Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study

American Journal of Clinical Nutrition

Volumn 93, Issue 1, 2011, Pages 62-72

  Tzounis, Xenofon ^a   Rodriguez Mateos, Ana ^a   Vulevic, Jelena ^a   Gibson, Glenn R ^a   Kwik Uribe, Catherine ^b   Spencer, Jeremy P E ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b MARS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; FLAVANOL DERIVATIVE; PREBIOTIC AGENT; TRIACYLGLYCEROL;

ADULT; ARTICLE; BACTERIAL COUNT; BIFIDOBACTERIACEAE; CACAO; CLOSTRIDIUM; CROSSOVER PROCEDURE; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; FECES ANALYSIS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN EXPERIMENT; INTERVENTION STUDY; LACTOBACILLUS; MALE; NORMAL HUMAN; RANDOMIZED CONTROLLED TRIAL; TRIACYLGLYCEROL BLOOD LEVEL;

ADULT; ANTIOXIDANTS; BIFIDOBACTERIUM; BIOLOGICAL MARKERS; BLOOD PRESSURE; C-REACTIVE PROTEIN; CACAO; CROSS-OVER STUDIES; DIET; DOUBLE-BLIND METHOD; FECES; FEMALE; FLAVONOIDS; HUMANS; LACTOBACILLUS; MALE; PREBIOTICS;

BACTERIA (MICROORGANISMS); CLOSTRIDIA; THEOBROMA CACAO;

EID: 78651309432     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.110.000075     Document Type: Article

References (55)

