Weickert, Martin O., Arafat, Ayman M., Blaut, Michael, Alpert, Carl, Becker, Natalie, Leupelt, Verena, Rudovich, Natalia, Möhlig, Matthias and Pfeiffer, Andreas F. H.. (2011) Changes in dominant groups of the gut microbiota do not explain cereal-fiber induced improvement of whole-body insulin sensitivity. Nutrition & Metabolism, Vol.8 (No.1). p. 90. ISSN 1743-7075

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Abstract

Background Diets high in cereal-fiber (HCF) have been shown to improve whole-body insulin sensitivity. In search for potential mechanisms we hypothesized that a supplemented HCF-diet influences the composition of the human gut microbiota and/or biomarkers of colonic carbohydrate fermentation. Methods We performed a randomized controlled 18-week intervention in group-matched overweight participants. Fecal samples of 69 participants receiving isoenergetic HCF (cereal-fiber 43 g/day), or control (cereal-fiber 14 g/day), or high-protein (HP, 28% of energy-intake, cereal-fiber 14 g/day), or moderately high cereal fiber/protein diets (MIX; protein 23% of energy-intake, cereal-fiber 26 g/day) with comparable fat contents were investigated for diet-induced changes of dominant groups of the gut microbiota, and of fecal short-chain fatty-acids (SCFA) including several of their proposed targets, after 0, 6, and 18-weeks of dietary intervention. In vitro fermentation of the cereal fiber extracts as used in the HCF and MIX diets was analyzed using gas chromatography. Diet-induced effects on whole-body insulin-sensitivity were measured using euglycaemic-hyperinsulinemic clamps and re-calculated in the here investigated subset of n = 69 participants that provided sufficient fecal samples on all study days. Results Gut microbiota groups and biomarkers of colonic fermentation were comparable between groups at baseline (week 0). No diet-induced differences were detected between groups during this isoenergetic intervention, neither in the full model nor in uncorrected subgroup-analyses. The cereal-fiber extract as used for preparation of the supplements in the HCF and MIX groups did not support in vitro fermentation. Fecal acetate, propionate, and butyrate concentrations remained unchanged, as well as potential targets of increased SCFA, whereas valerate increased after 6-weeks in the HP-group only (p = 0.037). Insulin-sensitivity significantly increased in the HCF-group from week-6 (baseline M-value 3.8 ± 0.4 vs 4.3 ± 0.4 mg·kg-1·min-1, p = 0.015; full model 0-18-weeks, treatment-x-time interaction, p = 0.046). Conclusions Changes in the composition of the gut microbiota and/or markers of colonic carbohydrate fermentation did not contribute explaining the observed early onset and significant improvement of whole-body insulin sensitivity with the here investigated HCF-diet.

