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Bifidogenic effect and stimulation of short chain fatty acid production in human faecal slurry cultures by oligosaccharides derived from lactose and lactulose

Published online by Cambridge University Press:  18 May 2009

Alejandra Cardelle-Cobas
Affiliation:
Instituto de Fermentaciones Industriales (CSIC), Juan de la Cierva, 3, Madrid28006, Spain
María Fernández
Affiliation:
Instituto de Productos Lácteos de Asturias (CSIC), Crta. Infiesto s/n, 33300Villaviciosa (Asturias), Spain
Nuria Salazar
Affiliation:
Instituto de Productos Lácteos de Asturias (CSIC), Crta. Infiesto s/n, 33300Villaviciosa (Asturias), Spain
Cristina Martínez-Villaluenga
Affiliation:
Instituto de Fermentaciones Industriales (CSIC), Juan de la Cierva, 3, Madrid28006, Spain
Mar Villamiel*
Affiliation:
Instituto de Fermentaciones Industriales (CSIC), Juan de la Cierva, 3, Madrid28006, Spain
Patricia Ruas-Madiedo
Affiliation:
Instituto de Productos Lácteos de Asturias (CSIC), Crta. Infiesto s/n, 33300Villaviciosa (Asturias), Spain
Clara G de los Reyes-Gavilán
Affiliation:
Instituto de Productos Lácteos de Asturias (CSIC), Crta. Infiesto s/n, 33300Villaviciosa (Asturias), Spain
*
*For correspondence; e-mail: mvillamiel@ifi.csic.es

Abstract

Bifidogenic effect and stimulation of short chain fatty acid (SCFA) production by fractions of oligosaccharides with a DP⩾3 and Gal β(1-6) linkages synthesised from lactose or lactulose by Pectinex Ultra SP-L and Lactozym 3000 L HP G were evaluated in human faecal slurries. Results were compared with those obtained for the commercial oligosaccharide mixture Vivinal®-GOS. Quantitative real-time PCR showed that all galacto-oligosaccharide (GOS) fractions stimulated slightly higher bifidobacteria growth than lactose, lactulose and Vivinal®-GOS. GOS fractions promoted the production of total SCFA and acetic acid in a similar way to Vivinal®-GOS and more than glucose, lactose and lactulose. In conclusion, oligosaccharides derived from lactose and lactulose may represent a suitable alternative to lactulose for the design of new functional food ingredients.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2009

