Review article: Prebiotics in the gastrointestinal tract

Alimentary Pharmacology and Therapeutics

Volumn 24, Issue 5, 2006, Pages 701-714

  Macfarlane, S ^a   Macfarlane, G T ^a   Cummings, J H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

'SYNERGY'; AMOXICILLIN; ANTIBIOTIC AGENT; BETA DEFENSIN; CALCIUM; CYTOKINE; FRUCTOSE; FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; INTERLEUKIN 1ALPHA; INULIN; ISOMALTO OLIGOSACCHARIDE; ISPAGULA; LACTULOSE; LAXATIVE; METRONIDAZOLE; PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; PYRODEXTRIN; SHORT CHAIN FATTY ACID; SOYA OLIGOSACCHARIDE; SYNBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VANCOMYCIN; XYLO OLIGOSACCHARIDE;

ANTIBIOTIC ASSOCIATED DIARRHEA; BIFIDOBACTERIUM; BLOATING; CALCIUM ABSORPTION; CHEMICAL COMPOSITION; CLINICAL TRIAL; CONSTIPATION; COST BENEFIT ANALYSIS; CROHN DISEASE; DEFECATION HABIT; DIARRHEA; DIETARY FIBER; DIGESTIVE SYSTEM CANCER; ENTERITIS; EVIDENCE BASED MEDICINE; FERMENTATION TECHNIQUE; GASTROINTESTINAL DISEASE; HUMAN; ILEITIS; INTESTINE FUNCTION; IRRITABLE COLON; LACTOBACILLUS; META ANALYSIS; METEORISM; MUSCLE CRAMP; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SAFETY; SYSTEMATIC REVIEW; TRAVELLER DIARRHEA; ULCERATIVE COLITIS;

BONE AND BONES; CALCIUM; CONSTIPATION; DIARRHEA; DIETARY CARBOHYDRATES; DIETARY SUPPLEMENTS; FERMENTATION; GASTROINTESTINAL AGENTS; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; IRRITABLE BOWEL SYNDROME; LACTULOSE; OLIGOSACCHARIDES;

EID: 33747343668     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2006.03042.x     Document Type: Review

References (101)

