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Large bowel fermentation in rats given diets containing raw peas (Pisum sativum)

Published online by Cambridge University Press:  09 March 2007

J. S. Goodlad  and
J. C. Mathers
J. S. Goodlad
Affiliation:
Department of Agricultural Biochemistry and Nutrition, University of Newcastle upon Tyne, Newcastle upon Tyne NEI 7RU
J. C. Mathers*
Affiliation:
Department of Agricultural Biochemistry and Nutrition, University of Newcastle upon Tyne, Newcastle upon Tyne NEI 7RU
*
*For reprints.
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Abstract

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The digestion of non-starch polysaccharides (NSP) was studied in rats given semi-purified diets containing 0-500 g raw peas (Pisum sativum)/kg. NSP were equally well digested at all inclusion levels with digestibilities for individual constituents ranging from 0.58 for xylans to 0.99 for arabinose-containing polymers with a total NSP digestibility of 0.79. Increasing the dietary pea inclusion rate increased the amount of substrate flowing to the large bowel (LB) and this was associated with marked increases in caecal tissue and contents masses, a reduction in caecal transit time from 0.88 to 0.43 d and a threefold increase in faecal bacterial biomass output. Caecal pH fell as did the molar proportions of acetate, isobutyrate, isovalerate and valerate whilst butyrate increased when peas were included in the diet. Possible mechanisms for these fermentation end-product changes are discussed. Pea inclusion in the diet was associated with increased volatile fatty acid and 3-hydroxy butyrate concentrations in portal and heart blood. It was concluded that peas are a rich source of fermentable polysaccharides which produce a LB fermentation pattern of potential health benefit.

Keywords

Large bowel fermentationCarbohydrate digestionPeasRat
Type
Lower Gut Digestion
Information
British Journal of Nutrition , Volume 64 , Issue 2 , September 1990 , pp. 569 - 587
Copyright
Copyright © The Nutrition Society 1990

