Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-16T01:21:08.022Z Has data issue: false hasContentIssue false

Fermentation in the large intestine of single-stomached animals and its relationship to animal health

Published online by Cambridge University Press:  14 December 2007

Barbara A. Williams*
Affiliation:
Wageningen Institute of Animal Sciences, Animal Nutrition Group, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
Martin W. A. Verstegen
Affiliation:
Wageningen Institute of Animal Sciences, Animal Nutrition Group, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
Seerp Tamminga
Affiliation:
Wageningen Institute of Animal Sciences, Animal Nutrition Group, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
*
*Corresponding author: Dr Barbara Williams, fax +31 317 484260, 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.

The phasing out of antibiotic compounds as growth promoters from the animal industry means that alternative practices will need to be investigated and the promising ones implemented in the very near future. Fermentation in the gastrointestinal tract (GIT) is being recognized as having important implications for health of the gut and thus of the host animal. Fermentation in single-stomached animals occurs to the largest extent in the large intestine, mainly because of the longer transit time there. The present review examines the micro-ecology of the GIT, with most emphasis on the large intestine as the most important site of fermentative activity, and an attempt is made to clarify the importance of the microfloral activity (i.e. fermentation) in relation to the health of the host. The differences between carbohydrate and protein fermentation are described, particularly in relation to their endproducts. The roles of volatile fatty acids (VFA) and NH3 in terms of their relationship to gut health are then examined. The large intestine has an important function in relation to the development of diarrhoea, particularly in terms of VFA production by fermentation and its role in water absorption. Suggestions are made as to feeds and additives (particularly those which are carbohydrate-based) which could be, or are, added to diets and which could steer the natural microbial population of the GIT. Various methods are described which are used to investigate changes in microbial populations and reasons are given for the importance of measuring the kinetics of fermentation activity as an indicator of microbial activity.

Type
Research Article
Copyright
Copyright © CABI Publishing 2001

References

Adrian, J (1976) Gums and hydrocolloids in nutrition. World Review of Nutrition and Dietetics 25, 189216.CrossRefGoogle ScholarPubMed
Allison, C & Macfarlane, GT (1989) Ifluence of pH, nutrient availability, and growth rate on amine production by Bacteroides fragilis and Clostridium perfringens. Applied and Environmental Microbiology 55, 28942898.CrossRefGoogle Scholar
Annison, G & Topping, DL (1994) Nutritional role of resistant starch: chemical structure vs physiological function. Annual Reviews in Nutrition 14, 297320.Google Scholar
Argenzio, RA, Moon, HW, Kemeny, LJ & Whipp, SC (1984) Colonic compensation in transmissible gastroenteritis of swine. Gastroenterology 86, 15011509.Google Scholar
Asp, N-G, van Amelsvoort, JMM & Hautvast, JGAJ (1996) Nutritional implications of resistant starch. Nutrition Research Reviews 9, 131.CrossRefGoogle ScholarPubMed
Baker, F, Nasr, H, Morrice, F & Bruce, J (1950) Bacterial breakdown of structural starches and starch products in the digestive tract of ruminant and non-ruminant mammals. Journal of Pathological Bacteriology 62, 617638.Google Scholar
Bauer, E, Williams, BA, Voigt, C, Mosenthin, R & Verstegen, MWA (2001) Microbial activities of faeces from unweaned and adult pigs, in relation to selected fermentable carbohydrates. Animal Science (In the Press).CrossRefGoogle Scholar
Bergman, EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract of various species. Physiological Reviews 70, 567590.Google Scholar
Bertshinger, HV, Eggenberger, E, Jucker, H & Pfirter, HP (1978) Evaluation of low nutrient, high fibre diets for the prevention of porcine Escherichia coli enterotoxaemia. Veterinary Microbiology 3, 281290.CrossRefGoogle Scholar
Blakeney, AB (1993) The occurrence and chemistry of resistant starch. In Dietary Fibre and Beyond – Australian Perspectives, vol 1, pp. 3746. [Samman, S and; Annison, G editors ]. Perth, Australia: Nutrition Society of Australia Occasional Publications.Google Scholar
