Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T06:54:54.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Beneficial health effects of low-digestible carbohydrate consumption

Published online by Cambridge University Press:  09 March 2007

Wolfgang Scheppach ,
Hardi Luehrs  and
Thomas Menzel
Wolfgang Scheppach*
Affiliation:
Department of Medicine, University of Wuerzburg, D-97080 Wuerzburg, Germany
Hardi Luehrs
Affiliation:
Department of Medicine, University of Wuerzburg, D-97080 Wuerzburg, Germany
Thomas Menzel
Affiliation:
Department of Medicine, University of Wuerzburg, D-97080 Wuerzburg, Germany
*
*Corresponding author: Wolfgang Scheppach, fax +49-931-201-3534, 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.

Low-digestible carbohydrates represent a class of enzyme-resistant saccharides that have specific effects on the human gastrointestinal tract. In the small bowel, they affect nutrient digestion and absorption, glucose and lipid metabolism and protect against known risk factors of cardiovascular disease. In the colon they are mainly degraded by anaerobic bacteria in a process called fermentation. As a consequence, faecal nitrogen excretion is enhanced, which is used clinically to prevent or treat hepatic encephalopathy. Low-digestible carbohydrates are trophic to the epithelia of the ileum and colon, which helps to avoid bacterial translocation. Short-chain fatty acids are important fermentation products and are evaluated as new therapeutics in acute colitis. They are considered in the primary prevention of colorectal cancer. The bifidogenic effect of fructo-oligosaccharides merits further attention. Unfermented carbohydrates increase faecal bulk and play a role in the treatment of chronic functional constipation, symptomatic diverticulosis and, possibly, the irritable bowel syndrome. In conclusion, low-digestible carbohydrates may play a role in the maintenance of human digestive health. However, the strength of evidence differs between disease entities.

Keywords

Low-digestible carbohydratesDietary fibreNon-starch polysaccharidesShort-chain fatty acidsTotal parenteral nutritionColorectal cancer
Type
Research Article
Information
British Journal of Nutrition , Volume 85 , Issue S1 , March 2001 , pp. S23 - S30
Copyright
Copyright © The Nutrition Society 2001

References

Agheli, N, Kabir, M, Berni-Canani, S, Petitjean, E, Boussairi, A, Luo, J, Bornet, F, Slama, G & Rizkalla, SW (1998) Plasma lipids and fatty acid synthase activity are regulated by short-chain fructo-oligosaccharides in sucrose-fed insulin-resistant rats. Journal of Nutrition 128, 1283–1288.CrossRefGoogle ScholarPubMed
Aldoori, WH, Giovannucci, EL, Rimm, EB, Wing, AL, Trichopoulos, DV & Willett, WC (1994) A prospective study of diet and the risk of symptomatic diverticular disease in men. American Journal of Clinical Nutrition 60, 757–764.Google Scholar
Alfieri, MA, Pomerleau, J, Grace, DM & Anderson, L (1995) Fiber intake of normal weight, moderately obese and severely obese subjects. Obesity Research 3, 541–547.CrossRefGoogle ScholarPubMed
Alverdy, JC, Aoys, E & Moss, GS (1990) Effect of commercially available chemically defined liquid diets on the intestinal microflora and bacterial translocation from the gut. Journal of Parenteral and Enteral Nutrition 14, 1–5.Google Scholar
