Bioactive Carbohydrate: Prebiotics and Colorectal Cancer

  • Maya Raman
  • Padma Ambalam
  • Mukesh Doble


Prebiotics are defined as the indigestible food components that are selectively fermented by the intestinal microbes and promote changes in the gut environment, gut microbial community structure, and their metabolism. Prebiotics have been reported to avert colorectal cancer development by altering the composition and activity of the gut microflora. Administration of prebiotics has been reported to reduce colon cancer and its biomarkers. Oligosaccharides such as inulin, fructo-oligosaccharide, galacto-oligosaccharide, lactulose, soy-oligosaccharide, xylo-oligosaccharide, lactitol, resistant starch, etc., are some of the commercially available prebiotics. Short-chain fructo-oligosaccharides thwart colon carcinogenesis possibly by modulating the colonic ecosystem. Galacto-oligosaccharides, lactulose, and fructo-oligosaccharides are observed to increase the intestinal concentration of lactate, stool frequency, and weight; and decrease fecal concentration of secondary bile acids, fecal pH, and nitroreductase and β-glucuronidase activities, thus preventing colon carcinogenesis. Lactulose is reported to reduce the proliferation and occurrence of adenoma. Resistant starch prevents cancer by modulating gene expression and DNA methylation. Prebiotics undergo fermentation by gut microbes leading to the formation of short-chain fatty acids and enhance the immunity of the host. Butyrate has been observed to have direct effects in preventing colon cancer. Prebiotics are observed to modulate the colonic gut environment and aid in the growth and development of Bifidobacteria spp.


Prebiotics Short-chain fatty acids Oligosaccharides Inulin Fructo-oligosaccharides Galacto-oligosaccharides Lactulose Bifidogenic effects Colon Gut microbes 


  1. Aachary AA (2009) Prebiotics: specific colonic nutrients. Bioactive xylooligosaccharides from corncob: enzymatic production and applications. Thesis- submitted to University of Mysore, 19Google Scholar
  2. Aachary AA, Prapulla SG (2008) Corncob-induced endo-1, 4-β-D-xylanase of Aspergillus oryzae MTCC 5154: production and characterization of xylobiose from glucuronoxylan. J Agric Food Chem 56(11):3981–3988CrossRefGoogle Scholar
  3. Achour L, Flourie B, Briet F, Pellier P, Marteau P, Rambaud JC (1994) Gastrointestinal effects and energy value of polydextrose in healthy nonobese men. Am J Clin Nutr 59(6):1362–1368Google Scholar
  4. Alander M, Mättö J, Kneifel W, Johansson M, Kögler B, Crittenden R et al (2001) Effect of galacto-oligosaccharide supplementation on human faecal microflora and on survival and persistence of Bifidobacterium lactis Bb-12 in the gastrointestinal tract. Int Dairy J 11(10):817–825CrossRefGoogle Scholar
  5. Aller R, De Luis DA, Izaola O, Conde R, Gonzalez Sagrado M, Primo D, De La Fuente B, Gonzalez J (2011) Effect of a probiotic on liver aminotransferases in nonalcoholic fatty liver disease patients: a double blind randomized clinical trial. Eur Rev Med Pharmacol Sci 15(9):1090–1095Google Scholar
  6. Alles MS, Hartemink R, Meyboom S, Harryvan JL, Van Laere KM, Nagengast FM, Hautvast JG (1999) Effect of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. Am J Clin Nutr 69(5):980–991Google Scholar
  7. Anderson JW, Gilliland SE (1999) Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr 18(1):43–50CrossRefGoogle Scholar
  8. Apajalahti JH, Särkilahti LK, Mäki BR, Heikkinen JP, Nurminen PH, Holben WE (1998) Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 64(10):4084–4088Google Scholar
  9. Arslanoglu S, Moro GE, Schmitt J, Tandoi L, Rizzardi S, 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. J Nutr 138(6):1091–1095Google Scholar
  10. Baba S, Ohta A, Ohtsuki M, Takizawa T, Adachi T, Hara H (1996) Fructooligosaccharides stimulate the absorption of magnesium from the hindgut in rats. Nutr Res 16(4):657–666CrossRefGoogle Scholar
  11. Basu S, Haghiac M, Surace P, Challier JC, Guerre‐Millo M, Singh K et al (2011) Pregravid obesity associates with increased maternal endotoxemia and metabolic inflammation. Obesity 19(3):476–482CrossRefGoogle Scholar
  12. Bauer-Marinovic M, Florian S, Müller-Schmehl K, Glatt H, Jacobasch G (2006) Dietary resistant starch type 3 prevents tumor induction by 1,2-dimethylhydrazine and alters proliferation, apoptosis and dedifferentiation in rat colon. Carcinogen 27:1849–1859CrossRefGoogle Scholar
  13. Behall KM, Scholfield DJ, Hallfrisch JG, Liljeberg-Elmståhl HG (2006) Consumption of both resistant starch and β-glucan improves postprandial plasma glucose and insulin in women. Diab Care 29(5):976–981CrossRefGoogle Scholar
