Colonic health: Fermentation and short chain fatty acids

Journal of Clinical Gastroenterology

Volumn 40, Issue 3, 2006, Pages 235-243

  Wong, Julia M W ^a   De Souza, Russell ^a   Kendall, Cyril W C ^a   Emam, Azadeh ^a   Jenkins, David J A ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Carbohydrates; Fermentation; SCFAs

Indexed keywords

ACETIC ACID; BILE ACID; BUTYRIC ACID; CARBOHYDRATE; CHOLESTEROL; FRUCTOSE OLIGOSACCHARIDE; HISTONE DEACETYLASE; INULIN; LIPID; PREBIOTIC AGENT; PROBIOTIC AGENT; PROPIONIC ACID; SHORT CHAIN FATTY ACID; STARCH;

ABSORPTION; ACIDIFICATION; APOPTOSIS; CARDIOVASCULAR DISEASE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL TRANSFORMATION; CHOLESTEROL SYNTHESIS; COLITIS; COLON; COLON CANCER; COLON DISEASE; COLON MUCOSA; CONFERENCE PAPER; DIETARY FIBER; ENZYME INHIBITION; FERMENTATION; FOOD COMPOSITION; GASTROINTESTINAL DISEASE; HUMAN; INTESTINE CELL; LAVAGE; LIPID BLOOD LEVEL; MICROFLORA; NONHUMAN; PRIORITY JOURNAL; ULCERATIVE COLITIS;

CARBOHYDRATE METABOLISM; COLON; DIETARY FIBER; FATTY ACIDS, VOLATILE; FERMENTATION; GASTROINTESTINAL DISEASES; HUMANS; INTESTINAL ABSORPTION;

EID: 33748209543     PISSN: 01920790     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004836-200603000-00015     Document Type: Conference Paper

References (124)

