Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics

Beneficial Microbes

Volumn 1, Issue 4, 2010, Pages 423-431

  Bird, A R ^a   Conlon, M A ^a   Christophersen, C T ^a   Topping, D L ^a  

^a CSIRO   (Australia)

Author keywords

Colon; Fibre; Human health; Microbiota; Short chain fatty acids

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT; STARCH;

BACTERIUM; DIGESTION; FERMENTATION; HUMAN; LARGE INTESTINE; METABOLISM; MICROBIOLOGY; REVIEW;

BACTERIA; DIGESTION; FERMENTATION; HUMANS; INTESTINE, LARGE; PREBIOTICS; PROBIOTICS; STARCH;

EID: 84856372683     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2010.0041     Document Type: Article

References (89)

1. Abell, G.C.J., Cooke, C.M., Bennett, C.N., Conlon, M.A. and McOrist, A.L., 2008. Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS Microbiology Ecology 66: 505-515.
2. Ahmed R., Segal, I. and Hassan, H., 2000. Fermentation of dietary starch in humans. American Journal of Gastroenterology 95: 1017-1020.
3. Ardawi, M.S. and Newsholme, E.A., 1985. Fuel utilization in colonocytes of the rat. Biochemical Journal 231: 713-719.
4. Arslanoglou, S., Moror, G.E., Schmitt, J., Tandori, L., Rizzardi, S. and Boehm, G., 2008. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. Journal of Nutrition 138: 1091-1095.
5. Asp, N-G., 1992. Resistant starch. European Journal of Clinical Nutrition 46 Suppl. 2: S1.
6. Baghurst, P.A., Baghurst, K.I. and Record, S.J., 1996. Dietary fibre, non-starch polysaccharides and resistant starch - a review. Food Australia 48 Suppl.: S3-S35.
7. Bajka, B.H., Clarke, J.M., Cobiac, L. and Topping, D.L., 2008. Butyrylated starch protects colonocyte DNA against dietary proteininduced DNA damage in rats. Carcinogenesis 29: 2169-2174.
8. Bergman, E.N., 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70: 567-590.
9. Bingham, S.A., Day, N.E., Luben, R., Ferrari, P., Slimani, N., Norat, T., Clavel-Chapelon, F., Kesse, E., Nieters, A., Boeing, H., Tjonneland, A., Overvad, K., Martinez, C., Dorronsoro, M., Gonzalez, C.A., Key, T.J., Trichopoulou, A., Naska, A., Vineis, P., Tumino, R., Krogh, V., Bueno-de-Mesquita, H.B., Peeters, P.H., Berglund, G., Hallmans, G., Lund, E., Skeie, G., Kaaks, R. and Riboli, E., 2003. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. The Lancet 361: 1496-1501.
10. Bird, A.R., Brown, I.L. and Topping, D.L., 2000. Starches, resistant starches, the gut microflora and human health. Current Issues in Intestinal Microbiology 1: 25-37.
11. Bird, A.R., Vuaran, M., Crittenden, R., Hayakawa, T., Playne, M.J., Brown, I.L. and Topping, D.L., 2009. Comparative effects of a high amylose starch and a fructo-oliogsaccharide on faecal bifidobacteria numbers and short chain fatty acids in pigs fed Bifidobacterium animalis. Digestive Diseases and Sciences 54: 947-954.
12. Bloemen, J.G., Schreinemacher, M.H., De Bruine, A.P., Buurman, W.A., Bouvy, N.D. and De Jong, C.H., 2010. Butyrate enemas improve intestinal anastomotic strength in a rat model. Diseases of the Colon and Rectum 53: 1069-1075.
13. Brigidi, P., Swennen, E., Vitali, B., Rossi, M. and Matteuzzi, D., 2003. PCR detection of Bifidobacterium strains and Streptococcus thermophilus in feces of human subjects after oral bacteriotherapy and yogurt consumption. International Journal of Food Microbiology 81: 203-209.
14. Brinkworth, G.D., Noakes, M., Clifton, P.M. and Bird, A.R., 2009. Comparative effects of very low-carbohydrate, high-fat and highcarbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. British Journal of Nutrition 101: 1493-1502.
15. Brouns, F., Kettlitz, B. and Arrigoni, E., 2002. Resistant starch and the 'butyrate revolution'. Trends in Food Science and Technolology 13: 251-261.
16. Brown, I., Warhurst, M., Arcot, J., Playne, M., Illman, R.J. and Topping, D.L., 1997. Faecal numbers of bifidobacteria are higher in pigs fed Bifidobacterium longum with a high amylose cornstarch than with a low amylose cornstarch. Journal of Nutrition 127: 1822-1827.
