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Effect of isomalt consumption on faecal microflora and colonic metabolism in healthy volunteers

Published online by Cambridge University Press:  08 March 2007

A. Gostner*
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
M. Blaut
Affiliation:
German Institute of Human Nutrition Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, Arthur-Scheunert-Allee 114–116, D-14558 Nuthetal, Germany
V. Schäffer
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
G. Kozianowski
Affiliation:
Suedzucker AG, Wormser Strasse 11, D-67283 Obrigheim/Pfalz, Germany
S. Theis
Affiliation:
Suedzucker AG, Wormser Strasse 11, D-67283 Obrigheim/Pfalz, Germany
M. Klingeberg
Affiliation:
Suedzucker AG, Wormser Strasse 11, D-67283 Obrigheim/Pfalz, Germany
Y. Dombrowski
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
D. Martin
Affiliation:
Suedzucker AG, Wormser Strasse 11, D-67283 Obrigheim/Pfalz, Germany
S. Ehrhardt
Affiliation:
Suedzucker AG, Wormser Strasse 11, D-67283 Obrigheim/Pfalz, Germany
D. Taras
Affiliation:
German Institute of Human Nutrition Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, Arthur-Scheunert-Allee 114–116, D-14558 Nuthetal, Germany
A. Schwiertz
Affiliation:
German Institute of Human Nutrition Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, Arthur-Scheunert-Allee 114–116, D-14558 Nuthetal, Germany
B. Kleessen
Affiliation:
German Institute of Human Nutrition Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, Arthur-Scheunert-Allee 114–116, D-14558 Nuthetal, Germany
H. Lührs
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
J. Schauber
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
D. Dorbath
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
T. Menzel
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
W. Scheppach
Affiliation:
University of Würzburg, Department of Medicine II, Josef-Schneider-Strasse 2, D-97080 Würzburg, Germany
*
*Corresponding author:Dr Andrea Godtner, fax +49 931 201 36 101, email gostner_a@klinik.uni-wuerzburg.de
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Abstract

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Due to its low digestibility in the small intestine, a major fraction of the polyol isomalt reaches the colon. However, little is known about effects on the intestinal microflora. During two 4-week periods in a double-blind, placebo-controlled, cross-over design, nineteen healthy volunteers consumed a controlled basal diet enriched with either 30g isomalt or 30g sucrose daily. Stools were collected at the end of each test phase and various microbiological and luminal markers were analysed. Fermentation characteristics of isomalt were also investigated in vitro. Microbiological analyses of faecal samples indicated a shift of the gut flora towards an increase of bifidobacteria following consumption of the isomalt diet compared with the sucrose diet (P<0·05). During the isomalt phase, the activity of bacterial β-glucosidase decreased (P<0·05) whereas β-glucuronidase, sulfatase, nitroreductase and urease remained unchanged. Faecal polyamines were not different between test periods with the exception of cadaverine, which showed a trend towards a lower concentration following isomalt (P=0·055). Faecal SCFA, lactate, bile acids, neutral sterols, N, NH3, phenol and p-cresol were not affected by isomalt consumption. In vitro, isomalt was metabolized in several bifidobacteria strains and yielded high butyrate concentrations. Isomalt, which is used widely as a low-glycaemic and low-energy sweetener, has to be considered a prebiotic carbohydrate that might contribute to a healthy luminal environment of the colonic mucosa.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Alles, MS, Hartemink, R, Meyboom, S, Harryvan, JL, Van Laere, KM, Nagengast, FM & Hautvast, JGEffect of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. Am J Clin Nutr (1999) 69, 980991.CrossRefGoogle ScholarPubMed
Balmer, SE & Wharton, BADiet and fecal flora of the new born: breast milk and infant formula. Arch Dis Child (1989) 64, 16721677.CrossRefGoogle Scholar