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References

Aider, M & de Halleux, D 2007 Isomerization of lactose and lactulose production: a review. Trends in Food Science and Technology 18 356364Google Scholar
Al-Tamimi, MAY, Palframan, RJ, Cooper, JM, Gibson, GR & Rastall, RA 2006 In vitro fermentation of sugar beet arabinan and arabino-oligosaccharides by the human gut microflora. Journal of Applied Microbiology 100 407414CrossRefGoogle ScholarPubMed
Anthony, JC, Merriman, TN & Heimbach, JT 2006 90-Day oral (gavage) study in rats with galactooligosaccharides syrup. Food Chemistry and Toxicology 44 819826CrossRefGoogle ScholarPubMed
Barreteau, H, Delattre, C & Michaud, P 2006 Production of oligosaccharides as promising new food additive generation. Food Technology and Biotechnology 44 323333Google Scholar
Bouhnik, Y, Raskine, L, Simoneau, G, Vicaut, E, Neut, C, Flourie, B, Brouns, F & Bornet, FR 2004a The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. American Journal of Clinical Nutrition 80 16581664CrossRefGoogle ScholarPubMed
Bouhnik, Y, Attar, A, Joly, FA, Riottot, M, Dyard, F & Flourie, B 2004b Lactulose ingestion increases faecal bifidobacterial counts: a randomised double-blind study in healthy humans. European Journal of Clinical Nutrition 58 462466Google Scholar
Cardelle-Cobas, A, Villamiel, M, Olano, A & Corzo, N 2008a Study of galacto-oligosaccharide formation from lactose using Pectinex-Ultra SP-L. Journal of the Science of Food and Agriculture 88 954961CrossRefGoogle Scholar
Cardelle-Cobas, A, Martínez-Villaluenga, C, Villamiel, M, Olano, A & Corzo, N 2008b Synthesis of oligosacchariedes derived from lactulose and Pectinex Ultra SP L. Journal of Agricultural and Food Chemistry 56 33283333CrossRefGoogle ScholarPubMed
Chockchaisawasdee, S, Athanasopoulos, VI, Niranjan, K & Rastall, RA 2005 Synthesis of galacto-oligosaccharides from lactose using, β-galactosidase from Kluyveromyces lactis: Studies on batch and continuous UF membrane fitted bioreactors. Biotechnology and Bioengineering 89 434443CrossRefGoogle ScholarPubMed
Chow, J 2002 Probiotics and Prebiotics: a brief overview. Journal of Renal Nutrition 12 7686CrossRefGoogle ScholarPubMed
Cristl, SU, Murgatroyd, PR, Gibson, GR & Cummings, JH 1992 Production metabolism and excretion of hydrogen in the large intestine. Gastroenterology 102 12691277CrossRefGoogle Scholar
Cummings, JH 1981 Short chain fatty acids in the human colon. Gut 22 763779Google Scholar
De Preter, V, Vanhoutte, T, Huys, G, Swings, J, Rutgeerts, P & Verbeke, K 2008 Baseline microbiota activity and influence responses to prebiotic initial bifidobacteria counts dosing in healthy subjects. Alimentary Pharmacology and Therapeutics 27 504513Google Scholar
Delzenne, NM 2003 Oligosaccharides: state of the art. Proceedings of the Nutrition Society 62 177182CrossRefGoogle ScholarPubMed
Djouzi, Z & Andrieux, C 1997 Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. British Journal of Nutrition 78 313324CrossRefGoogle ScholarPubMed
Dongowski, G, Jacobasch, G & Schmiedl, D 2005 Structural stability and prebiotic properties of resistant starch type 3 increase bile acid turnover and lower secondary bile acid formation. Journal of Agricultural and Food Chemistry 53 92579267CrossRefGoogle ScholarPubMed
Gibson, GR & Roberfroid, MB 1995 Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 125 14011412CrossRefGoogle ScholarPubMed
Gueimonde, M, Tölkko, S, Korpimäki, T & Salminen, S 2004 New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples. Applied and Environmental Microbiology 70 41654169CrossRefGoogle ScholarPubMed
Holt, SM, Miller-Fosmore, CM & Côté, GL 2005 Growth of various intestinal bacteria on alternansucrase-derived oligosaccharides. Letters in Applied Microbiology 40 385390CrossRefGoogle ScholarPubMed
Hsu, CA, Lee, SL, Chou, CC 2007 Enzymatic production of galactooligosaccharides by β-galactosidase from Bifidobacterium longum BCRC 15708. Journal of Agricultural and Food Chemistry 55 22252230CrossRefGoogle ScholarPubMed
Kaneko, T, Kohmoto, T, Kikuchi, H, Shiota, M, Iino, H & Mitsuoka, T 1994 Effects of isomaltooligosaccharides with different degrees of polymerization on human faecal Bifidobacteria. Bioscience Biotechnology and Biochemistry 58 22882290Google Scholar