17. Burkitt, D.P., 1970. Relationship as a clue to causation. The Lancet 296: 1237-1240.
18. Butler, R.N., Topping, D.L., Illman, R.J., Goland, G., Lawson, M.J. and Roberts-Thomson, I., 1990. Effects of starvation and refeeding on volatile fatty acid distribution in the large bowel of the rat. Nutrition Research 10: 91-98.
19. Cassidy, A., Bingham, S.A. and Cummings, J.H., 1994. Starch intake and colorectal-cancer risk-an international comparison. British Journal of Cancer 69: 937-942.
20. Cats, A., De Vries, E.G., Mulder, N.H. and Kleibeuker, J.H., 1996. Regional differences of physiological functions and cancer susceptibility in the human large intestine. International Journal of Oncology 9: 1055-1069.
21. Cherbut, C., Ferrier, L. and Roze, C., 1998. Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. American Journal of Physiology 275: G1415-G1422.
22. Clarke, J.M., Bird, A.R., Topping, D.L. and Cobiac, L., 2007. Excretion of starch and esterified short chain fatty acids by ileostomists after the ingestion of acylated starches. American Journal of Clinical Nutrition 86: 1146-1151.
23. Clarke, J.M., Topping, D.L., Bird, A.R., Young, G.P. and Cobiac, L., 2008. Effects of high-amylose maize starch and butyrylated highamylose maize starch on azoxymethane-induced intestinal cancer in rats. Carcinogenesis 29: 2190-2194.
24. Coppa, G.V., Zampini, L., Galeazzi, T. and Gabrielli, O., 2006. Prebiotics in human milk: a review. Digestive and Liver Diseases 38: S291-S294.
25. Crew, T.E., Elder, D.J.E. and Paraskeva, C., 2000. A cyclooxygenase-2 (COX-2) selective non-steroidal anti-inflammatory drug enhances the growth inhibitory effect of butyrate in colorectal carcinoma cells expressing COX-2 protein:regulation of COX-2 by butyrate. Carcinogenesis 21: 69-77.
26. Cummings, J.H. and Englyst, H.N., 1987. Fermentation in the human large intestine and the available substrates. American Journal of Clinical Nutrition 45 Suppl. 5: 1243-1255.
27. Cummings, J.H. and Macfarlane, G.T., 1991. The control and consequences of bacterial fermentation in the human colon. Journal of Applied Bacteriology 70: 443-459.
28. Davie, J.R., 2003. Inhibition of histone deacetylase activity by butyrate. Journal of Nutrition 133: 2485S-2493S.
29. Delcour, J.A., Courtin, C.M., Fierens, E., Verbeke, K. and Brockaert, W.F., 2010. Wheat bran derived arabinoxylan-oligosaccharides: a novel prebiotic concept? In: Van der Kamp, J.W., Jones, J., McCleary, B. and Topping, D. (eds.) Dietary fibre: new frontiers for food and health, Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 311-321.
30. Dronmaraju, S.S., Coxhead, J.M., Kelly, S.B., Burn, J.B. and Mathers, J.C., 2009. Cell kinetics and gene expression changes in colorectal cancer patients given resistant starch: a randomised controlled trial. Gut 58: 413-420.
31. Duncan, S.H., Belenguer, A., Holtrop, G., Johnstone, A.M., Flint, H.J. and Lobley, G.E., 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Applied and Environmental Microbiology 73: 1073-1078.
32. Edwards, C.A. and Parrett, A.M., 2002. Intestinal flora during the first few months of life: new perspectives. British Journal of Nutrition 88: S11-S18.
33. Finnie, I.A., Dwarakanath, A.D., Taylor, B.A. and Rhodes, J.M., 1995. Colonic mucin synthesis is increased by sodium-butyrate. Gut 36: 93-99.
34. Fujiwara, S., Seto, Y., Kimura, A. and Hashiba, H., 2001. Intestinal transit of an orally administered streptomycin-rifampicin-resistant variant of Bifidobacterium longum SBT2928: its long-term survival and effect on the intestinal microflora and metabolism. Journal of Applied Microbiology 90: 43-52.
35. Fung, K.Y.C., Lewanowitsch, T., Henderson, S.T., Priebe, I., Hoffman P., McColl, S.R., Lockett, T., Head, R. and Cosgrove, L.J., 2009. Proteomic analysis of butyrate effects and loss of butyrate sensitivity in HT29 colorectal cancer cells. Journal of Proteome Research 8: 1220-1227.