Bourquin, LD, Titgemeyer, EC, Fahey, GC & Garleb, KA (1993) Fermentation of dietary fibre by human colonic bacteria: disappearance of short-chain fatty acid production from, and potential water-holding capacity of, various substrates. Scandinavian Journal of Gastroenterology 28, 249255.Google Scholar
Britton, R & Krehbiel, C (1993) Nutrient metabolism by gut tissues. Journal of Dairy Science 76, 21252131.Google Scholar
Bruininx, EMAM, & van der Peet-Schwering, CMC (1996) Post-weaning Diarrhoea of Piglets: Feeding and Escherichia coli. Proefverslag nummer P 1.159. Rosmalen: Proefstation voor de Varkenshouderij.Google Scholar
Bugaut, M (1987) Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comparative Biochemistry and Physiology 86, 439472.Google ScholarPubMed
Bugaut, M, & Bentéjac, M (1993) Biological effects of short-chain fatty acids in nonruminant mammals. Annual Reviews in Nutrition 13, 217241.Google Scholar
Calloway, DH (1968) Gas in the alimentary canal In Handbook of Physiology, Section 6: Alimentary Canal, vol. VBile, Digestion, Ruminal Physiology, pp. 28392860 [Heidel, W editor ]. Washington: American Physiological Society.Google Scholar
Canh, TT, Verstegen, MWA, Aarnink, AJA & Schrama, JW (1997) Influence of dietary factors on N partitioning and composition of urine and faeces of fattening pigs. Journal of Animal Science 75, 700706.Google Scholar
Cheng, B-O, Trimble, RP, Illman, RJ, Stone, BA & Topping, DL (1987) Comparative effects of dietary wheat bran and its morphological components (aleurone and pericarp-seed coat) on volatile fatty acid concentrations in the rat. British Journal of Nutrition 57, 6976.Google Scholar
Clarke, RTJ (1977) Methods for studying gut microbes. In Microbial Ecology of the Gut, pp. 1333 [Clarke, RJ and Bauchop, T editors ]. London: Academic Press.Google Scholar
Crittenden, RG & Playne, MJ (1996) Production, properties, and applications of food-grade oligosaccharides. Trends in Food Science and Technology 7, 353361.CrossRefGoogle Scholar
Cummings, JH (1983) Fermentation in the human large intestine: evidence and implications for health. Lancet i, 12061209.CrossRefGoogle Scholar
Cummings, JH & Englyst, HN (1987) Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45, 12431255.CrossRefGoogle ScholarPubMed
Cummings, JH, Pomare, EW, Branch, WJ, Naylor, CPE & Macfarlane, GT (1987) Short chain fatty acids in human large intestine, portal, hepatic, and venous blood. Gut 28, 12211227.CrossRefGoogle ScholarPubMed
De Wilde, R (1980) Influence of supplementing citrus pectin to a diet with and without antibiotics on the digestibility of pectins and other nutrients. Zeitschrift Tierphysiologie 43, 109116.Google Scholar
Djouzi, Z & Andrieux, C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rate inoculated with a human faecal flora. British Journal of Nutrition 78, 313324.Google Scholar
Dobbins, JW & Binder, HJ (1981) Pathophysiology of diarrhoea: alterations in fluid and electrolyte transport. Journal of Clinical Gastroenterology 10, 605626.Google Scholar
Dohgen, M, Hayaahshi, H, Yajima, T & Suzuki, Y (1994) Stimulation of bicarbonate secretion by luminal short-chain fatty acid in the rat and human colon in vitro. Japanese Journal of Physiology 44, 519531.Google Scholar
Dong, G, Zhou, A, Yang, F, Chen, K, Wang, K, and Dao, D (1996) Effect of dietary protein levels on the bacterial breakdown of protein in the large intestine, and diarrhoea in early weaned piglets. Acta Veterinaria et Zootechnica Sinica 27, 293302.Google Scholar
Drasar, BS (1988) The bacterial flora of the intestine. In Role of the Gut Flora in Toxicity and Cancer, pp. 2328 [Rowland, IR editor ]. London: Academic Press.Google Scholar
Drasar, BS (1989) The bacterial flora of the stomach and small intestine. Gastroenterologie Clinique et Biologique 13, 18B20B.Google Scholar
Drochner, W, Hazem, SA & Oelfke, S (1987) Intracaecal infusion of carbohydrates – a model for ‘fermentative diarrhea’ in the young pig? Advances in Animal Physiology and Animal Nutrition 17, 1535.Google Scholar
Eastwood, MA (1992) The physiological effect of dietary fibre: an update. Annual Reviews in Nutrition 12, 1935.Google Scholar
Edwards, SA (1996) A new look on the role of fibre in the diet of pigs. In Proceedings of the 6th European Society of Veterinary Internal Medicine, pp. 9091. Veldhoven, The Netherlands: Organizing Committee of the 6th ESVIM Congress.Google Scholar