References

Aas, M. (1971). Organ and subcellular distribution of fatty acid activating enzymes in the rat. Biochimica et Biophysica Acta 231, 32–47.Google Scholar
Ardawi, M. S. M. & Newsholme, E. A. (1985). Fuel utilization in colonocytes of the rat. Biochemical Journal 231, 713–719.Google Scholar
Ash, R. & Baird, G. D. (1973). Activation of volatile fatty acids in bovine liver and rumen epithelium. Evidence for control by autoregulation. Biochemical Journal 136, 311–319.Google Scholar
Bergman, E. N. (1975). Production and utilization of metabolites by the alimentary tract as measured in portal and hepatic blood. In Digestion and Metabolism in the Ruminant, pp. 292–305 [McDonald, I. W. and Warner, A. C. I., editors]. Armidale: University of New England Publishing Unit.Google Scholar
Buckley, B. M. & Williamson, D. H. (1977). Origins of blood acetate in the rat. Biochemical Journal 166, 539–545.Google Scholar
Chacko, A. & Cummings, J. H. (1988). Nitrogen losses from the human small bowel: obligatory losses and the effect of physical form of food. Gut 29, 809–815.CrossRefGoogle ScholarPubMed
Chapman, R. W., Sillery, J. K., Graham, M. M. & Saunders, D. R. (1985). Absorption of starch by healthy ileostomates: effect of transit time and of carbohydrate load. American Journal of Clinical Nutrition 41, 1244–1248.CrossRefGoogle ScholarPubMed
Chen, W. L., Anderson, J. W. & Jennings, D. (1984). Propionate may mediate the hypocholesterolemic effects of certain soluble plant fibres in cholesterol-fed rats. Proceedings of the Society for Experimental Biology and Medicine 177, 372–376.Google Scholar
Cheng, B.-Q., Trimble, R. P., Illman, R. J., Stone, B. A. & Topping, D. L. (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, 69–76.CrossRefGoogle ScholarPubMed
Cummings, J. H. & Branch, W. J. (1982). Postulated mechanisms whereby fiber may protect against large bowel cancer. In Dietary Fiber in Health and Disease, pp. 313–325 [Vahouny, G. V. and Kritchevsky, D., editors]. London: Plenum Press.CrossRefGoogle Scholar
Cummings, J. H. & Englyst, H. N. (1987). Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45, 1243–1245.Google Scholar
Demeyer, D. I. & Van Nevel, C. J. (1975). Methanogenesis, an integrated part of carbohydrate fermentation, and its control. In Digestion and Metabolism in the Ruminant, pp. 366–382 [McDonald, I. W. and Warner, A. C. I., editors]. Armidale: University of New England Publishing Unit.Google Scholar
Demigné, C. & Rémésy, C. (1985). Stimulation of absorption of volatile fatty acids and minerals in the cecum of rats adapted to a very high fiber diet. Journal of Nutrition 115, 53–60.Google Scholar
Demigné, C., Yacoub, C. & Rémésy, C. (1986 a). Effects of absorption of large amounts of volatile fatty acids on rat liver metabolism. Journal of Nutrition 116, 77–86.CrossRefGoogle ScholarPubMed
Demigné, C., Yacoub, C., Rémésy, C. & Fafournoux, P. (1986 b). Propionate and butyrate metabolism in rat or sheep hepatocytes. Biochimica et Biophysica Acta 875, 535–542.CrossRefGoogle ScholarPubMed
El-Shazly, K. (1952). Degradation of protein in the rumen of sheep. II. Amino acid degradation by washed suspensions of rumen bacteria. Biochemical Journal 51, 647–653.Google Scholar
Englyst, H. N. & Cummings, J. H. (1984). Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as the alditol acetates. Analyst 109, 937–942.CrossRefGoogle Scholar
Englyst, H. N. & Cummings, J. H. (1985). Digestion of the polysaccharides of some cereal foods in the human small intestine. American Journal of Clinical Nutrition 42, 778–787.Google Scholar
Englyst, H. N. & Cummings, J. H. (1987). Resistant starch, a ‘new’ food component: a classification of starch for nutritional purposes. In Cereals in a European Context, pp. 221–233 [Morton, I. D., editor]. Chichester: Ellis Horwood Ltd.Google Scholar
Englyst, H. N., Hay, S. & Macfarlane, G. T. (1987). Polysaccharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiological Letters 45, 163–171.CrossRefGoogle Scholar
Faichney, G. J. (1975). The use of markers to partition digestion within the gastro-intestinal tract of ruminants. In Digestion and Metabolism in the Ruminant, pp. 277–291 [McDonald, I. W. and Warner, A. C. I., editors]. Armidale: University of New England Publishing Unit.Google Scholar
Faulks, R. M., Southon, S. & Livesey, G. (1989). Utilization of α-amylase (EC 3.2.1. 1) resistant maize and pea (Pisum sativum) starch in the rat. British Journal of Nutrition 61, 291–300.Google Scholar
Finlayson, H. J. (1986). The effect of pH on the growth and metabolism of Streptococcus bovis in continuous culture. Journal of Applied Bacteriology 61, 201–208.CrossRefGoogle ScholarPubMed
Fleming, S. E. & Vose, J. R. (1979). Digestibility of raw and cooked starches from legume seeds using the laboratory rat. Journal of Nutrition 109, 2067–2075.CrossRefGoogle ScholarPubMed
Gibson, G. R., Cummings, J. H. & Macfarlane, G. T. (1988). Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Applied and Environmental Microbiology 54, 2750–2755.Google Scholar
Gibson, J. A., Sladen, G. E. & Dawson, A. M. (1976). Protein absorption and ammonia production: the effects of dietary protein and removal of the colon. British Journal of Nutrition 35, 61–65.Google Scholar
