Release of small phenolic compounds from Brewer's spent grain and its lignin fractions by human intestinal microbiota in vitro

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 40, 2013, Pages 9744-9753

  Aura, Anna Marja ^a   Niemi, Piritta ^a   Mattila, Ismo ^a   Niemelä, Klaus ^a   Smeds, Annika ^b   Tamminen, Tarja ^a   Faulds, Craig ^a   Buchert, Johanna ^a   Poutanen, Kaisa ^a,c  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

brewer's spent grain; in vitro colon model; intestinal microbiota; lignan; lignin

Indexed keywords

BREWING; FATTY ACIDS; PHENOLS;

BREWER'S SPENT GRAIN; IN-VITRO; LIGNAN; MICROBIOTAS; NON-STARCH POLYSACCHARIDES; PHENOLIC COMPONENTS; PHENOLIC COMPOUNDS; SHORT-CHAIN FATTY ACIDS;

LIGNIN;

ANIMALIA;

LIGNAN; LIGNIN; PHENOL DERIVATIVE; VOLATILE FATTY ACID;

ARTICLE; CEREAL; CHEMISTRY; FERMENTATION; GAS CHROMATOGRAPHY; HUMAN; HYDROLYSIS; INTESTINE; METABOLISM; METABOLOME; MICROBIOLOGY; MICROFLORA; PLANT STRUCTURES;

CEREALS; CHROMATOGRAPHY, GAS; FATTY ACIDS, VOLATILE; FERMENTATION; HUMANS; HYDROLYSIS; INTESTINES; LIGNANS; LIGNIN; METABOLOME; MICROBIOTA; PHENOLS; PLANT STRUCTURES;

EID: 84885446513     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4024195     Document Type: Article

References (44)