  14. Ben XM, Zhou XY, Zhao WH, Yu WL, Pan W, Zhang WL et al (2004) Supplementation of milk formula with galacto-oligosaccharides improves intestinal micro-flora and fermentation in term infants. Chin Med J 117(6):927–931Google Scholar
  15. Benjamin JL, Hedin CR, Koutsoumpas A, Ng SC, McCarthy NE, Hart AL, Kamm MA, Sanderson JD, Knight SC, Forbes A, Stagg AJ, Whelan K, Lindsay JO (2011) Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn’s disease. Gut 60(7):923–929Google Scholar
  16. Blaut M (2002) Relationship of prebiotics and food to intestinal microflora. Eur J Nutr 41(1):i11–i16Google Scholar
  17. Bode L (2006) Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr 136:2127–2130Google Scholar
  18. Boehm G, Stahl B, Jelinek J, Knol J, Miniello V, Moro GE (2005) Prebiotic carbohydrates in human milk and formulas. Acta Pediatr 94:18–21CrossRefGoogle Scholar
  19. Bolognani F, Rumney CJ, Pool-Zobel BL, Rowland IR (2001) Effect of lactobacilli, bifidobacteria and inulin on the formation of aberrant crypt foci in rats. Eur J Nutr 40:293–300CrossRefGoogle Scholar
  20. Bouhnik Y, Flourie B, D’Agay-Abensour L, Pochart P, Gramet G, Durand M, Rambaud JC (1997) Administration of trans-galacto-oligosaccharides increases faecal bifidobacteria and modifies colonic fermentation metabolism in healthy humans. J Nutr 127:444–448Google Scholar
  21. 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 faecal bifidobacteria in healthy humans. J Nutr 129:113–116Google Scholar
  22. Bouhnik Y, Attar A, Joly FA, Riottot M, Dyard F, Flourie B (2004) Lactulose ingestion increases faecal bifidobacterial counts: a randomised double-blind study in healthy humans. Eur J Clin Nutr 58:462–466CrossRefGoogle Scholar
  23. Boutron-Ruault MC, Marteau P, Lavergne-Slove A, Myara A, Gerhardt MF, Franchisseur C, Bornet F, Eripolyp Study Group (2005) Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutr Cancer 53(2):160–168CrossRefGoogle Scholar
  24. Brighenti F, Casiraghi MC, Canzi E, Ferrari A (1999) Effect of consumption of a ready-to-eat breakfast cereal containing inulin on the intestinal milieu and blood lipids in healthy male volunteers. Eur J Clin Nutr 53:726–733CrossRefGoogle Scholar
  25. Brisbin JT, Gong J, Sharif S (2008) Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim Health Res Rev 9:101–110CrossRefGoogle Scholar
  26. Brommage R, Binacua C, Antille S, Carrié A-L (1993) Intestinal calcium absorption in rats is stimulated by dietary lactulose and other resistant sugars. J Nutr 123:2186–2194Google Scholar
  27. Brown I (1996) Complex carbohydrates and resistant starch. Nutr Rev 54(11):S115–S119CrossRefGoogle Scholar
  28. Bruno-Barcena JM, Azcarate-Peril MA (2015) Galacto-oligosaccharides and colorectal cancer: feeding our intestinal probiome. J Funct Foods 12:92–108CrossRefGoogle Scholar
  29. Bucke C, Rastall RA (1990) Synthesising sugars by enzymes in reverse. Chem Br 26(7):675–678Google Scholar
  30. Buddington RK, Williams CH, Chen SC, Witherly SA (1996) Dietary supplement of neosugar alters the faecal flora and decreases activities of some reductive enzymes in human subjects. Am J Clin Nutr 63:709–716Google Scholar
  31. Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R (2006) Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 55(5):1484–1490CrossRefGoogle Scholar
  32. Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D et al (2009) Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr 90(5):1236–1243CrossRefGoogle Scholar
  33. Cashman K (2003) Prebiotics and calcium bioavailability. Curr Issues Intest Microbiol 4(1):21–32Google Scholar
  34. Causey JL, Feirtag JM, Gallaher DD, Tungland BC, Slavin JL (2000) Effects of dietary inulin on serum lipids, blood glucose and the gastrointestinal environment in hypercholesterolemic men. Nutr Res 20(2):191–201CrossRefGoogle Scholar
  35. Challa A, Rao DR, Chawan CB, Shackelford L (1997) Bifidobacterium longum and lactulose suppress azoxymethane induced aberrant crypt foci in rats. Carcinogenesis 18:517–521CrossRefGoogle Scholar
  36. Champ M, Langkilde AM, Brouns F, Kettlitz B, Bail-Collet YL (2003) Advances in dietary fibre characterisation. 2. Consumption, chemistry, physiology and measurement of resistant starch; implications for health and food labelling. Nutr Res Rev 16(2):143–161CrossRefGoogle Scholar
  37. Cherbut C, Michel C, Lecannu G (2003) The prebiotic characteristics of fructo-oligosaccharides are necessary for reduction of TNBS-induced colitis in rats. J Nutr 133:21–27Google Scholar
  38. Chonan O, Watanuki M (1996) The effect of 6'-galactooligosaccharides on bone mineralization of rats adapted to different levels of dietary calcium. Int J Vitam Nutr Res 66:244–249Google Scholar