1. Gibson GR, Roberfroid M. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995; 125: 1401-12.
2. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid M. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 2004; 17: 259-75.
3. Roberfroid M. Inulin-type Fructans. Functional Food Ingredients. Boca Raton, Florida: CRC Press, 2005.
4. Stephen AM, Cummings JH. Mechanism of action of dietary fibre in the human colon. Nature 1980; 284: 283-4.
5. Macfarlane GT, Cummings JH. The colonic flora, fermentation and large bowel digestive function. In: Phillips SF, Pemberton JH, Shorter RG, eds. The Large Intestine: Physiology, Pathophysiology and Disease. New York: Raven Press, 1991: 51-92.
6. Cummings J, Kong SC. Probiotics, prebiotics and antibiotics in inflammatory bowel disease. In: Chadwick D, Goode J, eds. Inflamm Bowel Dis. Chichester: John Wiley & Sons, 2004: 99-114.
7. Langlands SJ, Hopkins MJ, Coleman N, Cummings JH. Prebiotic carbohydrates modify the mucosa-associated microflora of the human large bowel. Gut 2004; 53: 1610-6.
8. Duncan SH, Scott KP, Ramsay AG, et al. Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl Environ Microbiol 2003; 69: 1136-42.
9. Macfarlane S, Macfarlane GT. Bacterial diversity in the large intestine. Adv Appl Microbiol 2004; 54: 261-89.
10. Cummings JH, Antoine J-M, Azpiroz F, et al. Gut health and immunity. Eur J Nutr 2004; 43: II/118-73.
11. Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 1991; 70: 443-59.
12. Gibson GR, McCartney AL, Rastall RA. Prebiotics and resistance to gastrointestinal infections. Br J Nutr 2005; 93: S31-4.
13. Bartosch S, Woodmansey EJ, Paterson JCM, McMurdo MET, Macfarlane GT. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis and oligofructose in elderly persons, determined by real-rime polymerase chain reaction and counting of viable bacteria. Clin Infect Dis 2005; 40: 28-37.
14. Macfarlane S, Cummings JH, Macfarlane GT. Bacterial colonisation of surfaces in the large intestine. In: Gibson GR, Roberfroid M, eds. Colonic Microflora, Nutrition and Health. London: Chapman & Hall, 1999: 71-87.
15. Macfarlane S, Hopkins MJ, Macfarlane GT. Bacterial growth and metabolism on surfaces in the large intestine. Microb Ecol Health Dis 2000; 2: 64-72.
16. Macfarlane S, Furrie E, Cummings JH, Macfarlane GT. Chemotaxonomic analysis of bacterial populations colonizing the rectal mucosa in patients with ulcerative colitis. Clin Infect Dis 2004; 38: 1690-9.
17. Lu L, Walker A. Pathologic and physiologic interactions of bacteria with the gastrointestinal epithelium. Am J Clin Nutr 2001; 73: 1124S-30S.
18. Furrie E, Macfarlane S, Kennedy A, et al. Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 2005; 54: 242-9.
19. Prindiville T, Cantrell M, Wilson K. Ribosomal DNA Sequence analysis of mucosa-associated bacteria in Crohn's disease. Inflamm Bowel Dis 2004; 10: 824-33.
20. Cummings JH, Macfarlane GT. Gastrointestinal effects of prebiotics. Br J Nutr 2002; 87: S145-151.
21. Rycroft CE, Jones MR, Gibson GR, Rastall RA. A comparative in vitro evaluation of the fermentation properties of probiotic oligosaccharides. J Appl Microbiol 2001; 91: 878-87.
22. Van Laere KMJ, Hartemink R, Bosveld M, Schols HA, Voragen AGJ. Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. J Agric Food Chem 2000; 48: 1644-52.
23. Ito M, Deguchi Y, Miyamori A, et al. Effects of administration of galactooligosaccharides on the human faecal microflora, stool weight and abdominal sensation. Microb Ecol Health Dis 1990; 3: 285-92.
24. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 1995; 108: 975-82.
25. Alles MS, Hautvast JGAJ, Nagengast FM, Hartemink R, Van Laere KMJ, Jansen JBMJ. Fate of fructo-oligosaccharides in the human intestine. Br J Nutr 1996; 76: 211-21.
26. Bouhnik Y, Flourié B, D'Agay-Abensour L, et al. Administration of transgalacto-oligosaccharides increases fecal bifidobacteria and modifies colonic fermentation metabolism in healthy humans. J Nutr 1997; 127: 444-8.
27. Castiglia-Delavaud C, Verdier E, Bessle JM, et al. Net energy value of non-starch polysaccharide isolates (sugarbeet fibre and commercial inulin) and their impact on nutrient digestive utilization in healthy human subjects. Br J Nutr 1998; 80: 343-52.
