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Mechanisms of cholesterol-lowering effects of dietary insoluble fibres: relationships with intestinal and hepatic cholesterol parameters

Published online by Cambridge University Press:  08 March 2007

Ariëtte M. van Bennekum
Affiliation:
Department of GI/Nutrition, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, 3615 Civic Center Blvd, Philadelphia, PA 19104-4318, USA
David V. Nguyen
Affiliation:
Department of GI/Nutrition, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, 3615 Civic Center Blvd, Philadelphia, PA 19104-4318, USA
Georg Schulthess
Affiliation:
Department of Internal Medicine, Medical Policlinic, University Hospital, CH-8091 Zurich, Switzerland
Helmut Hauser
Affiliation:
Institute of Biochemistry, Swiss Federal Institute of Technology, Zürich, Switzerland
Michael C. Phillips*
Affiliation:
Department of GI/Nutrition, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, 3615 Civic Center Blvd, Philadelphia, PA 19104-4318, USA
*
*Corresponding author: Dr Michael C. Phillips, fax +1 215 590 0583, email phillipsmi@email.chop.edu
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Abstract

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Fibres with a range of abilities to perturb cholesterol homeostasis were used to investigate how the serum cholesterol-lowering effects of insoluble dietary fibres are related to parameters of intestinal cholesterol absorption and hepatic cholesterol homeostasis in mice. Cholestyramine, chitosan and cellulose were used as examples of fibres with high, intermediate and low bile acid-binding capacities, respectively. The serum cholesterol levels in a control group of mice fed a high fat/high cholesterol (HFHC) diet for 3 weeks increased about 2-fold to 4·3 mm and inclusion of any of these fibres at 7·5 % of the diet prevented this increase from occurring. In addition, the amount of cholesterol accumulated in hepatic stores due to the HFHC diet was reduced by treatment with these fibres. The three kinds of fibres showed similar hypocholesterolaemic activity; however, cholesterol depletion of liver tissue was greatest with cholestyramine. The mechanisms underlying the cholesterol-lowering effect of cholestyramine were (1) decreased cholesterol (food) intake, (2) decreased cholesterol absorption efficiency, and (3) increased faecal bile acid and cholesterol excretion. The latter effects can be attributed to the high bile acid-binding capacity of cholestyramine. In contrast, incorporation of chitosan or cellulose in the diet reduced cholesterol (food) intake, but did not affect either intestinal cholesterol absorption or faecal sterol output. The present study provides strong evidence that above all satiation and satiety effects underlie the cholesterol-lowering properties of insoluble dietary fibres with moderate or low bile acid-binding capabilities.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Ausar, SF, Morcillo, M, Leon, AE et al. (2003) Improvement of HDL- and LDL-cholesterol levels in diabetic subjects by feeding bread containing chitosan. J Med Food 6, 397399.CrossRefGoogle ScholarPubMed
Bartlett, GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234, 466468.CrossRefGoogle ScholarPubMed
Bokura, H & Kobayashi, S (2003) Chitosan decreases total cholesterol in women: a randomized, double-blind, placebo-controlled trial. Eur J Clin Nutr 57, 721725.CrossRefGoogle ScholarPubMed