  39. Cloetens L, Broekaert WF, Delaedt Y, Ollevier F, Courtin CM, Delcour JA, Rutgeerts P, Verbeke K (2010) Tolerance of arabinoxylan-oligosaccharides and their prebiotic activity in healthy subjects: a randomised, placebo-controlled cross-over study. Br J Nutr 103:703–713CrossRefGoogle Scholar
  40. Costabile A, Kolida S, Klinder A, Gietl E, Bäuerlein M, Frohberg C, Landschütze V, Gibson GR (2010) A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104(07):1007–1017CrossRefGoogle Scholar
  41. Conway PL (2001) Prebiotics and human health: the state-of-the-art and future perspectives. Food Nutr Res 45:13–21CrossRefGoogle Scholar
  42. Coudray C, Demigné C, Rayssiguier Y (2003) Effects of dietary fibers on magnesium absorption in animals and humans. J Nutr 133(1):1–4Google Scholar
  43. Cummings JH, Stephen AM (2007) Carbohydrate terminology and classification. Eur J Clin Nutr 61:S5–S18CrossRefGoogle Scholar
  44. Cummings JH, Macfarlane GT, Englyst HN (2001) Prebiotic digestion and fermentation. Am J Clin Nutr 73:415S–420SGoogle Scholar
  45. Dal Bello F, Walter J, Hertel C, Hammes WP (2001) In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst Appl Microbiol 24:1–6CrossRefGoogle Scholar
  46. Davidson MH, Maki KC, Synecki C, Torri SA, Drennan KB (1998) Evaluation of the influence of dietary inulin on serum lipids in adults with hypercholesterolemia. Nutr Res 18(6):503–517CrossRefGoogle Scholar
  47. Deguchi Y, Matsumoto K, Ito A, Watanuki M (1997) Effects of beta 1–4 galactooligosaccharides administration on defeacation of healthy volunteers with a tendency to constipation. Jap J Nutr 55(1):13–22CrossRefGoogle Scholar
  48. Delzenne N (2003) Oligosaccharides: state of art. Proc Nutr Soc 62:177CrossRefGoogle Scholar
  49. Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7(11):639–646CrossRefGoogle Scholar
  50. Den Hond E, Geypens B, Ghoos Y (2000) Effect of high performance chicory inulin on constipation. Nutr Res 20:731–736CrossRefGoogle Scholar
  51. Drakoularakou A, Tzortzis G, Rastall RA, Gibson GR (2010) A double-blind, placebo-controlled, randomized human study assessing the capacity of a novel galacto-oligosaccharide mixture in reducing travellers' diarrhoea. Eur J Clin Nutr 64(2):146–152CrossRefGoogle Scholar
  52. Ebringerova A, Hromadkova Z, Alfodi J, Hribalova V (1998) The immunologically active xylan from ultrasound-treated corncobs: extractability, structure and properties. Carbohydr Polym 37:231–239CrossRefGoogle Scholar
  53. Fanaro S, Boehm G, Garssen J, Knol J, Mosca F, Stahl B, Vigi V (2005) Galacto‐oligosaccharides and long‐chain fructo‐oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr 94(s449):22–26CrossRefGoogle Scholar
  54. Favier ML, Moundras C, Demigné C, Rémésy C (1995) Fermentable carbohydrates exert a more potent cholesterol-lowering effect than cholestyramine. Bioch Biophys Acta Lipid Meta 1258(2):115–121CrossRefGoogle Scholar
  55. Femia AP, Luceri C, Dolara P, Giannini A, Biggeri A, Salvadori M, Clune Y, Collins KJ, Paglierani M, Caderni G (2002) Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogen 23:1953–1960CrossRefGoogle Scholar
  56. Fernandez ML, Roy S, Vergara-Jimenez M (2000) Resistant starch and cholestyramine have distinct effects on hepatic cholesterol metabolism in guinea pigs fed a hypercholesterolemic diet. Nutr Res 20(6):837–849CrossRefGoogle Scholar
  57. Figdor SK, Rennhart HH (1981) Caloric utilisation and disposition of [14C] polydextrose in man. J Agri Food Chem 29:1181–1189CrossRefGoogle Scholar
  58. Frohberg C, Quanz M (2008) Use of linear poly-alpha-1,4-glucans as resistant starch. United States Patent Application 20080249297Google Scholar
  59. Fuentes-Zaragoza E, Sánchez-Zapata E, Sendra E, Sayas E, Navarro C, Fernández-López J, Pérez-Alvarez JA (2011) Resistant starch as prebiotic. Starch 63:406–415CrossRefGoogle Scholar
  60. Fuller R (1992) The effect of probiotics on the gut micro-ecology of farm animals. In: Wood BJB (ed) The lactic acid bacteria in health and disease, vol 1. Elsevier Science Publishers, Cambridge, UK, pp 171–192Google Scholar
  61. Fuller R, Gibson GR (1997) Modification of the intestinal microflora using probiotics and prebiotics. Scand J Gastroenterol 32:28–31Google Scholar
  62. Fuller R, Gibson GR (1998) Probiotics and prebiotics: microflora management for improved gut health. Clin Microbiol Infect 4(9):477–480CrossRefGoogle Scholar
  63. Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, Fernandez-Real JM, Dandona P (2009) Increase in plasma endotoxin concentrations and the expression of toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal implications for insulin resistance. Diabetes Care 32(12):2281–2287CrossRefGoogle Scholar
