In recent years, research has focused on the positive effects of prebiotics on intestinal health and gut microbiota. The relationship between their chemical structure and their fermentation pattern by human intestinal microbiota is still not well understood. The aim of this study was to improve understanding of this relationship and identify factors that may be used to design galactooligosaccharides that reach more distal regions than commercial prebiotics which mainly target the proximal colon. The following factors were investigated: monomer type, linkage, substitution, and degree of polymerisation. Total organic acid production from sugars by faecal bacteria was fitted to a model which allowed an estimate of the time when half of the maximal organic acid concentration was reached (T50) in static faecal batch cultures. The different factors can be grouped by their effectiveness at prolonging fermentation time as follows: substitution is most effective, with methylgalactose, -galactose-pentaacetate, D-fucose, and galactitol fermented more slowly than D-galactose. Monomers and linkage also influence fermentation time, with L rhamnose, arabinose, melezitose, and xylose being fermented significantly slower than D-glucose ( ), maltose, isomaltose, cellobiose, and gentiobiose showing that Glc 1-6Glc and Glc 1-4Glc were utilised slowest. Chain length had the smallest effect on fermentation time. 1. Introduction Epidemiological data [1–4] indicate that a diet high in dietary fibres from vegetables and grains is correlated to a reduced risk of certain diseases in humans, among them colon cancer, ulcerative colitis, and cardiovascular disease. Experimental evidence suggests that the short-chain fatty acids (SCFA), butyric, acetic, and propionic acids [3–5], play a role in this risk reduction. They are produced by the intestinal microbiota as a result of dietary fibre fermentation. Dietary fibres are plant materials, mostly storage carbohydrates or cell wall components, that cannot be digested in the human small intestine and reach the colon intact. They are available as substrates for the resident microbiota [6]. Some dietary fibres may also have prebiotic potential. Prebiotics are “non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacterial species already resident in the colon, and thus attempt to improve host health” [7]. Bacterial fermentation of carbohydrates in the colon results in the production of SCFA, mainly acetic, propionic, and butyric acid. Other
References
[1]
D. P. Burkitt, “Related disease—related cause?” The Lancet, vol. 2, no. 7632, pp. 1229–1231, 1969.
[2]
F. Levi, C. Pasche, C. La Vecchia, F. Lucchini, and S. Franceschi, “Food groups and colorectal cancer risk,” British Journal of Cancer, vol. 79, no. 7-8, pp. 1283–1287, 1999.
[3]
W. Scheppach, H. Sommer, T. Kirchner et al., “Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis,” Gastroenterology, vol. 103, no. 1, pp. 51–56, 1992.
[4]
B. F. Hinnebusch, S. Meng, J. T. Wu, S. Y. Archer, and R. A. Hodin, “The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation,” Journal of Nutrition, vol. 132, no. 5, pp. 1012–1017, 2002.
[5]
S. Tedelind, F. Westberg, M. Kjerrulf, and A. Vidal, “Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease,” World Journal of Gastroenterology, vol. 13, no. 20, pp. 2826–2832, 2007.
[6]
A. D. Blackwood, J. Salter, P. W. Dettmar, and M. F. Chaplin, “Dietary fibre, physicochemical properties and their relationship to health,” Journal of The Royal Society for the Promotion of Health, vol. 120, no. 4, pp. 242–247, 2000.
[7]
G. R. Gibson and M. B. Roberfroid, “Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics,” Journal of Nutrition, vol. 125, no. 6, pp. 1401–1412, 1995.
[8]
I. R. Rowland, C. J. Rumney, J. T. Coutts, and L. C. Lievense, “Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats,” Carcinogenesis, vol. 19, no. 2, pp. 281–285, 1998.
[9]
B. L. Pool-Zobel, S. L. Abrahamse, and G. Rechkemmer, “Protective effects of short-chain fatty acids on early events of carcinogenesis: antigenotoxic effects of butyrate in rat and human colon cells,” in Proceedings of COST Action 92th Workshop on Dietary Fibre and Fermentation in the Colon, pp. 350–357, Espoo, Finland, 1996.
[10]
H. K. Biesalski, P. Fürst, H. Kasper, et al., Ern？hrungsmedizin. 2. überarbeitete Auflage, Georg Thieme, Stuttgart, Germany, 1999.
[11]
T. R. Licht, M. Hansen, M. Poulsen, and L. O. Dragsted, “Dietary carbohydrate source influences molecular fingerprints of the rat faecal microbiota,” BMC Microbiology, vol. 6, article 98, 2006.
[12]
J. M. W. Wong, R. De Souza, C. W. C. Kendall, A. Emam, and D. J. A. Jenkins, “Colonic health: fermentation and short chain fatty acids,” Journal of Clinical Gastroenterology, vol. 40, no. 3, pp. 235–243, 2006.
