Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T03:33:46.710Z Has data issue: false hasContentIssue false
  • English
  • Français

Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora

Published online by Cambridge University Press:  09 March 2007

Brigitta Kleessen ,
Ludger Hartmann  and
Michael Blaut
Brigitta Kleessen*
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, D-14558 Bergholz-Rehbrücke, Germany
Ludger Hartmann
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, D-14558 Bergholz-Rehbrücke, Germany
Michael Blaut
Affiliation:
German Institute of Human Nutrition (DIFE) Potsdam-Rehbrücke, Department of Gastrointestinal Microbiology, D-14558 Bergholz-Rehbrücke, Germany
*
*Corresponding author: Dr Brigitta Kleessen, fax +49 331 74 06 950, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Dietary incorporation of fermentable, indigestible fructans may be of benefit to gastrointestinal health by providing short-chain fatty acids, stimulating the proliferation of bifidobacteria or lactobacilli and suppressing potential pathogenic organisms in the gut. We tested the hypothesis that the effects of fructans on caecal, colonic and faecal short-chain fatty acid concentration and microflora composition depend on their chain length. Germ-free rats associated with a human faecal flora were randomly assigned to one of four treatments as follows: (1) commercial standard diet as a control (Con); (2) Con+50 g short-chain oligofructose/kg (OF); (3) C+50 g long-chain inulin/kg (lcIN); or (4) Con+50 g OF–lcIN/kg (Mix OF–lcIN). Changes in bacterial population groups in response to feeding these diets were investigated with 16S rRNA-targeted probes applied in in situ hybridization. Mix OF–lcIN- and lcIN-containing diets resulted in larger numbers of caecal, colonic and faecal bacteria of the Clostridium coccoides–Eubacterium rectale cluster than Con (10·6 and 10·3 v. 9·5 log10/g wet wt), whereas OF alone did not affect this bacterial group in caecum, colon or faeces. A bifidogenic effect was only observed in the colon and faeces of OF-treated rats. More lactobacilli were found in caecal and colonic contents of Mix OF–lcIN-fed rats and in faeces of OF-fed rats compared with Con. Mix OF–lcIN and OF led to significantly smaller numbers of caecal, colonic and faecal bacteria belonging to the Clostridium histolyticum and C. lituseburense groups than Con (6·8 and 6·9 v. 7·9 log10/g wet wt). Counts of total bacteria, Bacteroides–Prevotella and Enterobacteriaceae did not differ between the groups. OF and/or lcIN-containing diets significantly increased the caecal and colonic concentration of butyrate and its relative molar proportion. Only lcIN-containing diets resulted in a higher faecal concentration of butyrate than Con. Higher molar proportions of faecal butyrate were observed with all diets that had been supplemented with OF and/or lcIN. Stimulation of butyrate production could be of interest for the prevention of ulcerative colitis and colon cancer.

Keywords

ButyrateOligofructoseInulinIntestinal microfloraGnotobiotic rats
Type
Research Article
Information
British Journal of Nutrition , Volume 86 , Issue 2 , August 2001 , pp. 291 - 300
Copyright
Copyright © The Nutrition Society 2001