36. Gibson, G.R., Probert, H.M., Loo, J.V., Rastall, R.A. and Roberfroid, M.B., 2004. Dietary modulation of the human colonic microbioita: updating the concept of prebiotics. Nutrition Research Reviews 17: 259-275.
37. Gork, A.S., Usui, N., Ceriati, E., Drongowski, R.A., Epstein, M.D., Coran, A.G. and Harmon, C.M., 1999. The effect of mucin on bacterial translocation in I-407 fetal and Caco-2 adult enterocyte cultured cell lines. Pediatric Surgery International 15: 155-159.
38. Harmsen, H.J.M., Wildeboer-Veloo, A.C.M., Raangs, G.C., Wagendorp, A.A., Nicolette, N., Bindels, J.G. and Welling, G.W., 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition 30: 61-67.
39. Hill, M.J., 1995. Bacterial fermentation of complex carbohydrate in the human colon. European Journal of Cancer Prevention 4: 353-358.
40. Illman, R.J., Topping, D.L. and Trimble, R.P., 1986. Effects of food restriction and starvation-refeeding on volatile fatty acid concentrations in the rat. Journal of Nutrition 116: 1694-1700.
41. Joint FAO/WHO Working Group on drafting guidelines for the evaluation of probiotics in food, 2002. Guidelines for the evaluation of probiotics in food, London, UK. Available at: http://www.who. int/foodsafety/fs_management/en/probiotic_guidelines.pdf.
42. Kaufmann, S.H.E., 2008. Elie Metchnikoff's and Paul Ehrlich's impact on infection biology. Microbes and Infection 10: 1417-1419.
43. Kelly, D., King, T. and Aminov, R., 2007. Importance of microbial colonization of the gut in early life to the development of immunity. Mutation Research 622: 58-69.
44. Kishida, T., Nakai, Y. and Ebihara, K., 2001. Hydroxypropyl-distarch phosphate from Tapioca starch reduces zinc and iron absorption, but not calcium and magnesium absorption, in rats. Journal of Nutrition 131: 294-300.
45. Larsen, N., Vogensen, F.K, Van den Berg, F.W.J., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., Al-Soud, W.A., Sorensen, S.J., Hansen, L.H. and Jakobsen, M., 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PloS One 5: e9085.
46. Lebouvier, T., Chaumette, T., Paillusson, S., Duyckaerts, C., Bruley des Varannes, S., Neunlist, M. and Derkinderen, P., 2009. The second brain and Parkinson's disease. European Journal of Neuroscience 30: 735-741.
47. Ley, R.E., Turnbaugh, P.J., Klein, S. and Gordon, J.I., 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444: 1027-1031.
48. Lopez de Silanes, I., Olmo, N., Turnay, J., Gonzalaez de Buitrago, G., Perez-Ramos, P., Guzman-Aranguez, A., Garcia-Diez, M., Lecona, E., Gorospe, M. and Lizarbe, M.A., 2004. Acquisition of resistance to butyrate enhances survival after stress and induces malignancy of human colon carcinoma cells. Cancer Research 64: 4593-4600.
49. Macfarlane, G.T. and McBain, A.J., 1999. The human colonic microbiota. In: Gibson, G.R. and Roberfroid, M.B. (eds.) Colonic microbiota, nutrition and health. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp. 1-25.
50. Mariadason, J.M., Velcich, A., Wilson, A.J., Augenlicht, L.H. and Gibson, P.R., 2001. Resistance to butyrate-induced cell differentiation and apoptosis during spontaneous Caco-2 cell differentiation. Gastroenterology 120: 889-899.
51. Mascie-Taylor, C.G. and Karim, E., 2003. The burden of chronic disease. Science 302: 1921-1922.
52. Mattila-Sandholm, T., Blum, S., Collins, J.K., Crittenden, R., De Vos, W., Dunne, C., Fondén, R., Grenov, B., Isolauri, E., Kiely, B., Marteau, P., Morelli, L., Ouwehand, A., Reniero, R., Saarela, M., Salminen, S., Saxelin, M., Schiffrin, E., Shanahan, F., Vaughan, E. and Von Wright, A., 1999. Probiotics: towards demonstrating efficacy. Trends in Food Science and Technology 10: 393-399.