Brown, WV (1990) Clinical trials including an update on the Helsinki Heart study. Am J Cardiol 66, 11A15A.Google Scholar
Burton-Freeman, B (2000) Dietary fiber and energy regulation. J Nutr 130, 272S275S.Google Scholar
Carter, CP, Howles, PN & Hui, DY (1997) Genetic variation in cholesterol absorption efficiency among inbred strains of mice. J Nutr 127, 13441348.CrossRefGoogle ScholarPubMed
Casdorph, HR (1967) Treatment of hypercholesterolemia with cholestyramine, a bile acid sequestering resin. Vasc Dis 4, 305308.Google ScholarPubMed
Castelli, WP (1984) Epidemiology of coronary heart disease: The Framingham study. Am J Med 76, 412.CrossRefGoogle ScholarPubMed
Chen, WJL & Anderson, JW (1979) Effects of plant fiber in decreasing plasma total cholesterol and increasing high-density lipoprotein cholesterol. Proc Soc Exp Biol Med 162, 310313.CrossRefGoogle ScholarPubMed
Cohen, DE (1999) Hepatocellular transport and secretion of biliary lipids. Curr Opin Lipidol 10, 295302.Google Scholar
Farkas, J, Angel, A & Avigan, MI (1973) Studies on the compartmentation of lipid in adipose cells. II. Cholesterol accumulation and distribution in adipose tissue components. J Lipid Res 14, 344356.CrossRefGoogle ScholarPubMed
Fernandez, ML (2001) Soluble fiber and nondigestible carbohydrate effects on plasma lipids and cardiovascular risk. Curr Opin Lipidol 12, 3540.CrossRefGoogle ScholarPubMed
Furda, I (1983) Aminopolysaccharides – their potential as dietary fiber. In Unconventional Sources of Dietary Fiber, pp. 105122 [Furda, I, editor]. ACS Symposium Series no. 214 Washington DC USA: American Chemical Society.Google Scholar
Furda, I (1990) Interaction of dietary fiber with lipids – mechanistic theories and their limitations. Adv Exp Med Biol 270, 6782.CrossRefGoogle ScholarPubMed
Gallaher, CM, Munion, J, Hesslink, RJ, Wise, J & Gallaher, DD (2000) Cholesterol reduction by glucomannan and chitosan is mediated by changes in cholesterol absorption and bile acid and fat excretion in rats. J Nutr 130, 27532759.CrossRefGoogle ScholarPubMed
Grundy, SM (1983) Absorption and metabolism of dietary cholesterol. Annu Rev Nutr 3, 7196.CrossRefGoogle ScholarPubMed
Grundy, SM, Ahrens, EH & Salen, G (1968) Dietary β-sitosterol as an internal standard to correct for cholesterol losses in sterol balance studies. J Lipid Res 9, 374387.CrossRefGoogle ScholarPubMed
Gylling, H, Vanhanen, H & Miettinen, TA (1989) Effects of acipimox and cholestyramine on serum lipoproteins, non-cholesterol sterols and cholesterol absorption and elimination. Eur J Clin Pharmacol 37, 111115.CrossRefGoogle Scholar
Han, LK, Kimura, Y & Okuda, H (1999) Reduction in fat storage during chitin-chitosan treatment in mice fed a high-fat diet. Int J Obesity 23, 174179.CrossRefGoogle ScholarPubMed
Homan, R & Krause, BR (1997) Established and emerging strategies for inhibition of cholesterol absorption. Curr Pharm Design 3, 2944.CrossRefGoogle Scholar
Ishikawa, TT, MacGee, J, Morrison, JA & Glueck, CJ (1974) Quantitative analysis of cholesterol in 5 to 20 μl of plasma. J Lipid Res 15, 286291.Google Scholar
Jennings, CD, Boleyn, K, Bridges, SR, Wood, PJ & Anderson, JW (1988) A comparison of the lipid-lowering and intestinal morphological effects of cholestyramine, chitosan, and oat gum in rats. Proc Soc Exp Biol Med 189, 1320.CrossRefGoogle ScholarPubMed
Kesaniemi, YA & Miettinen, TA (1987) Cholesterol absorption efficiency regulates plasma cholesterol level in the Finnish population. Eur J Clin Invest 17, 391395.Google Scholar