Eisemann, JH & Nienaber, JA (1990) Tissue and whole body oxygen uptake in fed and fasted steers. British Journal of Nutrition 64, 399411.Google Scholar
Englyst, HN & Cummings, JH (1985) Digestion of the polysaccharides of some cereal foods in the human small intestine. American Journal of Clinical Nutrition 42, 778787.CrossRefGoogle ScholarPubMed
Englyst, HN, Hay, S, & Macfarlane, GT (1987) Polysaccharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiology Ecology 95, 163171.Google Scholar
Erickson, KL, & Hubbard, NE (2000) Probiotic immunomodulation in health and disease. Journal of Nutrition 130, 403S409S.CrossRefGoogle ScholarPubMed
Ewing, WN & Cole, DJA (1994) The Living Gut: An Introduction to Micro-organisms in Nutrition. Dungannon, Ireland: Context.Google Scholar
Finegold, SM & Sutter, VL (1978) Faecal flora in different populations with special reference to diet. American Journal of Clinical Nutrition 31, S116S122.CrossRefGoogle ScholarPubMed
Florent, C, Flourie, B, Leblond, A, Rautureau, M, Bernier, J-J & Rambaud, J-C (1985) Influence of chronic lactulose ingestion on the colonic metabolism of lactulose in man (an in vivo study). Journal of Clinical Investigation 75, 608613.CrossRefGoogle ScholarPubMed
Freter, R (1992) Factors affecting the microecology of the gut. In Probiotics – The Scientific Basis, pp. 111114 [Fuller, R editor ]. London: Chapman & Hall.CrossRefGoogle Scholar
Freter, R, Brickner, H, Fekete, J, Vickerman, MM & Carey, KE (1983) Survival and implantation of Escherichia coli in the intestinal tract. Infection and Immunity 39, 686703.Google Scholar
Gálfi, P & Bokori, J. (1990) Feeding trials in pigs with a diet containing sodium n-butyrate. Acta Veterinaria Hungarica 38, 317.Google Scholar
Gálfi, P & Neogrády, S (1996) Short chain fatty acids (acidifiers) as probiotics in diets for piglets. In Fourth International Feed Production|Conference, Piacenza, pp. 2526 [Piva, G editor ], Milan: Bureau Veritas.Google Scholar
Gibson, GR, & Fuller, R (2000) Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. Journal of Nutrition 130, 391S395S.CrossRefGoogle ScholarPubMed
Gibson, GR., Willis, CL, & van Loo, J (1994) Non-digestible oligosaccharides and Bifidobacteria – implications for health. International Sugar Journal 96, 381387.Google Scholar
Goldin, BR & Gorbach, SL (1976) The relationship between diet and rat faecal enzymes implicated in colon cancer. Journal of the National Cancer Institute 57, 371375.CrossRefGoogle ScholarPubMed
Goodlad, JS, & Mathers, JC (1988) Effects of food carbohydrates on large intestinal fermentation in vitro. Proceedings of the Nutrition Society 47, 176A.Google Scholar
Goodlad, JS, & Mathers, JC (1990) Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). British Journal of Nutrition 64, 569587.CrossRefGoogle ScholarPubMed
Gottschalk, G (1979) Bacterial fermentation. In Bacterial Metabolism, pp. 167224 [Gottschalk, G editor ]. New York: Springer-Verlag.CrossRefGoogle Scholar
Grubb, JA & Dehority, BA (1976) Variation in colony counts of total viable anaerobic rumen bacteria as influenced by media and cultural methods. Applied and Environmental Microbiology 31, 262267.CrossRefGoogle ScholarPubMed
Hackstein, JHP, van Alen, TA, op den Kamp, H, Smits, A & Mariman, E (1995) Intestinal methanogenesis in primates – a genetic and evolutionary approach. Deutsches Tierärzliches Wochenschau 102, 143178.Google ScholarPubMed
Hawe, SM, Walker, N & Moss, BW (1991) The effects of dietary fibre, lactose and antibiotic on the levels of skatole and indole in faeces and subcutaneous fat in growing pigs. Animal Production 54, 413419.Google Scholar
Hayakawa, K, Mizutani, J, Wada, K, Masai, T, Yoshihara, I & Mitsuoka, T (1990) Effects of soybean oligosaccharides on human faecal microflora. Microbial Ecology in Health and Disease 3, 293303.Google Scholar
Heneghan, JB (1988) Alimentary tract physiology: interactions between the host and its microbial flora. In Role of the Gut Flora in Toxicity and Cancer, pp. 3978 [Rowland, IR editor ]. London: Academic Press.Google Scholar
Henning, SJ & Hird, FJR (1972) Transport of acetate and butyrate in the hind-gut of rabbits. Biochemistry Journal 130, 791796.CrossRefGoogle ScholarPubMed
Hentges, DJ (1978) Faecal flora of volunteers on controlled diets. American Journal of Clinical Nutrition 31, S123S124.CrossRefGoogle ScholarPubMed