References

Alles, MS, Hautfast, JG, Nagengast, FM, Hartemink, R, Van Laere, KM & Jansen, FM (1996) Fate of fructo-oligosaccharides in the human intestine. British Journal of Nutrition 76, 211–221.CrossRefGoogle ScholarPubMed
Amann, RI, Ludwig, W & Schleifer, K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbial Reviews 59, 143–169.CrossRefGoogle ScholarPubMed
Andrieux, C, Lory, S, Dufour-Lescoat, CD, de Baynast, R & Szylit, O (1991) Physiological effects of inulin in germ-free rats and in heteroxenic rats inoculated with a human flora. Food Hydrocolloids 5, 49–56.CrossRefGoogle Scholar
Barcenilla, A, Pryde, SE, Martin, JC, Duncan, SH, Stewart, CS, Henderson, C & Flint, HJ (2000) Phylogenetic relationship of butyrate-producing bacteria from the human gut. Applied and Environmental Microbiology 66, 1654–1661.CrossRefGoogle ScholarPubMed
Beimfohr, C, Krause, A, Amann, RI, Ludwig, W & Schleifer, K-H (1993) In situ identification of lactococci, enterococci and streptococci. Systematic and Applied Microbiology 16, 450–456.CrossRefGoogle Scholar
Bouhnik, Y, Flourie, B, Andrieux, C, Bisetti, N, Briet, F & Rambaud, J-C (1996) Effects of Bifidobacterium sp. fermented milk ingested with or without inulin on colonic bifidobacteria and enzymatic activities in healthy humans. European Journal of Clinical Nutrition 50, 269–273.Google ScholarPubMed
Bouhnik, Y, Vahedi, K, Achour, L, Attar, A, Salfati, J, Pochart, P, Marteau, P, Flourie, B, Bornet, F & Rambaud, J-C (1999) Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. Journal of Nutrition 129, 113–116.CrossRefGoogle ScholarPubMed
Buddington, RK, Williams, CH, Chen, SC & Whitherly, SA (1996) Dietary supplement of neosugar alters the fecal flora and decreases activities of some reductive enzymes in human subjects. American Journal of Clinical Nutrition 63, 709–716.CrossRefGoogle ScholarPubMed
Burke, A, Lichtenstein, GR & Rombeau, JL (1997) Nutrition and ulcerative colitis. Baillieres Clinical Gastroenterology 11, 153–174.CrossRefGoogle ScholarPubMed
Campbell, JM, Fahey, GC & Bryan, WW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. Journal of Nutrition 127, 130–136.CrossRefGoogle ScholarPubMed
Collins, MD, Lawson, PA, Willems, A, Cordoba, JJ, Fernandez-Garayzabal, J, Garcia, P, Cai, J, Hippe, H & Farrow, JAE (1994) The phylogeny of the genus Clostridium: proposal of five genera and eleven new species combinations. International Journal of Systematic Bacteriology 44, 812–826.CrossRefGoogle ScholarPubMed
Cummings, JH (1981) Short chain fatty acids in the human colon. Gut 22, 763–779.CrossRefGoogle ScholarPubMed
Cummings, JH, Beatty, ER, Kingman, SM, Bingham, SA & Englyst, HN (1996) Digestion and physiological properties of resistant starch in the human large bowel. British Journal of Nutrition 75, 733–747.CrossRefGoogle ScholarPubMed
Cummings, JH & Macfarlane, GT (1991) The control and consequences of bacteria fermentation in the human colon. Journal of Applied Microbiology 70, 443–459.Google ScholarPubMed
Cummings, JH & Macfarlane, GT (1997) Role of intestinal bacteria in nutrient metabolism. Clinical Nutrition 16, 3–11.CrossRefGoogle Scholar
Djouzi, Z & Andrieux, C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. British Journal of Nutrition 78, 313–324.CrossRefGoogle ScholarPubMed
Franks, AH, Harmsen, HJM, Raangs, GC, Jansen, GJ, Shut, F & Welling, GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Applied and Environmental Microbiology 64, 3336–3345.CrossRefGoogle ScholarPubMed
Gibson, GR (1999) Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. Journal of Nutrition 129, 1438S–1441S.CrossRefGoogle ScholarPubMed
Gibson, GR, Beatty, EB, Wang, X & Cummings, JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125, 1401–1412.CrossRefGoogle ScholarPubMed
Gibson, GR & Wang, X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. Journal of Applied Bacteriology 74, 667–674.Google Scholar
Hague, A, Butt, AJ & Paraskeva, A (1996) The role of butyrate in human colonic epithelial cells: an energy source or inducer of differentiation and apoptosis? Proceedings of the Nutrition Society 55, 937–943.CrossRefGoogle ScholarPubMed
