In vitro evaluation of the fermentation properties and potential prebiotic activity of caprine cheese whey oligosaccharides in batch culture systems

BioFactors

Volumn 38, Issue 6, 2012, Pages 440-449

  Oliveira, Diana L ^a,b   Costabile, Adele ^a   Wilbey, R Andrew ^a   Grandison, Alistair S ^a   Duarte, Luis C ^b   Roseiro, Luisa B ^b  

^a UNIVERSITY OF READING   (United Kingdom)

^b LABORATÓRIO NACIONAL DE ENERGIA E GEOLOGIA   (Portugal)

Author keywords

Antimicrobial activity; Caprine whey; Oligosaccharide; Prebiotic; Prebiotic index

Indexed keywords

LACTIC ACID; NORLEUCINE; OLIGOSACCHARIDE; PREBIOTIC AGENT; PROPIONIC ACID; SHORT CHAIN FATTY ACID;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BATCH FERMENTATION; BIFIDOBACTERIUM; CASE REPORT; CHEESE; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE IN SITU HYBRIDIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; INTESTINE FLORA; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; WHEY;

ANIMALS; BATCH CELL CULTURE TECHNIQUES; BIFIDOBACTERIUM; CHEESE; DAIRY PRODUCTS; FATTY ACIDS, VOLATILE; FERMENTATION; GASTROINTESTINAL TRACT; GOATS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; OLIGOSACCHARIDES; PREBIOTICS;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; CAPRA; ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

EID: 84871219498     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1043     Document Type: Article

References (48)