  64. Ghoneum M, Abedi S (2004) Enhancement of natural killer cell activity of aged mice by modified arabinoxylan rice bran (MGN-3/biobran). J Pharma Pharmacol 56:1581–1588CrossRefGoogle Scholar
  65. Gibson GR, Rastall RA (2006) Prebiotics: development and application. Wiley, ChichesterCrossRefGoogle Scholar
  66. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microflora introducing the concept of probiotics. J Nutr 125:1401–1412Google Scholar
  67. Gibson GR, Roberfroid MB (1999) Colonic microbiota, nutrition and health. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  68. Gibson GR, Beatty ER, Wang X, Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108:975–982CrossRefGoogle Scholar
  69. Gibson GR, Probert HM, van Loo JAE, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275CrossRefGoogle Scholar
  70. Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A et al (2010) Dietary prebiotics: current status and new definition. Food Sci Tech Bull Funct Foods 7:1–19CrossRefGoogle Scholar
  71. Goldin BR, Gorbach SL (1992) Probiotics for humans. In: Fuller R (ed) Probiotics. The scientific basis. Chapman and Hall, London, pp 355–376Google Scholar
  72. Goldring JM (2004) Resistant starch: safe intakes and legal status. J AOAC Int 87:733–739Google Scholar
  73. Gopalakrishnan A, Clinthorne JF, Rondini EA, McCaskey SJ, Gurzell EA, Langohr IM et al (2012) Supplementation with galacto-oligosaccharides increases the percentage of NK cells and reduces colitis severity in Smad3-deficient mice. J Nutr 142(7):1336–1342CrossRefGoogle Scholar
  74. Griessen M, Cochet B, Infante F, Jung A, Bartholdi P, Donath A, Loizeau E, Courvoisier B (1989) Calcium absorption from milk in lactase-deficient subjects. Am J Clin Nutr 49(2):377–384Google Scholar
  75. Gronlund MM, Lehtonen OP, Eerola E, Kero P (1999) Faecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after Cesarean delivery. J Paediatr Gastroenterol Nutr 28:19–25CrossRefGoogle Scholar
  76. Guerin-Deremaux L, Pochat M, Reifer C, Wils D, Cho S, Miller LE (2011) The soluble fibre Nutriose induces a dose dependent beneficial impact on satiety over time in humans. Nutr Res 31:665–672CrossRefGoogle Scholar
  77. Hamilton-Miller JMT (2004) Probiotics and prebiotics in the elderly. Postgrad Med J 80(946):447–451CrossRefGoogle Scholar
  78. Hammers HJ, Verheul H, Wilky B, Salumbides B, Holleran J, Egorin MJ et al (2008) Phase I safety and pharmacokinetic/pharmacodynamic results of the histone deacetylase inhibitor vorinostat in combination with bevacizumab in patients with kidney cancer. ASCO Annu Meet Proc 26(15), S16094Google Scholar
  79. Hayakawa K, Mizutani J, Wada K, Masai T, Yoshihara I, Mitsuoka T (1990) Effects of soybean oligosaccharides on human faecal flora. Microl Ecol Health Dis 3:293–303CrossRefGoogle Scholar
  80. Hijová E, Bomba A, Bertková I, Strojný L, Szabadosová V, Šoltésová A (2012) Prebiotics and bioactive natural substances induce changes of composition and metabolic activities of the colonic microflora in cancerous rats. Acta Biochim Pol 59(2):271Google Scholar
  81. Hijová E, Szabadosova V, Štofilová J, Hrčková G (2013) Chemopreventive and metabolic effects of inulin on colon cancer development. J Vet Sci 14(4):387–393CrossRefGoogle Scholar
  82. Hooper LV, Midtvedt T, Gordon JI (2002) How hostmicrobial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307CrossRefGoogle Scholar
  83. Hopping BN, Erber E, Grandinetti A, Verheus M, Kolonel LN, Maskarinec G (2009) Dietary fiber, magnesium, and glycemic load alter risk of type 2 diabetes in a multiethnic cohort in Hawaii. J Nutr 140(1):68–74CrossRefGoogle Scholar
  84. Hsu CK, Liao JW, Chung YC, Hsieh C, Chan YC (2004) Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr 134(6):1523–1528Google Scholar
  85. Hughes R, Rowland IR (2001) Stimulation of apoptosis by two prebiotic chicory fructans in the rat colon. Carcinogenesis 22:43–47CrossRefGoogle Scholar
  86. Ito M, Deguchi Y, Miyamori A, Matsumoto K, Kikuchi H, Matsumoto K, Kobayashi Y, Yajima T, Kan T (1990) Effects of administration of galactooligosaccharides on the human fecal microflora, stool weight and abdominal sensation. Microbial Ecol Health Dis 3:285–292CrossRefGoogle Scholar
  87. Ito M, Kimura M, Deguchi Y, Miyamori-Watabe A, Yajima T, Kan T (1993) Effects of transgalactosylated disaccharides on the human intestinal microflora and their metabolism. J Nutr Sci Vitamin 39:279–288CrossRefGoogle Scholar
  88. Izumi K, Ikemizu S, Shizuka F (2004) Anti-hyperlipidemics containing acidic xylooligosaccharides. Japan Patent JP 2004182615:2004Google Scholar