1. Roediger WE. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut. 1980;21:793-798.
2. Jenkins DJ, Kendall CW, Vuksan V. Inulin, oligofructose and intestinal function. J Nutr. 1999;129(Suppl 7):1431S-1433S.
3. Floch MH, Hong-Curtiss J. Probiotics and functional foods in gastrointestinal disorders. Curr Treat Options Gastroenterol. 2002;5:311-321.
4. Miller TL, Wolin MJ. Fermentations by saccharolytic intestinal bacteria. Am J Clin Nutr. 1979;32:164-172.
5. Cummings JH. Fermentation in the human large intestine: evidence and implications for health. Lancet. 1983;1:1206-1209.
6. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol. 1991;70:443-459.
7. Macfarlane GT, Gibson GR. Microbiological aspects of production of short-chain fatty acids in the large bowel. In: Cummings JH, Rombeau JL, Sakata T, eds. Physiological and Clinical Aspects of Short-chain Fatty Acids. Cambridge (England), New York, NY: Cambridge University Press; 1995:87-105.
8. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81:1031-1064.
9. Cummings JH, Hill MJ, Bone ES, et al. The effect of meat protein and dietary fiber on colonic function and metabolism. II. Bacterial metabolites in feces and urine. Am J Clin Nutr. 1979;32:2094-2101.
10. Cummings JH. Short chain fatty acids in the human colon. Gut. 1981;22:763-779.
11. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62:67-72.
12. Roberfroid, MB, ed. Inulin-Type Fructans: Functional Food Ingredients. Boca Raton: CRC Press; 2005.
13. Cook SI, Sellin JH. Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther. 1998;12:499-507.
14. Argenzio RA, Southworth M. Sites of organic acid production and absorption in gastrointestinal tract of the pig. Am. J. Physiol. 1974;226:454-460.
15. Owens FN, Isaacson HR. Ruminal microbial yields: factors influencing synthesis and bypass. Fed Proc. 1977;36:198-202.
16. Hill MJ. Bacterial fermentation of complex carbohydrate in the human colon. Eur J Cancer Prev. 1995;4:353-358.
17. Savage DC. Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr. 1986;6:155-178.
18. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401-1412.
19. Macfarlane GT, Gibson GR, Cummings JH. Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol. 1992;72:57-64.
20. Jenkins DJ, Kendall CW. Resistant starches. Curr Opin Gastroenterol. 2000;16:178-183.
21. Marsono Y, Illman RJ, Clarke JM, et al. Plasma lipids and large bowel volatile fatty acids in pigs fed on white rice, brown rice and rice bran. Br J Nutr. 1993;70:503-513.
22. Topping DL, Illman RJ, Clarke JM, et al. Dietary fat and fiber alter large bowel and portal venous volatile fatty acids and plasma cholesterol but not biliary steroids in pigs. J Nutr. 1993;123:133-143.
23. Bird AR, Hayakawa T, Marsono Y, et al. Coarse brown rice increases fecal and large bowel short-chain fatty acids and starch but lowers calcium in the large bowel of pigs. J Nutr. 2000;130:1780-1787.
24. Cummings JH, Englyst HN, Wiggins HS. The role of carbohydrates in lower gut function. Nutr Rev. 1986;44:50-54.
25. Cummings JH, Englyst HN. Fermentation in the human large intestine and the available substrates. Am J Clin Nutr. 1987;45(Suppl 5):1243-1255.
26. Anderson IH, Levine AS, Levitt MD. Incomplete absorption of the carbohydrate in all-purpose wheat flour. N Engl J Med. 1981;304:891-892.
27. Stephen AM, Haddad AC, Phillips SF. Passage of carbohydrate into the colon. Direct measurements in humans. Gastroenterology. 1983;85:589-595.
28. Wolever TM, Cohen Z, Thompson LU, et al. Ileal loss of available carbohydrate in man: comparison of a breath hydrogen method with direct measurement using a human ileostomy model. Am J Gastroenterol. 1986;81:115-122.
29. Jenkins DJ, Cuff D, Wolever TM, et al. Digestibility of carbohydrate foods in an ileostomate: relationship to dietary fiber, in vitro digestibility, and glycemic response. Am J Gastroenterol. 1987;82:709-717.
30. Jenkins DJ, Vuksan V, Kendall CW, et al. Physiological effects of resistant starches on fecal bulk, short chain fatty acids, blood lipids and glycemic index. J Am Coll Nutr. 1998;17:609-616.
31. Fredstrom SB, Lampe JW, Jung HJ, et al. Apparent fiber digestibility and fecal short-chain fatty acid concentrations with ingestion of two types of dietary fiber. JPEN J Parenter Enteral Nutr. 1994;18:14-19. Erratum in: JPEN J Parenter Enteral Nutr. 1994;18:197.
32. Lampe JW, Fredstrom SB, Slavin JL, et al. Sex differences in colonic function: a randomised trial. Gut. 1993;34:531-536.
33. Lampe JW, Wetsch RF, Thompson WO, et al. Gastrointestinal effects of sugarbeet fiber and wheat bran in healthy men. Eur J Clin Nutr. 1993;47:543-548.
