Bioavailability of dietary monomeric and polymeric flavan-3-ols

Flavonoids and Related Compounds: Bioavailability and Function

Volumn , Issue , 2012, Pages 45-78

  Crozier, Alan ^a   Clifford, Michael N ^b   Rio, Daniele Del ^c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

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EID: 84884887688     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (110)

1. Appeldoom, M.M., Vincken, J.-P., Aura, A.-M. et al. (2009). Procyanidin dimers are metabolized by human microbiota with 2-(3,4-dihydroxyphenyl)acetic acid and 5-(3,4-dihydroxyphenyl)-γ-valerolactone as the major metabolites. J. Agric. Food Chem., 57, 1084-1092.
2. Aron, P.M. and Kennedy, J.A. (2008). Flavan-3-ols: Nature, occurrence and biological activity. Mol. Nutr. Food Res., 52, 79-104.
3. Auger, C., Al Awwadi, N., Bornet, A. et al. (2004). Catechins and procyanidins in Mediterranean diets. Food Res. Int., 37, 233-245.
4. Auger, C., Hara, Y., and Crozier, A. (2008). Bioavailability of Polyphenon E flavan-3-ols in humans with an ileostomy. J. Nutr., 138, 1535S-1542S.
5. Baba, S., Osakabe, N., Yasuda, A. et al. (2000). Bioavailability of (-)-epicatechin upon intake of chocolate and cocoa in human volunteers. Free Rad. Res., 33, 635-641.
6. Bartolomè, B., Monagas, M., Garrido, I. et al. (2010). Almond (Prunus dulcis [Mill.] D.A. Webb) polyphenols: From chemical characterization to targeted analysis of phenolic metabolites in humans. Arch. Biochem. Biophys., 501, 124-133.
7. Borges, G., Mullen, W., Mullan, A. et al. (2010). Bioavailability of multiple components following acute ingestion of a polyphenol-rich juice drink. Mol. Nutr. Food Res. 54, S268-277.
8. Bridges, J.W., French, M.R., Smith, R.L. et al. (1970). The fate of benzoic acid in various species. Biochem. J., 118, 47-51.
9. Chow, H.H., Cai, Y., Alberts, D.S. et al. (2001). Phase I pharmacokinetic study of tea polyphenols following single-dose administration of epigallocatechin gallate and Polyphenon E. Cancer Epidemiol. Biomarkers Prev., 10, 53-58.
10. Clifford, M.N. (2004). Diet-derived phenols in plasma and tissues and their implications for health. Planta Med., 12, 1103-1114.
11. Clifford, M.N. and Brown, J.E. (2006). Dietary flavonoids and health-broadening the perspective. In O. Andersen and K.R. Markham (eds.), Flavonoids: Chemistry, Biochemistry and Applications. CRC Press, Boca Raton, FL, pp. 320-370.
12. Clifford, M.N. and Crozier, A. (2011). Phytochemicals in teas and tisanes and their bioavailability. In A. Crozier, H. Ashihara, and F. Tomás-Barberán (eds.), Teas, Cocoa and Coffee. Blackwell Publishing, Oxford, pp. 45-98.
13. Clifford, M.N., Copeland, E.L., Bloxsidge, J.P. et al. (2000). Hippuric acid as a major excretion product associated with black tea consumption. Xenobiotica, 30, 317-326.
14. Corder, R. (2008). Red wine, chocolate and vascular health: Developing the evidence base. Heart, 94, 821-823.
15. Crozier, A., Jaganath, I.B., and Clifford, M.N. (2006). Phenols, polyphenols and tannins: An overview. In A. Crozier, M.N. Clifford, H. Ashihara (eds.), Plant Secondary Metabolites:Occurrence, Structure and Role in the Human Diet. Blackwell Publishing, Oxford, pp. 1-24.
16. Crozier, A., Del Rio, D., and Clifford, M.N. (2010). Bioavailability of dietary flavonoids and phenolic compounds. Mol. Aspects Med., 31, 446-67.
17. Crozier, A., Jaganath, I.B., and Clifford, M.N. (2009). Dietary phenolics: Chemistry, bioavailability and effects on health. Nat. Prod. Rep., 26, 1001-1043.