1. Kunz, C. and Rudloff, S. (2006) Health promoting aspects of milk oligosaccharides. Int. Dairy J. 16, 1341-1346.
2. Bhat, Z. and Bhat, H. (2011) Milk and dairy products as functional foods: a review. Int. J. Dairy Sci. 6, 1-12.
3. Boehm, G. and Stahl, B. (2007) Oligosaccharides from milk. J. Nutr. 137, 847S-849S.
4. Gibson, G.R. and Roberfroid, M.B. (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 125, 1401-1412.
5. Roberfroid, M., Gibson, G.R., Hoyles, L., McCartney, A.L., Rastall, R., et al (2010) Prebiotic effects: metabolic and health benefits. Br. J. Nutr. 104 (Suppl 2), S1-S63.
6. Kunz, C., Rudloff, S., Baier, W., Klein, N., and Strobel, S., (2000) Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr. 20, 699-722.
7. Newburg, D.S. and Neubauer, S.H. (1995) Carbohydrates in milk: analysis, quantities and significance, in Handbook of Milk Composition, (Robert G. J., ed) Academic Press: San Diego; London. p. xxiii, 919 p.
8. Boehm, G. and Stahl, B., eds. (2003) Oligosaccharides. Functional dairy products, ed. Mattila - Sandholm T. Woodhead Publishers, Cambridge.
9. Boehm, G., Stahl, B., Knol, J., and Garssen, J. (2008) Carbohydrates in human milk and infant formulas, in Carbohydrate Chemistry, Biology and Medical Application, (Hari G. G., Mary K. G., Charles A. H., eds.). p. 275-291, Elsevier, Oxford.
10. Boehm, G., Stahl, B., Knol, J., and Garssen, J., eds. (2008)Carbohydrates in Human Milk and Infant Formulas, 1st ed. Carbohydrate Chemistry, Biology and Medical Application, (Gowman, M. K. Hales, C. A., and Garg, H. G., eds.). Vol. 12, Elsevier, Oxford.
11. Daddaoua, A., Puerta, V., Requena, P., Martinez-Ferez, A., Guadix, E., et al. (2006) Goat milk oligosaccharides are anti-inflammatory in rats with hapten-induced colitis. J Nutr. 136, 672-676.
12. Park, Y.W. and Haenlein, G.F.W. (2006) Handbook of Milk of Non-Bovine mammalsames. 449 p, Iowa, Oxford: Blackwell Pub. x
13. Raynal-Ljutovac, K., Lagriffoul, P.G., Guillet, I., and Chillard, Y. (2008) Composition of goat and sheep milk products: an update. Small Ruminant Res. 79, 57-72.
14. Lara-Villoslada, F., Debras, E., Nieto, A., Concha, A., Galvez, J., et al. (2006) Oligosaccharides isolated from goat milk reduce intestinal inflammation in a rat model of dextran sodium sulfate-induced colitis. Clin Nutr. 25, 477-88.
15. Martinez-Ferez, A., Rudloff, S., Guadix, A., Henkel, C.A., Pohlentz, G., et al. (2006) Goat's milk as a natural source of lactose-derived oligosaccharides: isolation by membrane technology. Int. Dairy J. 16, 173-181.
16. Oliveira, D.L., Wilbey, R.A., Grandison, A.S., Duarte, L.C., and Roseiro, L.B., (2012) Separation of oligosaccharides from caprine milk whey prior to prebiotic evaluation. Int. Dairy J.. 24, 102-106.
17. Hernández, O., Ruiz-Matute, A.I., Olano, A., Moreno, F.J., and Sanz, M.L. (2009) Comparison of fractionation techniques to obtain prebiotic galactooligosaccharides. Int. Dairy J. 19, 531-536.
18. Martin-Pelaez, S., Gibson, G.R., Martin-Orue, S.M., Klinder, A., Rastall, R.A., et al. (2008) In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems. FEMS Microbiol. Ecol. 66, 608-619.
19. Langendijk, P.S., Schut, F., Jansen, G.J., Raangs, G.C., Kamphuis, G.R., et al. (1995) Quantitative fluorescence in-situ hybridization of bifidobacterium spp with genus-specific 16s ribosomal-rna-targeted probes and its application in fecal samples. Appl. Environ. Microb. 61, 3069-3075.
20. Manz, W., Amann, R., Ludwig, W., Vancanneyt, M., and Schleifer, K.H., (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142 (Part 5), 1097-1106.
21. Franks, A.H., Harmsen, H.J., Raangs, G.C., Jansen, G.J., Schut, F., and Welling, G.W., (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 64, 3336-3345.
22. Harmsen, H.J.M., Elfferich, P., Schut, F., and Welling, G.W., (1999) A 16S rRNA-targeted probe for detection of Lactobacilli and Enterococci in faecal samples by fluorescent in situ hybridization. Microb. Ecol. Health Dis. 11, 3-12.
23. Walker, A.W., Duncan, S.H., McWilliam Leitch, E.C., Child, M.W., and Flint, H.J., (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 71, 3692-3700.
24. Daims, H., Bruhl, A., Amann, R., Schleifer, K.H., and Wagner, M. (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434-444.
25. Gomez, E., Tuohy, K.M., Gibson, G.R., Klinder, A., and Costabile, A. (2010) In vitro evaluation of the fermentation properties and potential prebiotic activity of Agave fructans. J. Appl. Microbiol. 108, 2114-2121.
26. Palframn, R., Gibson, G.R., and Rastall, R.A. (2003) Development of a quantitative tool for the comparison of the prebiotica effect of dietary oligosaccharides. Lett. Appl. Microbiol. 37, 281-281.