Goodlad, J. S. (1989). Digestion and large intestinal fermentation of pea (Pisum sativum) carbohydrates. PhD Thesis, University of Newcastle upon Tyne.Google Scholar
Goodlad, J. S. & Mathers, J. C. (1987). Digesta flow from the ileum and transit time through the caecum of rats given diets containing graded levels of peas. Proceedings of the Nutrition Society 46, 149A.Google Scholar
Goodlad, J. S. & Mathers, J. C. (1988). Effects of food carbohydrates on large intestinal fermentation in vitro. Proceedings of the Nutrition Society 47, 176A.Google Scholar
Goodlad, R. A., Ratcliffe, B., Fordham, J. P. & Wright, N. A. (1989). Does dietary fibre stimulate intestinal epithelial cell proliferation in germ free rats? Gut 30, 820–825.Google Scholar
Graham, H., Åman, P., Newman, R. K. & Newman, C. W. (1985). Use of a nylon-bag technique for pig feed digestibility studies. British Journal of Nutrition 54, 719–726.CrossRefGoogle ScholarPubMed
Groot, P. H. E., Scholte, H. R. & Hülsmann, W. C. (1976). Fatty acid activation: specificity, localisation and function. Advances in Lipid Research 14, 75–126.CrossRefGoogle ScholarPubMed
Illman, R. J., Topping, D. L. & Trimble, R. P. (1986). Effects of food restriction and starvation-refeeding on volatile fatty acid concentrations in the rat. Journal of Nutrition 116, 1694–1700.CrossRefGoogle ScholarPubMed
Key, F. B. & Mathers, J. C. (1987). Response of rat caecal metabolism to varying proportions of white and wholemeal bread. Proceedings of the Nutrition Society 46, 11A.Google Scholar
Key, F. B. & Mathers, J. C. (1989). Effects on volatile fatty acid production and gut epithelial proliferation of adding haricot beans to a wholemeal bread diet. Proceedings of the Nutrition Society 48, 47A.Google Scholar
Keys, J. E. Jr & DeBarthe, J. V. (1974). Cellulose and hemicellulose digestibility in the stomach, small intestine and large intestine of swine. Journal of Animal Science 39, 53–56.CrossRefGoogle ScholarPubMed
Leng, R. A. (1970). Formation and production of volatile fatty acids in the rumen. In Physiology of Digestion and Metabolism in the Ruminant, pp. 406–421 [Philipson, A. T., editor]. Newcastle upon Tyne: Oriel Press.Google Scholar
Lloyd, B., Burrin, J., Smythe, P. & Alberti, K. G. M. M. (1978). Enzymic fluorometric continuous-flow assays for blood glucose, lactate, pyruvate, alanine, glycerol and 3-hydroxybutyrate. Clinical Chemistry 34, 1724–1729.CrossRefGoogle Scholar
Longstaff, M. & McNab, J. M. (1987). Digestion of starch and fibre carbohydrates in peas by adult cockerels. British Poultry Science 28, 261–285.Google Scholar
Longstaff, M. & McNab, J. M. (1989). Digestion of fibre polysaccharides of pea (Pisum sativum) hulls, carrot and cabbage by adult cockerels. British Journal of Nutrition 62, 563–577.CrossRefGoogle ScholarPubMed
Macfarlane, G. T. & Englyst, H. N. (1986). Starch utilization by the human large intestinal microflora. Journal of Applied Bacteriology 60, 195–201.Google Scholar
McMeniman, N. P. & Armstrong, D. G. (1979). The flow of amino acids into the small intestine of cattle when fed heated and unheated beans (Vicia faba). Journal of Agricultural Science, Cambridge 93, 181–188.CrossRefGoogle Scholar
McNeil, N. I., Cummings, J. H. & James, W. P. T. (1978). SCFA absorption by the human large intestine. Gut 19, 819–822.CrossRefGoogle Scholar
Mallett, A. K., Bearne, C. A., Young, P. J., Rowland, I. R. & Berry, C. (1988). Influence of starches of low digestibility on the rat caecal microflora. British Journal of Nutrition 60, 597–604.CrossRefGoogle ScholarPubMed
Mathers, J. C., Fernandez, F., Hill, M. J., McCarthy, P. T., Shearer, M. J. & Oxley, A. (1990). Dietary modification of potential vitamin K supply from enteric bacterial menaquinones in rats. British Journal of Nutrition 63, 639–652.CrossRefGoogle ScholarPubMed
Millard, P. & Chesson, A. (1984). Modification to swede (Brassica napus L.) anterior to the terminal ileum of pigs: some implications for the analysis of dietary fibre. British Journal of Nutrition 52, 583–594.CrossRefGoogle Scholar
Nyman, M., Asp, N.-G., Cummings, J. & Wiggins, H. (1986). Fermentation of dietary fibre in the intestinal tract: comparison between man and rat. British Journal of Nutrition 55, 487–496.Google Scholar
Parker, D. S. (1976). The measurement of production rates of volatile fatty acids in the caecum of the conscious rabbit. British Journal of Nutrition 36, 61–70.Google Scholar
Pedroso, L. M. R., Finlayson, H. J. & Mathers, J. C. (1989). Effects of dietary wheat bran on activities of key enzymes of lipid and carbohydrate metabolism in rat liver. Proceedings of the Nutrition Society 48, 54A.Google Scholar
Pedroso, L. M. R., Mathers, J. C. & Finlayson, H. J. (1990). Effects of feeding raw peas on activities of key enzymes of lipid and carbohydrate metabolism in rat liver. Proceedings of the Nutrition Society 49, 52A.Google Scholar
Rasmussen, H. S., Holtug, K. & Mortensen, P. B. (1988). Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scandinavian Journal of Gastroenterology 23, 178–182.CrossRefGoogle ScholarPubMed