18. Day, A.J., Mellon, F., Barron, D. et al. (2001). Human metabolites of dietary flavonoids:Identification of plasma metabolites of quercetin. Free Rad. Res. 35, 941-952.
19. Day, A.J. and Morgan M.R.A. (2003). Methods of polyphenol extraction from biological fluids and tissues. In C. Santos-Buelga and G. Williamson (eds.), Methods in Polyphenol Analysis. Royal Society of Chemistry, Cambridge, pp. 17-47.
20. Daykin, C.A., Van Duynhoven, J.P., Groenewegen, A. et al. (2005). Nuclear magnetic resonance spectroscopic based studies of the metabolism of black tea polyphenols in humans. J Agric. Food Chem., 53, 1428-1434.
21. Del Rio, D., Stewart, A.J., Mullen, W. et al. (2004). HPLC-MSn analysis of phenolic compounds and purine alkaloids in green and black tea. J. Agric. Food Chem. 52, 2807-2815.
22. Del Rio, D., Calani, L., Cordero, C. et al. (2010). Bioavailability and catabolism of green tea flavan-3-ols in humans. Nutrition, 11/12, 1110-1116.
23. Del Rio, D., Calani, L., Dall’Asta, M. et al. (2011). Polyphenolic composition of hazelnut skins. J. Agric. Food Chem., 59, 9935-9941.
24. Déprez, S., Brezillon, C., Rabot, S. et al. (2000). Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J. Nutr., 130, 2733-2738.
25. Donovan, J.L., Manach, C., Rios, L. et al. (2002). Procyanidins are not bioavailable in rats fed a single meal containing a grape seed extract or the procyanidin dimer B3. Br. J. Nutr., 87, 299-306.
26. Donovan, J.L., Crespy, V., Oliveira, M. et al. (2006a). (+)-Catechin is more bioavailable then (-)-catechin: Relevance to the bioavailability of catechin from cocoa. Free Rad. Res., 40, 1029-1034.
27. Donovan, J.L., Manach, C., Faulks, R.M. et al. (2006b). Absorption and metabolism of dietary secondary metabolites. In A. Crozier, M.N. Clifford, and H. Ashihara (eds.), Plant Secondary Metabolites. Occurrence, Structure and Role in the Human Diet. Blackwell Publishing, Oxford, pp. 303-351.
28. Drynan, J.W., Clifford, M.N., Obuchowicz, J. et al. (2010). The chemistry of low molecular weight black tea polyphenols. Nat. Prod. Rep. 27, 417-462.
29. Espín, J.C., García-Conesa, M.T., and Tomás-Barberán, F.A. (2007). Nutraceuticals: Facts and fiction. Phytochemistry, 68, 2986-3008.
30. Gonthier, M.P., Donovan, J.L., Texier, O. et al. (2003). Metabolism of dietary procyanidins in rats. Free Rad. Biol. Med., 35, 837-844.
31. Gosnay, S.L., Bishop, J.A., New, S.A. et al. (2002). Estimation of the mean intakes of fourteen classes of dietary phenolics in a population of young British women aged 20-30 years. Proc. Nutr. Soc., 61, 125A.
32. Gossai, D. and Lau-Cam, C.A. (2009). Assessment of the effect of type of dairy product and chocolate matrix on the oral absorption of momomeric chocolate flavanols in a small animal model. Pharmazie, 64, 202-209.
33. Goto, K., Kanaya, S., Nishikawa, T. et al. (1998). The influence of tea catechins on fecal flora of elderly residents in long-term care facilities. Ann. Long-Term Care, 6, 43-48.
34. Green, R.J., Murphy, A.S., Schulz, B. et al. (2007). Common tea formulations modulate in vitro digestive recovery of green tea catechins. Mol. Nutr. Food Res., 51, 1152-1162.
35. Grumer, H.D. (1961). Formation of hippuric acid from phenylalanine labelled with carbon-14 in phenylketonuric subjects. Nature, 189, 63-64.