[13]
G. A. Dienel and N. F. Cruz, “Astrocyte activation in working brain: energy supplied by minor substrates,” Neurochemistry International, vol. 48, no. 6-7, pp. 586–595, 2006.
[14]
M. T. Wyss, B. Weber, V. Treyer et al., “Stimulation-induced increases of astrocytic oxidative metabolism in rats and humans investigated with 1-11C-acetate,” Journal of Cerebral Blood Flow and Metabolism, vol. 29, no. 1, pp. 44–56, 2009.
[15]
A. J. McBain and G. T. Macfarlane, “Modulation of genotoxic enzyme activities by non-digestible oligosaccharide metabolism in in-vitro human gut bacterial ecosystems,” Journal of Medical Microbiology, vol. 50, no. 9, pp. 833–842, 2001.
[16]
G. Tzortzis, A. K. Goulas, J. M. Gee, and G. R. Gibson, “A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo,” Journal of Nutrition, vol. 135, no. 7, pp. 1726–1731, 2005.
[17]
G. T. Macfarlane, G. R. Gibson, and J. H. Cummings, “Comparison of fermentation reactions in different regions of the human colon,” Journal of Applied Bacteriology, vol. 72, no. 1, pp. 57–64, 1992.
[18]
G. T. Macfarlane and A. J. McBain, “The human colonic microbiota,” in Colonic Microbiota, Nutrition and Health, G. R. Gibson MB Roberfroid, Ed., pp. 1–25, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1999.
[19]
M. H. M. C. Van Nuenen, K. Venema, J. C. J. Van Der Woude, and E. J. Kuipers, “The metabolic activity of fecal microbiota from healthy individuals and patients with inflammatory bowel disease,” Digestive Diseases and Sciences, vol. 49, no. 3, pp. 485–491, 2004.
[20]
A. McIntyre, G. P. Young, T. Taranto, P. R. Gibson, and P. B. Ward, “Different fibers have different regional effects on luminal contents of rat colon,” Gastroenterology, vol. 101, no. 5, pp. 1274–1281, 1991.
[21]
E. Olano-Martin, K. C. Mountzouris, G. R. Gibson, and R. A. Rastall, “In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria,” British Journal of Nutrition, vol. 83, no. 3, pp. 247–255, 2000.
[22]
E. Olano-Martin, G. R. Gibson, and R. A. Rastall, “Comparison of the in vitro bifidogenic properties of pectins and pectic-oligosaccharides,” Journal of Applied Microbiology, vol. 93, no. 3, pp. 505–511, 2002.
[23]
S. Perrin, C. Fougnies, J. P. Grill, H. Jacobs, and F. Schneider, “Fermentation of chicory fructo-oligosaccharides in mixtures of different degrees of polymerization by three strains of bifidobacteria,” Canadian Journal of Microbiology, vol. 48, no. 8, pp. 759–763, 2002.
[24]
K. M. J. Van Laere, M. Bosveld, H. A. Schols, et al., “Fermentative degradation of plant cell wall derived oligosaccharides by intestinal bacteria,” in Proceedings of the International Symposium on “Non-Digestible Oligosaccharides: Healthy Food for the Colon”, R. Hartemink, Ed., pp. 37–46, Wageningen Graduate School VLAG, 1997.
[25]
H. Ruppin, S. Bar-Meir, and K. H. Soergel, “Absorption of short-chain fatty acids by the colon,” Gastroenterology, vol. 78, no. 6, pp. 1500–1507, 1980.
[26]
J. A. Vogt and T. M. S. Wolever, “Fecal acetate is inversely related to acetate absorption from the human rectum and distal colon,” Journal of Nutrition, vol. 133, no. 10, pp. 3145–3148, 2003.
[27]
G. O. Guerrant, M. A. Lambert, and C. W. Moss, “Analysis of short-chain acids from anaerobic bacteria by high-performance liquid chromatography,” Journal of Clinical Microbiology, vol. 16, no. 2, pp. 355–360, 1982.
[28]
J. L. Campbell, C. V. Williams, and J. H. Eisemann, “Fecal inoculum can be used to determine the rate and extent of in vitro fermentation of dietary fiber sources across three lemur species that differ in dietary profile: varecia variegata, Eulemur fulvus and Hapalemur griseus,” Journal of Nutrition, vol. 132, no. 10, pp. 3073–3080, 2002.
[29]
Y. Benjamini and Y. Hochberg, “Controlling the false discovery rate: a practical and powerful approach to multiple testing,” Journal of the Royal Statistical Society B, vol. 57, pp. 289–300, 1995.