  89. Janardhana V, Broadway MM, Bruce MP, Lowenthal JV, Geier MS, Hughes RJ, Bean AGD (2009) Prebiotics modulate immune responses in the gut-associated lymphoid tissue of chickens. J Nutr 139(7):1404–1409CrossRefGoogle Scholar
  90. Jenkins DJA, Kendall CWC, Vuksan V (1999) Inulin, oligofructose and intestinal function. J Nutr 129:1431S–1433SGoogle Scholar
  91. Jie Z, Bang-Yao L, Ming-Jie X, Hai-Wei L, Zu-Kang Z, Ting-Song W, Craig SA (2000) Studies on the effects of polydextrose intake on physiologic functions in Chinese people. Am J Clin Nutr 72:1503–1509Google Scholar
  92. Johansen M, Bækbo P, Thomsen LK (1996) Control of edema disease in Danish pig herds. In: Proceedings of the 14th international pig veterinary society congress, vol 14, BolognaGoogle Scholar
  93. Johnson CH, Patterson AD, Idle JR, Gonzalez FJ (2012) Xenobiotic metabolomics: major impact on the metabolome. Annu Rev Pharmacol Toxicol 52:37–56CrossRefGoogle Scholar
  94. Kim YS, Tsao D, Morita A, Bella A (1982) Effect of sodium butyrate and three human colorectal adenocarcinoma cell lines in culture. Falk Symp 31:317–323Google Scholar
  95. Kim S, Kim W, Hwang IK (2003) Optimization of the extraction and purification of oligosaccharides from defatted soybean meal. Int J Food Sci Technol 38:337–342CrossRefGoogle Scholar
  96. Kneifel W, Rajal A, Kulbe D (2000) In vitro growth behaviour of probiotic bacteria in culture media with carbohydrates of prebiotic importance. Microb Ecol Health Dis 12:27–34CrossRefGoogle Scholar
  97. Kohmoto T, Fukui F, Takaku H, Machida Y, Arai M, Mitsuoka T (1988) Effect of isomalto-oligosaccharides on human fecal flora. Bifidobact Microflora 7:61–69CrossRefGoogle Scholar
  98. Kohmoto T, Fukui F, Takaku H, Mitsuoka T (1991) Dose–response test of isomaltooligosaccharides for increasing fecal bifidobacteria. Agric Biol Chem 55:2157–2159CrossRefGoogle Scholar
  99. Kolida S, Tuohy K, Gibson GR (2002) Prebiotic effects of inulin and oligofructose. Br J Nutr 87(S2):S193–S197CrossRefGoogle Scholar
  100. Kontula P, Suihko ML, Von Wright A, Mattila-Sandholm T (1999) The effect of lactose derivatives on intestinal lactic acid bacteria. J Dairy Sci 82:249–256CrossRefGoogle Scholar
  101. Kunz C, Rudloff S (1993) Biological functions of oligosaccharides in human milk. Acta Paediatr 82:903–912CrossRefGoogle Scholar
  102. Lafiandra D, Riccardi G, Shewry PR (2014) Improving cereal grain carbohydrates for diet and health. J Cereal Sci 59(3):312–326CrossRefGoogle Scholar
  103. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2), e9085CrossRefGoogle Scholar
  104. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N et al (2011) Peripheral education of the immune system by colonic commensal microbiota. Nature 478(7368):250–254CrossRefGoogle Scholar
  105. Lefranc-Millot C (2008) NUTRIOSE®06: a useful soluble dietary fibre for added nutritional value. Nutr Bull 33:234–239CrossRefGoogle Scholar
  106. Letexier D, Diraison F, Beylot M (2003) Addition of inulin to a moderately high-carbohydrate diet reduces hepatic lipogenesis and plasma triacylglycerol concentrations in humans. Am J Clin Nutr 77(3):559–564Google Scholar
  107. Lin CC, Ferguson LR, Tannock GW (2005) Dietary fibres as “prebiotics”: implications for colorectal cancer. Mol Nutr Food Res 49(6):609–619CrossRefGoogle Scholar
  108. Lina BAR, Jonker D, Kozianowski G (2002) Isomaltulose (Palatinose): a review of biological and toxicological studies. Food Chem Toxicol 40:1375–1381CrossRefGoogle Scholar
  109. Lishaut ST, Rechkemmer G, Rowland I, Dolara P, Pool-Zobel BL (1999) The carbohydrate crystalean and colonic microflora modulate expression of glutathione S-transferase subunits in colon of rats. Eur J Nutr 38:76–83CrossRefGoogle Scholar
  110. Liu R, Xu G (2008) Effects of resistant starch on colonic preneoplastic aberrant crypt foci in rats. Food Chem Toxicol 46:2672–2679CrossRefGoogle Scholar
  111. Tratnik L (1998) Milk technology, biochemistry and microbiology. Croatian Milk Soc, Zagreb, pp 345–380Google Scholar
  112. Lopez HW, Levrat-Verny MA, Coudray C, Besson C, Krespine V, Messager A, Demigné C, Rémésy C (2001) Class 2 resistant starches lower plasma and liver lipids and improve mineral retention in rats. J Nutr 131:1283–1289Google Scholar
  113. Macfarlane GT, Cummings JH (1991) The colonic flora, fermentation and large bowel digestive function. In: Phillips SF, Pemberton JH, Shorter RG (eds) The large intestine: physiology, pathophysiology and disease. Raven, New York, pp 51–88Google Scholar
  114. Macfarlane S, Macfarlane GT, Cummings JH (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24:701–714CrossRefGoogle Scholar