Aminosharie, ME & Weber, FL (1993) Comparison of starch and lactulose, alone and in combination with antibiotics, on ammonia production in a fecal incubation system. Gastroenterology 104, A859.Google Scholar
Ascherio, A, Hennekens, C, Willett, WC, Sacks, F, Rosner, B, Manson, J, Witteman, J & Stampfer, MJ (1996) Prospective study of nutritional factors, blood pressure, and hypertension among US women. Hypertension 27, 1065–1072.CrossRefGoogle ScholarPubMed
Ascherio, A, Rimm, EB, Giovannucci, EL, Colditz, GA, Rosner, B, Willett, WC, Sacks, F & Stampfer, MJ (1992) A prospective study of nutritional factors and hypertension among US men. Circulation 86, 1475–1484.CrossRefGoogle ScholarPubMed
Ascherio, A, Rimm, EB, Hernan, MA, Giovannucci, EL, Kawachi, I, Stampfer, MJ & Willett, WC (1998) Intake of potassium, magnesium, calcium, and fiber and risk of stroke among US men. Circulation 98, 1198–1204.Google Scholar
Bagger, M, Andersen, O, Nielsen, JB & Ryttig, KR (1996) Dietary fibres reduce blood pressure, serum total cholesterol and platelet aggregation in rats. British Journal of Nutrition 75, 483–493.Google Scholar
Barber, AE, Jones, WG, Minei, JP, Fahey, TJ, Moldawer, LL, Rayburn, JL, Fischer, E, Keogh, CV, Shires, GT & Lowry, SF (1990) Glutamine or fiber supplementation of a defined formula diet: Impact on bacterial translocation, tissue composition, and response to endotoxin. Journal of Parenteral and Enteral Nutrition 14, 335–343.Google Scholar
Bartram, HP, Scheppach, W, Schmid, H, Hofmann, A, Dusel, G, Richter, F, Richter, A & Kasper, H (1993) Proliferation of human colonic mucosa as an intermediate biomarker of carcinogenesis: effects of butyrate, deoxycholate, calcium, ammonia, and pH. Cancer Research 53, 3283–3288.Google ScholarPubMed
Bircher, J, Müller, J, Guggenheim, P & Haemmerli, UP (1966) Treatment of chronic portal-systemic encephalopathy with lactulose. Lancet i, 890–892.Google Scholar
Blackburn, NA & Johnson, IT (1983) The influence of guar gum on the movement of inulin, glucose and fluid in rat intestine during perfusion in vivo. Pfluegers Archiv 397, 144–148.Google Scholar
Blackburn, NA, Redfern, JS, Jarjis, H, Holgate, AM, Hanning, I, Scarpello, JHB, Johnson, IT & Read, NW (1984) The mechanism of action of guar gum in improving glucose tolerance in man. Clinical Science 66, 329–336.CrossRefGoogle ScholarPubMed
Bouhnik, Y, Vahedi, K, Achour, L, Attar, A, Salfati, J, Pochart, P, Marteau, P, Flourie, B, Bornet, F & Rambaud, JC (1999) Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. Journal of Nutrition 129, 113–116.Google Scholar
Breuer, RI, Soergel, KH, Lashner, BA, Christ, ML, Hanauer, SB, Vanaguas, A, Harig, JM, Keshavarzian, A, Robinson, M, Sellin, JH, Weinberg, D, Vidican, DE, Flemal, KL & Rademaker, AW (1997) Short chain fatty acid rectal irrigation for left-sided ulcerative colitis: a randomised, placebo controlled trial. Gut 40, 485–491.CrossRefGoogle ScholarPubMed
Brodribb, AJM & Humphreys, DM (1976) Diverticular disease: three studies. British Medical Journal i, 424–430.CrossRefGoogle ScholarPubMed
Brown, L, Rosner, B, Willett, WC & Sacks, FM (1999) Cholesterol-lowering effects of dietary fiber: a meta-analysis. American Journal of Clinical Nutrition 69, 30–42.Google Scholar
Burkitt, DP (1969) Related disease, related cause?. Lancet ii, 1229–1231.CrossRefGoogle ScholarPubMed
Burkitt, DP (1971) Epidemiology of cancer of the colon and rectum. Cancer 28, 3–13.Google Scholar