1. Eyre H, Kahn R, Robertson RM, et al. Preventing cancer, cardiovascular disease, and diabetes: a common agenda for the American Cancer Society, the American Diabetes Association, and the American Heart Association. Stroke 2004;35:1999-2010.
2. Hertog MG, Feskens EJ, Hollman PC, Katan MB, Kromhout D. Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly Study. Lancet 1993;342:1007-11.
3. Hertog MG, Feskens EJ, Kromhout D. Antioxidant flavonols and coronary heart disease risk. Lancet 1997;349:699.
4. Knekt P, Kumpulainen J, Jarvinen R, et al. Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 2002;76:560-8.
5. Gu L, Kelm MA, Hammerstone JF, et al. Concentrations of proanthocyanidins in common foods and estimations of normal consumption. J Nutr 2004;134:613-7.
6. Lazarus SA, Hammerstone JF, Schmitz HH. Chocolate contains additional flavonoids not found in tea. Lancet 1999;354:1825.
7. Kondo K, Hirano R, Matsumoto A, Igarashi O, Itakura H. Inhibition of LDL oxidation by cocoa. Lancet 1996;348:1514.
8. Holt RR, Schramm DD, Keen CL, Lazarus SA, Schmitz HH. Chocolate consumption and platelet function. JAMA 2002;287:2212-3.
9. Grassi D, Necozione S, Lippi C, et al. Cocoa reduces blood pressure and insulin resistance and improves endothelium-dependent vasodilation in hypertensives. Hypertension 2005;46:398-405.
10. Heiss C, Finis D, Kleinbongard P, et al. Sustained increase in flow-mediated dilation after daily intake of high-flavanol cocoa drink over 1 week. J Cardiovasc Pharmacol 2007;49:74-80.
11. Balzer J, Rassaf T, Heiss C, et al. Sustained benefits in vascular function through flavanol-containing cocoa in medicated diabetic patients a double-masked, randomized, controlled trial. J Am Coll Cardiol 2008;51:2141-9.
12. Schroeter H, Heiss C, Balzer J, et al. (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc Natl Acad Sci USA 2006;103:1024-9.
13. Heiss C, Jahn S, Taylor M, et al. Improvement of endothelial function with dietary flavanols is associated with mobilization of circulating angiogenic cells in patients with coronary artery disease. J Am Coll Cardiol 2010;56:218-24.
14. Holt RR, Lazarus SA, Sullards MC, et al. Procyanidin dimer B2 [epicatechin-(4β-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am J Clin Nutr 2002;76:798-804.
15. Robbins RJ, Leonczak J, Johnson JC, et al. Method performance and multi-laboratory assessment of a normal phase high pressure liquid chromatography-fluorescence detection method for the quantitation of flavanols and procyanidins in cocoa and chocolate containing samples. J Chromatogr A 2009;1216:4831-40.
16. Keen CL, Holt RR, Oteiza PI, Fraga CG, Schmitz HH. Cocoa antioxidants and cardiovascular health. Am J Clin Nutr 2005;81(suppl):298S-303S.
17. Saulnier DM, Kolida S, Gibson GR. Microbiology of the human intestinal tract and approaches for its dietary modulation. Curr Pharm Des 2009;15:1403-14.
18. Gibson GR. Dietary modulation of the human gut microflora using prebiotics. Br J Nutr 1998;80:S209-12.
19. Collins MD, Gibson GR. Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 1999;69:1052S-7S.
20. Gibson GR, Fuller R. Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J Nutr 2000;130(2S suppl):391S-5S.
21. Macfarlane GT, Steed H, Macfarlane S. Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J Appl Microbiol 2008;104:305-44.
22. Burcelin R, Luche E, Serino M, Amar J. The gut microbiota ecology: a new opportunity for the treatment of metabolic diseases? Front Biosci 2009;14:5107-17.
23. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 2009;15:1546-58.
24. Kelly D, Conway S. Bacterial modulation of mucosal innate immunity. Mol Immunol 2005;42:895-901.
25. Tzounis X, Vulevic J, Kuhnle GG, et al. Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr 2008;99:782-92.
26. Lee HC, Jenner AM, Low CS, Lee YK. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res Microbiol 2006;157:876-84.
27. Klinder A, Karlsson PC, Clune Y, et al. Fecal water as a non-invasive biomarker in nutritional intervention: comparison of preparation methods and refinement of different endpoints. Nutr Cancer 2007;57:158-67.
28. Burns AJ, Rowland IR. Antigenotoxicity of probiotics and prebiotics on faecal water-induced DNA damage in human colon adenocarcinoma cells. Mutat Res 2004;551:233-43.
29. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 1995;108:975-82.
30. Clavel T, Fallani M, Lepage P, et al. Isoflavones and functional foods alter the dominant intestinal microbiota in postmenopausal women. J Nutr 2005;135:2786-92.
31. O'Sullivan L, Ross RP, Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie 2002;84:593-604.
32. Pompei A, Cordisco L, Amaretti A, Zanoni S, Matteuzzi D, Rossi M. Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol 2007;73:179-85.
33. Tahri K, Crociani J, Ballongue J, Schneider F. Effects of three strains of bifidobacteria on cholesterol. Lett Appl Microbiol 1995;21:149-51.
34. Corthesy B, Gaskins HR, Mercenier A. Cross-talk between probiotic bacteria and the host immune system. J Nutr 2007;137(suppl 2):781S-90S.
35. Kelly D, Conway S, Aminov R. Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol 2005;26:326-33.
36. Hage FG, Szalai AJ. C-reactive protein gene polymorphisms, C-reactive protein blood levels, and cardiovascular disease risk. J Am Coll Cardiol 2007;50:1115-22.
37. Ridker PM, Cook NR. Biomarkers for prediction of cardiovascular events. N Engl J Med 2007;356:1472-3.
38. Ridker PM. C-reactive protein and the prediction of cardiovascular events among those at intermediate risk: moving an inflammatory hypothesis toward consensus. J Am Coll Cardiol 2007;49:2129-38.
39. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet 2003;361:512-9.
40. Murphy KJ, Chronopoulos AK, Singh I, et al. Dietary flavanols and procyanidin oligomers from cocoa (Theobroma cacao) inhibit platelet function. Am J Clin Nutr 2003;77:1466-73.
41. Deprez S, Brezillon C, Rabot S, et al. Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J Nutr 2000;130:2733-8.
42. Stoupi S, Williamson G, Drynan JW, Barron D, Clifford MN. A comparison of the in vitro biotransformation of (-)-epicatechin and procyanidin B2 by human faecal microbiota. Mol Nutr Food Res 2010;54:747-59.
43. Stoupi S, Williamson G, Drynan JW, Barron D, Clifford MN. Procyanidin B2 catabolism by human fecal microflora: partial characterization of 'dimeric' intermediates. Arch Biochem Biophys 2010;501:73-8.
44. Lee SYH, Munerol B, Pollard S, et al. The reaction of flavanols with nitrous acid protects against N-nitrosamine formation and leads to the formation of nitroso derivatives which inhibit cancer cell growth. Free Radic Biol Med 2006;40:323-34.
45. Taubert D, Roesen R, Lehmann C, Jung N, Schomig E. Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial. JAMA 2007;298:49-60.
46. Delzenne NM, Kok N. Effects of fructans-type prebiotics on lipid metabolism. Am J Clin Nutr 2001;73(suppl):456S-8S.
47. Delzenne NM, Williams CM. Prebiotics and lipid metabolism. Curr Opin Lipidol 2002;13:61-7.
48. Trautwein EA, Rieckhoff D, Erbersdobler HF. Dietary inulin lowers plasma cholesterol and triacylglycerol and alters biliary bile acid profile in hamster. J Nutr 1998;128:1937-43.
49. Monagas M, Khan N, Andres-Lacueva C, et al. Effect of cocoa powder on the modulation of inflammatory biomarkers in patients at high risk of cardiovascular disease. Am J Clin Nutr 2009;90:1144-50.
50. Wan Y, Vinson JA, Etherton TD, Proch J, Lazarus SA, Kris-Etherton PM. Effects of cocoa powder and dark chocolate on LDL oxidative susceptibility and prostaglandin concentrations in humans. Am J Clin Nutr 2001;74:596-602.
51. Wang-Polagruto JF, Villablanca AC, Polagruto JA, et al. Chronic consumption of flavanol-rich cocoa improves endothelial function and decreases vascular cell adhesion molecule in hypercholesterolemic postmenopausal women. J Cardiovasc Pharmacol 2006;47(suppl 2):S177-86.
52. Probert HM, Gibson GR. Investigating the prebiotic and gas-generating effects of selected carbohydrates on the human colonic microflora. Lett Appl Microbiol 2002;35:473-80.
53. Rycroft CE, Jones MR, Gibson GR, Rastall RA. A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol 2001;91:878-87.
54. Tuohy KM, Kolida S, Lustenberger AM, Gibson GR. The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides-a human volunteer study. Br J Nutr 2001;86:341-8.
55. Langlands SJ, Hopkins MJ, Coleman N, Cummings JH. Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 2004;53:1610-6.