  115. Macfarlane GT, Steed H, Macfarlane S (2008) Bacterial metabolism and health‐related effects of galactooligosaccharides and other prebiotics. J Appl Microbiol 104(2):305–344Google Scholar
  116. Matijevic B, Bozanic R, Tratnik L (2009) The influence of lactulose on growth and survival of probiotic bacteria Lactobacillus acidophilus La-5 and Bifidobacterium subsp. lactis BB-12 in reconstituted sweet whey. Mljekarstvo 59(1):20–27Google Scholar
  117. Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620–625CrossRefGoogle Scholar
  118. McBain AJ, Macfarlane GT (2001) Modulation of genotoxic enzyme activities by nondigestible oligosaccharide metabolism in in-vitro human gut bacterial systems. J Med Microbiol 50:833–842CrossRefGoogle Scholar
  119. Mizota T, Tamura Y, Tomita M, Okonogi S (1987) Lactulose as a sugar with physiological significance. Bull Intl Dairy Fed 212:69–76Google Scholar
  120. Mizota T, Mori T, Yaeshima T, Yanagida T, Iwatsuki K, Ishibashi N, Tamura Y, Fukuwatari Y (2002) Effects of low dosages of lactulose on the intestinal function of healthy adults. Milchwissenschaft 57(6):312–315Google Scholar
  121. Morisse JP, Maurice R, Boilletot E, Cotte JP (1993) Assessment of the activity of a fructooligosaccharide on different caecal parameters in rabbits experimentally infected with E. coli 0.103. Ann Zootechnol 42:81–87CrossRefGoogle Scholar
  122. Mortensen A, Poulsen M, Frandsen H (2002) Effect of a long-chained fructan Raftiline HP on blood lipids and spontaneous atherosclerosis in low density receptor knockout mice. Nutr Res 22(4):473–480CrossRefGoogle Scholar
  123. Munjal U, Glei M, Pool-Zobel BL, Scharlau D (2009) Fermentation products of inulin-type fructans reduce proliferation and induce apoptosis in human colon tumour cells of different stages of carcinogenesis. Br J Nutr 102:663–671CrossRefGoogle Scholar
  124. Mussatto SI, Mancilha IM (2007) Non-digestible oligosaccharides: a review. Carb Poly 68:587–597CrossRefGoogle Scholar
  125. Mustapha A, Jiang T, Savaiano DA (1997) Improvement of lactose digestion by humans following ingestion of unfermented acidophilus milk: influence of bile sensitivity, lactose transport, and acid tolerance of Lactobacillus acidophilus. J Dairy Sci 80(8):1537–1545CrossRefGoogle Scholar
  126. Nabarlatz D, Farriol X, Montane D (2005) Autohydrolysis of almond shells for the production of xylo-oligosaccharides: product characteristics and reaction kinetics. Ind Eng Chem Res 44:7746–7755CrossRefGoogle Scholar
  127. National Institutes of Health (2010) NIH Consensus Development Conference Statement: lactose intolerance and health. NIH Consens State Sci Statement 27(2):1–27Google Scholar
  128. Nemcova R, Bomba A, Gancarcikova S, Heich R, Guba P (1999) Study of the effect of Lactobacillus paracasei and fructooligosacharides on the faecal microflora in weanling piglets. Berl Munch Tierarztl Wochenschr 112:225–228Google Scholar
  129. Niittynen L, Kajander K, Korpela R (2007) Galacto-oligosaccharides and bowel function. Scand J Food Nutr 51(2):62CrossRefGoogle Scholar
  130. Nilsson U, Oste R, Jagerstad M, Birkhed D (1988) Cereal fructans: in vitro and in vivo studies on availability in rats and humans. J Nutr 118:1325–1330Google Scholar
  131. Ohkuma K, Wakabayashi S (2001) Fibersol-2: a soluble, non-digestible, starch-derived dietary fibre. In: McCleary BV, Prosky L (eds) Advanced dietary fibre technology. Blackwell Science Ltd, Oxford, pp 509–523Google Scholar
  132. Oku T, Tokunaga T, Hosoya N (1984) Non-digestibility of a new sweetener, ‘Neosugar’ in the rat. J Nutr 114:1574–1581Google Scholar
  133. Oliveira RPS, Perego P, Oliveira MN, Converti A (2011) Effect of inulin as prebiotic and synbiotic interactions between probiotics to improve fermented milk firmness. J Food Eng 107:36–40CrossRefGoogle Scholar
  134. Onyango C, Bley T, Jacob A (2006) Influence of incubation temperature and time on resistant starch type III formation from autoclaved and acid-hydrolysed cassava starch. Carb Polym 66:497–499CrossRefGoogle Scholar
  135. Oosterveld A, Beldman G, Voragen AGJ (2002) Enzymatic modifiation of pectic polysaccharides obtained from sugar beet pulp. Carb Poly 48:7–81CrossRefGoogle Scholar
  136. Pasman W, Wils D, Saniez MH, Kardinaal A (2006) Long-term gastrointestinal tolerance of NUTRIOSE® FB in healthy men. Eur J Clin Nutr 60(8):1024–1034CrossRefGoogle Scholar
  137. Pool-Zobel BL (2005) Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. Br J Nutr 93:S73–S90CrossRefGoogle Scholar
  138. Probert HM, Apajalahti JH, Rautonen N, Stowell J, Gibson GR (2004) Polydextrose, lactitol, and fructo-oligosaccharide fermentation by colonic bacteria in a three-stage continuous culture system. Appl Envtl Microbiol 70:4505–4511CrossRefGoogle Scholar