28. van Dokkum W, Wezendonk B, Srikumar TS, van den Heuvel EGHM. Effect of nondigestible oligosaccharides on large-bowel functions, blood lipid concentrations and glucose absorption in young healthy male subjects. Eur J Clin Nutr 1999; 53: 1-7.
29. Gostner A, Schäffer V, Theis S, et al. Effects of isomalt consumption on gastrointestinal and metabolic parameters in healthy volunteers. Br J Nutr 2005; 94: 575-81.
30. Cummings JH. The effect of dietary fiber on fecal weight and composition. In: Spiller GA, ed. CRC Handbook of Dietary Fiber in Human Nutrition, 3rd edn. Tampa, Florida: CRC Press LLC, 2001: 183-252.
31. Van Loo J. The specificity of the interaction with intestinal bacterial fermentation by prebiotics determines their physiological efficacy. Nutr Res Rev 2004; 17: 89-98.
32. Lewis HB. The value of inulin as a foodstuff. J Am Med Assoc 1912; LVIII: 1176-7.
33. Hidaka H, Mirayama M. Useful characteristics and commercial applications of fructo-oligosaccharides. Biochem Soc Trans 1991; 19: 561-5.
34. Kleessen B, Sykura B, Zunft H-J, Blaut M. Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr 1997; 65: 1397-402.
35. Teuri U, Korpel R. Galacto-oligosaccharides relieve constipation in elderly people. Ann Nutr Metab 1998; 42: 319-27.
36. Den Hond E, Geypens B, Ghoos Y. Effect of high performance chicory inulin on constipation. Nutr Res 2000; 20: 731-6.
37. Chen H-L, Lu Y-H, Lin J-J, Ko L-Y. Effects of fructooligosaccharide on bowel function and indicators of nutritional status in constipated elderly men. Nutr Res 2000; 20: 1725-33.
38. Chen H-L, Lu Y-H, Lin J-J, Ko L-Y. Effects of isomalto-oligosaccharides on bowel functions and indicators of nutritional status in constipated elderly men. J Am Coll Nutr 2001; 20: 44-9.
39. Bouhnik Y, Neut C, Raskine L, et al. Prospective, randomized, parallel-group trial to evaluate the effects of lactulose and polyethylene glycol-4000 on colonic flora in chronic idiopathic constipation. Aliment Pharmacol Ther 2004; 19: 889-99.
40. Cummings JH, Christie S, Cole TJ. A study of fructo oligosaccharides in the prevention of travellers' diarrhoea. Aliment Pharmacol Ther 2001; 15: 1139-45.
41. Azpiroz F. Intestinal perception: mechanisms and assessment. Br J Nutr 2005; 93: S7-S12.
42. Smith AP. The concept of well-being: relevance to nutrition research. Br J Nutr 2005; 93: S1-S5.
43. Hasler WL. Fecal flora in irritable bowel syndrome: characterization using molecular methods. Gastroenterology 2005; 129: 759-61.
44. King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998; 352: 1187-9.
45. Dear KLE, Elia M, Hunter JO. Do interventions which reduce colonic bacterial fermentation improve symptoms of irritable bowel syndrome? Dig Dis Sci 2005; 50: 758-66.
46. Serra J, Azpiroz A, Malagelada J-R. Impaired transit and tolerance of intestinal gas in the irritable bowel syndrome. Gut 2001; 48: 14-9.
47. Malinen E, Rinttila T, Kajander K, et al. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 2005; 100: 373-82.
48. Macfarlane GT, Gibson GR. Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In: Mackie RI, White BA, eds. Ecology and Physiology of Gastrointestinal Microbes, Vol. 1: Gastrointestinal Fermentations and Ecosystems. New York: Chapman & Hall, 1996: 269-318.
49. Stone-Dorshow T, Levitt MD. Gaseous response to ingestion of a poorly absorbed fructo-oligosaccharide sweetener. Am J Clin Nutr 1987; 46: 61-5.
50. Hunter JO, Tuffnell Q, Lee AJ. Controlled trial of oligofructose in the management of irritable bowel syndrome. J Nutr 1999; 129: 1451S-3S.
51. Hopkins MJ, Macfarlane GT. Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro. Appl Environ Microbiol 2003; 69: 1920-7.
52. Lewis S, Burmeister S, Cohen S, Brazier J, Awasthi A. Failure of dietary oligofructose to prevent antibiotic-associated diarrhoea. Aliment Pharmacol Ther 2005; 21: 469-77.
53. Lewis S, Burmeister S, Brazier J. Effect of the prebiotic oligofructose on relapse of Clostridium difficile-associated diarrhea: a randomized, controlled study. Clin Gastroenterol Hepatol 2005; 3: 442-8.
