Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T13:43:14.219Z Has data issue: false hasContentIssue false

Changes to the quantity and processing of starchy foods in a Western diet can increase polysaccharides escaping digestion and improve in vitro fermentation variables

Published online by Cambridge University Press:  09 March 2007

Anne M. Birkett
Affiliation:
School of Nutrition and Public Health, Deakin University, Geelong, Victoria, Australia3217
John C. Mathers
Affiliation:
Human Nutrition Research Centre, Department of Biological and Nutritional Sciences, University of Newcastle Upon Tyne, NE1 7RU, UK
Gwyn P. Jones
Affiliation:
School of Nutrition and Public Health, Deakin University, Geelong, Victoria, Australia3217
Karen Z. Walker
Affiliation:
Centre for Population Health and Nutrition, Monash University, Clayton, Victoria, Australia3168
Melinda J. Roth
Affiliation:
School of Nutrition and Public Health, Deakin University, Geelong, Victoria, Australia3217
Jane G. Muir*
Affiliation:
Centre for Population Health and Nutrition, Monash University, Clayton, Victoria, Australia3168
*
*Corresponding author: Dr Jane Muir, fax +61 3 9550 5509, 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.

This study investigated how readily achievable changes to the quantity and processing of starchy foods in a typical Western diet: (1) were reflected in levels of resistant starch (RS) and NSP excreted from the small intestine; and (2) more favourable profiles of butyrate, NH3 and phenol production. Two diets, a low-starch diet (LSD) and a high-starch, low-fat diet (HSLFD) were compared. The LSD with 20 % total energy (%E) from starch was based on a ‘typical’ Australian diet, while the HSLFD (40 %E as starch) was the same Australian diet modified by an increased content of legumes, starchy foods and coarsely-ground cereals and by a reduced fat content. Four subjects with iliostomies consumed each diet for 2 d, with ileal effluent collection on the second day. On the HSLFD compared with the LSD, RS in ileal effluent increased from from 0·49 to 1·7 g/MJ per d (P < 0·005) while ileal NSP excretion increased from 2·0 to 3·3 g/MJ per d (P < 0·05). Ileal effluents obtained after each diet were incubated for 24 h in vitro with a human faecal innoculum. After fermentation, ileal effluent from the HSLFD produced more butyrate relative to other short-chain fatty acids (17·5 v. 15·8 molar %, P < 0·005) and less phenol (2·3 v. 5·7 mg/l, P < 0·05) and NH3 (20·3 v. 23·1 mmol/l, P < 0·005) than the LSD diet. The HSLFD also generated a lower pH (6·15 v. 6·27, P < 0·05). On a wt/wt basis, RS was 2·3-fold higher in the HSLFD effluent while NSP did not increase, suggesting that the change in RS largely contributed to the fermentation effects. Changes in in vitro variables when the HSLFD ileal effluent was ground before fermentation indicated the importance of physical structure in determining ileal excretion of RS. We conclude that: (1) readily achievable modifications to the amount and processing of starchy foods in an Australian diet would produce potential benefits for in vitro fermentation variables; and (2) the physical structure of grains and cereals is important in determining access by colonic bacteria to a carbohydrate substrate.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Aman, P, Pettersson, D, Zhang, JX, Tidehag, P and Hallmans, G (1995) Starch and dietary fiber components are excreted and degraded to variable extents in ileostomy subjects consuming mixed diets with wheat- or oat-bran bread. Journal of Nutrition 125, 23412347.CrossRefGoogle ScholarPubMed
Asp, NG (1991) Summary of general discussion on the breath test method, the ileostomy model and the intubation studies. In Methodological Aspects of in vivo Methods for Measurement of Starch Digestibility. Report of a European Flair Concerted Action Workshop, pp. 3234 [Gudmand-Hoyer, E, editor]. Copenhagen: EURESTA.Google Scholar