  139. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P (2009) Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101(04):541–550CrossRefGoogle Scholar
  140. Ramnani P, Gaudier E, Bingham M, Van Bruggen P, Tuohy KM, Gibson GR (2010) Prebiotic effect of fruit and vegetable shots containing Jerusalem artichoke inulin: a human intervention study. Br J Nutr 104(02):233–240CrossRefGoogle Scholar
  141. Riggio O, Balducci G, Ariosto F, Merli M, Tremiterra S, Ziparo V, Capocaccia L (1990) Lactitol in the treatment of chronic hepatic encephalopathy–a randomized cross-over comparison with lactulose. Hepatogastroenterology 37(5):524–527Google Scholar
  142. Rizzello V, Bonaccorsi I, Dongarra ML, Fink LN and Ferlazzo G (2011) Role of natural killer and dendritic cell crosstalk in immunomodulation by commensal bacteria probiotics. BioMed Res Int 2011:1–10Google Scholar
  143. Roberfroid M (2007) Prebiotics: the concept revisited. J Nutr 137:830S–837SGoogle Scholar
  144. Rochfort S, Panozzo J (2007) Phytochemicals for health, the role of pulses. J Agric Food Chem 55:7981–7994CrossRefGoogle Scholar
  145. Rodríguez-Cabezas ME, Camuesco D, Arribas B, Garrido-Mesa N, Comalada M, Bailón E et al (2010) The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats. Clin Nutr 29(6):832–839CrossRefGoogle Scholar
  146. Rowland IR, Tanaka R (1993) The effects of transgalactosylated oligosaccharides on gut flora metabolism in rats associated with a human faecal microflora. J Appl Bacteriol 74:667–674CrossRefGoogle Scholar
  147. Rowland IR, Rumney CJ, Coutts JT, Lievense LC (1998) Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogene 19:281–285CrossRefGoogle Scholar
  148. Roy CC, Kien CL, Bouthillier L, Levy E (2006) Short-chain fatty acids: ready for prime time? Nutr Clin Pract 21(4):351–366CrossRefGoogle Scholar
  149. Rycroft CE, Jones MR, Gibson GR, Rastall RA (2001) Fermentation properties of gentio-oligosaccharides. Lett Appl Microbiol 32:156–161CrossRefGoogle Scholar
  150. Sabater-Molina M, Larqué E, Torrella F, Zamora S (2009) Dietary fructooligosaccharides and potential benefits on health. J Physiol Biochem 65(3):315–328CrossRefGoogle Scholar
  151. Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri I, Moreau MC, Roberfroid M, Rowland IR (1998) Functional food science and gastrointestinal physiology and function. Br J Nutr 80:S147–S171CrossRefGoogle Scholar
  152. Saavedra JM, Tschernia A (2002) Human studies with probiotics and prebiotics: clinical implications. Br J Nutr 87(S2):S241–S246CrossRefGoogle Scholar
  153. Sánchez-Mata MC, Peñuela-Teruel MJ, Cámara-Hurtado M, Díez-Marqués C, Torija-Isasa ME (1998) Determination of mono-, di-, and oligosaccharides in legumes by high-performance liquid chromatography using an amino-bonded silica column. J Agric Food Chem 46(9):3648–3652CrossRefGoogle Scholar
  154. Schaafsma G, Meuling WJ, Van Dokkum W, Bouley C (1998) Effects of a milk product, fermented by Lactobacillus acidophilus and with fructo-oligosaccharides added, on blood lipids in male volunteers. Eur J Clin Nutr 52(6):436–440CrossRefGoogle Scholar
  155. Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35(1S):S35–S38CrossRefGoogle Scholar
  156. Scheppach W, Weiler F (2004) The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care 7:563–567CrossRefGoogle Scholar
  157. Scholtens PA, Alles MS, Willemsen LE, van den Braak C, Bindels JG, Boehm G, Govers MJ (2006) Dietary fructo-oligosaccharides in healthy adults do not negatively affect faecal cytotoxicity: a randomised, double-blind, placebo-controlled crossover trial. Br J Nutr 95(06):1143–1149CrossRefGoogle Scholar
  158. Scholz-Ahrens KE, Schrezenmeir J (2002) Inulin, oligofructose and mineral metabolism-experimental data and mechanism. Br J Nutr 87(S2):S179–S186CrossRefGoogle Scholar
  159. Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Aςil Y et al (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137(3):838S–846SGoogle Scholar
  160. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60CrossRefGoogle Scholar
  161. Seki N, Hamano H, Iiyama Y, Asano Y, Kokubo S, Yamauchi K et al (2007) Effect of lactulose on calcium and magnesium absorption: a study using stable isotopes in adult men. J Nutr Sci Vitaminol 53(1):5–12CrossRefGoogle Scholar
  162. Serpelloni M (2011) Use of branched malto-dextrins as granulation binders. U.S. Patent No. 7,943,171. U.S. Patent and Trademark Office, Washington, DCGoogle Scholar
  163. Silvi S, Rumney CJ, Cresci A, Rowland IR (1999) Resistant starch modifies gut microflora and microbial metabolism in human flora-associated rats inoculated with faeces from Italian and UK donors. J Appl Microbiol 86:521–530CrossRefGoogle Scholar