34. van Munster IP, Tangerman A, Nagengast FM. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig Dis Sci. 1994;39:834-842.
35. Noakes M, Clifton PM, Nestel PJ, et al. Effect of high-amylose starch and oat bran on metabolic variables and bowel function in subjects with hypertriglyceridemia. Am J Clin Nutr. 1996;64:944-951.
36. Takahashi H, Yang SI, Hayashi C, et al. Effect of partially hydrolysed guar gum on fecal output in human volunteers. Nutr Res. 1993;13:649-657.
37. Bridges SR, Anderson JW, Deakins DA, et al. Oat bran increases serum acetate of hypercholesterolemic men. Am J Clin Nutr. 1992;56:455-459.
38. Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol. 1993;75:373-380.
39. Gibson GR, Wang X. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J Appl Bacteriol. 1994;77:412-420.
40. Jenkins DJ, Kendall CW, Hamidi M, et al. Effect of antibiotics as cholesterol-lowering agents. Metabolism. 2005;54:103-112.
41. Luo J, Rizkalla S, Alamowitch C, et al. Chronic consumption of short-chain fructooligosaccharides by healthy subjects decreased basal hepatic glucose production but had no effect on insulin-stimulated glucose metabolism. Am J Clin Nutr. 1996;63:939-945.
42. Thacker PA, Salamons MO, Aherne FX, et al. Influence of propionic acid on the cholesterol metabolism of pigs fed hypercholesterolemic diets. Can J Anim Sci. 1981;61:969-975.
43. Amaral L, Hoppel C, Stephen AM. Effect of propionate on lipid metabolism in healthy human subjects. Falk Symposium. 1993;73:E2.
44. Scheppach W, Fabian C, Ahrens F, et al. Effect of starch malabsorption on colonic function and metabolism in humans. Gastroenterology. 1988;95:1549-1555.
45. Holt PR, Atillasoy E, Lindenbaum J, et al. Effects of acarbose on fecal nutrients, colonic pH, and short-chain fatty acids and rectal proliferative indices. Metabolism. 1996;45:1179-1187.
46. Weaver GA, Tangel CT, Krause JA, et al. Acarbose enhances human colonic butyrate production. J Nutr. 1997;127:717-723.
47. Phillips J, Muir JG, Birkett A, et al. Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. Am J Clin Nutr. 1995;62:121-130.
48. Englyst HN, Hay S. Macfarlane GT. Polysaccharide breakdown by mixed populations of human fecal bacteria. FEMS Microbiol Ecol. 1987;95:163-171.
49. Vogt JA, Pencharz PB, Wolever TM. L-Rhamnose increases serum propionate in humans. Am J Clin Nutr. 2004;80:89-94.
50. Vogt JA, Ishii-Schrade KB, Pencharz PB, et al. L-Rhamnose increases serum propionate after long-term supplementation, but lactulose does not raise serum acetate. Am J Clin Nutr. 2004;80:1254-1261.
51. Macfarlane GT, Englyst HN. Starch utilization by the human large intestinal microflora. J Appl Bacteriol. 1986;60:195-201.
52. Cummings JH, Rombeau JL, Sakata T, eds. Physiological and Clinical Aspects of Short-chain Fatty Acids. Cambridge (England), New York, NY: Cambridge University Press; 1995.
53. McNeil NI, Cummings JH, James WP. Short chain fatty acid absorption by the human large intestine. Gut. 1978;19:819-822.
54. Ruppin H, Bar-Meir S, Soergel KH, et al. Absorption of short-chain fatty acids by the colon. Gastroenterology. 1980;78:1500-1507.
55. Roediger WE, Moore A. Effect of short-chain fatty acid on sodium absorption in isolated human colon perfused through the vascular bed. Dig Dis Sci. 1981;26:100-106.
56. Fleming SE, Choi SY, Fitch MD. Absorption of short-chain fatty acids from the rat cecum in vivo. J Nutr. 1991;121:1787-1797.
57. Bowling TE, Raimundo AH, Grimble GK, et al. Reversal by shortchain fatty acids of colonic fluid secretion induced by enteral feeding. Lancet. 1993;342:1266-1268.
58. Wolever TM, Josse RG, Leiter LA, et al. Time of day and glucose tolerance status affect serum short-chain fatty acid concentrations in humans. Metabolism. 1997;46:805-811.
59. Engelhardt WV. Absorption of short-chain fatty acids from the large intestine. In: Cummings JH, Rombeau JL, Sakata T, eds. Physiological and Clinical Aspects of Short-chain Fatty Acids. Cambridge (England), New York, NY: Cambridge University Press; 1995:149-170.
60. Peters SG, Pomare EW, Fisher CA. Portal and peripheral blood short chain fatty acid concentrations after caecal lactulose instillation at surgery. Gut. 1992;33:1249-1252.
61. Ardawi MS, Newsholme EA. Fuel utilization in colonocytes of the rat. Biochem J. 1985;231:713-719.
62. Roediger WE. The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In: Cummings JH, Rombeau JL, Sakata T, eds. Physiological and Clinical Aspects of Short-chain Fatty Acids. Cambridge (England), New York, NY: Cambridge University Press; 1995:337-351.