Augeron, C and Laboisse, CL (1984) Emergence of permanently differentiated cell clones in a human colonic cancer cell line after treatment with sodium butyrate. Cancer Research 44, 39613969.Google Scholar
Baghurst, K, Record, S, Powis, G & Stafford, H (1993) CSIRO Division of Human Nutrition and the Food and Nutrition Program. What are Australians Eating? Results from the 1985 and 1990 Victorian Nutrition Surveys. Adelaide: CSIRO Division of Human Nutrition.Google Scholar
Baghurst, PA, Baghurst, KI and Record, SJ (1996) Dietary fibre, non-starch polysaccharides and resistant starch. A review. Food Australia 48, S2S35.Google Scholar
Barry, J-L, Hoebler, C, Macfarlane, GT, Macfarlane, S, Mathers, JC, Reed, KA, Mortensen, PB, Nordgaard, I, Rowland, IR and Rumney, CJ (1995) Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study. British Journal of Nutrition 74, 303322.CrossRefGoogle ScholarPubMed
Bingham, S (1988) Meat, starch, and nonstarch polysaccharides and large bowel cancer. American Journal of Clinical Nutrition 48, 762767.CrossRefGoogle ScholarPubMed
Bingham, SA, Williams, DRR and Cummings, JH (1985) Dietary fibre consumption in Britain: new estimates and their relation to large bowel cancer mortality. British Journal of Cancer 52, 399402.CrossRefGoogle ScholarPubMed
Birkett, AM, Jones, GP, de Silva, AM, Young, GP and Muir, JG (1997) Dietary intake and faecal excretion of carbohydrate by Australians: importance of achieving stool weights greater than 150 g to improve faecal markers relevant to colon cancer risk. European Journal of Clinical Nutrition 51, 625632.CrossRefGoogle ScholarPubMed
Birkett, AM, Jones, GP and Muir, JG (1995) Simple high-performance liquid chromatographic analysis of phenol and ρ-cresol in urine and feces. Journal of Chromatography Biomedical Applications 674, 187191.CrossRefGoogle Scholar
Birkett, AM, Muir, JG, Phillips, J, Jones, G and O'Dea, K (1996) Resistant starch lowers fecal concentrations of ammonia and phenols in humans. American Journal of Clinical Nutrition 63, 766772.CrossRefGoogle ScholarPubMed
Boutwell, RK and Bosch, DK (1959) The tumor-promoting action of phenol and related compounds for mouse skin. Cancer Research 19, 413427.Google ScholarPubMed
Candido, EPM, Reeves, R and Davie, JR (1978) Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14, 105113.CrossRefGoogle ScholarPubMed
Cassidy, A, Bingham, SA and Cummings, JH (1994) Starch intake and colorectal cancer risk: an international comparison. British Journal of Cancer 69, 937942.CrossRefGoogle ScholarPubMed
Cummings, JH, Beatty, ER, Kingman, SM, Bingham, SA and Englyst, HN (1996) Digestion and physiological properties of resistant starch in the human large bowel. British Journal of Nutrition 75, 733747.CrossRefGoogle ScholarPubMed
Cummings, JH, Bingham, SA, Heaton, KW and Eastwood, MA (1992) Fecal weight, colon cancer risk, and dietary intake of nonstarch polysaccharides (dietary fiber). Gastroenterology 103, 17831789.CrossRefGoogle ScholarPubMed
Cummings, JH and Englyst, HN (1995) Gastrointestinal effects of food carbohydrates. American Journal of Clinical Nutrition 61, 938S945S.CrossRefGoogle Scholar
D'Argenio, G, Cosenza, V, Cave, MD, Iovino, P, Valle, ND, Lombardi, G and Mazzacca, G (1996) Butyrate enemas in experimental colitis and protection against large bowel cancer in a rat model. Gastroenterology 110, 17271734.CrossRefGoogle ScholarPubMed
Edwards, CA, Gibson, GR, Champ, M, Jensen, BB, Mathers, J, Nagengast, F, Rumney, C and Quehl, A (1996) In vitro method for quantification of the fermentation of starch by human faecal bacteria. Journal of the Science of Food and Agriculture 71, 209217.3.0.CO;2-4>CrossRefGoogle Scholar
Englyst, HN and Cummings, JH (1988) Improved method for measurement of dietary fiber as non-starch polysaccharides in plant foods. Journal of the Association of Official Analytical Chemists 71, 808814.Google ScholarPubMed
Englyst, HN, Hay, S and Macfarlane, GT (1987) Polysaccharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiology Letters 45, 163171.CrossRefGoogle Scholar