  164. Slavin JL, Savarino V, Paredes-Diaz A, Fotopoulos G (2009) A review of the role of soluble fiber in health with specific reference to wheat dextrin. J Int Medical Res 37(1):1–17Google Scholar
  165. Storey D, Lee A, Bornet F, Brouns F (2007) Gastrointestinal tolerance of erythritol and xylitol ingested in a liquid. Eur J Clin Nutr 61(3):349–354CrossRefGoogle Scholar
  166. Sugawara M, Suzuki K, Endo K, Kumemura M, Takeuchi M, Mitsuoka T (1990) Effect of the dietary supplementation of corn hemicellulose on fecal flora and bacterial enzyme activities in human adults. Agric Biol Chem 54(7):1683–1688CrossRefGoogle Scholar
  167. Tanaka R, Takayama H, Morotomi M, Kuroshima T, Ueyama S, Matsumoto K, Kuroda A, Mutai M (1983) Effects of administration of TOS and Bifidobacterium breve 4006 on the human fecal flora. Bifidobact Microflora 2:17–24CrossRefGoogle Scholar
  168. Taper HS, Delzenne NM, Roberfroid MB (1997) Growth inhibition of transplantable mouse tumors by non‐digestible carbohydrates. Int J Cancer 71(6):1109–1112CrossRefGoogle Scholar
  169. Teuri U, Korpela R, Saxelin M, Montonen L, Salminen S (1998) Increased faecal frequency and gastrointestinal symptoms following ingestion of galacto-oligosaccharide-containing yogurt. J Nutr Sci Vitaminol 44:465–471CrossRefGoogle Scholar
  170. Torres DP, Gonçalves MDPF, Teixeira JA, Rodrigues LR (2010) Galacto‐oligosaccharides: production, properties, applications, and significance as prebiotics. Comp Rev Food Sci Food Safety 9(5):438–454CrossRefGoogle Scholar
  171. Transparency Market Release, Press Report (2015) Prebiotics in Animal Feed Market to Exhibit 11.9% CAGR from 2013 to 2019 due to Health Benefits for Animals.
  172. Tuohy KM, Kolida S, Lustenberger A, Gibson GR (2001) The prebiotic effects of biscuits containing partially hydrolyzed guar gum and fructooligosaccharides – a human volunteer study. Br J Nutr 86:341–348CrossRefGoogle Scholar
  173. Tuohy KM, Ziemer CJ, Klinder A, Knobel Y, PoolZobel BL, Gibson GR (2002) A human volunteer study to determine the prebiotic effects of lactulose powder on human colonic bacteria. Microbial Ecol Health Dis 14:165–173CrossRefGoogle Scholar
  174. van den Heuvel EG, Schoterman MH, Muijs T (2000) Trans-galactooligosaccharides stimulate calcium absorption in postmenopausal women. J Nutr 130:2938–2942Google Scholar
  175. Van Loo J, Cummings J, Delzenne N, Englyst H, Franck A, Hopkins M, Kok N, Macfarlane G, Newton D, Quigley M, Roberfroid M, Van Vliet T, Van den Heuvel E (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br J Nutr 81:121–132CrossRefGoogle Scholar
  176. Vazquez MJ, Alonso JL, Domınguez H, Parajó JC (2000) Xylooligosaccharides: manufacture and applications. Trends Food Sci Technol 11(11):387–393CrossRefGoogle Scholar
  177. Verghese M, Rao DR, Chawan CB, Williams LL, Shackelford L (2002) Dietary inulin suppresses azoxymethane-induced aberrant crypt foci and colon tumours at the promotion stage in young Fisher 344 rats. J Nutr 132(9):2809–2813Google Scholar
  178. Wang SJ, Yu JL, Liu HY, Chen WP (2008) Characterisation and preliminary lipid-lowering evaluation of starch from Chinese Yam. Food Chem 108:176–181CrossRefGoogle Scholar
  179. White LA, Newman MC, Comwell GL, Lindemann MD (2002) Brewers dried yeast as a source of mannan oligosaccharides for weaning pigs. J Anim Sci 80:2619–2628Google Scholar
  180. WHO (2009) Cardiovascular disease. Fact sheet 317, WHO, Geneva.
  181. Wolever TMS, Schrade KB, Vogt JA, Tsihlias EB, McBurney MI (2002) Do colonic short chain fatty acids contribute to the long-term adaptation of blood lipids in subjects with type 2 diabetes consuming a high-fiber diet? Am J Clin Nutr 75:1023–1030Google Scholar
  182. Wollowski I, Rechkemmer G, Pool-Zobel BL (2001) Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr 73(2):451–455Google Scholar
  183. Younes H, Coudray C, Bellanger J, Demigné C, Rayssiquier Y, Rémésy C (2001) Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br J Nutr 86:479–485CrossRefGoogle Scholar
  184. Zetterstrom R, Bennett R, Nord K-E (1994) Early infant feeding and micro-ecology of the gut. Acta Paediatr Jpn 36:562–571CrossRefGoogle Scholar

Copyright information

© Springer India 2016

Authors and Affiliations

  • Maya Raman
    • 1
  • Padma Ambalam
    • 2
  • Mukesh Doble
    • 1
  1. 1.Bioengineering and Drug Design Lab Department of BiotechnologyIndian Institute of Technology MadrasChennaiIndia
  2. 2.Department of BiotechnologyChrist College, Saurashtra UniversityRajkotIndia

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