36. Gu, L., Kelm, M.A., Hammerstone, J.F. et al. (2004). Concentrations of proanthocyanidins in common foods and estimations of normal consumption. J. Nutr., 134, 613-617.
37. Gu, L., Laly, M., Chang, H.C. et al. (2005). Isoflavone conjugates are underestimated in tissues using enzymatic hydrolysis. J. Agric. Food Chem., 53, 6858-6863.
38. Hammerstone, J.F., Lazarus, S.A., Mitchell, A.E. et al. (1999). Identification of procyanidins in cocoa (Theobroma cocao) and chocolate using high-performance liquid chromatography/mass spectrometry. J. Agric. Food Chem., 47, 490-496.
39. Haslam, E. (1998). Practical Polyphenolics. From Structure to Molecular Recognition and Physiological Action. Cambridge University Press, Cambridge.
40. Henning, S.M., Niu, Y., Lee, N.H. et al. (2004). Bioavailability and antioxidant activity of tea flavanols after consumption of green tea, black tea, or a green tea extract supplement. Am. J. Clin. Nutr., 80, 1558-1564.
41. Ho, Y., Lee, Y.-L., and Hsu, K.-Y. (1995). Determination of (+)-catechin in plasma by highperformance liquid chromatography using fluorescence detection. J. Chromatogr. B, 665, 383-389.
42. Hodgson, J.M., Morton, L.W., Puddey, I.B. et al. (2000). Gallic acid metabolites are markers of black tea intake in humans. J. Agric. Food Chem., 48, 2276-2280.
43. Hodgson, J.M., Chan, S.Y., Puddey, I.B. et al. (2004). Phenolic acid metabolites as biomarkers for tea- and coffee-derived polyphenol exposure in human subjects. Br. J. Nutr., 91, 301-306.
44. Holt, R.R., Lazarus, S.A., Sullards, M.C. et al. (2002). Procyanidin dimer B2 [epicatechin- (4β-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am. J. Clin. Nutr., 76, 798-804.
45. Kahle, K., Huemmer, W., Kempf, M. et al. (2007). Polyphenols are extensively metabolized in the human gastrointestinal tract after apple juice consumption. J. Agric Food Chem., 55, 10695-10614.
46. Keogh, J.B., McInerney, J., and Clifton P.M. (2007). The effect of milk protein on the bioavailability of cocoa polyphenols. J. Food Sci., 72, S230-233.
47. Kida, T., Suzuki, Y., Matsumoto, N. et al. (2000). Identification of biliary metabolites of (-)-epigallocatechin gallate in rats. J. Agric. Food Chem., 48, 4151-4155.
48. Knight, S. (2004). Metabolism of Dietary Polyphenols by Gut Flora. PhD Dissertation, University of Surrey, UK.
49. Kohri, T., Nanjo, F., Suziki, M. et al. (2001). Synthesis of (-)-[4-3H]epigallocatechin gallate and its metabolic fate in rats after intravenous administration. J. Agric. Food Chem., 49, 1042-1048.
50. Kuhnert, N., Clifford, M.N., and Muller, A. (2010a). Oxidative cascade reactions yielding polyhydroxy-theaflavins and theacitrins in the formation of black tea thearubigins:Evidence by tandem LC MS. Food Funct., 1, 180-199.
51. Kuhnert, N., Drynan, J.W., Obuchowicz, J. et al. (2010b). Mass spectrometric characterization of black tea thearubigins leading to an oxidative cascade hypothesis for thearubigin formation. Rapid Commun. Mass Spectrom., 24, 3387-3404.
52. Kutschera, M., Engst, W., Blaut, M. et al. (2011). Isolation of catechin-converting human intestinal bacteria. J. Appl. Microbiol. 111, 165-175.
53. Kyle, J.A., Morrice, P.C., McNeill, G. et al. (2007). Effects of infusion time and addition of milk on content and absorption of polyphenols from black tea. J. Agric. Food Chem., 55, 4889-4894.
54. Li, C., Lee, M.J., Sheng, S. et al. (2000). Structural identification of two metabolites of catechins and their kinetics in human urine and blood after tea ingestion. Chem. Res. Toxicol., 3, 177-184.