Harmsen, HJM, Elfferich, P, Shut, F & Welling, G.W. (1999) A 16SrRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microbial Ecology in Health and Disease 11, 3–12.CrossRefGoogle Scholar
Hentges, DJ (1967) Influence of pH on the inhibitory activity of formic and acetic acids for Shigella. Journal of Bacteriology 93, 2029–2030.CrossRefGoogle ScholarPubMed
Hidaka, H, Eida, T, Takizawa, T, Tokunaga, T & Tashiro, Y (1986) Effects of fructooligosaccharides on intestinal flora and human health. Bifidobacteria Microflora 5, 37–50.CrossRefGoogle Scholar
Jacobasch, G, Schmiedl, D, Kruschewski, M & Schmehl, K (1999) Dietary resistant starch and chronic inflammatory bowel diseases. International Journal of Colorectal Diseases 14, 201–211.CrossRefGoogle ScholarPubMed
Kleessen, B, Noack, J & Blaut, M (1999) Distribution of viable and non-viable bacteria in the gastrointestinal tract of gnotobiotic and conventional rats. Microbiology Ecology in Health and Disease 11, 218–225.CrossRefGoogle Scholar
Kleessen, B, Sykura, B, Zunft, H-J & Blaut, M (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. American Journal of Clinical Nutrition 65, 1397–1402.CrossRefGoogle ScholarPubMed
Kruse, H-P, Kleessen, B & Blaut, M (1999) Effects of inulin on faecal bifidobacteria in human subjects. British Journal of Nutrition 82, 375–382.CrossRefGoogle ScholarPubMed
Langendijk, PS, Schut, F, Jansen, GJ, Raangs, GC, Kamphuis, GR, Wilkinson, MHF & Welling, GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16 S rRNA-targeted probes and its application in fecal samples. Applied and Environmental Microbiology 61, 3069–3075.CrossRefGoogle Scholar
Le Blay, G, Michel, C, Blottiere, HM & Cherbut, C (1999) Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. Journal of Nutrition 129, 2231–2235.CrossRefGoogle Scholar
Manz, W, Amann, R, Ludwig, W, Vancanneyt, M & Schleifer, K-H (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142, 1097–1106.CrossRefGoogle ScholarPubMed
Manz, W, Szewzyk, U, Eriksson, P, Amann, R, Schleifer, K-H & Stenström, TA (1993) In situ identification of bacteria in drinking water and adjoining biofilms by hybridization with 16S and 23S rRNA-directed fluorescent oligonucleotide probes. Applied and Environmental Microbiology 59, 2293–2298.CrossRefGoogle ScholarPubMed
Mallet, AK, Bearne, CA, Roland, IR, Farthing, MJG, Cole, CB & Fuller, R (1987) The use of rats associated with a human faecal flora as a model for studying the effect of diet on the human gut microflora. Journal of Applied Bacteriology 63, 39–45.CrossRefGoogle Scholar
Massimino, SP, McBurney, MI, Field, CJ, Thomson, ABR, Keelan, M, Hayek, MG & Sunvold, GD (1998) Fermentable dietary fiber increases GLP-1 secretion and improves glucose homeostasis despite increased intestinal glucose transport capacity in healthy dogs. Journal of Nutrition 128, 1786–1793.CrossRefGoogle ScholarPubMed
Menne, E, Guggenbuhl, N & Roberfroid, M (2000) Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. Journal of Nutrition 130, 1197–1199.CrossRefGoogle Scholar
Morita, T, Kasaoka, S, Hase, K & Kiriyama, S (1999) Psyllium shifts the fermentation site of high-amylose cornstarch toward the distal colon and increases fecal butyrate concentration in rats. Journal of Nutrition 129, 2081–2087.CrossRefGoogle ScholarPubMed
Poulsen, LK, Licht, TR, Rang, C, Krogfelt, KA & Molin, S (1995) Physiological state of E. coli BJ4 growing in the large intestines of streptomycin-treated mice. Journal of Bacteriology 177, 5840–5845.CrossRefGoogle ScholarPubMed
Prosky, L, Asp, N-G, Schweizer, TF, De Vries, J & Furda, I (1988) Determination of insoluble, soluble, and total dietary fiber in foods and food products: interlaboratory study. Journal of the Association Analytical Chemists 71, 1017–1023.Google ScholarPubMed
Rao, AV (1999) Dose-response effects of inulin and oligofructose on intestinal bifidogenesis effects. Journal of Nutrition 129, 1442S–1445S.CrossRefGoogle ScholarPubMed