Kaplan, H & Hutkins, RW 2000 Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Applied and Environmental Microbiology 66 26822684CrossRefGoogle ScholarPubMed
Louis, P, Scott, KP, Duncan, SH & Flint, HJ 2007 Understanding the effects of diet on bacterial metabolism in the large intestine. Journal of Applied Microbiology 102 11971208Google Scholar
Macfarlane, S & Macfarlane, GT 2003 Regulation of short-chain fatty acid production. Proceedings of the Nutrition Society 62 6772CrossRefGoogle ScholarPubMed
Macfarlane, S, Macfarlane, GT, Cummings, JH 2006 Review article: prebiotics in the gastrointestinal tract. Alimentary Pharmacology & Therapeutics 24 701714Google Scholar
Mahoney, RR 1998 Galactosyl-oligosaccharide formation during lactose hydrolysis: a review. Food Chemistry 63 147154Google Scholar
Martínez-Villaluenga, C, Cardelle-Cobas, A, Corzo, N, Olano, A & Villamiel, M 2008a Optimization of conditions for galactooligosaccharide synthesis during lactose hydrolysis by β-galactosidase from Kluyveromyces lactis (Lactozym 3000 L HP G). Food Chemistry 107 258264CrossRefGoogle Scholar
Martínez-Villaluenga, C, Cardelle-Cobas, A, Olano, A, Corzo, N, Villamiel, M, Jimeno, ML 2008b Enzymatic synthesis and identification of two trisaccharides produced from lactulose by transgalactosylation. Journal of Agricultural and Food Chemistry 56 557563CrossRefGoogle ScholarPubMed
Matteuzzi, D, Swennen, E, Rossi, M, Hartman, T & Lebet, V 2004 Prebiotic effects of a wheat germ preparation in human healthy subjects. Food Microbiology 21 119124CrossRefGoogle Scholar
Mendez, A & Olano, A 1979 Lactulose. A review of some chemical properties and application in infant nutrition and medicine. Dairy Sciences Abstracts 41 531535Google Scholar
Onishi, N, Yamashiro, A & Yokozeki, K 1995 Production of galactooligosaccharide from lactose by Sterignatomyces elviae CBS8119. Applied and Environmental Microbiology 61 40224025Google Scholar
Panesar, PS, Panesar, R, Singh, RS, Kennedy, JF & Kumar, H 2006 Microbial production, immobilization and applications of β-galactosidase. Journal of Chemical Technology and Biotechnology 81 530543CrossRefGoogle Scholar
Rycroft, CE, Jones, MR, Gibson, GR, Rastall, RA 2001 A comparative in vitro evaluation of the fermentation properties of prebiotic. Journal of Applied Microbiology 91 878887Google Scholar
Salazar, N, Gueimonde, M, Hernández-Barranco, MH, Ruas-Madiedo, P & de los Reyes-Gavilan, CG 2008 Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Applied and Environmental Microbiology 74 47374745CrossRefGoogle ScholarPubMed
Sanz, ML, Gibson, GR & Rastall, RA 2005 Influence of disaccharide structure on prebiotic selectivity in vitro. Journal of Agricultural and Food Chemistry 53 51925199CrossRefGoogle ScholarPubMed
Shin, HJ & Yang, JW 1998 Enzymatic production of galactoligosacchatides by Bullera singularis β-galactosidase. Journal of Microbiology and Biotechnology 8 484489Google Scholar
Splechtna, B, Nguyen, TH, Steinbock, M, Kulbe, KD, Lorenz, W & Haltrich, D 2006 Production of prebiotic galactooligosacchairdes from lactose using β-galactosidase from Lactobacillus reuteri. Journal of Agricultural and Food Chemistry 54 49995006CrossRefGoogle Scholar
Tomomatsu, H 1994 Health effects of oligosaccharides Food Technology 48 6165Google Scholar
Topping, DL & Clifton, PM 2001 Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81 10311064CrossRefGoogle ScholarPubMed
Tuohy, KM, Rouzaud, GCM, Brück, WM & Gibson, GR 2005 Modulation of the human gut microflora towards improved health using prebiotics-Assessment of efficacy. Current Pharmaceutical Design 11 7590Google Scholar
Vanhoutte, T, De Preter, V, Brandt, E, Verbeke, K, Swings, J & Huys, G 2006 Molecular monitoring of the fecal microbiota of healthy human subjects during administration of lactulose and Saccharomyces boulardii. Environmental Microbiology 72 59905997CrossRefGoogle ScholarPubMed
Wong, JMW, Souza, de R, Kendall, CWC, Emam, A & Jenkins, DJA 2006 Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology 40 235243CrossRefGoogle ScholarPubMed