Hentges, DJ (1983) Role of intestinal flora in host defence against infection. In Human Intestinal Flora in Health and Disease, pp. 311331 [Hentges, DJ editor ]. New York: Academic Press.CrossRefGoogle Scholar
Hentges, DJ (1986) The protective function of the indigenous intestinal flora. Pediatric Infectious Disease 5, S17S20.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, 3750.Google Scholar
Hill, MJ (1983) Bacterial adaptation to lactase deficiency. In Milk Intolerance and Rejection, pp. 2226 [Delmont, JC editor ]. Basel: Karger.Google Scholar
Holdeman, LV, Cato, EP & Moore, WEC (1977) Anaerobe Laboratory Manual, 4th ed. Blacksburg, VA: Blacksburg Virginia Polytechnic Institute and State University.Google Scholar
Holloway, WD, Tasman-Jones, C & Mather, K (1983) Pectin digestion in humans. American Journal of Clinical Nutrition 37, 253255.Google Scholar
Houdijk, J (1998) Effects of non-digestible oligosaccharides in young pig diets. PhD Thesis, Wageningen Agricultural University, Wageningen.Google Scholar
Hungate, RE (1966) The Rumen and its Microbes. London and New York: Academic Press.Google Scholar
Ito, M, Kimura, M, Deguchi, Y, Miyamori-Watabe, A, Yamjima, T & Kan, T (1993) Effects of transgalactosylated disaccharides on the human intestinal microflora and their metabolism. Journal of Nutritional Science and Vitaminology 39, 279288.Google Scholar
Jensen, BB & Jørgensen, H (1994) Effect of dietary fibre on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Applied and Environmental Microbiology 60, 18971904.Google Scholar
Kaneko, T, Kohmoto, T, Kikuchi, H, Shiota, M, Iino, H & Mitsuoka, T (1994) Effects of isomaltooligosaccharides with different degrees of polymerization on human faecal Bifidobacteria. Bioscience Biotechnology and Biochemistry 58, 22882290.Google Scholar
Key, FB & Mathers, JC (1993) Complex carbohydrate digestion and large bowel fermentation in rats given wholemeal bread and cooked haricot beans (Phaseous vulgaris) fed in mixed diets. British Journal of Nutrition 69, 497509.CrossRefGoogle ScholarPubMed
Kirchgessner, M, Kreuzer, M, Machmüller, A & Roth-Maier, DA (1993) Evidence for a high efficiency of bacterial protein synthesis in the digestive tract of adult sows fed supplements of fibrous feedstuffs. Animal Feed Science and Technology 46, 293306.Google Scholar
Knowles, SE, Jarrett, IG, Filsell, OH & Ballard, FJ (1974) Production and utilization of acetate in mammals. Biochemistry Journal 142, 401411.Google Scholar
Liebler, EM, Pohlenz, JF & Whipp, SC (1992) Digestive system. In Diseases of Swine, 7th ed., pp. 331348 [Leman, AD, Straw, BE, Mengeling, WL, D’Allaire, S and Taylor, DJ editors ]. Ames: Iowa State University Press.Google Scholar
Linton, AH, Handley, B & Osbourne, AD (1978) Fluctuations in E. coli O-serotypes in pigs throughout life in the presence and absence of antibiotic treatment. Journal of Applied Bacteriology 44, 285298.CrossRefGoogle Scholar
McBurney, MI, Cuff, DJ & Thompson, LU (1990) Rates of fermentation and short chain fatty acid and gas production of six starches by human faecal microbiota. Journal of the Science of Food and Agriculture 50, 7988.CrossRefGoogle Scholar
McBurney, MI, Thompson, LU, Cuff, DJ & Jenkins, DJA (1988) Comparison of ileal effluents, dietary fibers, and whole foods in predicting the physiologic importance of colonic fermentation. American Journal of Gastroenterology 83, 536540.Google Scholar
Macfarlane, GT, Gibson, GR, Beatty, E & Cummings, JH (1992) Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiology Ecology 101, 8188.Google Scholar
McNeil, NI, Cummings, JH & James, WPT (1978) Short-chain fatty acid absorption by the human large intestine. Gut 19, 819822.CrossRefGoogle ScholarPubMed
Madec, F & Josse, J (1983) Influence of environmental factors on the onset of digestive disorders of the weaned piglet. Annales de Recherches Véterinaires 14, 456462.Google ScholarPubMed
Makkink, CA (1993) Of piglets, dietary proteins, and pancreatic proteases. PhD Thesis, Wageningen Agricultural University, Wageningen.Google Scholar
Mallett, AK, Bearne, CA, Young, PJ & Rowland, IR (1988) Influence of starches of low digestibility on the rat caecal microflora. British Journal of Nutrition 60, 597604.CrossRefGoogle ScholarPubMed
Mallett, AK & Rowland, IR (1988) Factors affecting the gut microflora. In Role of the Gut Flora in Toxicity and Cancer, pp. 347382 [Rowland, IR editor ]. London: Academic Press.CrossRefGoogle Scholar