55. Li, M., Wang, B., Zhang, M. et al. (2008). Symbiotic gut microbes modulate human metabolic phenotypes. Proc. Natl. Acad. Sci. USA, 105, 2117-2122.
56. Luck, G. Liao, H., Murray, N.J. et al. (1994). Polyphenols, astringency and proline-rich proteins. Phytochem. 37, 357-371.
57. Manach, C., Williamson, G., Morand, C. et al. (2005). Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr., 81, 230S-242S.
58. Meng, X., Sang, S., Zhu, N. et al. (2002). Identification and characterization of methylated and ring-fission metabolites of tea catechins formed in humans, mice, and rats. Chem. Res. Toxicol., 15, 1042-1050.
59. Miller, K, B., Hurst, W.J., Payne, M.J. et al. (2008). Impact of alkalization on the antioxidant and flavanol content of commercial cocoa powders. J. Agric. Food Chem., 56, 8527-8533.
60. Mulder, T.P., van Platerink, C.J., Wijnand Schuyl, P.J. et al. (2001). Analysis of theaflavins in biological fluids using liquid chromatography-electrospray mass spectrometry. J. Chromatogr. B, 760, 271-279.
61. Mulder, T.P., Rietveld, A.G., and van Amelsvoort, J.M. (2005). Consumption of both black tea and green tea results in an increase in the excretion of hippuric acid into urine. Am. J. Clin. Nutr., 81, 256S-260S.
62. Mullen, W., Borges, G., Donovan, J. L. et al. (2009). Milk decreases urinary excretion but not plasma pharmacokinetics of cocoa flavan-3-ol metabolites in humans. Am. J Clin. Nutr., 89, 1784-1791.
63. Neilson, A.P., George, J.C., Janle, E.M. et al. (2009). Influence of chocolate matrix composition of cocoa flavan-3-ol bioaccessibility in vitro and bioavailability in humans. J. Agric. Food. Chem., 57, 9418-9426.
64. Neilson, A.P., Sapper, T.N., Janle, E.M. et al. (2010). Chocolate matrix factors modulate the pharmacokinetic behaviour of cocoa flavan-3-ol phase II metabolites following oral consumption by Sprague-Dawley rats. J. Agric. Food Chem., 58, 6685-6691.
65. Ottaviani, J.I., Momma, T.Y., Heiss, C. et al. (2011). The sterochemical configuration of flavanols influences the level and metabolism of flavanols in humans and their biological activity in vivo. Free Rad. Biol. Med., 50, 237-244.
66. Record, I.R. and Lane, J.M. (2001). Simulated intestinal digestion of green and black teas. Food Chem., 73, 481-486.
67. Reeve, D.R. and Crozier, A. (1980). Quantitative analysis of plant hormones. In J. MacMillan, ed., Hormonal Regulation of Development 1. Molecular Aspects of Plant Hormones. Encyclopedia of Plant Physiology New Series, Vol. 9, Springer-Verlag, Heidelberg, pp. 203-280.
68. Rein, D., Lotito, S., Holt, R.R. et al. (2000). Epicatechin in plasma: In vivo determination and effect of chocolate consumption on plasma oxidative status. J. Nut., 130, 2109S-2114S.
69. Richelle, M., Tavazzi, I., Enslen, M. et al. (1999). Plasma kinetics in man of epicatechin from black chocolate. Eur. J. Clin. Nut. 53, 22-26.
70. Rios, L.Y., Bennett, R.N., Lazarus, S.A. et al. (2002). Cocoa procyanidins are stable during gastric transit in humans. Am. J. Clin. Nut., 76, 1106-1110.
71. Rios, L.Y., Gonthier, M.P., Remesy, C. et al. (2003). Chocolate intake increases urinary excretion of polyphenol-derived phenolic acids in healthy human subjects. Am. J. Clin. Nutr., 77, 912-918.
72. Roowi, S., Stalmach, A., Mullen, W. et al. (2010). Green tea flavan-3-ols: Colonic degradation and urinary excretion of catabolites by humans. J. Agric. Food Chem., 58, 1296-1304.
