Complex flavonoids in cocoa: Synthesis and degradation by intestinal microbiota

Journal of Agricultural and Food Chemistry

Volumn 58, Issue 15, 2010, Pages 8879-8886

  Van'T Slot, Gordon ^a   Mattern, Wera ^a   Rzeppa, Sebastian ^a   Grewe, Dagmar ^a   Humpf, Hans Ulrich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

bioavailability; C glycoside; cocoa; degradation; flavan 3 ol; Flavonoids; gastrointestinal tract; intestinal metabolism; microbiota; pig cecum; procyanidin

Indexed keywords

BIOAVAILABILITY; C-GLYCOSIDE; FLAVAN-3-OLS; GASTROINTESTINAL TRACT; INTESTINAL METABOLISM; MICROBIOTAS; PIG CECUM; PROCYANIDINS;

BIOCHEMISTRY; COCOA; DEGRADATION; FOOD PROCESSING; METABOLISM; OLIGOMERS; PHYSIOLOGY; STEREOCHEMISTRY; SUGARS;

FLAVONOIDS;

FLAVONOID; PLANT EXTRACT;

ANIMAL; ARTICLE; BACTERIUM; CACAO; CHEMISTRY; INTESTINE; METABOLISM; MICROBIOLOGY; SWINE; SYNTHESIS;

ANIMALS; BACTERIA; CACAO; FLAVONOIDS; INTESTINES; PLANT EXTRACTS; SWINE;

SUIDAE; THEOBROMA CACAO;

EID: 77955667460     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf1012242     Document Type: Article

References (51)