1. Mussatto, S. I.; Dragone, G.; Roberto, I. C. Brewers' spent grain: generation, characteristics and potential applications J. Cereal Sci. 2006, 43, 1-14 (Pubitemid 41741835)
2. Garleb, K. A.; Fahey, G. C.; Lewis, S. M.; Kerley, M. S.; Montgomery, L. Chemical composition and digestibility of fiber fractions of certain by-product feedstuffs fed to ruminants J. Anim. Sci. 1988, 66, 2650-2662
3. Silanikove, N.; Brosh, A. Lignocellulose degradation and subsequent metabolism of lignin fermentation products by the desert black Bedouin goat fed on wheat straw as a single-component diet Br. J. Nutr. 1989, 62, 509
4. Begum, A. N.; Nicolle, C.; Mila, I.; Lapierre, C.; Nagano, K.; Fukushima, K.; Heinonen, S.; Adlercreutz, H.; Rémésy, C.; Scalbert, A. Dietary lignins are precursors of mammalian lignans in rats J. Nutr. 2004, 134, 120-127 (Pubitemid 38057433)
5. Aura, A.-M.; Oikarinen, S.; Mutanen, M.; Heinonen, S.-M.; Adlercreutz, H. C. T.; Virtanen, H.; Poutanen, K. S. Suitability of a batch in vitro fermentation model using human faecal microbiota for prediction of conversion of flaxseed lignans to enterolactone with reference to an in vivo rat model Eur. J. Nutr. 2006, 45, 45-51 (Pubitemid 43221283)
6. Aura, A.-M.; Mattila, I.; Seppänen-Laakso, T.; Miettinen, J.; Oksman-Caldentey, K.; Orešič, M. Microbial metabolism of catechin stereoisomers by human faecal microbiota: comparison of targeted analysis and a non-targeted metabolomics method Phytochem. Lett. 2008, 1, 18-22 (Pubitemid 351445363)
7. Bazzocco, S.; Mattila, I.; Guyot, S.; Renard, C.; Aura, A.-M. Factors affecting the conversion of apple polyphenols to phenolic acids and fruit matrix to short-chain fatty acids by human faecal microbiota in vitro Eur. J. Nutr. 2008, 47, 442-452
8. Aura, A.-M.; Mattila, I.; Hyötyläinen, T.; Gopalacharyulu, P.; Cheynier, V.; Souquet, J.; Bes, M.; Bourvellec, C.; Guyot, S.; Orešič, M. Characterization of microbial metabolism of Syrah grape products in an in vitro colon model using targeted and non-targeted analytical approaches Eur. J. Nutr. 2012, 1-14
9. Boerjan, W.; Ralph, J.; Baucher, M. Lignin biosynthesis Annu. Rev. Plant Biol. 2003, 54, 519-546 (Pubitemid 37400004)
10. Scalbert, A. Antimicrobial properties of tannins Phytochemistry 1991, 30, 3875-3883
11. Niemi, P.; Tamminen, T.; Smeds, A.; Viljanen, K.; Ohra-aho, T.; Holopainen-Mantila, U.; Faulds, C. B.; Poutanen, K.; Buchert, J. Characterization of lipids and lignans in brewer's spent grain and its enzymatically extracted fraction J. Agric. Food Chem. 2012, 60, 9910-9917
12. Van Craeyveld, V.; Holopainen, U.; Selinheimo, E.; Poutanen, K.; Delcour, J. A.; Courtin, C. M. Extensive dry ball milling of wheat and rye bran leads to in situ production of arabinoxylan oligosaccharides through nanoscale fragmentation J. Agric. Food Chem. 2009, 57, 8467-8473
13. Barry, J.-L.; Hoebler, C.; MacFarlane, G. T.; MacFarlane, S.; Mathers, J. C.; Reed, K. A.; Mortensen, P. B.; Nordgaard, I.; Rowland, I. R.; Rumney, C. J. Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study Br. J. Nutr. 1995, 74, 303-322
14. Karppinen, S.; Liukkonen, K.; Aura, A.-M.; Forssell, P.; Poutanen, K. In vitro fermentation of polysaccharides of rye, wheat and oat brans and inulin by human faecal bacteria J. Sci. Food Agric. 2000, 80, 1469-1476 (Pubitemid 30597630)
15. Schooley, D. L.; Kubiak, F. M.; Evans, J. V. Capillary gas chromatographic analysis of volatile and non-volatile organic acids from biological samples as the t-butyldimethylsilyl derivatives J. Chromatogr. Sci. 1985, 23, 385-390 (Pubitemid 15585024)
16. Castillo, S.; Mattila, I.; Miettinen, J.; Orešič, M.; Hyötyläinen, T. Data analysis tool for comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry Anal. Chem. 2011, 83, 3058-3067
17. Golm metabolome database, http://gmd.mpimp-golm.mpg.de/search.aspx (accessed May 30, 2013).
18. Smeds, A. I.; Hakala, K.; Hurmerinta, T. T.; Kortela, L.; Saarinen, N. M.; Mäkelä, S. I. Determination of plant and enterolignans in human serum by high-performance liquid chromatography with tandem mass spectrometric detection J. Pharm. Biomed. Anal. 2006, 41, 898-905 (Pubitemid 44269075)
19. Smeds, A. I.; Eklund, P. C.; Willför, S. M. Content, composition, and stereochemical characterisation of lignans in berries and seeds Food Chem. 2012, 134, 1991-1998
20. Jacobs, E.; Kulling, S. E.; Metzler, M. Novel metabolites of the mammalian lignans enterolactone and enterodiol in human urine J. Steroid Biochem. Mol. Biol. 1999, 68, 211-218 (Pubitemid 29290657)
21. Niemelä, K. Low-molecular-weight organic compounds in birch kraft black liquor Ann. Acad. Sci. Fenn., Ser. A II, Chem. 1990, 229, 1-142
22. Braune, A.; Bunzel, M.; Yonekura, R.; Blaut, M. Conversion of dehydrodiferulic acids by human intestinal microbiota J. Agric. Food Chem. 2009, 57, 3356-3362