Carpaneto, EM, Mariani, MR & Ferrini, S (1991) Stimulation of DNA synthesis in primary culture of human lymphocytes by sodium butyrate. Proceedings of the American Association of Cancer Research 32, 331–336.Google Scholar
Cassidy, A, Bingham, SA & Cummings, JH (1994) Starch intake and colorectal cancer risk: an international comparison. British Journal of Cancer 69, 937–942.Google Scholar
Catala, I, Butel, MJ, Bensaada, M, Popot, F, Tessedre, AC, Rimbault, A & Szylit, O (1999) Oligofructose contributes to the protective role of bifidobacteria in experimental necrotising enterocolitis in quails. Journal of Medical Microbiology 48, 89–94.CrossRefGoogle Scholar
Cook, IJ, Irvine, EJ, Campbell, D, Shannon, S, Reddy, SN & Collins, SM (1990) Effect of dietary fiber on symptoms and rectosigmoid motility in patients with irritable bowel syndrome. Gastroenterology 98, 66–72.CrossRefGoogle ScholarPubMed
Cummings, JH, Branch, W, Jenkins, DJA, Southgate, DAT, Houston, H & James, WPT (1978) Colonic response to dietary fibre from carrot, cabbage, apple, bran, and guar gum. Lancet i, 5–9.CrossRefGoogle Scholar
Cummings, JH (1997) Short-chain fatty acid enemas in the treatment of distal ulcerative colitis. European Journal of Gastroenterology and Hepatology 9, 149–153.CrossRefGoogle ScholarPubMed
DaZhong, X & Deitch, EA (1998) Elemental diet-induced bacterial translocation associated with systemic and intestinal immune suppression. Journal of Parenteral and Enteral Nutrition 22, 37–41.Google Scholar
Deng, G, Liu, G, Hu, L, Gum, JR & Kim, YS (1992) Transcriptional regulation of the human placental-like alkaline phosphatase gene and mechanisms involved in its induction by sodium butyrate. Cancer Research 52, 3378–3383.Google Scholar
Drossman, DA, Whitehead, WE & Camillieri, M (1997) American Gastroenterological Association medical position statement: irritable bowel syndrome. Gastroenterology 112, 2118–2137.Google Scholar
Fearon, ER & Vogelstein, B (1990) A genetic model for colorectal tumorigenesis. Cell 61, 759–767.Google Scholar
Fisher, N, Berry, CS, Fearn, T, Gregory, JA & Hardy, J (1985) Cereal dietary fibre consumption and diverticular disease: a lifespan study in rats. American Journal of Clinical Nutrition 42, 788–804.CrossRefGoogle ScholarPubMed
Fuchs, CS, Giovannucci, EL, Colditz, GA, Hunter, DJ, Stampfer, MJ, Rosner, B, Speizer, FE & Willett, WC (1999) Dietary fiber and the risk of colorectal cancer and adenoma in women. New England Journal of Medicine 340, 169–176.Google Scholar
Gear, JS, Ware, A, Fursdon, P, Mann, JI, Nolan, DJ, Brodribb, AJ & Vessey, MP (1979) Symptomless diverticular disease and intake of dietary fibre. Lancet i, 511–514.CrossRefGoogle Scholar
Gibson, GR, Beatty, ER, Wang, X & Cummings, JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.Google Scholar
Gibson, GR, Moeller, I, Kagelari, O, Folino, M & Young, GP (1992) Contrasting effects of butyrate on the expression of phenotypic markers of differentiation in neoplastic and non-neoplastic colonic epithelial cells in vitro. Journal of Gastroenterology and Hepatology 7, 165–172.Google Scholar
Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125, 1401–1412.CrossRefGoogle ScholarPubMed
Goodlad, RA, Ratcliffe, B, Fordham, JP & Wright, NA (1989) Does dietary fibre stimulate intestinal epithelial cell proliferation in germ free rats? Gut 30, 820–825.Google Scholar