54. Brunser O, Gotteland M, Cruchet S, Garrido D, Figueroa G, Steenhout P. Effect of an infant formula with prebiotics on the intestinal microbiota after an antibiotic treatment. J Pediatr Gastroenterol Nutr 2005; 40: 691-2.
55. Rayes N, Seehofer D, Theruvath T, et al. Supply of pre- and probiotics reduces bacterial infection rates after liver transplantation - a randomized, double-blind trial. Am J Transplant 2005; 5: 125-30.
56. Anderson ADG, McNaught CE, Jain PK, MacFie J. Randomised clinical trial of synbiotic therapy in elective surgical patients. Gut 2004; 53: 241-5.
57. Hart AL, Kamm MA. Use of probiotics in the treatment of inflammatory bowel disease. J Clin Gastroenterol 2003; 36: 111-9.
58. Kruis W, Fric P, Paokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004; 53: 1617-23.
59. Cherbut C, Michel C, Lecannu G. The prebiotic characteristics of fructooligosaccharides are necessary for reduction of TNBS-induced colitis in rats. J Nutr 2003; 133: 21-7.
60. Camuesco D, Peran L, Comalada M, et al. Preventative effects of lactulose in the trinitrobenzenesulphonic acid model of rat colitis. Inflamm Bowel Dis 2005; 11: 265-71.
61. Videla S, Vilaseca J, Antolin M, et al. Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am J Gastroenterol 2001; 96: 1486-93.
62. Moreau NM, Martin LJ, Toquet CS, et al. Restoration of the integrity of rat caecocolonic mucosa by resistant starch, but not by fructo-oligosaccharides, in dextran sulfate sodium-induced experimental colitis. Br J Nutr 2003; 90: 75-85.
63. Rumi G, Tsubouchi R, Okayama M, Kato S, Mozsik G, Takeuchi K. Protective effect of lactulose on dextran sulfate sodium-induced colonic inflammation in rats. Dig Dis Sci 2004; 49: 1466-72.
64. Hoentjen F, Welling GW, Harmsen HJM, et al. Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 2005; 11: 977-85.
65. Hanai H, Kanauchi O, Mitsuyama K, et al. Germinated barley foodstuff prolongs remission in patients with ulcerative colitis. Int J Mol Med 2004; 13: 643-7.
66. Lindsay JO, Whelan K, Stagg AJ, et al. Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn's disease. Gut 2006; 55: 348-55.
67. Welters CFM, Heineman E, Thunnissen BJM, van den Bogaard AEJM, Soeters PB, Baeten CGMI. Effect of dietary inulin supplementation on inflammation of pouch mucosa in patients with an ileal pouch-anal anastomosis. Dis Colon Rectum 2002; 45: 621-7.
68. Zitterman A, Bock P, Drummer C, Scheld K, Heer M, Stehle P. Lactose does not enhance calcium bioavailability in lactose-tolerant, healthy adults. Am J Clin Nutr 2000; 71: 931-6.
69. Ohta A, Ohtsuki M, Baba S, Adachi T, Sakata T, Sakaguchi E. Calcium and magnesium absorption from the colon and rectum are increased in rats fed fructooligosaccharides. J Nutr 1995; 125: 2417-24.
70. Ohta A, Ohtsuki M, Baba S, Takizawa T, Adachi T, Kimura S. Effects of fructooligosaccharides on the absorption of iron, calcium and magnesium in irondeficient anemic rats. J Nutr Sci Vitaminol (Tokyo) 1995; 41: 281-91.
71. Motohashi T, Sano T, Ohta A, Yamada S. True calcium absorption in the intestine is enhanced by fructooligosaccharides feeding in rats. J Nutr 1998; 128: 1815-8.
72. Chonan O, Watanuki M. Effect of galactooligosaccharides on calcium-absorption in rats. J Nutr Sci Vitaminol (Tokyo) 1995; 41: 95-104.
73. Younes H, Coudray C, Bellanger J, Demingné C, Rayssiguier Y, Rémésy C. Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br J Nutr 2001; 86: 479-85.
74. Delzenne N, Aertssens J, Verplaetse H, Roccaro M, Roberfroid M. Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci 1995; 57: 1579-87.
75. Chonan O, Watanuki M. The effect of 6′galactooligosaccharides on bone mineralization of rats adapted to different levels of dietary calcium. Int J Vitam Nutr Res 1996; 66: 244-9.
76. Ohta A, Ohtsuki M, Uehara M, et al. Dietary fructooligosaccharides prevent postgastrectomy anemia and osteopenia in rats. J Nutr 1998; 128: 485-90.
77. Scholz-Ahrens KE, Acil Y, Schrezenmeir J. Effect of oligofructose or dietary calcium on repeated calcium and phosphorus balances, bone mineralization and trabecular structure in ovariectomized rats. Br J Nutr 2002; 88: 365-77.