Item Type:	Journal Article
Subjects:	Q Science > QP Physiology
Divisions:	Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH):	Cereal products -- Physiological effect, Insulin -- Physiological effect, Fiber in human nutrition -- Physiological effect, Gastrointestinal system
Journal or Publication Title:	Nutrition & Metabolism
Publisher:	Bio Med Central
ISSN:	1743-7075
Date:	17 December 2011
Volume:	Vol.8
Number:	No.1
Page Range:	p. 90
Identification Number:	10.1186/1743-7075-8-90
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	Germany. Bundesministerium für Bildung und Forschung (BMBF), Deutsches Institut für Ernährungsforschung Potsdam-Rehbrücke [German Institute of Human Nutrition Potsdam-Rehbrücke], Charité University Medicine Berlin, Rettenmayr Inc., Anona Inc., Kathi Inc.
Grant number:	0313826A (BMBF), 0313826B (BMBF)
References:	1. Freeland KR, Wilson C, Wolever TM: Adaptation of colonic fermentation and glucagon-like peptide-1 secretion with increased wheat fibre intake for 1 year in hyperinsulinaemic human subjects. Br J Nutr 2010, 103:82-90. 2. Hamedani A, Akhavan T, Samra RA, Anderson GH: Reduced energy intake at breakfast is not compensated for at lunch if a high-insoluble-fiber cereal replaces a low-fiber cereal. Am J Clin Nutr 2009, 89:1343-1349. 3. Nilsson AC, Ostman EM, Knudsen KE, Holst JJ, Bjorck IM: A cereal-based evening meal rich in indigestible carbohydrates increases plasma butyrate the next morning. J Nutr 2010, 140:1932-1936. 4. Thorburn A, Muir J, Proietto J: Carbohydrate fermentation decreases hepatic glucose output in healthy subjects. Metabolism 1993, 42:780-785. 5. Liese AD, Roach AK, Sparks KC, Marquart L, D’Agostino RB Jr, Mayer- Davis EJ: Whole-grain intake and insulin sensitivity: the Insulin Resistance Atherosclerosis Study. Am J Clin Nutr 2003, 78:965-971. 6. Steffen LM, Jacobs DR Jr, Murtaugh MA, Moran A, Steinberger J, Hong CP, Sinaiko AR: Whole grain intake is associated with lower body mass and greater insulin sensitivity among adolescents. Am J Epidemiol 2003, 158:243-250. 7. de Munter JS, Hu FB, Spiegelman D, Franz M, van Dam RM: Whole grain, bran, and germ intake and risk of type 2 diabetes: a prospective cohort study and systematic review. PLoS Med 2007, 4:e261. 8. Schulze MB, Schulz M, Heidemann C, Schienkiewitz A, Hoffmann K, Boeing H: Fiber and magnesium intake and incidence of type 2 diabetes: a prospective study and meta-analysis. Arch Intern Med 2007, 167:956-965. 9. Fukagawa NK, Anderson JW, Hageman G, Young VR, Minaker KL: Highcarbohydrate, high-fiber diets increase peripheral insulin sensitivity in healthy young and old adults. Am J Clin Nutr 1990, 52:524-528. 10. Pereira MA, Jacobs DR Jr, Pins JJ, Raatz SK, Gross MD, Slavin JL, Seaquist ER: Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr 2002, 75:848-855. 11. Weickert MO, Möhlig M, Schöfl 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, 29:775-780. 12. Weickert MO, Roden M, Isken F, Hoffmann D, Nowotny P, Osterhoff M, Blaut M, Alpert C, Gogebakan O, Bumke-Vogt C, Mueller F, Machann J, Barber TM, Petzke KJ, Hierholzer J, Hornemann S, Kruse M, Illner AK, Kohl A, Loeffelholz CV, Arafat AM, Möhlig M, Pfeiffer AF: Effects of supplemented isoenergetic diets differing in cereal fiber and protein content on insulin sensitivity in overweight humans. Am J Clin Nutr 2011, 94:459-471. 13. Andersson A, Tengblad S, Karlstrom B, Kamal-Eldin A, Landberg R, Basu S, Aman P, Vessby B: Whole-grain foods do not affect insulin sensitivity or markers of lipid peroxidation and inflammation in healthy, moderately overweight subjects. J Nutr 2007, 137:1401-1407. 14. Weickert MO, Pfeiffer AF: Metabolic effects of dietary fiber consumption and prevention of diabetes. J Nutr 2008, 138:439-442. 15. Reimer RA, McBurney MI: Dietary fiber modulates intestinal proglucagon messenger ribonucleic acid and postprandial secretion of glucagon-like peptide-1 and insulin in rats. Endocrinology 1996, 137:3948-3956. 16. Tarini J, Wolever TM: The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl Physiol Nutr Metab 2010, 35:9-16. 17. 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, 82:559-567. 18. Robertson MD, Currie JM, Morgan LM, Jewell DP, Frayn KN: Prior shortterm consumption of resistant starch enhances postprandial insulin sensitivity in healthy subjects. Diabetologia 2003, 46:659-665. 19. Verhoef SP, Meyer D, Westerterp KR: Effects of oligofructose on appetite profile, glucagon-like peptide 1 and peptide YY3-36 concentrations and energy intake. Br J Nutr 2011, 1-6. 20. Weickert MO, Möhlig M, Koebnick C, Holst JJ, Namsolleck P, Ristow M, Osterhoff M, Rochlitz H, Rudovich N, Spranger J, Pfeiffer AF: Impact of cereal fibre on glucose-regulating factors. Diabetologia 2005, 48:2343-2353. 21. Alberti KG, Zimmet P, Shaw J: The metabolic syndrome–a new worldwide definition. Lancet 2005, 366:1059-1062. 22. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, Clavel T, Koebnick C, Zunft HJ, Dore J, Blaut M: Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 2006, 72:1027-1033. 23. Rigottier-Gois L, Bourhis AG, Gramet G, Rochet V, Dore J: Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human faeces using 16S rRNA probes. FEMS Microbiol Ecol 2003, 43:237-245. 24. 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, 66:1654-1661. 25. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ: Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr 2004, 91:915-923. 26. Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HJ: Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 2003, 69:4320-4324. 27. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE: Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 2007, 73:1073-1078. 28. Widdel F, Kohring G-W, Mayer F: Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the filamentous gliding Desulfonema magnum sp. nov. Arch Microbiol 1983, 134:286-294. 29. Wolin EA, Wolfe RS, Wolin MJ: Viologen dye inhibition of methane formation by Methanobacillus omelianskii. J Bacteriol 1964, 87:993-998. 30. Parnell JA, Reimer RA: Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr 2009, 89:1751-1759. 31. Costabile A, Klinder A, Fava F, Napolitano A, Fogliano V, Leonard C, Gibson GR, Tuohy KM: Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 2008, 99:110-120. 32. Samra RA, Anderson GH: Insoluble cereal fiber reduces appetite and short-term food intake and glycemic response to food consumed 75 min later by healthy men. Am J Clin Nutr 2007, 86:972-979. 33. Geypens B, Claus D, Evenepoel P, Hiele M, Maes B, Peeters M, Rutgeerts P, Ghoos Y: Influence of dietary protein supplements on the formation of bacterial metabolites in the colon. Gut 1997, 41:70-76. 34. Isken F, Klaus S, Osterhoff M, Pfeiffer AF, Weickert MO: Effects of long-term soluble vs. insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6J mice. J Nutr Biochem 2010, 21:278-284. 35. Track NS, Cawkwell ME, Chin BC, Chiu SS, Haberer SA, Honey CR: Guar gum consumption in adolescent and adult rats: short- and long-term metabolic effects. Can J Physiol Pharmacol 1985, 63:1113-1121. 36. McNeil NI: The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 1984, 39:338-342. 37. Jenkins DJ, Kendall CW, Axelsen M, Augustin LS, Vuksan V: Viscous and nonviscous fibres, nonabsorbable and low glycaemic index carbohydrates, blood lipids and coronary heart disease. Curr Opin Lipidol 2000, 11:49-56. 38. Gallaher D, Schneeman BO: Intestinal interaction of bile acids, phospholipids, dietary fibers, and cholestyramine. Am J Physiol 1986, 250: G420-426. 39. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI: A core gut microbiome in obese and lean twins. Nature 2009, 457:480-484. 40. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R: Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 2009, 106:2365-2370.
URI:	http://wrap.warwick.ac.uk/id/eprint/41141

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