Goodlad, RA & Wright, NA (1983) Effects of addition of kaolin or cellulose to an elemental diet in intestinal cell proliferation in the mouse. British Journal of Nutrition 50, 91–98.CrossRefGoogle ScholarPubMed
Hague, A, Diaz, GD, Hicks, DJ, Krajewski, S, Reed, JC & Paraskeva, C (1997) Bcl-2 and bak may play a pivotal role in sodium butyrate-induced apoptosis in colonic epithelial cells; however over expression of bcl-2 does not protect against bak-mediated apoptosis. International Journal of Cancer 72, 898–905.Google Scholar
Hague, A, Elder, DJE, Hicks, DJ & Paraskeva, C (1995) Apoptosis in colorectal tumour cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate. International Journal of Cancer 60, 400–406.CrossRefGoogle ScholarPubMed
Hague, A, Manning, AM, Hanlon, KA, Huschtscha, LI, Hart, D & Paraskeva, C (1993) Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer. International Journal of Cancer 55, 498–505.CrossRefGoogle Scholar
Havenaar, R, Brink, BT, Huis in't Veld, JHT (1992) Selection of strains for probiotic use. In Probiotics: The Scientific Basis. 209–224. [R, Fuller, editor]. London: Chapman and Hall.CrossRefGoogle Scholar
Howe, GR, Benito, E, Castelleto, R, Cornee, J, Esteve, J, Gallgher, RP, Iscovich, JM, Deng-ao, J, Kaaks, R, Kune, GA, Kune, S, L'Abbe, KA, Lee, HP, Lee, M, Miller, AB, Peters, RK, Potter, JD, Riboli, E, Slattery, ML, Trichopoulos, D, Tuyns, A, Tzonou, A, Whittemore, AS, Wu-Williams, AH & Shu, Z (1992) Dietary intake of fiber and decreased risk of cancers of the colon and rectum: evidence from the combined analysis of 13 case-control studies. Journal of the National Cancer Institute 84, 1887–1896.Google Scholar
Humble, CG, Malarcher, AM & Tyroler, HA (1993) Dietary fiber and coronary heart disease in middle-aged hypercholesterolemic men. American Journal of Preventive Medicine 9, 197–202.Google Scholar
Hylla, S, Gostner, A, Dusel, G, Anger, H, Bartram, H-P, Christl, SU, Kasper, H & Scheppach, W (1998) Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. American Journal of Clinical Nutrition 67, 136–142.Google Scholar
Jacobs, LR & Lupton, JR (1984) Effect of dietary fibers on rat large bowel mucosal growth and cell proliferation. American Journal of Physiology 246, G378–G385.Google ScholarPubMed
Jenkins, DJA, Wolever, TMS, Taylor, RH, Barker, H, Fielden, H, Baldwin, JM, Bowling, AC, Newman, HC, Jenkins, AL & Goff, DV (1981) Glycemic index of foods: a physiological basis for carbohydrate exchange. American Journal of Clinical Nutrition 34, 362–366.Google Scholar
Kasper, H (1988) Einfluss von Ballaststoffen auf die Serum-Lipidkonzentration. Aktuelle Ernährungsmedizin 13, 75–76.Google Scholar
Khaw, KT & Barret-Connor, E (1987) Dietary fiber and reduced ischemic disease mortality rates in men and women: a 12-year prospective study. American Journal of Epidemiology 126, 1093–1102.Google Scholar
Koruda, MJ, Rolandelli, RH, Settle, RG, Saul, SH & Rombeau, JL (1986) The effect of a pectin supplemented elemental diet on intestinal adaptation to massive small bowel resection. Journal of Parenteral and Enteral Nutrition 10, 343–350.Google Scholar
Kripke, SA, Fox, AD, Berman, JM, Settle, RG & Rombeau, JL (1989) Stimulation of intestinal mucosal growth with intracolonic infusion of short-chain fatty acids. Journal of Parenteral and Enteral Nutrition 12, 109–116.Google Scholar