Lee, JK, Kim, SU & Kim, JH (1999) Modification of chitosan to improve its hypocholesterolemic capacity. Biosci Biotechnol Biochem 63, 833839.Google Scholar
Maezaki, Y, Tsuji, K, Nakagawa, Y, Kawai, Y, Akimoto, M, Tsugita, T, Takekawa, W, Terada, A, Hara, H & Mitsuoka, T (1993) Hypocholesterolemic effect of chitosan in adult males. Biosci Biotech Biochem 57, 14391444.CrossRefGoogle Scholar
Mhurchu, CN, Poppitt, SD, McGill, AT, Leahy, FE, Bennett, DA, Lin, R, Ormod, D, Ward, L, Strik, C & Rodgers, A (2004) The effect of the dietary supplement, chitosan, on body weight; a randomized controlled trial in 250 overweight and obese adults. Int J Obes Relat Metab Disord 28, 11491156.CrossRefGoogle ScholarPubMed
Pittler, MH, Abbot, NC, Harkness, EF & Ernst, E (1999) Randomized, double-blind trial of chitosan for body weight reduction. Eur J Clin Nutr 53, 379381.CrossRefGoogle ScholarPubMed
Schiller, LR, Bilhartz, LE, Santa, Ana CA & Fordtran, JS (1990) Comparison of endogenous and radiolabeled bile acid excretion in patients with idiopathic chronic diarrhea. Gastroenterology 98, 10361043.Google Scholar
Sehayek, E, Nath, C, Heinemann, T, McGee, M, Seidman, CE, Samuel, P & Breslow, JL (1998) U-shape relationship between change in dietary cholesterol absorption and plasma lipoprotein responsiveness and evidence for extreme interindividual variation in dietary cholesterol absorption in humans. J Lipid Res 39, 24152422.Google Scholar
Shurpalekar, KS, Doraiswamy, TR, Sundaravalli, OE, Narayana Rao, M (1971) Effect of inclusion of cellulose in an ‘atherogenic’ diet on the blood lipids of children. Nature 232, 554555.CrossRefGoogle Scholar
Stanley, MM, Paul, D, Gacke, D & Murphy, J (1973) Effects of cholestyramine, metamucil, and cellulose on fecal bile salt excretion in man. Gastroenterology 65, 889894.CrossRefGoogle ScholarPubMed
Story, JA, Furumoto, EJ & Buhman, KK (1997) Dietary fiber and bile acid metabolism–an update. Adv Exp Med Biol 427, 259266.Google Scholar
Trautwein, EA, Jürgensen, U & Erbersdobler, HF (1997) Cholesterol-lowering and gallstone-preventing action of chitosans with different degrees of deacetylation in hamsters fed cholesterol-rich diets. Nutr Res 17, 10531065.CrossRefGoogle Scholar
Turley, SD, Daggy, BP & Dietschy, JM (1994) Psyllium augments the cholesterol-lowering action of cholestyramine in hamsters by enhancing sterol loss from the liver. Gastroenterology 107, 444452.CrossRefGoogle ScholarPubMed
Turley, SD, Daggy, BP & Dietschy, JM (1996) Effect of feeding psyllium and cholestyramine in combination on low density lipoprotein metabolism and fecal bile acid excretion in hamsters with dietary-induced hypercholesterolemia. J Cardiovasc Pharmacol 27, 7179.Google Scholar
Turley, SD & Dietschy, JM (1978) Re-evaluation of the 3 alpha-hydroxysteroid dehydrogenase assay for total bile acids in bile. J Lipid Res 19, 924928.Google Scholar
Vahouny, GV, Roy, T, Gallo, LL, Story, JA, Kritchevsky, D & Cassidy, M (1980a) Dietary fibers III. Effects of chronic intake on cholesterol absorption and metabolism in the rat. Am J Clin Nutr 33, 21822191.CrossRefGoogle ScholarPubMed
Vahouny, GV, Tombes, R, Cassidy, MM, Kritchevsky, D & Gallo, LL (1980b) Dietary fibers: V. Binding of bile salts, phospholipids and cholesterol from mixed micelles by bile acid sequestrants and dietary fibers. Lipids 15, 10121018.Google Scholar
Ylitalo, R, Lehtinen, S, Wuolijoki, E, Ylitalo, P & Lehtimaki, T (2002) Cholesterol-lowering properties and safety of chitosan. Arzneimittelforschung 52, 17.Google ScholarPubMed