Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T05:27:30.391Z Has data issue: false hasContentIssue false
  • English
  • Français

Gastrointestinal responses to oats consumption in young adult and elderly rats: digestion, large bowel fermentation and crypt cell proliferation rates

Published online by Cambridge University Press:  09 March 2007

J. C. Mathers ,
Julia Kennard  and
O. F. W. James
J. C. Mathers
Affiliation:
Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne, NEl 7RU
Julia Kennard
Affiliation:
Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne, NEl 7RU
O. F. W. James
Affiliation:
Department of Medicine, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH
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 present experiment was designed to test the hypothesis that ageing modifies the gastrointestinal responses to a change in diet composition. Rats of the Wag/Rij strain, either young adult (4 months of age) or elderly (27 months of age), were given a basal semi-purified diet or a diet of similar major nutrient composition containing 500 g oatmeal/kg for 17–18 d. Elderly rats digested the dry matter (DM) and organic matter (OM) of both diets less well than did their young adult counterparts, with more of this digestion occurring in the distal intestine. The greater flow of OM to the caecum of oats-fed animals was accompanied by significant reductions in caecal pH and increases in caecal total short-chain fatty acids (SCFA) concentration which appeared to be independent of age. However, young adults responded to feeding on oats by showing a much larger increase in the molar proportion of butyrate (332%) than did elderly animals (79%). Elderly rats had longer duodenal villi than did young adults but effects of age or diet were not detectable at other sites. With both age-groups oats consumption was associated with significant stimulation of crypt cell proliferation rate (CCPR) in the small intestine and caecum, but for the colon there was a significant reduction in CCPR with oats feeding. A reduced ability of the aged large bowel (LB) to produce butyrate may contribute to the prevelance of LB disorders in the elderly.

Keywords

AgeingOatsLarge bowel fermentationCrypt cell proliferation rateRats
Type
Gastro-Intestinal Effects of Diets Containing Complex Caebohydrates
Information
British Journal of Nutrition , Volume 70 , Issue 2 , September 1993 , pp. 567 - 584
Copyright
Copyright © The Nutrition Society 1993