27. Mandalari, G., Nueno Palop, C., Tuohy, K., Gibson, G., Bennett, R., et al. (2007) In vitro evaluation of the prebiotic activity of a pectic oligosaccharide-rich extract enzymatically derived from bergamot peel. Appl. Microbiol. Biotechnol. 73, 1173-1179.
28. Soleimani, N.A., Kermanshahi, R.K., Yakhchali, B., and Sattari, T.N. (2010) Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. African J. Microbiol. Res. 4, 2169-2173.
29. Costabile, A., Kolida, S., Klinder, A., Gietl, E., Bauerlein, M., et al. (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, 1007-1017.
30. Depeint, F., Tzortzis, G., Vulevic, J., I'Anson, K., and Gibson, G.R. (2008) 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. Am. J. Clin. Nutr. 87, 785-791.
31. Wichienchot, S., Prasertsan, P., Hongpattarakere, T., Gibson, G.R. and Rastall, R.A. (2006) In vitro three-stage continuous fermentation of gluco-oligosaccharides produced by Gluconobacter oxydans NCIMB 4943 by the human colonic microflora. Curr Issues Intest. Microbiol. 7, 13-18.
32. Lefranc-Millot, C., Guerin-Deremaux, L., Wils, D., Neut, C., Miller, L.E., et al. (2012) Impact of a resistant dextrin on intestinal ecology: how altering the digestive ecosystem with NUTRIOSE(R), a soluble fibre with prebiotic properties, may be beneficial for health. J. Int. Med. Res. 40, 211-224.
33. Marcobal, A., Barboza, M., Froehlich, J.W., Block, D.E., German, J.B., et al. (2010) Consumption of human milk oligosaccharides by gut-related microbes. J. Agri. Food Chem. 58, 5334-5340.
34. Salazar, N., Ruas-Madiedo, P., Kolida, S., Collins, M., Rastall, R., et al. (2009) Exopolysaccharides produced by Bifidobacterium longum IPLA E44 and Bifidobacterium animalis subsp lactis IPLA R1 modify the composition and metabolic activity of human faecal microbiota in pH-controlled batch cultures. Int. J. Food Microbiol.. 135, 260-267.
35. Delzenne, N.M. and Kok, N. (2001) Effects of fructans-type prebiotics on lipid metabolism. Am. J. Clin. Nutr. 73, 456s-458s.
36. Rigottier-Gois, L., Rochet, V., Garrec, N., Suau, A., and Doré, J. (2003) Enumeration of bacteroides species in human faeces by fluorescent in situ hybridisation combined with flow cytometry using 16S rRNA probes. Syst. Appl. Microbiol. 26, 110-118.
37. Alles, M.S., Hartemink, R., Meyboom, S., Harryvan, J.L., Van Laere, K.M., et al. (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, 980-991.
38. Bouhnik, Y., Raskine, L., Simoneau, G., Vicaut, E., Neut, C., et al. (2004) The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. Am. J. Clin. Nutr. 80, 1658-1664.
39. Hudcovic, T., Kolinska, J., Klepetar, J., Stepankova, R., Rezanka, T., et al. (2012) Protective effect of Clostridium tyrobutyricum in acute dextran sodium sulphate-induced colitis: differential regulation of tumour necrosis factor-α and interleukin-18 in BALB/c and severe combined immunodeficiency mice. Clin. Exp. Immunol. 167, 356-365.
40. Ruhal, R. and Choudhury, B. (2012) Use of an osmotically sensitive mutant of Propionibacterium freudenreichii subspp. shermanii for the simultaneous productions of organic acids and trehalose from biodiesel waste based crude glycerol. Bioresource Technol. 109, 131-139.
41. Schwab, C. and Ganzle, M. (2011) Lactic acid bacteria fermentation of human milk oligosaccharide components, human milk oligosaccharides and galactooligosaccharides. FEMS Microbiol. Lett. 315, 141-148.
42. De Vuyst, L. and Leroy, F. (2007) Bacteriocins from lactic acid bacteria: Production, purification, and food applications. J. Mol. Microb. Biotech. 13, 194-199.
43. Salminen, S., Bouley, C., Boutron-Ruault, M.C., Cummings, J.H., Franck, A., et al. (1998) Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 80, S147-S171.
44. Wong, J.M.W., de Souza, R., Kendall, C.W.C., Emam, A., and Jenkins, D.J.A., (2006) Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol.. 40, 235-243.
45. Hernandez-Hernandez, O., Cote, G.L., Kolida, S., Rastall, R.A., and Sanz, M.L. (2011) In vitro fermentation of alternansucrase raffinose-derived oligosaccharides by human gut bacteria. J. Agri. Food Chemistry. 59, 10901-10906.
46. Cummings, J.H., Macfarlane, G.T., and Englyst, H.N. (2001) Prebiotic digestion and fermentation. Am. J. Clin. Nutr. 73, 415s-420s.
47. Manderson, K., Pinart, M., Tuohy, K.M., Grace, W.E., Hotchkiss, A.T., et al. (2005) In vitro determination of prebiotic properties of oligosaccharides derived from an orange juice manufacturing by-product stream. Appl. Environ. Microbiol. 71, 8383-8389.
48. Rycroft, C.E., Jones, M.R., Gibson, G.R., and Rastall, R.A. (2001) A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J. Appl. Microbiol. 91, 878-887.