Reichert, R. D. (1981). Quantitative isolation and estimation of cell wall material from dehulled pea (Pisum sativum) flours and concentrates. Cereal Chemistry 58, 266–270.Google Scholar
Rémésy, C. & Demigné, C. (1989). Specific effects of fermentable carbohydrates on blood urea flux and ammonia absorption in the rat cecum. Journal of Nutrition 119, 560–565.CrossRefGoogle ScholarPubMed
Rodwell, V. W., Nordstrom, J. L. & Mitschelen, J. J. (1976). Regulation of HMG CoA reductase. Advances in Lipid Research 14, 1–74.CrossRefGoogle ScholarPubMed
Roediger, W. E. W. (1980). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa of man. Gut 21, 793–798.CrossRefGoogle ScholarPubMed
Roediger, W. E. W. (1982). Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424–429.Google Scholar
Ruppin, H., Bar-Meir, S., Soergel, K. H. & Schmitt, M. G. (1980). Absorption of SCFA by the colon. Gastroenterology 78, 1500–1507.Google Scholar
Russel, J. B. & Hespell, R. B. (1981). Microbial rumen fermentation. Journal of Dairy Science 64, 1153–1160.Google Scholar
Sakata, T. (1987). Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: a possible explanation for trophic effects of fermentable fibre, gut microbes and luminal trophic factors. British Journal of Nutrition 58, 95–103.Google Scholar
Sambrooke, I. E. (1979). Studies on digestion and absorption in the intestine of growing pigs. 8. Measurement of the flow of total lipid, acid-detergent fibre and volatile fatty acids. British Journal of Nutrition 42, 279–287.Google Scholar
Samson, F. E., Dahl, N. & Dahl, D. R. (1956). A study on the narcotic actions of the short chain fatty acids. Journal of Clinical Investigation 35, 1291–1298.Google Scholar
Scheppach, W., Fabian, C., Sachs, M. & Kasper, H. (1988). The effect of starch malabsorption on fecal short-chain fatty acid excretion in man. Scandinavian Journal of Gastroenterology 23, 755–759.Google Scholar
Seal, C. J. & Mathers, J. C. (1989). Intestinal zinc transfer by everted gut sacs from rats given diets containing different amounts and types of dietary fibre. British Journal of Nutrition 62, 151–163.Google Scholar
Selvendran, R. R. (1984). The plant cell wall as a source of dietary fiber: chemistry and structure. American Journal of Clinical Nutrition 39, 320–337.Google Scholar
Silley, P. & Armstrong, D. G. (1984). Changes in metabolism of the rumen bacterium Streptococcus bovis H13/1 resulting from alteration in dilution rate and glucose supply per unit time. Journal of Applied Bacteriology 57, 345–353.CrossRefGoogle ScholarPubMed
Snoswell, A. M., Trimble, R. P., Fishlock, R. C., Storer, G. B. & Topping, D. L. (1982). Metabolic effects of acetate in perfused rat liver. Studies on ketogenesis, glucose output, lactate uptake and lipogenesis. Biochimtca et Biophysica Acta 716, 290–297.CrossRefGoogle ScholarPubMed
Snow, P. & O'Dea, K. (1981). Factors affecting the rate of hydrolysis of starch in food. American Journal of Clinical Nutrition 34, 2721–2727.Google Scholar
Stephen, A. M. & Cummings, J. H. (1980). The microbial contribution to human faecal mass. Journal of Medical Microbiology 13, 45–56.Google Scholar
Stephen, A. M., Wiggins, H. S., Englyst, H. N., Cole, T. J., Wayman, B. J. & Cummings, J. H. (1986). The effect of age, sex and level of intake of dietary fibre from wheat on large-bowel function in thirty healthy subjects. British Journal of Nutrition 56, 349–361.Google Scholar
Thompson, A. (1970). Rat metabolism cage. Journal of the Institute of Animal Technicians 21, 12–21.Google Scholar
Tulung, B., Rémésy, C. & Demigné, C. (1987). Specific effects of guar gum or gum arabic on adaptation of caecal digestion to high fibre diets in the rat. Journal of Nutrition 117, 1556–1561.Google Scholar
Walter, D. J., Eastwood, M. A., Brydon, W. G. & Elton, R. A. (1988). Fermentation of wheat bran and gum arabic in rats fed on an elemental diet. British Journal of Nutrition 60, 225–232.Google Scholar
Weaver, G. A., Krause, J. A., Miller, T. L. & Wolin, M. J. (1989). Constancy of glucose and starch fermentations by two different faecal microbial communities. Gut 30, 19–25.Google Scholar
Williams, R. D. & Olmsted, W. H. (1936). The effect of cellulose, hemicellulose and lignin on the weight of the stool; contribution to the study of laxation in man. Journal of Nutrition 11, 433–439.Google Scholar
Windmuller, H. G. & Spaeth, A. E. (1980). Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Journal of Biological Chemistry 255, 107–112.CrossRefGoogle Scholar
Wolever, T. M. S., Cohen, Z., Thompson, L. U., Thorne, M. J., JenkinsM. J., A. M. J., A., Prokipchuk, E. J. & Jenkins, D. J. A. (1986). Ileal loss of available carbohydrate in man: comparison of a breath hydrogen method with direct measurement using a human ileostomy model. American Journal of Gastroenterology 81, 115–122.Google ScholarPubMed
Woodnutt, G. (1984). Absorption and utilization of metabolites in the rabbit. PhD Thesis, University of Reading.Google Scholar
Wyatt, G. M., Horn, N., Gee, J. M. & Johnson, I. T. (1988). Intestinal microflora and gastrointestinal adaptation in the rat in response to non-digestible dietary polysaccharides. British Journal of Nutrition 60, 197–207.CrossRefGoogle ScholarPubMed