References

REFERENCES

Augeron, C. & Laboisse, C. L. (1984). Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Research 44, 3961–3969.Google Scholar
Beaumont, D. M., Cobden, I., Sheldon, W. L., Laker, M. F. & James, O. F. W. (1987). Passive and active carbohydrate absorption by the ageing gut. Age and Ageing 16, 294–300.CrossRefGoogle ScholarPubMed
Beaumont, D. M. & James, O. F. W. (1986). Unsuspected giardiasis as a cause of malnutrition and diarrhoea in the elderly. British Medical Journal 293, 554–555.CrossRefGoogle ScholarPubMed
Belosevic, M., Faubort, G. M. & MacLean, J. D. (1989). Disaccharidase activity in the small intestine of gerbils (Meriones unguiculatus) during primary and challenge infections with Giardia lamblia. Gut 30, 1213–1219.CrossRefGoogle ScholarPubMed
Bhanthumnavin, K. & Schuster, M. M. (1977). Aging and gastrointestinal function. In Handbook of the Biology of Aging pp. 709–723 [Finch, C. E. and Hayflick, L., editors]. New York: Van Nostrand Reinhold.Google Scholar
Bianchini, F., Caderni, G., Magno, C., Testolin, G. & Dolara, P. (1992). Profile of short-chain fatty acids and rectal proliferation in rats fed sucrose or cornstarch diets. Journal of Nutrition 122, 254–261.CrossRefGoogle ScholarPubMed
Bingham, S. A. (1990). Mechanisms and experimental and epidemiological evidence relating dietary fibre (non- starch polysaccharides) and starch to protection against large bowel cancer. Proceedings of the Nutrition Society 49, 153–171.CrossRefGoogle ScholarPubMed
Bird, T., Hall, M. R. P. & Schade, R. O. K. (1977). Gastric histology and its relation to anaemia in the elderly. Gerontology 23, 309–321.CrossRefGoogle ScholarPubMed
Breuer, R. I., Buto, S. K., Christ, M. L., Bean, J., Vernia, P., Paoluzi, P., Di Paolo, M. C. & Caprilli, R. (1991). Rectal irrigation with short-chain fatty acids for distal ulcerative colitis. Preliminary report. Digestive Diseases and Sciences 36, 185–187.CrossRefGoogle ScholarPubMed
Burek, J. D. (1978). Pathology of Aging Rats. A Morphological and E-xperirnental Study of the Age-associated Lesions in Aging BN/Bi. WAG/Rij and (WAG × BN) F1 Rats. West Palm Beach: CRC Press Inc.Google Scholar
Campbell, D., Bunker, V. W., Thomas, A. J. & Clayton, B. E. (1989). Selenium and vitamin E status of healthy and institutionalized elderly subjects: analysis of plasma, erythrocytes and platelets. Brirish Journal of Nutrition 62, 221–227.CrossRefGoogle ScholarPubMed
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
Clarke, R. M. (1972). The effect of growth and of fasting on the number of villi and crypts in the small intestine of the albino rat. Journal of Anatomy 112, 27–33.Google ScholarPubMed
Clarke, R. M. (1977). The effects of age on mucosal morphology and epithelial cell production in rat small intestine. Journal of Anatomy 123, 805–811.Google ScholarPubMed
Collington, G. K., Parker, D. S. & Armstrong, D. G. (1990). The influence of inclusion of either an antibiotic or a probiotic in the diet on the development of digestive enzyme activity in the pig. British Journal of Nutrition 64, 59–70.CrossRefGoogle ScholarPubMed
Cummings, J. H. & Englyst, H. N. (1987). Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45, 1243–1255.CrossRefGoogle ScholarPubMed
Darmenton, P., Raul, F., Doffoel, M. & Wessely, J.-Y. (1989). Age influence on sucrose hydrolysis and on monosaccharide absorption along the small intestine of rat. Mechanism in Ageing and Development 50, 49–55.CrossRefGoogle ScholarPubMed
Ecknauer, R., Vadakel, T. & Wepler, R. (1982). Intestinal morphology and cell production rate in aging rats. Journal of Gerontology 37, 151–155.CrossRefGoogle ScholarPubMed
Edwards, C. A., Wilson, R. G., Hanlon, L. & Eastwood, M. A. (1992). Effect of the dietary fibre content of lifelong diet on colonic cellular proliferation in the rat. Gut 33, 1076–1079.CrossRefGoogle ScholarPubMed
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
Esposito, A., Faelli, A., Tosco, M., Orsenigo, M. N. & Battistessa, R. (1985). Age-related changes in rat intestinal transport of D-glucose, sodium and water. American Journal of Physiology 249, G328–G334.Google ScholarPubMed
Feibusch, J. M. & Holt, P. R. (1982). Impaired absorptive capacity for carbohydrate in the aging human. Digestive Diseases and Sciences 27, 1095–1110.CrossRefGoogle ScholarPubMed
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., Fitch, M. D. & De Vries, S. (1992). The influence of dietary fiber on proliferation of intestinal mucosal cells in miniature swine may not be mediated primarily by fermentation. Journal of Nutrition 122, 906–916.CrossRefGoogle Scholar