Bär, A Factorial calculation model for the estimation of the physiological caloric value of polyols. In Proceedings of the International Symposium on Caloric Evaluation of Carbohydrates, pp. 209257 [N, Hosoxa, editor]. Tokyo: Research Foundation for Sugar Metabolism (1990).Google Scholar
Batta, AK, Salen, G, Rapole, KR, Batta, M, Batta, P & Alberts, EDHighly simplified method for gas-liquid chromatographic quantitation of bile acids and sterols in human stool. J Lipid Res (1999) 40, 11481154.CrossRefGoogle ScholarPubMed
Bartram, HP, Scheppach, W, Heid, C, Fabian, C & Kasper, HEffect of starch malabsorption on fecal bile acids and neutral sterols in humans: possible implications for colonic carcinogenesis. Cancer Res (1991) 51, 42384242.Google ScholarPubMed
Benamouzig, R, Mahé, S, Luengo, C, Rautureau, J & Tomé, DFasting and postprandial polyamine concentrations in human digestive lumen. Am J Clin Nutr (1997) 65, 766770.CrossRefGoogle ScholarPubMed
Bezkorovainy, AProbiotics: determinants of survival and growth in the gut. Am J Clin Nutr (2001) 73, Suppl. 3, 99S405S.CrossRefGoogle ScholarPubMed
Blei, ATDiagnosis and treatment of hepatic encephalopathy. Baillieres Best Pract Res Clin Gastroenterol (2000) 14, 959974.CrossRefGoogle ScholarPubMed
Bone, E, Tamm, A & Hill, MThe production of urinary phenols by gut bacteria and their possible role in the causation of large bowel cancer. Am J Clin Nutr (1976) 29, 14481454.CrossRefGoogle ScholarPubMed
Bouhnik, Y, Vahedi, K, Achour, L, Attar, A, Salfati, J, Pochart, P, Marteau, P, Flourie, B, Bornet, F & Rambaud, JCShortchain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. J Nutr (1999) 129, 113116.CrossRefGoogle ScholarPubMed
Brighenti, F, Casiraghi, C, Canzi, E & Ferari, AEffect of consumption of a ready-to eat breakfast cereal containing inulin on the intestinal milieu and blood lipids in healthy male volunteers. Eur J Clin Nutr (1999) 53, 726733.CrossRefGoogle ScholarPubMed
Bryan, GTThe role of urinary tryptophan metabolites in the etiology of bladder cancer. Am J Clin Nutr (1971) 24, 841847.CrossRefGoogle ScholarPubMed
Buddington, RK, Williams, CH, Chen, SC & Witherly, SADietary supplement of neosugar alters the fecal flora and decreases activities of some reductive enzymes in human subjects. Am J Clin Nutr (1996) 63, 709716.CrossRefGoogle ScholarPubMed
Cummings, JH, Macfarlane, GT & Englyst, HNPrebiotic digestion and fermentation. Am J Clin Nutr (2001) 73, Suppl. 4, 15S420S.CrossRefGoogle ScholarPubMed
Edwards, CA & Prrett, AMIntestinal flora during the first months of life: new perspectives. Br J Nutr (2002) 88, Suppl., S11S18.CrossRefGoogle ScholarPubMed
Franks, AH, Harmsen, HJM, Raangs, GC, Jansen, GJ, Schut, F & Welling, GVariations of bacterial populations in human faeces measured by fluorescent in situ hybridisation with groupspecific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol (1998) 64, 33363345.CrossRefGoogle ScholarPubMed
Gee, JM, Cooke, D, Gorick, S, Wortley, GM, Greenwood, RH, Zumbe, A & Johnson, ITEffects of conventional sucrose-based, fructose-based and isomalt-based chocolates on postprandial metabolism in non-insulin-dependent diabetics. Eur J Clin Nutr (1991) 45, 561566.Google ScholarPubMed
Gehring, F & Karle, EJSweetening agent, Palatinit under specific consideration as to microbiological and caries-prophylactic aspects. Z Ernahrungswiss (1981) 20, 96106.CrossRefGoogle ScholarPubMed
Giaffer, MH, Holdsworth, CD & Duerden, BIThe assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol (1991) 35, 238243.CrossRefGoogle ScholarPubMed
Gibson, GR, Beatty, ER, Wang, X & Cummings, JHSelective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology (1995) 108, 975982.CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MBDietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr (1995) 125, 14011412.CrossRefGoogle ScholarPubMed
Gostner, A, Schäffer, V, Theis, S et al. , Effects of isomalt consumption on gastrointestinal and metabolic parameters in healthy volunteers. Br J Nutr (2005) 94, 575581.CrossRefGoogle ScholarPubMed
Grasten, SM, Juntunen, KS, Poutanen, KS, Gylling, HK, Miettinen, TA & Mykkanen, HMRye bread improves bowel function and decreases the concentrations of some compounds that are putative colon cancer risk markers in middle-aged women and men. J Nutr (2000) 130, 22152221.CrossRefGoogle ScholarPubMed