63. Butler RN, Stafford I, Triantafillos E, et al. Pyruvate sparing by butyrate and propionate in proliferating colonic epithelium. Comp Biochem Physiol B. 1990;97:333-337.
64. Jenkins DJ, Wolever TM, Jenkins A, et al. Specific types of colonic fermentation may raise low-density-lipoprotein-cholesterol concentrations. Am J Clin Nutr. 1991;54:141-147.
65. Vince A, Killingley M, Wrong OM. Effect of lactulose on ammonia production in a fecal incubation system. Gastroenterology. 1978;74:544-549.
66. Jackson AA. Aminoacids: essential and non-essential? Lancet. 1983;1:1034-1037.
67. Jenkins DJ, Wolever TM, Collier GR, et al. Metabolic effects of a low-glycemic-index diet. Am J Clin Nutr. 1987;46:968-975.
68. Wolever TM, Brighenti F, Royall D, et al. Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterol. 1989;84:1027-1033.
69. Royall D, Wolever TM, Jeejeebhoy KN. Clinical significance of colonic fermentation. Am J Gastroenterol. 1990;85:1307-1312.
70. Chen WJ, Anderson JW, Jennings D. Propionate may mediate the hypocholesterolemic effects of certain soluble plant fibers in cholesterol-fed rats. Proc Soc Exp Biol Med. 1984;175:215-218.
71. Bell LP, Hectorne K, Reynolds H, et al. Cholesterol-lowering effects of psyllium hydrophilic mucilloid. Adjunct therapy to a prudent diet for patients with mild to moderate hypercholesterolemia. JAMA. 1989;261:3419-3423.
72. Anderson JW, Zettwoch N, Feldman T, et al. Cholesterol-lowering effects of psyllium hydrophilic mucilloid for hypercholesterolemic men. Arch Intern Med. 1988;148:292-296.
73. Todesco T, Rao AV, Bosello O, et al. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am J Clin Nutr. 1991;54:860-865.
74. Venter CS, Vorster HH, Cummings JH. Effects of dietary propionate on carbohydrate and lipid metabolism in healthy volunteers. Am J Gastroenterol. 1990;85:549-553.
75. Wolever TM, Spadafora P, Eshuis H. Interaction between colonic acetate and propionate in humans. Am J Clin Nutr. 1991;53:681-687.
76. Hara H, Haga S, Kasai T, et al. Fermentation products of sugarbeet fiber by cecal bacteria lower plasma cholesterol concentration in rats. J Nutr. 1998;128:688-693.
77. Cheng HH, Lai MH. Fermentation of resistant rice starch produces propionate reducing serum and hepatic cholesterol in rats. J Nutr. 2000;130:1991-1995.
78. Wolever TM, Fernandes J, Rao AV. Serum acetate: propionate ratio is related to serum cholesterol in men but not women. J Nutr. 1996;126:2790-2797.
79. Baird GD, Lomax MA, Symonds HW, et al. Net hepatic and splanchnic metabolism of lactate, pyruvate and propionate in dairy cow in vivo in relation to lactation and nutrient supply. Biochem J. 1984;186:47-57.
80. Blaird JD, Cook DE, Lardy HA. Interaction of propionate and lactate in the perfused rat liver. Effects of glucagon and oleate. J Biol Chem. 1973;248:3608-3614.
81. Foley JE. Rationale and application of fatty acid oxidation inhibitors in treatment of diabetes mellitus. Diabetes Care. 1992;15:773-781.
82. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr. 2002;22:283-307. Epub 2002 April 4.
83. Bush RS, Milligan LP. Study of the mechanism of inhibition of ketogenesis by propionate in bovine liver. Can J Anim Sci. 1971;51:121-127.
84. Rodwell VW, Nordstrom JL, Mitschelen JJ. Regulation of HMG CoA reductase. Adv Lipid Res. 1976;14:l-74.
85. Yamashita K, Kawai K, Itakura M. Effects of fructo-oligosaccharides on blood glucose and serum lipids in diabetic subjects. Nutr Res. 1984;4:961-966.
86. Delzenne NM, Williams CM. Prebiotics and lipid metabolism. Curr Opin Lipidol. 2002;13:61-67.
87. Davidson MH, Maki KC, Synecki C, et al. Effects of dietary inulin on serum lipids in men and women with hypercholesterolemia. Nutr Res. 1998;18:503-517.
88. Wright RS, Anderson JW, Bridges SR. Propionate inhibits hepatocyte lipid synthesis. Proc Soc Exp Biol Med. 1990;195:26-29.
89. Nishina PM, Freedland RA. Effects of propionate on lipid biosynthesis in isolated rat hepatocytes. J Nutr. 1990;120:668-673.
90. Hara H, Haga S, Aoyama Y, et al. Short-chain fatty acids suppress cholesterol synthesis in rat liver and intestine. J Nutr. 1999;129:942-948.
91. Illman RJ, Topping DL. Effects of dietary oat bran on faecel steroid excretion, plasma volatile fatty acids and lipid synthesis in rats. Nutr Res. 1985;5:839-846.
92. Ahrens F, Hagemeister H, Pfeuffer M, et al. Effects of oral and intracecal pectin administration on blood lipids in minipigs. J Nutr. 1986;116:70-76.
93. Illman RJ, Topping DL, McIntosh GH, et al. Hypocholesterolaemic effects of dietary propionate: studies in whole animals and perfused rat liver. Ann Nutr Metab. 1988;32:95-107.