1. Rice-Evans, C. A.; Miller, N. J.; Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids Free Radical Biol. Med. 1996, 20, 933-956
2. Feng, Y.; McDonald, C. E.; Vick, B. A. C-Glycosylflavones from hard and red spring wheat bran Cereal Chem. 1988, 65, 452-456
3. Colombo, R.; Yariwake, J. H.; Queiroz, E. F.; Ndjoko, K.; Hostettmann, K. On-line identification of further flavone C-and O-glycosides from sugarcane (Saccharum officinarum L., Gramineae) by HPLC-UV-MS Phytochem. Anal. 2006, 17, 337-343
4. Hong, Y. J.; Tomas-Barberan, F. A.; Kader, A. A.; Mitchell, A. E. The flavonoid glycosides and procyanidin composition of Deglet Noor dates (Phoenix dactylifera) J. Agric. Food Chem. 2006, 54, 2405-2411
5. Bramati, L.; Minoggio, M.; Gardana, C.; Simonetti, P.; Mauri, P.; Pietta, P. Quantitative characterization of flavonoid compounds in rooibos tea (Aspalathus linearis) by LC-UV/DAD J. Agric. Food Chem. 2002, 50, 5513-5519
6. Zhou, Z. H.; Zhang, Y. J.; Xu, M.; Yang, C. R. Puerins A and B, two new 8-C substituted flavan-3-ols from pu-er tea J. Agric. Food Chem. 2005, 53, 8614-8617
7. Kashiwada, Y.; Nonaka, G.; Nishioka, I. Tannins and related compounds. XLV. Rhubarb. (5). Isolation and characterization of flavan-3-ol and procyanidin glucosides Chem. Pharm. Bull. 1986, 34, 3208-3222 (Pubitemid 17172384)
8. Stark, T.; Hofmann, T. Application of a molecular sensory science approach to alkalized cocoa (Theobroma cacao): structure determination and sensory activity of nonenzymatically C-glycosylated flavan-3-ols J. Agric. Food Chem. 2006, 54, 9510-9521
9. Rasmussen, S. E.; Frederiksen, H.; Struntze Krogholm, K.; Poulsen, L. Dietary proanthocyanidins: Occurrence, dietary intake, bioavailability, and protection against cardiovascular disease Mol. Nutr. Food Res. 2005, 49, 159-174
10. Spencer, J. P.; Chaudry, F.; Pannala, A. S.; Srai, S. K.; Debnam, E.; Rice-Evans, C. Decomposition of cocoa procyanidins in the gastric milieu Biochem. Biophys. Res. Commun. 2000, 272, 236-241
11. Rios, L. Y.; Bennett, R. N.; Lazarus, S. A.; Remesy, C.; Scalbert, A.; Williamson, G. Cocoa procyanidins are stable during gastric transit in humans Am. J. Clin. Nutr. 2002, 76, 1106-1110
12. Spencer, J. P.; Schroeter, H.; Shenoy, B.; Srai, S. K.; Debnam, E. S.; Rice-Evans, C. Epicatechin is the primary bioavailable form of the procyanidin dimers B2 and B5 after transfer across the small intestine Biochem. Biophys. Res. Commun. 2001, 285, 588-593
13. Németh, K.; Plumb, G. W.; Berrin, J. G.; Juge, N.; Jacob, R.; Naim, H. Y.; Williamson, G.; Swallow, D. M.; Kroon, P. A. Deglycosylation by small intestinal epithelial cell β-glucosidases is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans Eur. J. Nutr. 2003, 42, 29-42
14. Day, A. J.; DuPont, M. S.; Ridley, S.; Rhodes, M.; Rhodes, M. J. C.; Morgan, M. R. A.; Williamson, G. Deglycosylation of flavonoid and isoflavonoid glycosides by human small intestine and liver β-glucosidase activity FEBS Lett. 1998, 436, 71-75
15. +/glucose transporter when expressed in Xenopus laevis oocytes, but effectively inhibit electrogenic glucose uptake J. Pharmacol. Exp. Ther. 2009, 322, 829-835
16. Tian, X. J.; Yang, X. W.; Yang, X.; Wang, K. Studies of intestinal permeability of 36 flavonoids using Caco-2 cell monolayer model Int. J. Pharm. 2009, 367, 58-64
17. Walgren, R. A.; Lin, J. T.; Kinne, R. K.; Walle, T. Cellular uptake of dietary flavonoid quercetin 4′-β-glucoside by sodium-dependent glucose transporter SGLT1 J. Pharmacol. Exp. Ther. 2000, 294, 837-843
18. Courts, F. L.; Williamson, G. The C-glycosyl flavonoid, aspalathin, is absorbed, methylated and glucuronidated intact in humans Mol. Nutr. Food Res. 2009, 53, 1104-1111
19. Baba, S.; Osakabe, N.; Natsume, M.; Terao, J. Absorption and urinary excretion of procyanidin B2 [epicatechin-(4β-8)-epicatechin] in rats Free Radical Biol. Med. 2002, 33, 142-148
20. Donovan, J. L.; Manach, C.; Rios, L. Y.; Morand, C.; Scalbert, A.; Remesy, C. Procyanidins are not bioavailable in rats fed a single meal containing a grapeseed extract or the procyanidin dimer B3 Br. J. Nutr. 2002, 87, 299-306
21. Winter, J.; Moore, L. H.; Dowell, V. R., Jr.; Bokkenheuser, V. D. C-ring cleavage of flavonoids by human intestinal bacteria Appl. Environ. Microbiol. 1989, 55, 1203-1208
22. vanöt Slot, G.; Humpf, H.-U. Degradation of catechin, epigallocatechin-3-gallate (EGCG) and related compounds by the intestinal microbiota in the pig cecum-model J. Agric. Food Chem. 2009, 57, 8041-8048
23. Stoupi, S.; Williamson, G.; Drynan, J. W.; Barron, D.; Clifford, M. N. A comparison of the in vitro biotransformation of (-)-epicatechin and procyanidin B2 by human faecal microbiota Mol. Nutr. Food Res. 2010, 54, 747-759
24. Manach, C.; Scalbert, A.; Morand, C.; Remesy, C.; Jimenez, L. Polyphenols: food sources and bioavailability Am. J. Clin. Nutr. 2004, 79, 727-747
25. Zhang, Y.; Tie, X.; Bao, B.; Wu, X. Metabolism of flavone C-glucosides and p-coumaric acid from antioxidant of bamboo leaves (AOB) in rats Br. J. Nutr. 2007, 97, 484-494
26. Hasslauer, I.; Oehme, A.; Locher, S.; Valotis, A.; vanöt Slot, G.; Humpf, H.-U.; Schreier, P. Biologically relevant flavan-3-ol C-glycosides-preparation and model experiments mimicking their human and intestinal transit. Mol. Nutr. Food Res. 2010, 54, submitted for publication.