23. Heinonen, S.; Nurmi, T.; Liukkonen, K.; Poutanen, K.; Wähälä, K.; Deyama, T.; Nishibe, S.; Adlercreutz, H. In vitro metabolism of plant lignans: New precursors of mammalian lignans enterolactone and enterodiol J. Agric. Food Chem. 2001, 49, 3178-3186 (Pubitemid 32845044)
24. Blaut, M.; Clavel, T. Metabolic diversity of the intestinal microbiota: implications for health and disease J. Nutr. 2007, 137, 751-755
25. Aura, A.-M.; O'Leary, K. A.; Williamson, G.; Ojala, M.; Bailey, M.; Puupponen-Pimiä, R.; Nuutila, A. M.; Oksman-Caldentey, K.; Poutanen, K. Quercetin derivatives are deconjugated and converted to hydroxyphenylacetic acids but not methylated by human fecal flora in vitro J. Agric. Food Chem. 2002, 50, 1725-1730 (Pubitemid 34233254)
26. Rechner, A. R.; Smith, M. A.; Kuhnle, G.; Gibson, G. R.; Debnam, E. S.; Srai, S. K. S.; Moore, K. P.; Rice-Evans, C. A. Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products Free Radical Biol. Med. 2004, 36, 212-225 (Pubitemid 38117239)
27. Gonthier, M.-P.; Remesy, C.; Scalbert, A.; Cheynier, V.; Souquet, J.-M.; Poutanen, K.; Aura, A.-M. Microbial metabolism of caffeic acid and its esters chlorogenic and caftaric acids by human faecal microbiota in vitro Biomed. Pharmacother. 2006, 60, 536-540 (Pubitemid 44740368)
28. Araújo, J. D. P.; Grande, C. A.; Rodrigues, A. E. Vanillin production from lignin oxidation in a batch reactor Chem. Eng. Res. Des. 2010, 88, 1024-1032
29. Csonka, F. A.; Phillips, M.; Jones, D. B. Studies on lignin metabolism J. Biol. Chem. 1929, 85, 65-75
30. Kelsay, J. L.; Goering, H. K.; Behall, K. M.; Prather, E. S. Effect of fiber from fruits and vegetables on metabolic responses of human subjects: fiber intakes, fecal excretions, and apparent digestibilities Am. J. Clin. Nutr. 1981, 34, 1849-1852 (Pubitemid 12245286)
31. Holloway, W. D.; Tasman-Jones, C.; Lee, S. P. Digestion of certain fractions of dietary fiber in humans Am. J. Clin. Nutr. 1978, 31, 927-930 (Pubitemid 8374399)
32. Nordlund, E.; Aura, A.-M.; Mattila, I.; Kössö, T.; Rouau, X.; Poutanen, K. Formation of phenolic microbial metabolites and short-chain fatty acids from rye, wheat, and oat bran and their fractions in the metabolical in vitro colon model J. Agric. Food Chem. 2012, 60, 8134-8145
33. Mateo Anson, N.; van den Berg, R.; Havenaar, R.; Bast, A.; Haenen, G. R. M. M. Bioavailability of ferulic acid is determined by its bioaccessibility J. Cereal Sci. 2009, 49, 296-300
34. Niemi, P.; Faulds, C. B.; Sibakov, J.; Holopainen, U.; Poutanen, K.; Buchert, J. Effect of a milling pre-treatment on the enzymatic hydrolysis of carbohydrates in brewer's spent grain Bioresour. Technol. 2012, 116, 155-160
35. Hernanz, D.; Nuñez, V.; Sancho, A. I.; Faulds, C. B.; Williamson, G.; Bartolomé, B.; Gómez-Cordovés, C. Hydroxycinnamic acids and ferulic acid dehydrodimers in barley and processed barley J. Agric. Food Chem. 2001, 49, 4884-4888 (Pubitemid 32988735)
36. Smeds, A. I.; Eklund, P. C.; Sjöholm, R. E.; Willför, S. M.; Nishibe, S.; Deyama, T.; Holmbom, B. R. Quantification of a broad spectrum of lignans in cereals, oilseeds, and nut J. Agric. Food Chem. 2007, 55, 1337-1346
37. Martins, C.; Pinho, M.; Lordelo, M. M.; Cunha, L. F.; Carvalho, J.; Freire, J. P. B. Effect of brewers grain on intestinal microbial activity and mucosa morphology of weaned piglets Livest. Sci. 2010, 133, 132-134
38. Aura, A.-M.; Härkönen, H.; Fabritius, M.; Poutanen, K. Development of an in vitro enzymic digestion method for removal of starch and protein and assessment of its performance using rye and wheat breads J. Cereal Sci. 1999, 29, 139-152 (Pubitemid 129550027)
39. Funk, C.; Weber, P.; Thilker, J.; Grabber, J. H.; Steinhart, H.; Bunzel, M. Influence of lignification and feruloylation of maize cell walls on the adsorption of heterocyclic aromatic amines J. Agric. Food Chem. 2006, 54, 1860-1867
40. Funk, C.; Braune, A.; Grabber, J. H.; Steinhart, H.; Bunzel, M. Model studies of lignified fiber fermentation by human fecal microbiota and its impact on heterocyclic aromatic amine adsorption Mutat. Res. 2007, 624, 41-48 (Pubitemid 47588293)
41. Vitaglione, P.; Napolitano, A.; Fogliano, V. Cereal dietary fibre: a natural functional ingredient to deliver phenolic compounds into the gut Trends Food Sci. Technol. 2008, 19, 451-463 (Pubitemid 352004153)
42. Dizhbite, T.; Telysheva, G.; Jurkjane, V.; Viesturs, U. Characterization of the radical scavenging activity of lignins-natural antioxidants Bioresour. Technol. 2004, 95, 309-317 (Pubitemid 39013372)
43. Lu, F.; Chu, L.; Gau, R. Free radical-scavenging properties of lignin Nutr. Cancer 1998, 30, 31-38 (Pubitemid 28150519)
44. Aura, A.-M. Microbial metabolism of dietary phenolic compounds in the colon Phytochem. Rev. 2008, 7, 407-429