Marsono, Y, Illman, RJ, Clarke, JM, Trimble, RP & Topping, DL (1993) Plasma lipids and large bowel volatile fatty acids in pigs fed on white rice, brown rice and rice bran. British Journal of Nutrition 70, 503513.CrossRefGoogle Scholar
Mason, VC & Just, A (1976) Bacterial activity in the hindgut of pigs. 1. Its influence on the apparent digestibility of dietary energy and fat. Zeitschrift für Tiererphysiologie, Tierernährung und Futtermittelkunde 36, 301310.Google Scholar
Mason, VC, Narang, MP, Ononiwu, JC & Kessank, P (1977) The relationship between nitrogen metabolism in the hind gut and nitrogen excretion. In Protein Metabolism and Nutrition, pp. 6163. Wageningen, The Netherlands: Centre for Agricultural Publishing and Documentation.Google Scholar
Mathers, JC & Annison, EF (1993) Stoichiometry of polysaccharide fermentation in the large intestine. In Dietary Fibre and Beyond – Australian Perspectives, vol 1, pp. 123135 [Samman, S and Annison, G editors ]. Perth, Australia: Nutrition Society of Australia Occasional Publications.Google Scholar
Mathers, JC, Fernandez, R, Hill, MJ, McCarthy, PT, Shearer, MJ & Oxley, A (1990) Dietary modification of potential vitamin K supply from enteric bacterial menaquinones in rats. British Journal of Nutrition 63, 639652.CrossRefGoogle ScholarPubMed
Mathers, JC, Smith, H & Carter, S (1997) Dose–response effects of raw potato starch on small-intestinal escape, large-bowel fermentation and gut transit time in the rat. British Journal of Nutrition 78, 10151029.CrossRefGoogle ScholarPubMed
Mathew, AG, Sutton, AL, Scheidt, AB, Patterson, JA, Kelly, DT & Meyerholz, KA (1993) Effect of galactan on selected microbial populations and pH and volatile fatty acids in the ileum of the weanling pig. Journal of Animal Science 71, 15031509.Google Scholar
Midtvedt, T (1989) In Recent Advances in Microbial Ecology, pp. 515519 [Hattori, T, Ischida, Y and Maruyama, Y editors ]. Tokyo: Japan Scientific Societies Press.Google Scholar
Misir, S & Sauer, WC (1982) Effect of starch infusion at the terminal ileum on N balance and apparent digestibilities of nitrogen and amino acids in pigs fed meat-and-bone and soybean meal diets. Journal of Animal Science 55, 599607.Google Scholar
Moore, WEC, Cato, EP & Holdeman, LV (1978) Some current concepts in intestinal bacteriology. American Journal of Clinical Nutrition 31 S33S42.Google Scholar
Moore, WEC & Holdeman, LV (1974) Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Applied Microbiology 27, 961979.Google Scholar
Newby, TJ, Miller, BG, Stokes, CR & Bourne, FJ (1984) Hypersensitivity to dietary antigens as the predisposing factor in post-weaning diarrhoea. Pig Veterinary Society Proceedings 16, 5058.Google Scholar
Nousiainen, JT (1991) Comparative observations on selected probiotics and olaquindox as feed additives for piglets around weaning. 2. Effect on villus length and crypt depth in the jejunum, ileum, caecum and colon. Journal of Animal Physiology and Animal Nutrition 66, 224230.CrossRefGoogle Scholar
Ofek, I, Mirelman, D & Sharon, N (1977) Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature 265, 623625.CrossRefGoogle ScholarPubMed
Paul, PS & Stevenson, GW (1992) Rotavirus and Reovirus. In Diseases of Swine – 7th ed., pp. 331348 [Leman, AD, Straw, BE, Mengeling, WL, D'Allaire, S and Taylor, DJ editors ]. Ames: Iowa State University Press.Google Scholar
Piva, A, Panciroli, A, Meola, E & Formigoni, A (1995) Lactitol enhances short-chain fatty acid and gas production by swine cecal microflora to a greater extent when fermenting low rather than high fibre diets. Journal of Nutrition 126, 280289.Google Scholar
Pomare, EW, Branch, WJ and; Cummings, JH (1985) Carbohydrate fermentation in the human colon and its relation to acetate concentrations in venous blood. Journal of Clinical Investigation 75, 14481454.CrossRefGoogle ScholarPubMed
Que, JU, Casey, SW, & Hentges, DJ (1986) Factors responsible for increased susceptibility of mice to intestinal colonization after treatment with streptomycin. Infection and Immunity 53, 116123.Google Scholar
Radcliffe, BC, Nance, SH, Deakin, EJ & Roediger, WEW (1987) Effect of luminal or circulating nitrite on colonic ion movement in the rat. American Journal of Physiology 253, G246G252.Google ScholarPubMed
Raibaud, P (1992) Bacterial interactions in the gut. In Probiotics – The Scientific Basis, pp. 928 [Fuller, R editor ]. London: Chapman & Hall.Google Scholar
Rall, GD, Wood, AJ, Wescott, RB & Dommert, AR (1970) Distribution of bacteria in feces of swine. Applied Microbiology 20, 789792.CrossRefGoogle ScholarPubMed