Harmsen, HJM, Elferrich, P, Schut, F & Welling, GWA 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridisation. Microb Ecol Health Dis (1999) 11, 312.Google Scholar
Harmsen, HJ, Raangs, GC, He, T, Degener, JE & Welling, GExtensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol (2002a) 68, 29822990.CrossRefGoogle ScholarPubMed
Harmsen, HJ, Wildeboer-Veloo, AC, Grijpstra, J, Knol, J, Degener, JE & Welling, GWDevelopment of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol (2000) 66, 45234527.CrossRefGoogle ScholarPubMed
Harmsen, HJM, Raangs, GC, Franks, AH, Wildeboer-Veloo, AC & Welling, GWThe effect of the prebiotic inulin and the prebiotic Bifidobacterium longum on the fecal microflora of healthy volunteers measured by FISH and DGGE. Microbiol Ecol Health Dis (2002b) 14, 211219.Google Scholar
Hold, GL, Schwiertz, A, Aminov, R, Blaut, M & Flint, HJOligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria within the human fecal flora. Appl Environ Microbiol (2003) 69, 43204324.CrossRefGoogle Scholar
Hütter, R, Böswart, F & Irsigler, KInsulinverbrauch von Typ-IDiabetikern nach oraler Gabe von Isomalt. Akt Ernähr (1993) 18, 149154.Google Scholar
Hylla, S, Gostner, A, Dusel, G, Anger, H, Bartram, HP, Christl, SU, Kasper, H & Scheppach, WEffects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. Am J Clin Nutr (1998) 67, 136142.CrossRefGoogle Scholar
Johanson, GK, Ottova, L & Gustafsson, JAShift from a mixed diet to a lactovegetarian diet: influence on some cancer-associated intestinal bacterial enzyme activities. Nutr Cancer (1990) 14, 239246.CrossRefGoogle Scholar
Kleessen, B, Hartmann, L & Blaut, MOligofructose and longchain inulin influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr (2001) 86, 291300.CrossRefGoogle ScholarPubMed
Kleessen, B, Sykura, B, Zunft, HJ & Blaut, MEffects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr (1997) 65, 13971402.CrossRefGoogle ScholarPubMed
Kruse, HP, Kleessen, B & Blaut, MEffects of inulin on faecal bifidobacteria in human subjects. Br J Nutr (1999) 82, 375382.CrossRefGoogle ScholarPubMed
Langendijk, PS, Schut, F, Jansen, GJ, Raangs, GC, Kamphuis, GR, Wilkinson, MHF & Welling, GWQuantitative fluorescence in situ hybridisation of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol (1995) 61, 30693075.CrossRefGoogle ScholarPubMed
Langkilde, AM, Andersson, H, Schweizer, TF & Wursch, PDigestion and absorption of sorbitol, maltitol and isomalt from the small bowel. A study in ileostomy subjects. Eur J Clin Nutr (1994) 48, 768775.Google ScholarPubMed
Lin, HC & Visek, WJColon mucosal cell damage by ammonia in rats. J Nutr (1991) 121, 887893.CrossRefGoogle ScholarPubMed
Linskens, RK, Huijsdens, XW, Savelkoul, PH, Vandenbroucke-Grauls, CM& Meuwissen, SGThe bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics. Scand J Gastroenterol (2001) 234, Suppl., 2940.CrossRefGoogle Scholar
Livesey, GHealth potential of polyols as sugar replacers, with emphasis on low glycaemic properties. Nutr Res Rev (2003) 16, 163191.CrossRefGoogle ScholarPubMed
McBain, AJ & Macfarlane, GTEcological and physiological studies on large intestinal bacteria in relation to production of hydrolytic and reductive enzymes involved in formation of genotoxic metabolites. J Med Microbiol (1998) 47, 407416.CrossRefGoogle ScholarPubMed
McBain, AJ & Macfarlane, GTModulation of genotoxic enzyme activities by non-digestible oligosaccharide metabolism in in-vitro human gut bacterial ecosystems. J Med Microbiol (2001) 50, 833842.CrossRefGoogle ScholarPubMed
Mallett, AK, Rowland, IR & Farthing, MJDietary modification of intestinal bacterial enzyme activities — potential formation of toxic agents in the gut. Scand J Gastroenterol (1987) 129, Suppl., 251257.CrossRefGoogle ScholarPubMed
Manz, W, Amann, R, Ludwig, W, Vancanneyt, M & Schleifer, K-HApplication of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga- flavobacter-bacteroides in the natural environment. Microbiology (1996) 142, 10971106.CrossRefGoogle ScholarPubMed
Manz, W, Amann, R, Ludwig, W, Wagner, M & Schleifer, K-HPhylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol (1992) 15, 593600.CrossRefGoogle Scholar
Marteau, P, Seksik, P & Jian, RProbiotics and intestinal health effects: a clinical perspective. Br J Nutr (2002) 88, Suppl., S51S57.CrossRefGoogle ScholarPubMed