Kruh, J, Tichonicky, L & Defer, N (1994) Effect of butyrate on gene expression. In Short Chain Fatty Acids, pp. 135–147. [HJ, Binder, JH, Cummings & K, Soergel, editors]. Dordrecht: Kluwer.Google Scholar
Lucey, MR, Clark, ML, Lowndes, J & Dawson, AM (1987) Is bran efficacious in irritable bowel syndrome? A double-blind placebo-controlled crossover study. Gut 28, 221–225.CrossRefGoogle ScholarPubMed
Luehrs, H, Schauber, J, Boxberger, F, Dusel, G, Krott, K, Kelber, E, Menzel, T & Scheppach, W (1999) Butyrate-mediated inhibition of nuclear factor kappa B activation. Gastroenterology 116, A563.Google Scholar
Macfarlane, GT & Cummings, JH (1991) The colonic flora, fermentation, and large bowel digestive function. In The Large Intestine: Physiology, Pathophysiology, and Disease. pp. 51–91. [SP, Phillips, JH, Pemberton & RG, Shorter, editors]. New York: Raven Press.Google Scholar
Pasman, WJ, Saris, WH, Wauters, MA & Westerterp-Plantenga, MS (1997) Effect of one week of fibre supplementation on hunger and satiety ratings and energy intake. Appetite 29, 77–87.CrossRefGoogle ScholarPubMed
Pierre, F, Perrin, P, Champ, M, Bornet, F, Meflah, K & Menanteau, J (1997) Short-chain fructo-oligosaccharides reduce the occurrence of colonic tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Research 57, 225–228.Google ScholarPubMed
Prynne, CJ & Southgate, DAT (1979) The effects of a supplement of dietary fibre on faecal excretion by human subjects. British Journal of Nutrition 41, 495–503.Google Scholar
Reddy, BS, Hamid, R & Rao, CV (1997) Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 18, 1371–1374.CrossRefGoogle ScholarPubMed
Rimm, EB, Ascherio, A, Giovannucci, E, Spiegelman, D, Stampfer, MJ & Willett, WC (1996) Vegetable, fruit, and cereal fiber intake and risk of coronary heart disease among men. Journal of the American Medical Association 275, 447–451.Google Scholar
Roberfroid, MB (1997) Health benefits of non-digestible oligosaccharides. Advances in Experimental Medicine and Biology 427, 211–219.Google Scholar
Roediger, WEW (1980 a) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21, 793–798.Google Scholar
Roediger, WEW (1980 b) The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet ii, 712–715.Google Scholar
Roediger, WEW (1990) The starved colon – diminished mucosal nutrition, diminished absorption, and colitis. Diseases of the Colon and Rectum 33, 858–862.Google Scholar
Rolandelli, RH, Koruda, MJ, Settle, RG & Rombeau, JL (1986) Effects of intraluminal infusion of short-chain acids on the healing of colonic anastomosis in the rat. Surgery 100, 198–203.Google ScholarPubMed
Schauber, J, Luehrs, H, Boxberger, F, Dusel, G, Krott, K, Kelber, E, Scheppach, W & Menzel, T (1999) Additive effects of combined treatment with butyrate and aspirin on human colon cancer cells. Gastroenterology 116, A498.Google Scholar
Scheppach, W, Bartram, P, Richter, A, Richter, F, Liepold, H, Dusel, G, Hofstetter, G, Rüthlein, J & Kasper, H (1992) The effect of short-chain fatty acids on the human colonic mucosa in vitro. Journal of Parenteral and Enteral Nutrition 16, 43–48.CrossRefGoogle ScholarPubMed
Scheppach, W, Bingham, S, Boutron-Ruault, MC, de Verdier, MG, Moreno, V, Nagengast, FM, Reifen, R, Riboli, E, Seitz, HK & Wahrendorf, J (1999) WHO consensus statement on the role of nutrition in colorectal cancer. European Journal of Cancer Prevention 8, 57–62.Google Scholar