Freeman, H. J. & Quamme, G. A. (1986). Age-related changes in sodium-dependent glucose transport in rat small intestine. American Journal of Physiology 251, G208–GZ17.Google ScholarPubMed
Gibson, G. R., Cummings, J. H., Macfarlane, G. T., Allison, C., Segal, I., Vorster, H. H. & Walker, A. R. P. (1990). Alternative pathways for hydrogen disposal in the human colon. Gut 31, 679–683.CrossRefGoogle ScholarPubMed
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, J. S. & Mathers, J. C. (1990). Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). Brilish Journal of Nutrition 64, 569–587.CrossRefGoogle ScholarPubMed
Goodlad, R. A., Lenton, W., Ghatei, M. A., Adrian, T. E., Bloom, S. R. & Wright, N. A. (1987). Proliferate efects of «fibre’ on the intestinal epithelium: relationship to gastrin, enteroglucagon and PYY. Gut 28, SI, 221–226.CrossRefGoogle Scholar
Goodlad, R. A. & Wright, N. A. (1982). Quantitative studies on epithelial replacement in the gut. In Techniques in Lfe Sciences. Digestive Physiology pp. 212/1–212/23 [Titchen, D. A., editor]. Limerick, Republic of Ireland: Elsevier Scientific Publishers Ireland Ltd.Google Scholar
Goodlad, R. A. & Wright, N. A. (1990). Changes in intestinal cell proliferation, absorptivecapacity and structure in young, adult and old rats. Journal of Anatomy 173, 109–118.Google ScholarPubMed
Haboui, N. Y., Cowley, P. A. & Lee, G. S. (1988). Small bowel bacterial overgrowth: a cause of malnutrition in the elderly? European Journal of Clinical Nutrition 42, 999–1005.Google Scholar
Haboui, N. Y., Lee, G. S. & Montgomery, R. D. (1991). Duodenal mucosal morphometry of elderly patients with small intestinal bacterial overgrowth: response to antibiotic treatment. Age and Ageing 20, 29–32.CrossRefGoogle Scholar
Heller, T. D., Holt, P. & Richardson, A. (1990). Food restriction retards age-related histological changes in the rat small intestine. Gastroenterology 98, 387–391.CrossRefGoogle ScholarPubMed
Hirst, B. H. & Wallis, J. L. (1990). Sodium-coupled D-glucose uptake in adult and aged mouse and rat jejunal brush border membrane vesicles in vitro. Journal of Physiology 422, 67P.Google Scholar
Höhn, P., Gabbert, H. & Wagner, R. (1978). Differential ageing of the rat intestinal mucosa. Mechanisms of Ageing and Development 7, 217–226.CrossRefGoogle ScholarPubMed
Holt, P. R., Pascal, R. R. & Kotler, D. P. (1984). Effect of aging upon small intestinal structure in the Fischer rat. Journal of Gerontology 39, 642–647.CrossRefGoogle ScholarPubMed
Holt, P. R., Tierney, A. R. & Kotler, D. P. (1985). Delayed enzyme expression: a defect of ageing rat gut. Gastroenterology 89, 1026–1034.CrossRefGoogle ScholarPubMed
Holt, P. R. & Yeh, K.-Y. (1989). Small intestinal crypt cell proliferation rates are increased in senescent rats. Journal of Gerontology: Biological Sciences 44, B9–BI4.CrossRefGoogle ScholarPubMed
Jacobs, L. R. & Lupton, J. R. (1984). Effect of dietary fibres on rat large bowel mucosal growth and cell proliferation. American Journal of Physiology 246, G378–G385.Google ScholarPubMed
Johnson, I. T., Gee, J. M. & Brown, J. C. (1988). Plasma enteroglucagon and small bowel cytokinetics in rats fed soluble non-starch polysaccharides. American Journal of Clinical Nutrition 47, 1004–1009.CrossRefGoogle Scholar
Koruda, M. J., Rolandelli, R. H., Settle, R. G., Zimmaro, D. M. & Rombeau, J. L. (1988). Effect of parented nutrition supplemented with short-chain fatty acids on adaptation to massive small bowel resection. Gastroenterology 95, 715–720.CrossRefGoogle Scholar
Kruh, J. (1982). Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Molecular and Cellular Biochemistry 42, 65–82.Google 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 [Phillipson, A. T., editor]. Newcastle upon Tyne: Oriel Press.Google Scholar
Livesey, G. (1990). Energy value of unavailable carbohydrates and diets: an inquiry and analysis. American Journal of Clinical Nutrition 51, 617–637.CrossRefGoogle ScholarPubMed
McEvoy, A., Dutton, J. & James, O. F. W. (1983). Bacterial contamination of the small intestine as an important cause of occult malabsorption in the elderly. British Medical Journal 287, 789–793.CrossRefGoogle ScholarPubMed
McEvoy, A. W., Fenwick, J. D., Boddy, K. & James, O. F. W. (1982). Vitamin B12 absorption from the gut does not decline with age in normal elderly humans. Age and Ageing 11, 180–183.CrossRefGoogle Scholar
Macfarlane, G. T. & Englyst, H. N. (1986). Starch utilization by the human large intestine microflora. Journal of Applied Bacteriology 60, 195–201.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