Ramakrishna, BS (1996) Colonic fluid handling in health and acute diarrhoea. Indian Journal of Medical Research 104, 5259.Google Scholar
Ramakrishna, BS & Mathan, VI (1993) Short chain fatty acids and colonic dysfunction in cholera. Gastroenterology 104, 273 Abst.Google Scholar
Ramakrishna, BS, Nance, SH, Roberts-Thomson, IC & Roediger, WEW (1990) The effects of enterotoxins and short-chain fatty acids on water and electrolyte fluxes in ileal and colonic loops in vivo in the rat. Digestion 45, 93101.CrossRefGoogle ScholarPubMed
Ramakrishna, BS, Venkatraman, S, Srinivasan, P, Dash, P, Young, GP & Binder, HJ (2000) Amylase-resistant starch plus oral rehydration solution for cholera. New England Journal of Medicine 342, 308313.CrossRefGoogle ScholarPubMed
Rasmussen, HS, Holtug, K & Mortensen, PB (1988) Degradation of amino acids to short-chain fatty acids in humans. Scandinavian Journal of Gastroenterology 23, 178182.Google Scholar
Read, NW (1982) Diarrhoea: the failure of colonic salvage. Lancet ii, 481483.Google Scholar
Rechkemmer, G, Rönnau, K & von Englelhardt, W (1988) Fermentation of polysaccharides and absorption of short chain fatty acids in the mammalian hindgut. Comparative Biochemistry and Physiology 90, 563568.CrossRefGoogle ScholarPubMed
Renault, L, Le Bourhis, E & Alamagny, A (1982) Les différents formes de colibacillose du porc en France selon les groupes sérologiques d'E. coli. (The different forms of porcine colibacillosis in France, according to serological grouping of E. coli). Journal Recherche Porc France 14, 387396.Google Scholar
Robinson, JA, Smolenski, WJ, Ogilvie, ML & Peters, JP (1989) In vitro total-gas, CH4, H2, volatile fatty acid, and lactate kinetic studies on luminal contents from the small intestine, caecum, and colon of the pig. Applied and Environmental Microbiology 55, 24602467.Google Scholar
Roediger, WEW (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424429.CrossRefGoogle ScholarPubMed
Roediger, WEW (1989) Faecal anions and lactate in severe ulcerative colitis. Digestive Diseases and Sciences 34, 18011805.CrossRefGoogle ScholarPubMed
Roediger, WEW (1989) Short-chain fatty acids as metabolic regulators of ion absorption in the colon. Acta Veterinaria Scandinavica 86, 116125.Google ScholarPubMed
Roediger, WEW (1994) Famine, fiber, fatty acids, and failed colonic absorption: does fiber fermentation ameliorate diarrhea? Journal of Parenteral and Enteral Nutrition 18, 48.Google Scholar
Roediger, WEW & Moore, A (1981) Effect of short-chain fatty acid on sodium absorption in isolated human colon perfused through the vascular bed. Digestive Diseases and Sciences 26, 100106.CrossRefGoogle ScholarPubMed
Roland, N, Nugon-Baudon, L, Andrieux, C & Szylit, O (1995) Comparative study of the fermentative characteristics of inulin and different types of fibre in rats inoculated with a human whole faecal flora. British Journal of Nutrition 74, 239249.Google Scholar
Rolfe, RD (1984) Role of volatile fatty acids in colonization resistance to Clostridium difficile. Infection and Immunity 45, 185191.CrossRefGoogle ScholarPubMed
Roth, JA, Frankel, WL, Wei Zhang, MD, Klurfeld, DM & Rombeau, JL (1995) Pectin improves colonic function in rat short bowel syndrome. Journal of Surgical Research 58, 240246.CrossRefGoogle ScholarPubMed
Rowland, IR (1992) Metabolic interactions in the gut. In Probiotics – The Scientific Basis, pp. 2953 [Fuller, R editor ]. London: Chapman & Hall.CrossRefGoogle Scholar
Rowland, IR & Wise, A (1985) The effect of diet on the mammalian flora and its metabolic activities. CRC Critical Reviews in Toxicology 16, 31103.CrossRefGoogle ScholarPubMed
Ruppin, H, Bar-Meir, S, Soergel, KH, Wood, CM & Schmitt, MG (1980) Absorption of short-chain fatty acids by the colon. Gastroenterology 78, 15001507.Google Scholar
Russell, JB, Sniffen, CJ & Van Soest, PJ (1983) Effect of carbohydrate limitation on degradation and utilization of casein by mixed rumen bacteria. Journal of Dairy Science 66, 763775.Google Scholar
Saif, LJ & Wesley, RD (1992) Transmissible gastroenteritis. In Diseases of Swine – 7th ed., pp. 362386 [Leman, AD, Straw, BE, Mengeling, WL, D'Allaire, S and Taylor, DJ editors ]. Ames: Iowa State University Press.Google Scholar
Salanitro, JP, Fairchilds, IG & Zgornicki, YD (1974) Isolation, culture characteristics, and identification of anaerobic bacteria from the chicken cecum. Applied Microbiology 27, 678687.Google Scholar