Englyst, HN, Kingman, SM and Cummings, JH (1992) Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition 46, S33S50.Google ScholarPubMed
Folch, J, Lees, M and Stanley, GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Foster-Powell, K and Brand-Miller, J (1995) International tables of glycemic index. American Journal of Clinical Nutrition 62, 871S893S.CrossRefGoogle ScholarPubMed
Goodlad, JS and Mathers, JC (1988) Effects of food carbohydrates on large intestinal fermentation n vitro. Proceedings of the Nutrition Society 47, 176A.Google Scholar
Hass, R, Busche, R, Luciano, L, Reale, E and van Englchardt, WV (1997) Lack of butyrate is associated with induction of Bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology 112, 875881.CrossRefGoogle ScholarPubMed
Holland, B, Unwin, I & Buss, DH (1988) Cereals and Cereal Products. The 3rd supplement to McCance & Widdowson's The Composition of Foods, 4th ed. London: H.M. Stationery Office.Google Scholar
Holland, B, Unwin, I & Buss, DH (1991) Vegetables, Herbs and Spices. The 5th supplement to McCance & Widdowson's The Composition of Foods, 4th ed. London: H.M. Stationery Office.CrossRefGoogle Scholar
Holland, B, Unwin, I & Buss, DH (1992) Fruit and Nuts. The 1st Supplement to McCance & Widdowson's The Composition of Foods, 5th ed. London: H.M. Stationery Office.CrossRefGoogle Scholar
Karoutis, AI, Tyler, RT and Slater, GP (1992) Analysis of legume oligosaccharides by high resolution gas chromatography. Journal of Chromatography 623, 186190.CrossRefGoogle ScholarPubMed
Lampe, JW, Wetsch, RF, Thomson, WO and Slavin, JL (1993) Gastrointestinal effects of sugarbeet fiber and wheat bran in healthy men. European Journal of Clinical Nutrition 47, 543548.Google ScholarPubMed
Jenkins, DJ, Cuff, D, Wolever, TM, Knowland, D, Thompson, L, Cohen, Z and Prokipchik, E (1987) Digestibility of carbohydrate foods in an ileostomate: relationship to dietary fiber, in vitro digestibility, and glycemic response. American Journal of Gastroenterology 82, 709717.Google Scholar
Key, FB, McClean, D and Mathers, JC (1996) Tissue hypertrophy and epithelial proliferation rate in the gut of rats fed on bread and haricot beans (Phaseolus vulgaris). British Journal of Nutrition 76, 273286.CrossRefGoogle ScholarPubMed
Liljeberg, H and Bjorck, I (1994) Bioavailability of starch in bread products. Postprandial glucose and insulin responses in healthy subjects and in vitro resistant starch content. European Journal of Clinical Nutrition 48, 151163.Google ScholarPubMed
Livesey, G, Wilkinson, JA, Roe, M, Faulks, R, Clark, S, Brown, JC, Kennedy, H and Elia, M (1995) Influence of the physical form of barley grain on the digestion of its starch in the human small intestine and implications for health. American Journal of Clinical Nutrition 61, 7581.CrossRefGoogle ScholarPubMed
McBurney, MI, Thompson, LU, Cuff, DJ and Jenkins, DJ (1988) Comparison of ileal effluents, dietary fibers, and whole foods in predicting the physiological importance of colonic fermentation. American Journal of Gastroenterology 83, 536540.Google ScholarPubMed
Macfarlane, GT and Allison, C (1986) Utilisation of protein by human gut bacteria. FEMS Microbiology and Ecology 38, 1924.CrossRefGoogle Scholar
Mathers, JC (1998) Nutrient regulation of intestinal proliferation and apoptosis. Proceedings of the Nutrition Society 57, 219223.CrossRefGoogle ScholarPubMed
Mathers, JC, Smith, H and 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
Mortensen, PB (1992) The effect of oral-administered lactulose on colonic nitrogen metabolism and excretion. Hepatology 16, 13501356.CrossRefGoogle ScholarPubMed
Muir, JG, Birkett, A, Brown, I, Jones, G and O'Dea, K (1995) Food processing and maize variety affects the amounts of starch escaping digestion in the small intestine. American Journal of Clinical Nutrition 61, 8289.Google ScholarPubMed