94. Dawson AM, Holdsworth CD, Webb J. Absorption of short chain fatty acids in man. Proc Soc Exp Biol Med. 1964;117:97-100.
95. Saunders D. Absorption of short chain fatty acids in human stomach and rectum. Nutr Res. 1991;11:841-847.
96. Dankert J, Zijlstra J, Wolthers B. Volatile fatty acids in human peripheral and portal blood: quantitative determination, vacuum distillation, and gas chromatography. Clin Chim Acta. 1981;110:301-307.
97. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology. 1982;83:424-429.
98. Fleming LL, Floch MH. Digestion and absorption of fiber carbohydrate in the colon. Am J Gastroenterol. 1986;81:507-511.
99. Bornet FR, Brouns F, Tashiro Y, et al. Nutritional aspects of short-chain fructooligosaccharides: natural occurrence, chemistry, physiology and health implications. Dig Liver Dis. 2002;34(Suppl 2):S111-S120.
100. Hague A, Elder DJ, Hicks DJ, et al. Apoptosis in colorectal tumour cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate. Int J Cancer. 1995;60:400-406.
101. Scheppach W, Bartram HP, Richter F. Role of short-chain fatty acids in the prevention of colorectal cancer. Eur J Cancer. 1995;31A:1077-1080.
102. Perrin P, Cassagnau E, Burg C, et al. An interleukin 2/sodium butyrate combination as immunotherapy for rat colon cancer peritoneal carcinomatosis. Gastroenterology. 1994;107:1697-1708.
103. Archer SY, Meng S, Shei A, et al. p21(WAF1) is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc Natl Acad Sci U S A. 1998;95:6791-6796.
104. Siavoshian S, Segain JP, Kornprobst M, et al. Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut. 2000;46:507-514.
105. Chai F, Evdokiou A, Young GP, et al. Involvement of p21(Waf1/Cip1) and its cleavage by DEVD-caspase during apoptosis of colorectal cancer cells induced by butyrate. Carcinogenesis. 2000;21:7-14.
106. Scheppach W, Weiler F. The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care. 2004;7:563-567.
107. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell. 1978;14:115-121.
108. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 1997;389:349-252.
109. Lupton JR. Microbial degradation products influence colon cancer risk: the butyrate controversy. J Nutr. 2004;134:479-482.
110. Young GP, Hu Y, Le Leu RK, et al. Dietary fiber and colorectal cancer: a model for environment-gene interactions. Mol Nutr Food Res. 2005;49:571-584.
111. Grubben MJ, van den Braak CC, Essenberg M, et al. Effect of resistant starch on potential biomarkers for colonic cancer risk in patients with colonic adenomas: a controlled trial. Dig Dis Sci. 2001;46:750-756.
112. Thornton JR. High colonic pH promotes colorectal cancer. Lancet. 1981;1:1081-1083.
113. Wargovich MJ, Eng VW, Newmark HL. Calcium inhibits the damaging and compensatory proliferative effects of fatty acids on mouse colon epithelium. Cancer Lett. 1984;23:253-258.
114. Roediger WE. The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet. 1980;2:712-715.
115. Harig JM, Soergel KH, Komorowski RA, et al. Treatment of diversion colitis with short-chain-fatty acid irrigation. N Engl J Med. 1989;320:23-28.
116. Guillemot F, Colombel JF, Neut C, et al. Treatment of diversion colitis by short-chain fatty acids. Prospective and double-blind study. Dis Colon Rectum. 1991;34:861-864.
117. Cummings JH. Short chain fatty acid enemas in the treatment of distal ulcerative colitis. Eur J Gastroenterol Hepatol. 1997;9:149-153.
118. Breuer RI, Buto SK, Christ ML, et al. Rectal irrigation with short-chain fatty acids for distal ulcerative colitis. Preliminary report. Dig Dis Sci. 1991;36:185-187.
119. Scheppach W, Sommer H, Kirchner T, et al. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology. 1992;103:51-56.
120. Breuer RI, Soergel KH, Lashner BA, et al. Short chain fatty acid rectal irrigation for left-sided ulcerative colitis: a randomized, placebo controlled trial. Gut. 1997;40:485-491.
121. Steinhart AH, Hiruki T, Brzezinski A, et al. Treatment of left-sided ulcerative colitis with butyrate enemas: a controlled trial. Aliment Pharmacol Ther. 1996;10:729-736.
122. Roediger WE. The starved colon-diminished mucosal nutrition, diminished absorption, and colitis. Dis Colon Rectum. 1990;33:858-862.
123. Scheppach W, Christl SU, Bartram HP, et al. Effects of short-chain fatty acids on the inflamed colonic mucosa. Scand J Gastroenterol Suppl. 1997;222:53-57.
124. Roediger WE, Duncan A, Kapaniris O, et al. Sulphide impairment of substrate oxidation in rat colonocytes: a biochemical basis for ulcerative colitis? Clin Sci (London). 1993;85:623-627.