Meier, H, Amann, R, Ludwig, W & Schleifer, K-HSpecific oligonucleotide probes for in situ detection of a major group of grampositive bacteria with low DNA G + C content. Syst Appl Microbiol (1999) 22, 186196.CrossRefGoogle Scholar
Menne, E, Guggenbuhl, N & Roberfroid, MFn-type chicory inulin hydrolysate has a prebiotic effect in humans. J Nutr (1997) 130, 11971199.CrossRefGoogle Scholar
Noack, J, Kleessen, B, Proll, J, Dongowski, G & Blaut, MDietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. J Nutr (1998) 128, 13851391.CrossRefGoogle ScholarPubMed
Petzoldt, R, Lauer, P, Spengler, M & Schoffling, KPalatinite in type II diabetics. Effect on blood-glucose, serum-insulin, C-peptide and free fatty acids. Dtsch Med Wochenschr (1982) 107, 19101913.CrossRefGoogle ScholarPubMed
Pistoli, S, Smejkal, C, McCartney, A & Gibson, GRDifferences in the faecal flora of healthy individual and patients with irritable bowel syndrome, and in vitro effects of a synbiotic upon gut flora composition Clin Nutr (2003) 22, 60.CrossRefGoogle Scholar
Poulsen, IK, Licht, TR, Rang, C, Krogfelt, KA & Molin, SPhysiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice. J Bacteriol (1995) 177, 58405845.CrossRefGoogle ScholarPubMed
Rao, AVThe prebiotic properties of oligofructose at low intake levels. Nutr Res (2001) 21, 843848.CrossRefGoogle Scholar
Roediger, WEUtilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology (1982) 83, 424429.CrossRefGoogle ScholarPubMed
Roller, C, Wagner, M, Amann, R, Ludwig, W & Schleifer, K-HIn situ probing of Gram-positive bacteria with high DNA G + C content using 23S rRNA-targeted oligonucleotides. Microbiology (1994) 140, 28492858.CrossRefGoogle Scholar
Scheppach, WEffects of short chain fatty acids on gut morphology and function. Gut (1994) 35, S35S38.CrossRefGoogle ScholarPubMed
Scheppach, W, Luehrs, H & Menzel, TBeneficial health effects of low-digestible carbohydrate consumption. Br J Nutr (2001) 85, Suppl. 1, S23S30.CrossRefGoogle ScholarPubMed
Schwiertz, A, Le Blay, G & Blaut, MQuantification of different Eubacterium spp. in human fecal samples with species-specific 16S rRNA-targeted oligonucleotid probes. Appl Environ Microbiol (2000) 66, 375382.CrossRefGoogle Scholar
Suau, A, Rochet, V, Sghir, A, Gramet, G, Brewaeys, S, Sutren, M, Rigottier-Gois, L & Dore, JFusobacterium praunitzii and related species represent a dominant group within the human fecal flora. Syst Appl Microbiol (2001) 24, 139145.CrossRefGoogle Scholar
Tuohy, AM, Finlay, RK, Wynne, AG& Gibson, GRA human volunteer study on the prebiotic effects of HP-inulin — fecal bacteria enumerated using fluorescent in situ hybridisation (FISH). Anaerobe (2001a) 7, 113119.CrossRefGoogle Scholar
Tuohy, KM, Kolida, S, Lustenberger, AM & Gibson, GRThe prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides — a human volunteer study. Br J Nutr (2001b) 86, 341348.CrossRefGoogle ScholarPubMed
van de Kamer, JH, Bokkel Ten Huining, H & Weyers, HAEinfache Methode zur Bestimmung des Fettgehalts im Stuhl. J Biol Chem (1949) 177, 347 & 350.CrossRefGoogle Scholar
Van Loo, J, Cummings, J, Delzenne, N et al. Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br J Nutr (1999) 81, 121132.Google ScholarPubMed
van Weerden, EJ & Huisman, JThe digestion process of the sugar alcohol isomalt in the intestinal tract of the pig. 1. Studies with administration of isomalt in the feed. Br J Nutr (1993) 69, 455466.CrossRefGoogle ScholarPubMed
Velazquez, OC, Lederer, HM & Rombeau, JLButyrate and the colonocyte. Implications for neoplasia Dig Dis Sci (1996) 41, 727739.CrossRefGoogle ScholarPubMed
Weber, FL JrEffects of lactulose on nitrogen metabolism. Scand J Gastroenterol (1997) 222, Suppl., 8387.CrossRefGoogle ScholarPubMed
Wheeler, LA, Soderberg, FB & Goldman, PThe relationship between nitrogroup reduction and the intestinal microflora. J Pharmacol Exp Ther (1975) 194, 135144.Google Scholar
Wise, A, Mallet, AK & Rowland, IRDietary fibre, bacterial metabolism and toxicity of nitrate in the rat. Xenobiotica (1982) 12, 111118.CrossRefGoogle ScholarPubMed
Zhong, J, Luo, B, Xiang, M, Liu, H, Zhai, Z, Ang, T & Craig, SStudies on the effects of polydextrose intake on physiologic functions in Chinese people. Am J Clin Nutr (2000) 72, 15031509.Google Scholar