53. Michel, C., Kravtchenko, T.P., David, A., Gueaneau, S., Kozlowski, F. and Cherbut, C., 1998. In vitro prebiotic effects of Acacia gums onto the human intestinal microbiota depends on both botanical origin and environmental pH. Anaerobe 4: 257-266.
54. Morita, T., Kasoka, S., Kiriyama, S., Brown, I.L. and Topping, D.L., 2005. Comaparative effects of acetylated and unmodified high amylsomaize starch in rats. Starch 57: 246-253.
55. Moro, G., Minoli, I., Mosca, M., Fanaro, S., Jelinek, J., Stahl, B. and Boehm, G., 2002. Dosage-related bifidogenic effects of galacto-and fructooligo-saccharides in formula-fed term infants. Journal of Pediatric Gastroenterology and Nutrition 34: 291-295.
56. Ng, S.C., Hart, A.L., Kamm, M.A., Stagg, A.J. and Knight, S.C., 2009. Mechanisms of action of probiotics. Recent Advances in Inflammatory Bowel Diseases 15: 300-310.
57. Petrovsky, N., 2010. Immunomodulation with microbial vaccines to prevent type 1 diabetes mellitus. Nature Reviews Endocrinolology 6: 131-138.
58. Ramakrishna, B.S., Venkataraman, S., Srinivasan, S., Dash, P., Young, G.P. and Binder, H.J., 2000. Amylase-resistant starch plus oral rehydration solution for cholera. New England Journal of Medicine 342: 308-313.
59. Roediger, W.E.W., 1989. Short chain fatty acids as metabolic regulators of ion absorption in the colon. Acta Veterinaria Scandinavica 86 Suppl.: 116-125.
60. Roediger, W.E.W., 1995. The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In: Cummings, J.H., Rombeau, J.L. and Sakata, T. (eds.) Physiological and clinical aspects of short-chain fatty acids, Cambridge University Press, Cambridge, UK, pp. 337-352.
61. Saavedra, J.M., 2007. Use of probiotics in pediatrics: rationale, mechanisms of action, and practical aspects. Nutrition in Clinical Practice 22: 351-65.
62. Santosa, S., Farnworth, E. and Jones, P. J., 2006. Probiotics and their potential health claims. Nutrition Reviews 64: 265-74.
63. Satokari, R.M., Vaughan, E.E., Akkermans, A.D.L., Saarela, M. and De Vos, W.M., 2001. Polymerase chain reaction and denaturing gradient gel electrophoresis monitoring of faecal Bifidobacterium populations in a prebiotic and probiotic feeding trial. Systematic and Applied Microbiology 24: 227-231.
64. Sazawal, S., Hiremath, G., Dhingra, U., Malik, P., Deb, S. and Black, R.E., 2006. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. The Lancet Infectious Diseases 6: 374-382.
65. Schatzkin, A., Mouw, T., Park, Y., Subar, A.F., Kipnis, V., Hollenbeck, A., Leitzmann, M.F. and Thompson, F.E., 2007. Dietary fiber and whole-grain consumption in relation to colorectal cancer in the NIH-AARP Diet and Health Study. American Journal of Clinical Nutrition 85: 1353-1360.
66. Segal, I., 2002. Physiological small bowel malabsorption of carbohydrates protects against large bowel diseases in Africans. Journal of Gastroentrology and Hepatology 17: 249-252.
67. Segal, I., Hassan, H., Walker, A.R.P., Becker, P. and Braganza, J., 1995. Faecal short chain fatty acids in South African urban Africans and whites. Diseases of the Colon and Rectum 38: 732-734.
68. Serpa, J., Caiado, F., Carvalho, T., Torre, C., Goncalves, L.G., Casalou, C., Lamosa, P., Rodrigues, M., Zhu, Z., Lam, E.W.F. and Dias, S., 2010. Butyrate rich colonic microenvironment is a relevant selection factor for metabolically adapted tumour cells. Journal of Biological Chemistry, in press. DOI: 10.1074/jbc. M110.156026
69. Sghir, A., Gramet, G., Suau, A., Rochet, V., Pochart, P. and Dore, J., 2000. Quantification of bacterial groups within the human faecal flora by oligonucleotide probe hybridization. Applied and Environmental Microbiology 66: 2263-2266.
70. Shimakawa, Y., Matsubara, S., Yuki, N., Ikeda, M. and Ishikawa, F., 2003. Evaluation of Bifidobacterium breve strain Yakult-fermented soymilk as a probiotic food. Interantional Journal of Food Microbiology 81: 131-136.
71. Smirnov, A., Perez, R., Amit-Romach, E., Sklan, D. and Uni, Z., 2005. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. Journal of Nutrition 135: 187-192.
