.
28. Goñi I, García-Diz L, Mañas E, Saura-Calixto F. Analysis of resistant starch: a method for foods and food products. Food Chem. 1996;56:445-9.
29. Salonen A, Nikkila J, Jalanka-Tuovinen J, Immonen O, Rajilic-Stojanovic M, Kekkonen RA, Palva A, de Vos WM. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Methods. 2010;81:127-34.
30. Konstantinov SR, Awati A, Smidt H, Williams BA, Akkermans AD, de Vos WM. Specific response of a novel and abundant Lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Appl Environ Microbiol. 2004;70:3821-30.
31. Muyzer G, deWaal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol. 1993;59:695-700.
32. Pérez Gutiérrez O, van den Bogert B, Derrien M, Koopmans SJ, Molenaar D, de Vos WM, Smidt H. Design of a high-throughput diagnostic microarray for the characterization of pig gastrointestinal tract microbiota. Chapter 3. Unraveling piglet gut microbiota dynamics in response to feed additives [dissertation]. Wageningen (Netherlands): Ponsen & Looijen; 2010. p. 40-67 [cited 2013 Jan 9]. Available from: http://library.wur.nl/WebQuery/wda/lang/1939249.
33. Claesson MJ, O'Sullivan O, Wang Q, Nikkila J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O'Toole PW. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE. 2009;4:e6669.
34. van den Bogert B, de Vos WM, Zoetendal EG, Kleerebezem M. Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl Environ Microbiol. 2011;77:2071-80.
35. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464: 59-65.
36. Rajilić-Stojanović M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H, de Vos WM. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol. 2009;11:1736-51.
37. Velu R, Reinsel GC. Multivariate reduced-rank regression: theory and applications: New York: Springer; 1998.
38. ter Braak CJF. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology. 1986;67: 1167-79.
39. Lepš J, Šmilauer P. Multivariate analysis of ecological data using CANOCO. Cambridge, UK: Cambridge University Press; 2003.
40. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289-300.
41. Wong MH, Oelkers P, Craddock AL, Dawson PA. Expression cloning and characterization of the hamster ileal sodium-dependent bile acid transporter. J Biol Chem. 1994;269:1340-7.
42. Bünger M, van den Bosch HM, van der Meijde J, Kersten S, Hooiveld GJ, Muller M. Genome-wide analysis of PPARalpha activation in murine small intestine. Physiol Genomics. 2007;30:192-204.
43. Mortensen K, Christensen LL, Holst JJ, Orskov C. GLP-1 and GIP are colocalized in a subset of endocrine cells in the small intestine. Regul Pept. 2003;114:189-96.
44. Yasuda K, Maiorano R, Welch RM, Miller DD, Lei XG. Cecum is the major degradation site of ingested inulin in young pigs. J Nutr. 2007;137:2399-404.
45. Patterson JK, Yasuda K, Welch RM, Miller DD, Lei XG. Supplemental dietary inulin of variable chain lengths alters intestinal bacterial populations in young pigs. J Nutr. 2010;140:2158-61.
46. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011; 5:220-30.
47. Martínez 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.
48. 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.
49. Lesmes U, Beards EJ, Gibson GR, Tuohy KM, Shimoni E. Effects of resistant starch type III polymorphs on human colon microbiota and short chain fatty acids in human gut models. J Agric Food Chem. 2008;56:5415-21.
50. Young W, Roy NC, Lee J, Lawley B, Otter D, Henderson G, McCann MJ, Tannock GW. Changes in bowel microbiota induced by feeding resistant starch stimulate transcriptomic and physiological responses in the weanling host. Appl Environ Microbiol. 2012.
51. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007;102:1197-208.
52. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9:577-89.
53. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008;105:16731-6.
54. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70:567-90.
55. Cummings JH. The large intestine in nutrition and disease. Brussels (Belgium): Institut Danone; 1997.
56. Bloemen JG, Venema K, van de Poll MC, Olde Damink SW, Buurman WA, Dejong CH. Short chain fatty acids exchange across the gut and liver in humans measured at surgery. Clin Nutr. 2009;28:657-61.
57. Cuff MA, Lambert DW, Shirazi-Beechey SP. Substrate-induced regulation of the human colonic monocarboxylate transporter, MCT1. J Physiol. 2002;539:361-71.
58. Borthakur A, Saksena S, Gill RK, Alrefai WA, Ramaswamy K, Dudeja PK. Regulation of monocarboxylate transporter 1 (MCT1) promoter by butyrate in human intestinal epithelial cells: involvement of NF-kappaB pathway. J Cell Biochem. 2008;103:1452-63.
59. Kaji I, Karaki S, Tanaka R, Kuwahara A. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J Mol Histol. 2011;42:27-38.
60. Karaki S, Mitsui R, Hayashi H, Kato I, Sugiya H, Iwanaga T, Furness JB, Kuwahara A. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res. 2006;324:353-60.
61. Chu ZL, Carroll C, Alfonso J, Gutierrez V, He H, Lucman A, Pedraza M, Mondala H, Gao H, Bagnol D, et al. A role for intestinal endocrine cell-expressed g protein-coupled receptor 119 in glycemic control by enhancing glucagon-like peptide-1 and glucose-dependent insulinotropic peptide release. Endocrinology. 2008;149:2038-47.
62. Lan H, Vassileva G, Corona A, Liu L, Baker H, Golovko A, Abbondanzo SJ, Hu W, Yang S, Ning Y, et al. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J Endocrinol. 2009;201:219-30.
63. Yoshida K, Shimizugawa T, Ono M, Furukawa H. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J Lipid Res. 2002;43:1770-2.