Reddy, SR, Hamid, R & Rao, CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18, 1371–1374.CrossRefGoogle ScholarPubMed
Roberfroid, MB (1997) Health benefits of non-digestible oligosaccharides. Advances in Experimental Medical Biology 427, 211–219.CrossRefGoogle ScholarPubMed
Roberfroid, MB (2000) Prebiotics and probiotics: are they functional foods? American Journal of Clinical Nutrition 71 Suppl., 1682S–1687S.CrossRefGoogle ScholarPubMed
Roberfroid, MB & Delzenne, NM (1998) Dietary fructans. Annual Review of Nutrition 18, 117–143.CrossRefGoogle ScholarPubMed
Roberfroid, MB, Van Loo, JA & Gibson, GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. Journal of Nutrition 128, 11–19.CrossRefGoogle ScholarPubMed
Roediger, WEW (1995) The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In Physiological and Clinical Aspects of Short-Chain Fatty Acids, pp. 337–351 [Cummings, JH, Rombeau, JL and Sakata, T, editors]. Cambridge: University Press.Google Scholar
Rumney, CJ & Rowland, IR (1992) In vivo and in vitro models of the human colonic flora. Critical Reviews in Food Science and Nutrition 31, 299–331.CrossRefGoogle ScholarPubMed
Sakata, T (1987) Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: a possible explanation for trophic effects on fermentable fibre, gut microbes and luminal trophic factors. British Journal of Nutrition 58, 95–103.CrossRefGoogle ScholarPubMed
Sghir, A, Chow, JM & Mackie, RI (1998) Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate. Journal of Applied Microbiology 85, 769–777.CrossRefGoogle ScholarPubMed
Simpson, EJ, Chapman, MAS, Dawson, J, Berry, D, Macdonald, A & Cole, A (2000) In vivo measurement of colonic butyrate metabolism in patients with quiescent ulcerative colitis. Gut 46, 73–77.CrossRefGoogle ScholarPubMed
Smith, JG, Yokoyama, WH & German, JB (1998) Butyric acid from the diet: Actions at the level of gene expression. Critical Reviews in Food Science and Nutrition 38, 259–297.CrossRefGoogle ScholarPubMed
Tappenden, KA, Drozdowski, LA, Thomson, ABR & McBurney, MI (1998) Short-chain fatty acid-supplemented total parenteral nutrition alters intestinal structure, glucose transporter 2 (GLUT2) mRNA and protein, and proglucagon mRNA abundance in normal rats. American Journal of Clinical Nutrition 68, 118–125.CrossRefGoogle ScholarPubMed
Treem, WR, Ahsan, N, Shoup, M & Hyams, JS (1994) Fecal short-chain fatty acids in children with inflammatory bowel disease. Journal of Pediatric Gastroenterology and Nutrition 18, 159–164.Google ScholarPubMed
Van Loo, J, Coussement, P, De Leenheer, L, Hoebregs, H & Smits, G (1995) On the presence of inulin and oligofructose as natural ingredients in the Western diet. Critical Reviews in Food Science and Nutrition 35, 525–552.CrossRefGoogle ScholarPubMed
Van Loo, J, Cummings, J, Delzenne, N, Englyst, H, Franck, A, Hopkins, M, Kok, N, Macfarlane, G, Newton, D, Quigley, M, Roberfroid, M, Van Vliet, T & Van den Heuvel, E (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). British Journal of Nutrition 81, 121–132.Google ScholarPubMed
Velazquez, OC, Lederer, HM & Rombeau, JL (1996) Butyrate and the colonocyte. Implications for neoplasia. Digestive Disease and Science 41, 729–739.CrossRefGoogle ScholarPubMed
Wang, X & Gibson, GR (1993) Effect of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75, 373–380.CrossRefGoogle ScholarPubMed
Weaver, GA, Krause, JA, Miller, TL & Wolin, MJ (1988) Short chain fatty acid distributions of enema samples from a sigmoidoscopy population: an association of high acetate and low butyrate ratios with adenomatous polyps and colon cancer. Gut 29, 1539–1543.CrossRefGoogle ScholarPubMed
Welling, GW, Elfferich, P, Raangs, GC, Wildeboer-Veloo, ACM, Jansen, GJ & Degener, JE (1997) 16S rRNA-targeted oligonucleotide probes for monitoring of intestinal tract bacteria. Scandinavian Journal of Gastroenterology 32 Suppl. 222, 17–19.CrossRefGoogle Scholar
Wilcoxon, F & Wilcox, RA (1964) Some Rapid Approximate Statistical Procedures, New York, NY: Lederle Laboratories.Google Scholar
Zar, JH (1984) Biostatistical Analysis, 2nd ed, New York, NY: Prentice-Hall.Google Scholar