Salas-Coll, CA, Kermode, JC & Edmonds, CJ (1976) Potassium transport across the distal colon in man. Clinical Science and Molecular Medicine 51, 287296.Google Scholar
Saunders, DR & Wiggens, HS (1981) Conservation of mannitol, lactulose, and raffinose by the human colon. American Journal of Physiology 21, G397G402.Google Scholar
Savage, DC (1977) Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology 31, 107133.CrossRefGoogle ScholarPubMed
Savage, DC (1980) Impact of antimicrobials on the microbial ecology of the gut. In Effects on Human Health of Subtherapeutic Use of Antimicrobials in Animal Feeds. Appendix D. Washington, DC: National Academy of Sciences.Google Scholar
Savage, DC (1986) Gastrointestinal microflora in mammalian nutrition. Annual Reviews in Nutrition 6, 155178.CrossRefGoogle ScholarPubMed
Savage, TF & Zakrzewska, EI (1996) The role of mannan oligosaccharide (Bio-Mos) in animal nutrition. In Alltech European and South African Lecture Tour 1996, pp. 5563. Nottingham: Nottingham University Press.Google Scholar
Scheppach, W. (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35, Suppl. 1, S35S38.Google Scholar
Scheppach, W, Fabian, C, Sachs, M & Kaspar, H (1988) The effect of starch malabsorption on fecal short-chain fatty acid excretion in man. Scandinavian Journal of Gastroenterology 23, 755759.CrossRefGoogle ScholarPubMed
Simon, GL, & Gorbach, SL (1984) Intestinal flora in health and disease. Gastroenterology 86, 174193.CrossRefGoogle ScholarPubMed
Skadhauge, E (1985) The secretory response of the digestive tract to the diet. In Digestive Physiology in the Pig [Just, A, Jörgensen, H and Fernandez, JA editors ]. Report from the National Institute of Animal Science, Denmark, No. 580 81100. Copenhagen, Denmark: National Institute of Animal Science.Google Scholar
Smith, JG & German, JB (1995) Molecular and genetic effects of dietary derived butyric acid. Food Technology 49, 8790.Google Scholar
Soergel, KH (1994) Colonic fermentation: metabolic and clinical implications. Clinical Investigations 72, 742748.Google ScholarPubMed
Spring, P, & Privulescu, M (1998) Mannan-oligosaccharide: its logical role as a natural feed additive for piglets. In ‘Biotechnology in the Feed Industry’, Proceedings of the 4th Annual Symposium of Alltech, pp. 553561. Nottingham: Nottingham University Press.Google Scholar
Stanogias, G & Pearce, GR (1985) The digestion of fibre by pigs. 2. Volatile fatty acid concentrations in large intestine digesta. British Journal of Nutrition 53, 531536.CrossRefGoogle ScholarPubMed
Stewart, CS, Hillman, K, Maxwell, F, Kelly, D & King, TP (1993) Recent advances in probiosis in pigs: observations on the microbiology of the pig gut. In Recent Advances in Animal Nutrition, pp. 197220 [Garnsworthy, PC and Cole, DJA editors ]. Nottingham: Nottingham University Press.Google Scholar
Sutton, AL & Patterson, JA (1996) Effects of dietary carbohydrates and organic acid additions on pathogenic E. coli and other microorganisms in the weanling pig. Proceedings of the 5th International Symposium on Animal Nutrition, Kaposvár, Hungary, pp. 3161. Kaposvár, Hungary: Pannon Agricultural University.Google Scholar
Svensmark, B, Nielsen, K, Willeberg, P & Jorsal, SE (1989) Epidemiological studies of piglet diarrhoea in intensively managed Danish sow herds. Acta Veterinaria Scandinavica 30, 5562.CrossRefGoogle ScholarPubMed
Tamura, Y, Mizota, T, Shimamura, S & Tomita, M (1993) Lactulose and its application to the food and pharmaceutical industries. Bulletin of the International Dairy Federation 289, 4353.Google Scholar
Tanaka, R, Takayama, H, Morotomi, M, Kuroshima, T, Ueyama, S, Matsumoto, K, Kuroda, A & Mutai, M (1983) Effects of administration of TOS and Bifidobacterium breve 4006 on the human faecal flora. Bifidobacteria Microflora 2, 1724.Google Scholar
Taylor, DJ & Bergeland, ME (1992) Clostridial infections. In Diseases of Swine – 7th ed., pp. 454469 [Leman, AD, Straw, BE, Mengeling, WL, D'Allaire, S and Taylor, DJ editors ]. Ames: Iowa State University Press.Google Scholar
Theodorou, MK, Williams, BA, Dhanoa, MS, McAllan, AB & France, J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology 48, 185197.Google Scholar
Tomomatsu, H (1994) Health effects of oligosaccharides. Food Technology 48, 6165.Google Scholar
Tsuji, K, Shimizu, M, Nishimura, Y, Nakagawa, Y & Ichikawa, T (1992) Simultaneous determination of hydrogen, methane, and carbon dioxide of breath using gas-solid chromatography. Journal of Nutritional Science and Vitaminology 38, 103109.CrossRefGoogle ScholarPubMed