72. Soret, R., Chevalier, J., De Coppet, P., Poupeau, G., Derkinderen, P., Segain, J.P. and Neunlist, M., 2009. Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats. Gastroenterology 1381: 772-782.
73. Strober, W., Fuss, I. and Mannon, P., 2007. The fundamental basis of inflammatory bowel disease. Journal of Clinical Investigation 117: 514-521.
74. Sullivan, A. and Nord, C.E., 2005. Probiotics and gastrointestinal diseases. Journal of Internal Medicine 257: 78-92.
75. Toden, S., Bird, A.R., Topping, D.L. and Conlon, M.A., 2006. Resistant starch abolishes increased colonic DNA damage induced by high dietary cooked red meat or casein in rats. Cancer Biology and Therapy 5: 267-272.
76. Toden, S., Bird, A.R., Topping, D.L. and Conlon, M.A., 2007. Dosedependent reduction of dietary protein-induced colonocyte DNA damage by resistant starch in rats correlates more highly with caecal butyrate than with other short chain fatty acids. Cancer Biology and Therapy 6: 253-258.
77. Topping, D.L. and Clifton, P., 2001. Short chain fatty acids and human colonic function - roles of resistant starch and non starch polysaccharides. Physiological Reviews 81: 1031-1064.
78. Topping, D.L., Bird, A.R. and Young, G.P., 2009. Effect of aspirin or resistant starch on colorectal neoplasia in the Lynch syndrome. New England Journal of Medicine 360: 1462.
79. Topping, D.L., Fukushima, M. and Bird, A.R., 2003. Resistant starch as a prebiotic and synbiotic: state of the art. Proceedings of the Nutrition Society 62: 171-176.
80. Topping, D.L., Segal, I., Regina, A., Conlon, M.A., Bajka, B.H., Toden, S., Clarke, J.M., Morell, M.K. and Bird, A.R., 2010. Resistant starch and human health. In: Van der Kamp, J.W., Jones, J., McCleary, B. and Topping, D. (eds.) Dietary fibre: new frontiers for food and health, Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 311-321.
81. Roediger, W.E.W., 1995. The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In: Cummings, J.H., Rombeau, J.L. and Sakata, T. (eds.) Physiological and clinical aspects of short-chain fatty acids, Cambridge University Press, Cambridge, UK, pp. 337-352.
82. Vanhoutvin, S.A.L.W., Troost, F.J., Kilkens, T.O.C., Lindsey, P.J., Hamer, H.M., Jonkers, D.M.A.E., Venema, K. and Brummer, R-J.M., 2009. The effects of butyrate enemas on visceral perception in healthy volunteers. Neurogastroenterology and Motility 21: 952-952.
83. Van Munster, I.P., Tangerman, A. and Nagengast, F.M., 1994. Effect of resistant starch on colonic fermentation, bile acid metabolism and mucosal proliferation. Digestive Diseases and Sciences 39: 834-842.
84. Von Wright, A., Vilpponen-Salmela, T., Llopis, M.P., Collins, K., Kiely, B., Shanahan, F. and Dunne, C., 2002. The survival and colonic adhesion of Bifidobacterium infantis in patients with ulcerative colitis. International Dairy Journal 12: 197-200.
85. Walker, A.R. and Walker, B.F., 1985. Bowel behaviour in South African young black and white children. Archives of Disease in Childhood 60: 967-970.
86. Walker, A.R., Walker, B.F. and Segal, I., 1979. Faecal pH value and its modification by dietary means in South African black and white schoolchildren. South African Medical Journal 55: 495-498.
87. Williams, E.A., Coxhead, J.M. and Mathers, J.C., 2003. Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proceedings of the Nutrition Society 62: 107-115.
88. Wong, J.M., De Souza, R., Kendall, C.W., Emam, A. and Jenkins, D.J.A., 2006. Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology 40: 235-243.
89. Worthley, D.L., Le Leu, R.K., Whitehall, V.L., Conlon, M., Christophersen, C., Belobrajdic, D., Mallitt, K.A., Hu, Y., Irahara, N., Ogino, S., Leggett, B.A. and Young, G.P., 2009. A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. American Journal of Clinical Nutrition 90: 578-586.