27. Labib, S.; Erb, A.; Kraus, M.; Wickert, T.; Richling, E. The pig caecum model: a suitable tool to study the intestinal metabolism of flavonoids Mol. Nutr. Food Res. 2004, 48, 326-332
28. Shoji, T.; Mutsuga, M.; Nakamura, T.; Kanda, T.; Akiyama, H.; Goda, Y. Isolation and structural elucidation of some procyanidins from apple by low-temperature nuclear magnetic resonance J. Agric. Food Chem. 2003, 51, 3806-3813
29. Muranaka, A.; Yoshida, K.; Shoji, T.; Moriichi, N.; Masumoto, S.; Kanda, T.; Ohtake, Y.; Kobayashi, N. Chiral recognition of apple procyanidins by complexation with oxotitanium phthalocyanine Org. Lett. 2006, 8, 2447-2450
30. 13C-nuclear magnetic resonance spectra of procyanidin B-5, epicatechin-(4β8)-epicatechin-(4β6)-epicatechin, and epicatechin-(4β6)-epicatechin-(4β8)-epicatechin-(4β6) -epicatechin Chem. Pharm. Bull. 1992, 40, 889-898
31. Miller, K. B.; Hurst, W. J.; Payne, M. J.; Stuart, D. A.; Apgar, J.; Sweigart, D. S.; Ou, B. Impact of alkalization on the antioxidant and flavanol content of commercial cocoa powders J. Agric. Food Chem. 2008, 56, 8527-8533
32. Fabre, N.; Rustan, I.; de Hoffmann, E.; Quetin-Leclercq, J. Determination of flavone, flavonol, and flavanone aglycones by negative ion liquid chromatography electrospray ion trap mass spectrometry J. Am. Soc. Mass. Spectrom. 2001, 12, 707-715
33. Justesen, U.; Arrigoni, E. Electrospray ionisation mass spectrometric study of degradation products of quercetin, quercetin-3-glucoside and quercetin-3-rhamnoglucoside, produced by in vitro fermentation with human faecal flora Rapid Commun. Mass Spectrom. 2001, 15, 477-483
34. Wu, W.; Liu, Z.; Song, F.; Liu, S. Structural analysis of selected characteristic flavones by electrospray tandem mass spectrometry Anal. Sci. 2004, 20, 1103-1105
35. Kofink, M.; Papagiannopoulos, M.; Galensa, R. (-)-Catechin in cocoa and chocolate: occurrence and analysis of an atypical flavan-3-ol enantiomer Molecules 2007, 12, 1274-1288
36. Sanugul, K.; Akao, T.; Li, Y.; Kakiuchi, N.; Nakamura, N.; Hattori, M. Isolation of a human intestinal bacterium that transforms mangiferin to norathyriol and inducibility of the enzyme that cleaves a C-glucosyl bond. Journal Name 2005, 28, 1672-1678.
37. Yasuda, T.; Kano, Y.; Saito, K.-I.; Ohsawa, K. Urinary and biliary metabolites of puerarin in rats Biol. Pharm. Bull. 1995, 18, 300-303
38. Simons, A. L.; Renouf, M.; Hendrich, S.; Murphy, P. A. Human gut microbial degradation of flavonoids: structure-function relationships J. Agric. Food Chem. 2005, 53, 4258-4263
39. Raab, T.; Barron, D.; Vera, F. A.; Crespy, V.; Oliveira, M.; Williamson, G. Catechin glucosides: occurrence, synthesis, and stability J. Agric. Food Chem. 2010, 58, 2138-2149
40. Kahle, K.; Huemmer, W.; Kempf, M.; Scheppach, W.; Erk, T.; Richling, E. Polyphenols are intensively metabolized in the human gastrointestinal tract after apple juice consumption J. Agric. Food Chem. 2007, 55, 10605-10614
41. Fallingborg, J. Intraluminal pH of the human gastrointestinal tract Dan. Med. Bull. 1999, 46, 183-196
42. Zhu, Q. Y.; Holt, R. R.; Lazarus, S. A.; Ensunsa, J. L.; Hammerstone, J. F.; Schmitz, H. H.; Keen, C. L. Stability of the flavan-3-ols epicatechin and catechin and related dimeric procyanidins derived from cocoa J. Agric. Food Chem. 2002, 50, 1700-1705
43. Depréz, S.; Brezillon, C.; Rabot, S.; Philippe, C.; Mila, I.; Lapierre, C.; Scalbert, A. Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids J. Nutr. 2000, 130, 2733-2738
44. Rechner, A. R.; Kuhnle, G.; Bremner, P.; Hubbard, G. P.; Moore, K. P.; Rice-Evans, C. A. The metabolic fate of dietary polyphenols in humans Free Radical Biol. Med. 2002, 33, 220-235
45. Gniechwitz, D.; Reichardt, N.; Blaut, M.; Steinhart, H.; Bunzel, M. Dietary fiber from coffee beverage: degradation by human fecal microbiota J. Agric. Food Chem. 2007, 55, 6989-6996
46. Appeldoorn, M.; Vincken, J.-P.; Aura, A. M.; Hollman, P. C. H.; Gruppen, H. Procyanidin dimers are metabolized by human microbiota with 2-(3,4-dihydroxyphenyl)-γ-valerolactone as the main metabolites J. Agric. Food Chem. 2009, 57, 1084-1092
47. Falk, P. G.; Hooper, L. V.; Midtvedt, T.; Gordon, J. I. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology Microbiol. Mol. Biol. Rev. 1998, 62, 1157-1170
48. Dicksved, J.; Floistrup, H.; Bergstrom, A.; Rosenquist, M.; Pershagen, G.; Scheynius, A.; Roos, S.; Alm, J. S.; Engstrand, L.; Braun-Fahrlander, C.; von Mutius, E.; Jansson, J. K. Molecular fingerprinting of the fecal microbiota of children raised according to different lifestyles Appl. Environ. Microbiol. 2007, 73, 2284-2289
49. de Freitas, V.; Mateus, N. Structural features of procyanidin interactions with salivary proteins J. Agric. Food Chem. 2001, 49, 940-945
50. Meselhy, M. R.; Nakamura, N.; Hattori, M. Biotransformation of (-)-epicatechin 3-O-gallate by human intestinal bacteria Chem. Pharm. Bull. 1997, 45, 888-893
51. Groenewoud, G.; Hundt, H. K. The microbial metabolism of (+)-catechin to two novel diarylpropan-2-ol metabolites in vitro Xenobiotica 1984, 14, 711-717