Tulung, B, Rémésy, C & Demigné, JVGA (1987) Specific effect of guar gum or gum arabic on adaptation of cecal digestion to high fiber diets in the rat. Journal of Nutrition 117, 15561561.CrossRefGoogle ScholarPubMed
Van der Waaij, D (1987) Colonization resistance of the digestive tract – mechanism and clinical consequences. Die Nahrung 31, 507517.CrossRefGoogle ScholarPubMed
Van der Waaij, D (1989) The ecology of the human intestine and its consequences for overgrowth of pathogens such as Clostridium difficile. Annual Reviews in Microbiology 43, 6987.Google Scholar
Van der Waaij, D, Berghuis de Vries, JM & Lekkerkerk van der Wees, JEC (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. Journal of Hygiene (London) 69, 405411.CrossRefGoogle ScholarPubMed
Vannier, P (1983) Gastroenteritis, nutrition and environment. Annales de Recherches Véterinaires 14, 449.Google Scholar
Vannier, P, Tillon, JP, Madec, F & Morisse, JP (1983) Environment and gastroenteritis. Annales de Recherches Véterinaires 14, 450455.Google Scholar
Vaughan, EE, Schut, F, Heilig, HGHJ, Zoetendahl, EG, de Vos, WM & Akkermans, ADL (2000) A molecular view of the intestinal ecosystem. Current Issues in Intestinal Microbiology 1, 112.Google ScholarPubMed
Vernia, P, Caprilli, R, Latella, G, Barbetti, F, Magliocca, FM & Cittadini, M (1988) Faecal lactate and ulcerative colitis. Gastroenterology 95, 15641568.Google Scholar
Visek, WJ (1984) Ammonia: its effects on biological systems, metabolic hormones, and reproduction. Journal of Dairy Science 67, 481498.CrossRefGoogle ScholarPubMed
Von Glawischnig, E (1990) Ein Beitrag zum antibioticafreien Absetzen der Ferkel (Antibiotic-free weaning of piglets). Deutscher Tierärztlicher Wochenschau 97, 4851.Google Scholar
Walter, DJ, Eastwood, MA, Brydon, WG & Elton, RA (1988) Fermentation of wheat bran and gum arabic in rats fed on an elemental diet. British Journal of Nutrition 60, 225232.Google Scholar
Wang, X & Gibson, GR (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. Journal of Applied Bacteriology 75, 373380.CrossRefGoogle ScholarPubMed
Williams, BA, Bhatia, SK, Boer, H & Tamminga, S (1995) A preliminary study using the cumulative gas production technique to compare the kinetics of different fermentations by use of standard substrates. Annales de Zootechnie 44, Suppl. 1, 35.Google Scholar
Williams, BA, Bosch, M, Houdijk, J & van de Camp, Y (1997 a) Differences in potential fermentative capablilities of four sections of porcine digestive tract. In Proceedings of the 48th EAAP meeting, Vienna. 195 Abstr. Wageningen, The Netherlands: Wageningen Pers.Google Scholar
Williams, BA, Tamminga, S & Verstegen, MWA (2000 a) Fermentation kinetics to assess microbial activity of gastro-intestinal microflora. In Proceedings of the Symposium ‘Gas Production: Fermentation kinetics for feed evaluation and to assess microbial activity’, Wageningen, Netherlands, pp. 97100. Penicuik, UK: British Society of Animal Sciences.Google Scholar
Williams, BA, Van Osch, LJM & Kwakkel, RP (1997) Fermentation characteristics of the caecal contents of broiler chickens fed fine- and coarse particle diets. British Poultry Science 38, S41S42.Google Scholar
Williams, BA, Zhu, W-Y, Akkermans, A & Tamminga, S (2000 b) An in vitro test for prebiotics. Reproduction Nutrition Development 40, 225.Google Scholar
Wrong, OM & Vince, AJ (1984) Urea and ammonia metabolism in the human large intestine. Proceedings of the Nutrition Society 43, 7786.CrossRefGoogle ScholarPubMed
Yazawa, K, Imai, K & Tamura, Z (1978) Oligosaccharides and polysaccharides specifically utilisable by bifidobacteria. Chemical and Pharmacological Bulletin 26, 33063311.Google Scholar
Yokoyama, MT, Tabori, C, Miller, ER & Hogberg, MG (1982) The effects of antibiotic in the weanling pig diet on growth and the excretion of volatile phenolic and aromatic bacterial metabolites. American Journal of Clinical Nutrition 35, 14171424.Google Scholar
Ziemer, CJ, Sharp, R, Stern, MD, Cotta, MA, Whitehead, TR & Stahl, DA (2000) Comparison of microbial populations in model and natural rumens using 165 ribosomal RNA-targeted probes. Environmental Microbiology 2, 632643.Google Scholar
Zoetendaal, EG, Akkermans, ADL & de Vos, WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human faecal samples reveals stable and host-specific communities of active bacteria. Applied and Environmental Microbiology 64, 38543859.CrossRefGoogle Scholar