78. Civitelli R, Avioli LV. Calcium, phosphate, and magnesium absorption. In: Johnson LR, Alpers DH, Christensen J, Jacobson ED, Walsh JH, eds. Physiology of the Gastrointestinal Tract, Vol. 2, 3rd edn. New York: Raven Press, 1994: 2173-81.
79. Ohta A, Motohashi Y, Sakai K, Hirayama M, Adachi T, Sakuma K. Dietary fructooligosaccharides increase calcium absorption and levels of mucosal calbindin-D9k in the large intestine of gastrectomized rats. Scand J Gastroenterol 1998; 33: 1062-8.
80. Ohta A, Motohashi Y, Ohtsuki M, Hirayama M, Adachi T, Sakuma K. Dietary fructooligosaccharides change the concentration of calbindin-D9k differently in the mucosa of the small and large intestine of rats. J Nutr 1998; 128: 934-9.
81. Suzuki T, Hara H. Various non-digestible saccharides increase intracellular calcium ion concentration in rat small-intestinal enterocytes. Br J Nutr 2004; 92: 751-5.
82. Chonan O, Matsumoto K, Watanuki M. Effect of galactooligosaccharides on calcium-absorption and preventing bone loss in ovariectomized rats. Biosci Biotechnol Biochemis 1995; 59: 236-9.
83. Remesy C, Levrat MA, Gamet L, Demigne C. Cecal fermentations in rats fed oligosaccharides (inulin) are modulated by dietary calcium level. Am J Physiol 1993; 264: G855-62.
84. Scholz-Ahrens KE, Schrezenmeir J. Inulin, oligofructose and mineral metabolism - experimental data and mechanism. Br J Nutr 2002; 87: S179-86.
85. Chonan O, Takahashi R, Watanuki M. Role of activity of gastrointestinal microflora in absorption of calcium and magnesium in rats fed beta 1-4 linked galactooligosaccharides. Biosci Biotechnol Biochem 2001; 65: 1872-5.
86. Abrams SA, Griffin IJ, Hawthorne KM, et al. A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 2005; 82: 471-6.
87. van den Heuvel EGHM, Schaafsma G, Muys T, van Dokkum W. Nondigestible oligosaccharides do not interfere with calcium an nonheme-iron absorption in young, healthy men. Am J Clin Nutr 1998; 67: 445-51.
88. van den Heuvel EGHM, Muys T, van Dokkum M, Schaafsma G. Oligofructose stimulates calcium absorption in adolescents. Am J Clin Nutr 1999; 69: 544-8.
89. Griffin IJ, Davila PM, Abrams SA. Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br J Nutr 2002; 87: S187-91.
90. Coudray C, Bellanger J, Castiglia-Delavaud C, Remesy C, Vermorel M, Rayssignuieer Y. Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men. Eur J Clin Nutr 1997; 51: 365-80.
91. Ellegard L, Andersson H, Bosaeus I. Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increases energy excretion in ileostomy subjects. Eur J Clin Nutr 1997; 51: 1-5.
92. Ducros V, Arnaud J, Tahiri M, et al. Influence of short-chain fructo-oligosaccharides (sc-FOS) on absorption of Cu, Zn, and Se in healthy post-menopausal women. J Am Coll Nutr 2005; 24: 30-7.
93. Pool-Zobel BL. Inulin-type fructans and reduction in colon cancer risk: a review of experimental and human data. Br J Nutr 2005; 93: S73-90.
94. Fanaro S, Boehm G, Garssen J, et al. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr 2005; 94: 22-6.
95. Butel M-J, Waligora-Dupriet A-J, Szylit O. Oligofructose and experimental model of neonatal necrotising enterocolitis. Br J Nutr 2002; 87: S213-9.
96. Williams CM, Jackson KG. Inulin and oligofructose: effects on lipid metabolism from human studies. Br J Nutr 2002; 87: S261-4.
97. Beylot M. Effects of inulin-type fructans on lipid metabolism in man and in animal models. Br J Nutr 2005; 93: S163-8.
98. Flickinger EA, Fahey GC Jr. Pet food and feed applications of inulin, oligofructose and other oligosaccharides. Br J Nutr 2002; 87: S297-300.
99. Tahiri M, Tressol JC, Arnaud J, et al. Effect of short-chain fructooligosaccharides on intestinal calcium absorption and calcium status in postmenopausal women: a stable-isotope study. Am J Clin Nutr 2003; 77: 449-57.
100. van den Heuvel EGHM, Schoterman MHC, Muijs T. Transgalactooligosaccharides stimulate calcium absorption in postmenopausal women. J Nutr 2000; 130: 2938-42.
101. López-Huertas E, Teucher B, Boza JJ, et al. Absorption of calcium from milks enriched with fructo-oligosaccharides, caseinophosphopepties, tricalcium phosphate, and milk solids. Am J Clin Nutr 2006; 83: 310-6.