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Tissue hypertrophy and epithelial proliferation rate in the gut of rats fed on bread and haricot beans (Phaseolus vulgaris)

Published online by Cambridge University Press:  09 March 2007

Fiona B. Key ,
Devina McClean  and
J. C. Mathers
Fiona B. Key
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NEI 7RU
Devina McClean
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NEI 7RU
J. C. Mathers
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NEI 7RU
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Abstract

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The present study was designed to test the hypothesis that increasing short-chain fatty acid (SCFA)production in the large bowel increases gut epithelial proliferation rate (EPR). Two experiments were carried out in which rats were fed on bread (wholemeal or white)-based diets containing graded amounts of cooked haricot (Phaseofus vulgaris) beans; the latter are a rich source of fermentable carbohydrates. Consumption of beans was associated with several-fold increases in SCFA production with the greatest relative increase being for butyrate. Despite the very large increase in SCFA production, there was no evidence that this had any effect on EPR in the duodenum. Where the basal diet contained wholemeal bread (Expt 1) there was no effect of enhanced SCFA supply on EPR in either the caecum or colon, but with the white bread-based diet (Expt 2) adding beans produced increments in both SCFA supply and EPR in the caecum. Evidence that SCFA are responsible for enhanced EPR above normal levels is not convincing. In those instances where enhanced SCFA supply is associated with increased EPR, the increase may be (1) from a hypoproliferative state towards normal, (2) a transient phenomenon accompanying tissue hypertrophy or (3) a homeostatic response to increased cell loss by cell sloughing or apoptosis. It is not likely that there is any direct link with risk of colon cancer