73. Roura, E., Andrés-Lacueva, C., Jáuregui, O. et al. (2005). Rapid liquid chromatography tandem mass spectrometer assay to quantify plasma (-)-epicatechin metabolites after ingestion of a standard portion of cocoa beverage in humans. J. Agric. Food Chem., 53, 6190-6194.
74. Roura, E., Almajano, M.P., Mata-Bilbao, M.L. et al. (2007a). Human urine: Epicatechin metabolites and antioxidant activity after cocoa intake. Free Rad. Res., 41, 943-949.
75. Roura, E., Andés-Lacueva, C., Estruch, R. et al. (2007b). Milk does not affect the bioavailability of cocoa powder flavonoid in healthy human. Ann. Nutr. Metab., 51, 493-498.
76. Roura, E., Andrés-Lacueva, C., Estruch, R. et al. (2008). The effects of milk as a food matrix for polyphenols on the excretion profile of cocoa (-)-epicatechin metabolites in healthy human subjects. Br. J. Nut., 100, 846-851.
77. Sang, S., Lee, M.J., Yang, I. et al. (2008). Human urinary metabolite profile of tea polyphenols analyzed by liquid chromatography/electrospray ionization tandem mass spectrometry with data-dependent acquisition. Rapid Comm. Mass Spectrom., 22, 1567-1578.
78. Schroeter, H., Holt, R.R., Orozco, T.J. et al. (2003). Milk and absorption of dietary flavanols. Nature, 426, 787-788.
79. Self, H.L., Brown, R.R., and Price, J.M. (1960). Quantitative studies on the metabolites of tryptophan in the urine of swine. J. Nutr., 70, 21-25.
80. Serafini, M., Ghiselli, A., and Ferro-Luzzi, A. (1996). In vivo antioxidant effect of green and black tea in man. Eur. J. Clin. Nutr., 50, 28-32.
81. Serafini, M., Bugianesi, R., Maiaini, G. et al. (2003). Plasma antioxidants from chocolate. Nature 424, 1013.
82. Seto, R., Nakamura, H., Nanjo, F. et al. (1997). Preparation of epimers of tea catechins by heat treatment. Biosci. Biotechnol. Biochem., 61, 1434-1439.
83. Shahrzad, S. and Bitsch, I. (1998). Determination of gallic acid and its metabolites in human plasma and urine by high-performance liquid chromatography. J. Chromatogr. B, 705, 87-95.
84. Shahrzad, S., Aoyagi, K., Winter, A. et al. (2001). Pharmacokinetics of gallic acid and its relative bioavailability from tea in healthy humans. J. Nutr. 131, 1207-1210.
85. Shoji, T., Masumoto, S., Moriichi, N. et al. (2006). Apple procyanidin oligomers absorption in rats after oral administration: Analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. J. Agric. Food Chem., 54, 884-892.
86. Spencer, J.P., Chaudry, F., Pannala, A.S. et al. (2000). Decomposition of cocoa procyanidins in the gastric milieu. Biochem. Biophys. Res. Commun., 272, 236-241.
87. Stalmach, A., Troufflard, S., Serafini M. et al. (2009). Absorption, metabolism and excretion of Choladi green tea flavan-3-ols by humans. Mol. Nutr. Food Res., 53, S44-S53.
88. Stalmach, A., Mullen, W., Steiling, H. et al. (2010). Absorption, metabolism, efflux and excretion of green tea flavan-3-ols in humans with an ileostomy. Mol. Nutr. Food Res., 54, 323-334.
89. Stoupi, S. (2010). In Vitro and In Vivo Metabolic Studies of Dietary Flavan-3-ols. PhD Dissertation, University of Surrey, UK.
90. Stoupi, S., Williamson, G., Drynan, J.W. et al. (2010a). Procyanidin B2 catabolism by human fecal microflora: Partial characterization of ‘dimeric’ intermediates. Arch. Biochem. Biophys., 501, 73-78.
91. Stoupi, S., Williamson, G., Drynan, J.W. et al. (2010b). A comparison of the in vitro biotransformation of (-)-epicatechin and procyanidin B2 by human faecal microbiota. Mol. Nutr. Food Res., 54, 747-759.