Muir, JG, Walker, KZ, Kaimakamis, MA, Cameron, MA, Govers MJAP, Lu, ZX, Young, GP and O'Dea, K (1998) Modulation of fecal markers relevant to colon cancer risk: a high-starch Chinese diet did not generate expected beneficial changes relative to a Western-type diet. American Journal of Clinical Nutrition 68, 372379.CrossRefGoogle Scholar
National Food Authority (1991) Composition of Foods Australia. Canberra: Australian Government Publishing Service.Google Scholar
Noakes, M, Clifton, PM, Nestel, PJ, Le Leu, R and McIntosh, G (1996) Effect of high-amylose starch and oat bran on metabolic variables and bowel function in individuals with hypertriglyceridemia. American Journal of Clinical Nutrition 64, 944951.CrossRefGoogle ScholarPubMed
Phillips, J, Muir, JG, Birkett, A, Lu, ZX, Jones, GP, O'Dea, K and Young, G (1995) Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. American Journal of Clinical Nutrition 62, 121130.CrossRefGoogle ScholarPubMed
Prosky, L, Asp, N-G, Furda, I, DeVries, JW, Schweizer, TF and Harland, BF (1985) Determination of total dietary fiber in foods and food products: collaborative study. Journal of the Association of Official Analytical Chemists 68, 677679.Google ScholarPubMed
Roediger, WEW (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424429.CrossRefGoogle ScholarPubMed
Rumney, CJ and Rowland, IR (1992) In vivo and in vitro models of the human colonic flora. Critical Reviews in Food Science and Nutrition 31, 299331.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 of fermentable fibre, gut microbes and luminal trophic factors. British Journal of Nutrition 58, 95103.CrossRefGoogle ScholarPubMed
Sakata, T (1988) Depression of intestinal epithelial cell proliferation rate by hindgut bypass in rats. Scandinavian Journal of Gastroenterology 23, 12001202.CrossRefGoogle ScholarPubMed
Scheppach, W, Fabian, C, Ahrens, F, Spengler, M and Kasper, H (1988) Effect of starch malabsorption on colonic function and metabolism in humans. Gastroenterology 95, 15491555.CrossRefGoogle ScholarPubMed
Scheppach, W, Fabian, C, Sachs, M and Kasper, H (1988) The effect of starch malabsorption on fecal short-chain fatty acid excretion in man. Scandinavian Journal of Gastroenterology 23, 755759.CrossRefGoogle ScholarPubMed
Silvester, KR, Englyst, HN and Cummings, JH (1995) Ileal recovery of starch from whole diets containing resistant starch measured in vitro and fermentation of ileal effluent. American Journal of Clinical Nutrition 62, 403411.CrossRefGoogle ScholarPubMed
Stephen, AM, Dahl, WJ, Sieber, GM, van Blaricom, JA and Morgan, DR (1995) Effect of green lentils on colonic function, nitrogen balance, and serum lipids in healthy human subjects. American Journal of Clinical Nutrition 62, 12611267.CrossRefGoogle ScholarPubMed
Sundberg, B, Wood, P, Lia, A, Andersson, H, Sandberg, AS, Hallmans, G and Aman, P (1996) Mixed-link beta-glucan from breads of different cereals is partly degraded in the human ileostomy model. American Journal of Clinical Nutrition 64, 878885.CrossRefGoogle Scholar
Tsao, D, Shi, Z, Wong, A and Kim, YS (1983) Effect of sodium butyrate on carcinoembryonic antigen production by human colonic adenocarcinoma cells in culture. Cancer Research 43, 12171222.Google ScholarPubMed
van Munster, IP, Tangerman, A and Nagengast, FM (1994) Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Digestive Diseases and Sciences 39, 834842.CrossRefGoogle ScholarPubMed
Visek, WJ (1978) Diet and cell growth modulation by ammonia. American Journal of Clinical Nutrition 31, S216S220.CrossRefGoogle ScholarPubMed
Walker, ARP, Walker, BF and Walker, AJ (1986) Faecal pH, dietary fibre intake, and proneness to colon cancer in four South African populations. British Journal of Cancer 53, 489495.CrossRefGoogle ScholarPubMed
Walker, KZ, Birkett, AM, Lu, ZX, Jones, G, O'Dea, K and Muir, JG (1997) Development of a simulated Australian diet for adults which may have use as a research tool. Australian Journal of Nutrition and Dietetics 54, 190197.Google Scholar