Scheppach, W, Fabian, C, Ahrens, F, Spengler, M & Kasper, H (1988) Effect of starch malabsorption on colonic function and metabolism in humans. Gastroenterology 95, 1549–1555.Google Scholar
Scheppach, W & German-Austrian SCFA Study Group (1996) Treatment of distal ulcerative colitis with short-chain fatty acid enemas. A placebo-controlled trial. Digestive Diseases and Sciences 41, 2254–2259.CrossRefGoogle ScholarPubMed
Scheppach, W, Müller, JG, Boxberger, F, Dusel, G, Richter, F, Bartram, HP, Dempfle, CE & Kasper, H (1997) Histological changes of the colonic mucosa following irrigation with short-chain fatty acids. European Journal of Gastroenterology and Hepatology 9, 163–168.CrossRefGoogle ScholarPubMed
Sedman, PC, Macfie, J, Sagar, P, Mitchell, CJ, May, J, Mancey-Jones, B & Johnstone, D (1994) The prevalence of gut translocation in humans. Gastroenterology 107, 643–649.Google Scholar
Spaeth, G, Specian, RD, Berg, RD & Deitch, EA (1990) Bulk prevents bacterial translocation induced by the oral administration of total parenteral nutrition solution. Journal of Parenteral and Enteral Nutrition 14, 442–447.Google Scholar
Stephen, AM & Cummings, JH (1980) The microbial contribution to human faecal mass. Journal of Medical Microbiology 13, 45–56.Google Scholar
Toeller, M, Buyken, AE, Heitkamp, G, de Pergola, G, Giorgino, F & Fuller, JH (1999) Fiber intake, serum cholesterol levels, and cardiovascular disease in European individuals with type 1 diabetes. EURODIAB IDDM complications study group. Diabetes Care 22, Suppl. 2, B21–B28.Google ScholarPubMed
Toscani, A, Soprano, DR & Soprano, KJ (1988) Molecular analysis of sodium butyrate-induced growth arrest. Onocogene Research 3, 223–238.Google Scholar
Trock, B, Lanza, E & Greenwald, P (1990) Dietary fiber, vegetables, and colon cancer; critical review and meta-analyses of the epidemiologic evidence. Journal of the National Cancer Institute 82, 650–661.Google Scholar
Tsujii, M & DuBois, RN (1995) Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxidase synthase 2. Cell 83, 493–501.CrossRefGoogle Scholar
Uribe-Esquivel, M, Moran, S, Poo, JL & Munoz, RM (1997) In vitro and in vivo lactose and lactulose effects on colonic fermentation and portal-systemic encephalopathy parameters. Scandinavian Journal of Gastroenterology 32(Suppl. 222), 49–52.Google Scholar
Voderholzer, WA, Schatke, W, Mühldorfer, BE, Klauser, AG, Birkner, B & Müller-Lissner, SA (1997) Clinical response to dietary fiber treatment of chronic constipation. American Journal of Gastroenterology 92, 95–98.Google ScholarPubMed
Wang, J & Friedman, EA (1998) Short-chain fatty acids induce cell cycle inhibitors in colonocytes. Gastroenterology 114, 940–946.Google Scholar
Weber, FL, Banwell, JG, Fresard, KM & Cummings, JH (1987) Nitrogen in fecal bacterial, fiber, and soluble fractions of patients with cirrhosis: effects of lactulose and lactulose plus neomycin. Journal of Laboratory and Clinical Medicine 110, 256–263.Google ScholarPubMed
Whitlock, JP, Galeazzi, D & Schulman, H (1983) Acetylation and calcium-dependent phosphorylation of histone H3 in nuclei from butyrate-treated HeLa cells. Journal of Biological Chemistry 258, 1299–1304.Google Scholar
Willett, WC, Stampfer, MJ, Colditz, GA, Rosner, BA & Speizer, FE (1990) Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. New England Journal of Medicine 323, 1664–1672.CrossRefGoogle Scholar