92. Stoupi, S., Williamson, G., Viton, F. et al. (2010c). In vivo bioavailability, absorption, excretion, and pharmacokinetics of [14C]procyanidin B2 in male rats. Drug Met. Disp., 38, 287-291.
93. Tomás-Barberán, F.A., Cienfuegos-Jovellanos, E., Marín, A. et al. (2007). A new process to develop a cocoa powder with higher flavonoid monomer content and enhanced bioavailability in healthy humans. J. Agric. Food Chem., 55, 3926-3935.
94. Tsang, C., Auger, C., Mullen, W. et al. (2005). The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br. J. Nutr., 94, 170-181.
95. Turnbaugh, P.J and Gordon, J.I. (2008). An invitation to the marriage of metagenomics and metabolomics. Cell, 134, 708-713.
96. Tzounis, X., Vulevic, J., Kuhnle, G.G. et al. (2008). Flavanol monomer-induced changes to the human faecal microflora. Br. J. Nutr., 99, 782-792.
97. Tzounis, X., Rodriguez-Mateos, A., Vulevic, J. et al. (2011). Prebiotic evaluation of cocoaderived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am. J. Clin. Nutr., 93, 62-72.
98. Urpi-Sarda, M., Monagas, M., Khan, N. et al. (2009). Epicatechin, procyanidins and phenolic microbial metabolites after cocoa intake in humans and rats. Anal. Bioanal. Chem., 394, 1545-1556.
99. Urpi-Sarda, M., Llorach, R., Khan, N. et al. (2010). Effect of milk on the urinary excretion of microbial phenolic acid after cocoa powder consumption in humans. J. Agric. Food Chem., 58, 4706-4711.
100. Unno, T., Kondo, K., Itakura, H. et al. (1996). Analysis of (-)-epigallocatechin gallate in human serum obtained after ingesting green tea. Biosci. Biotechnol. Biochem., 60, 2066-2068.
101. van Duynhoven, J., Vaughan, E.E., Jacobs, D.M. et al. (2011). Metabolic fate of polyphenols in the human superorganism. Proc. Natl. Acad. Sci. USA, 108 (Suppl. 1), 4531-4538.
102. van het Hof, K.H., Kivits, G.A., Weststrate, J.A. et al. (1998). Bioavailability of catechins from tea: The effect of milk. Eur. J. Clin. Nutr., 52, 356-359.
103. Vega, C. and Grover, M.K. (2011). Physico-chemical properties of acidified skim milk gels containing cocoa flavanols. J. Agric. Food Chem., 59, 6740-6747.
104. Walle, T, Hsieh, F., De Legge, M.H. et al. (2004). High absorption but very low bioavailability of oral resveratrol in humans. Drug Met. Disp., 32, 1377-1382.
105. Wang, J.F., Schramm, D.D., Holt, R.R. et al. (2000). A dose-response effect from chocolate consumption on plasma epicatechin and oxidative damage. J. Nutr., 130, 2115S-2119S.
106. Ward, N.C, Croft, K.D., Puddey, I.B. et al. (2004). Supplementation with grape seed polyphenols results in increased urinary excretion of 3-hydroxyphenylpropionic acid, an important metabolite of proanthocyanidins in humans. J. Agric. Food Chem. 52, 5545-5549.
107. Williamson G, Clifford MN. (2010). Colonic metabolites of berry polyphenols: The missing link to biological activity? Br. J. Nutr., 104, S48-S66.
108. Woods, E., Clifford M.N., Gibbs, M. et al. (2003). Estimation of mean intakes of 14 classes of dietary phenols in a population of male shift workers. Proc. Nutr. Soc. 62, 60A.
109. Yoshino, K., Suzuki, M., Sasaki, K. et al. (1999). Formation of antioxidants from (-)-epigallocatechin gallate in mild alkaline fluids, such as authentic intestinal juice and mouse plasma. J. Nutr. Biochem., 10, 223-229.
110. Zhu, Q.A., Zhang, A. Tsang, D. et al. (1997). Stability of green tea catechins. J. Agric. Food Chem., 45, 4624-4628.