[30]
E. Bauer, B. A. Williams, C. Voigt, R. Mosenthin, and M. W. A. Verstegen, “Microbial activities of faeces from unweaned and adult pigs, in relation to selected fermentable carbohydrates,” Animal Science, vol. 73, no. 2, pp. 313–322, 2001.
[31]
M. R. Smiricky-Tjardes, E. A. Flickinger, C. M. Grieshop, L. L. Bauer, M. R. Murphy, and G. C. Fahey, “In vitro fermentation characteristics of selected oligosaccharides by swine fecal microflora,” Journal of Animal Science, vol. 81, no. 10, pp. 2505–2514, 2003.
[32]
A. J. Vince, N. I. McNeil, J. D. Wager, and O. M. Wrong, “The effect of lactulose, pectin, arabinogalactan and cellulose on the production of organic acids and metabolism of ammonia by intestinal bacteria in a faecal incubation system,” British Journal of Nutrition, vol. 63, no. 1, pp. 17–26, 1990.
[33]
P. J. Wood, E. Arrigoni, S. Shea Miller, and R. Amadò, “Fermentability of oat and wheat fractions enriched in β-glucan using human fecal inoculation,” Cereal Chemistry, vol. 79, no. 3, pp. 445–454, 2002.
[34]
N. Peekhaus and T. Conway, “What's for dinner?: entner-Doudoroff metabolism in Escherichia coli,” Journal of Bacteriology, vol. 180, no. 14, pp. 3495–3502, 1998.
[35]
T. L. Miller and M. J. Wolin, “Fermentations by saccharolytic intestinal bacteria,” American Journal of Clinical Nutrition, vol. 32, no. 1, pp. 164–172, 1979.
[36]
G. T. Macfarlane and G. R. Gibson, “Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine,” in Gastrointestinal Microbiology, R. I. Mackie and B. A. White, Eds., vol. 1, pp. 269–318, Chapman & Hall, New York, NY, USA, 1997.
[37]
P. B. Mortensen, K. Holtug, and H. S. Rasmussen, “Short-chain fatty acid production from mono- and disaccharides in a fecal incubation system: Implications for colonic fermentation of dietary fiber in humans,” Journal of Nutrition, vol. 118, no. 3, pp. 321–325, 1988.
[38]
H. Hove, I. Nordgaard-Andersen, and P. B. Mortensen, “Effect of lactic acid bacteria on the intestinal production of lactate and short-chain fatty acids, and the absorption of lactose,” American Journal of Clinical Nutrition, vol. 59, no. 1, pp. 74–79, 1994.
[39]
S. A. Brooks, M. V. Dwek, and U. Schumacher, Functional and Molecular Glycobiology, BIOS Scientific, Oxford, UK, 2002.
[40]
F. Depeint, G. Tzortzis, J. Vulevic, K. I'Anson, and G. R. Gibson, “Prebiotic evaluation of a novel galactooligosaccharide mixture produced by the enzymatic activity of Bifidobacterium bifidum NCIMB 41171, in healthy humans: a randomized, double-blind, crossover, placebo-controlled intervention study,” American Journal of Clinical Nutrition, vol. 87, no. 3, pp. 785–791, 2008.
[41]
A. Bernalier, J. Dore, and M. Durand, “Biochemistry of fermentation,” in Colonic Microbiota, Nutrition and Health, G. R. Gibson and M. B. Roberfroid, Eds., pp. 37–53, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1999.
[42]
V. Van Craeyveld, K. Swennen, E. Dornez et al., “Structurally different wheat-derived arabinoxylooligosaccharides have different prebiotic and fermentation properties in rats,” Journal of Nutrition, vol. 138, no. 12, pp. 2348–2355, 2008.
[43]
M. L. Sanz, G. R. Gibson, and R. A. Rastall, “Influence of disaccharide structure on prebiotic selectivity in vitro,” Journal of Agricultural and Food Chemistry, vol. 53, no. 13, pp. 5192–5199, 2005.
[44]
P. Brobech Mortensen and I. Nordgaard-Andersen, “The dependence of the in vitro fermentation of dietary fibre to short-chain fatty acids on the contents of soluble non-starch polysaccharides,” Scandinavian Journal of Gastroenterology, vol. 28, no. 5, pp. 418–422, 1993.
[45]
M. L. Sanz, G. L. C？té, G. R. Gibson, and R. A. Rastall, “Prebiotic properties of alternansucrase maltose-acceptor oligosaccharides,” Journal of Agricultural and Food Chemistry, vol. 53, no. 15, pp. 5911–5916, 2005.
[46]
M. L. Sanz, G. L. C？té, G. R. Gibson, and R. A. Rastall, “Selective fermentation of gentiobiose-derived oligosaccharides by human gut bacteria and influence of molecular weight,” FEMS Microbiology Ecology, vol. 56, no. 3, pp. 383–388, 2006.