Keywords

Epithelial proliferation rateShort-chain fatty acidsHaricot beansTissue hypertrophy
Type
General Nutrition
Information
British Journal of Nutrition , Volume 76 , Issue 2 , August 1996 , pp. 273 - 286
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Bianchini, F., Caderni, G., Magno, C., Testolin, G. & Dolara, P. (1992). Profile of short-chain fatty acids and rectal proliferation in rats fed sucrose and cornstarch diets. Journal of Nutrition 122,254–261.CrossRefGoogle ScholarPubMed
Calvert, R. J., Otsuka, M. & Satchithanandam, S. (1989). Consumption of raw potato starch alters intestinal function and colonic cell proliferation in the rat.Journal of Nutrition,119,1610–1616.CrossRefGoogle ScholarPubMed
Dahlqvist, A. (1968). Assay of intestinal disaccharidases. Analytical Biochemistry 22, 99–107.CrossRefGoogle ScholarPubMed
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. & Warner, A. C. I., editors]. Armidale: University of New England Publishing Unit.Google Scholar
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
Goodlad, J. S. & Mathers, J. C. (1990). Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). British 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). Proliferative effects of ‘fibre’ on the intestinal epithelium: relationship to gastrin, enteroglucagon and PYY. Gut 28, Suppl.1,221–226.CrossRefGoogle ScholarPubMed
Goodlad, R. A., Ratcliffe, B., Fordham, J. P., Ghatei, M. A., Domin, J., Bloom, S. R. & Wright, N. A. (1989).Plasma enteroglucagon, gastrin and peptide YY in conventional and germ-free rats fed with a fibre-free or fibre-supplemented diet. Quarterly Journal of Experimental Physiology 74, 437–442.CrossRefGoogle ScholarPubMed
Goodlad, R. A. &Wright, N. A. (1982). Quantitative studies on epithelial replacement in the gut. In Techniques in Life Sciences. Digestive Physiology, pp. 212/1–212/13 [Titchen, D. A., edito]. Limerick, Republic of Ireland:Elsevier Scientific Publishers Ireland Ltd.Google Scholar
Goodlad, R. A. & Wright, N. A. (1987). Peptides and epithelial growth regulation. Experientia 43, 780–784.CrossRefGoogle ScholarPubMed
Hall, P. A., Coates, P. J., Ansari, B. & Hopwood, D. (1994). Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. Journal of Cell Science 107, 3569–3577.CrossRefGoogle ScholarPubMed
Ikegami, S., Tsuchihashi, F., Harada, H., Tsuchihashi, N., Nishide, E. & Innami, S. (1990). Effect of viscous indigestible polysaccharides on pancreatic-biliary secretion and digestive organs in rats. Journal of Nutrition 120, 353–360.CrossRefGoogle ScholarPubMed
Johnson, I. T., Gee, J. M. & Brown, J. C. (1988). Plasma enteroglucagon and small bowel cytokinetics in rats fed soluble nonstarch polysaccharides. American Journal of Clinical Nutrition 47, 1004–1009.CrossRefGoogle ScholarPubMed
Kamath, P. S., Phillips, S. F. & Zinsmeister, A. R. (1988). Short-chain fatty acids stimulate ileal motility in humans. Gastroenterology 95, 1496–1502.CrossRefGoogle ScholarPubMed
Key, F. B. (1990). Digestion and large bowel fermentation of breads and haricot beans (Phaseolus vulgaris). PhD Thesis, University of Newcastle upon Tyne.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
Key, F. B. & Mathers, J. C. (1993). Complex carbohydrate digestion and large bowel fermentation in rats given wholemeal bread and cooked haricot beans (Phaseolus vulgaris) fed in mixed diets. British Journal of Nutrition 69,497–509.CrossRefGoogle ScholarPubMed
Key, F. B. & Mathers, J. C. (1995). Digestive adaptations of rats given white bread and cooked haricot beans (Phaseolus vulgaris): large-bowel fermentation and digestion of complex carbohydrates. British Journal of Nutrition 74, 393–406.CrossRefGoogle ScholarPubMed
Koruda, M. J., Rolandelli, R. H., Settle, G., Zimmaro, D. M. & Rombeau, J. L. (1988). Effect of parenteral nutrition supplemented with short chain fatty acids on adaptation to massive small bowel resection. Gastroenterology 95, 715–720.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the Fohn phenol reagent. Journal of Biological Chemistry 193, 265–275.CrossRefGoogle Scholar
Malville-Shipan, K. & Fleming, S. E. (1992). Wheat bran and corn oil do not influence proliferation in the colon of healthy rats when energy intakes are equivalent. Journal of Nutrition 122, 37–45.CrossRefGoogle Scholar
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. & Fotso Tagny, J.-M. (1994). Diurnal changes in large-bowel metabolism: short-chain fatty acids and transit time in rats fed on wheat bran. British Journal of Nutrition 71, 209–222.CrossRefGoogle ScholarPubMed
Mathers, J. C., Kennard, J. &James, O. F. W. (1993). Gastrointestinal responses to oats consumption in young adult and elderly rats: digestion, large bowel fermentation and crypt cell proliferation. British Journal of Nutrition 70, 567–584.CrossRefGoogle ScholarPubMed
Mathers, J. C., McClean, D. & Key, F. B. (1990). Stimulation of large bowel fermentation has no effects on duodenal epithelial proliferation in rats given white bread-based diets. Proceedings of the Nutrition Society 49,38A.Google Scholar
Mathers, J. C. & Smith, H. (1993). Factors influencing caecal butyrate in rats fed on raw potato starch. Proceedings of the Nutrition Society 52, 376A.Google Scholar
Mills, S. J., Shepherd, N. A., Hall, P. A., Hastings, A., Mathers, J. C. & Gunn, A. (1995). Proliferative compartment deregulation in the non-neoplastic colonic epithelium of familial adenomatous polyposis. Gut 36,391–394.CrossRefGoogle ScholarPubMed
Mortensen, F. V., Nielson, H., Mulvany, M. J. & Hessov, I. (1990). Short chain fatty acids dilate isolated human colonic resistance arteries. Gut 31, 1391–1394.CrossRefGoogle ScholarPubMed
Nordgaard, I., Hansen, B. S. & Mortensen, P. B. (1994). Colon as a digestive organ in patients with short bowel.Lancet 343, 373–376.CrossRefGoogle ScholarPubMed
Preston-Martin, S., Pike, M. C., Ross, R. K., Jones, P. A. & Henderson, B. E. (1990). Increased cell division as a cause of human cancer. Cancer Research 50, 7415–7421.Google ScholarPubMed
Rémésy, C. & Demigné, C. (1989). Specific effects of fermentable carbohydrates on blood urea flux and ammonia absorption in the rat caecum. Journal of Nutrition 119, 560–565.CrossRefGoogle Scholar
Rombeau, J. C., Reilly, K. J. & Rolandelli, R. H. (1995). Short-chain fatty acids and intestinal surgery. In Physiological and Clinical Aspects of Short-chain Fatty Acids, pp. 401–425 [Cummings, J. H., Rombeau, J. L. & Sakata, T., editors]. Cambridge: Cambridge University Press.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.CrossRefGoogle ScholarPubMed
Sakata, T. (1988). Depression of intestinal epithelial cell production rate by hindgut bypass in rats. Scandinavian Journal of Gastroenterology 23, 1200–1202.CrossRefGoogle ScholarPubMed
Sakata, T. (1995). Effects of short-chain fatty acids on the proliferation of gut epithelial cells in vivo. In physiological and Clinical Aspects of Short-chain Fatty Acids, pp. 289–305 [Cummings, J. H., Rombeau, J. L. & Sakata, T., editors]. Cambridge: Cambridge University Press.Google Scholar
Sakata, T. & Tamate, H. (1978). Ruminal epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. Journai of Dairy Science 61, 1109–1113.CrossRefGoogle ScholarPubMed
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 62,157–163.CrossRefGoogle ScholarPubMed
Tamate, H., McGilliard, A. D., Jacobson, N. L. & Getty, R. (1962). EfTect of various dietaries on the anatomical development of the stomach in the calf. Journal of Dairy Science 45,408–420.CrossRefGoogle Scholar
Tannock, I. F. (1967). A comparison of the relative efficiencies of various metaphase arrest agents. Experimental Cell Research 47, 345–356.CrossRefGoogle Scholar
Thompson, A. (1970). Rat metabolism cage. Journal of the Institute of Animal Technicians 21, 12–21.Google Scholar
Wright, N. & Alison, M. (1984). The Biology of Epithelial Cell Populations, vol. 2. Oxford: Clarendon Press.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