Masoro, E. J. (1985). Nutrition and aging -a current assessment. Journal qf Nutrition 115, 842–848.CrossRefGoogle ScholarPubMed
Mathers, J. C. (1991). Digestion of non-starch polysaccharides by non-ruminant omnivores. Proceedings of the Nutrition Society 50, 161–172.CrossRefGoogle ScholarPubMed
Mathers, J. C. & Dawson, L. D. (1991). Large bowel fermentation in rats eating processed potatoes. British Journal of Nutrition 66, 313–329.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
Mathers, J. C., Kennard, J. & James, O. F. W. (1991). Effects of ageing on the caecal fermentation response to oats-feeding in rats. Proceedings of the Nutrition Society 50, 74A.Google Scholar
Meshinpour, H., Smith, M. & Hollander, D. (1981). Influence of aging on the surface area of the small intestine in the rat. Experimental Gerontology 16, 399–404.CrossRefGoogle Scholar
Miazza, B. M., Al-Mukhtar, M. Y. T., Salmeron, M., Ghatei, M. A., Felce-Dachez, M., Filali, A., Villet, R., Wright, N. A., Bloom, S. R. & Rambaud, J.-C. (1985). Hyperenteroglucagonaemia and small intestinal mucosa growth after colonic perfusion of glucose in rats. Gut 26, 518–524.CrossRefGoogle ScholarPubMed
Moog, F. (1977). The small intestine in old mice: growth, alkaline phosphatase and disaccharidase activities, and deposition of amyloid. Experimental Gerontology 12, 223–235.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Raul, F., Gosse, F., Doffoel, M., Darmenton, P. & Wessely, J. Y. (1988). Age-related increase in brush-border enzyme activities along the small intestine. Gut 29, 1557–1563.CrossRefGoogle ScholarPubMed
Roediger, W. E. W. (1982). Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424–429.CrossRefGoogle ScholarPubMed
Roediger, W. E. W. (1986). Metabolic basis of starvation diarrhoea: implications for treatment. Lancet i, 1082–1084.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Scheppach, W., Sommer, H., Kirchner, T., Paganelli, G.-M., Bartram, P., Christl, S., Richter, F., Dusel, G. & Kasper, H. (1992). Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103, 51–56.CrossRefGoogle ScholarPubMed
Schmitt, M. G., Soergel, K. H. & Wood, C. M. (1976). Absorption of short chain fatty acids from the human jejunum. Gastroenterology 70, 211–215.CrossRefGoogle ScholarPubMed
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
Smith, P. J. (1986). n-Butyrate alters chromatin accessibility to DNA repair enzymes. Carcinogenesis 7, 423–429.CrossRefGoogle ScholarPubMed
Szabo, J. (1979). Protein, carbohydrate and fat degrading enzymes in the intestine of germ-free and conventional piglets. In Clinical and Experimental Gnotobiotics p. 125 [Fliedner, T.Heit, H.Niethammer, D. and Pflieger, H., editors]. Stuttgart and New York: Fisher Verlag.Google Scholar
Thompson, A. B. R. (1980). Effect of age on uptake of homologous series of saturated fatty acids into rabbit jejunum. American Journal of Physiology 239, G363–G371.Google Scholar
Thompson, A. B. R. & Keelan, M. (1986). The aging gut. Canadian Journal of Physiology and Pharmacology 64, 30–38.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Walford, R. L., Harris, S. B. & Weindruch, R. (1987). Dietary restriction and aging: historical phases, mechanisms and current directions. Journal of Nutrition 117, 1650–1654.CrossRefGoogle ScholarPubMed
Wallis, J. L., Lipski, P. S., Mathers, J. C., James, O. F. W. & Hirst, B. H. (1993). Duodenal brush-border mucosal glucose transport and enzyme activities in aging man and effect of bacterial contamination of the small intestine. Digestive Diseases and Sciences 3, 403–409.CrossRefGoogle 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.CrossRefGoogle Scholar
Watson, A. J. M., Elliott, E. J., Rolston, D. D. K., Borodo, M. M., Farthing, M. J. G. & Fairclough, P. D. (1990). Acetate absorption in the normal and secreting rat jejunum. Gut 31, 170–174.CrossRefGoogle ScholarPubMed
Webster, S. G. P. & Leeming, J. T. (1975). The appearance of the small bowel mucosa in old age. Age and Ageing 4, 168–174.CrossRefGoogle ScholarPubMed
Webster, S. G. P., Wilkinson, E. M. & Gowland, E. (1977). A comparison of fat absorption in young and old subjects. Age and Ageing 6, 113–117.CrossRefGoogle Scholar
Woodnutt, G. (1984). Absorption and utilization of metabolites in the rabbit. PhD Thesis, University of Reading.Google Scholar
Yolton, D. P. & Savage, D. C. (1976). Influence of certain indigenous gastrointestinal microorganisms on duodeiial alkaline phosphatase in mice. Applied and Environmental Microbiology 31, 880–888.CrossRefGoogle ScholarPubMed