Modulation of metabolic syndrome-related inflammation by cocoa

Molecular Nutrition and Food Research

Volumn 57, Issue 6, 2013, Pages 948-961

  Gu, Yeyi ^a   Lambert, Joshua D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Cocoa; Inflammation; Metabolic syndrome; Polyphenols; Proanthocyanidins

Indexed keywords

ANTIINFLAMMATORY AGENT;

ANIMAL; CACAO; CELL CULTURE; CHEMISTRY; DIET THERAPY; DRUG SCREENING; HUMAN; INFLAMMATION; METABOLIC SYNDROME X; REVIEW;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CACAO; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; HUMANS; INFLAMMATION; METABOLIC SYNDROME X;

ANIMALIA; MALVACEAE; THEOBROMA CACAO;

EID: 84878912355     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200837     Document Type: Review

References (99)

1. Cocoa Market Updates. 2012. The World Cocoa Foundation. Available from: http://worldcocoafoundation.org/wp-content/uploads/Cocoa-Market-Update-as-of-3.20.2012.pdf
2. O'Neil, C. E., Fulgoni, V. L., Nicklas, T. A., Candy consumption was not associated with body weight measures, risk factors for cardiovascular disease, or metabolic syndrome in US adults: NHANES 1999-2004. Nutr. Res. 2011, 31, 122-130.
3. Hii, C. L., Law, C. L., Suzannah, S., Misnawi, Cloke. M., Polyphenols in cocoa (Theobroma cacao L.). As. J. Food Ag-Ind. 2010, 2, 702-722.
4. Wollgast, J., Pallaroni, L., Agazzi, M. E., Anklam, E., Analysis of procyanidins in chocolate by reversed-phase high-performance liquid chromatography with electrospray ionisation mass spectrometric and tandem mass spectrometric detection. J. Chromatogr. A 2001, 926, 211-220.
5. Hammerstone, J. F., Lazarus, S. A., Mitchell, A. E., Rucker, R. et al., Identification of procyanidins in cocoa (Theobroma cacao) and chocolate using high-performance liquid chromatography/mass spectrometry. J. Agric. Food Chem. 1999, 47, 490-496.
6. Lee, K. W., Kim, Y. J., Lee, H. J., Lee, C. Y., Cocoa has more phenolic phytochemicals and a higher antioxidant capacity than teas and red wine. J. Agric. Food Chem. 2003, 51, 7292-7295.
7. Selmi, C., Cocchi, C. A., Lanfredini, M., Keen, C. L. et al., Chocolate at heart: the anti-inflammatory impact of cocoa flavanols. Mol. Nutr. Food Res. 2008, 52, 1340-1358.
8. Katz, D. L., Doughty, K., Alli, A., Cocoa and chococlate in human health and disease. Antioxid. Redox Signal. 2011, 15, 2779-2811.
9. Dillinger, T. L., Barriga, P., Esca, S., Jimenez, M. et al., Food of the gods: cure for humanity? A cultural history of the medicinal and ritual use of chocolate. J. Nutr. 2000, 130, 2057-2072.
10. Almoosawi, S., Fyfe, L., Ho, C., Al-Dujaili, E., The effect of polyphenol-rich dark chocolate on fasting capillary whole blood glucose, total cholesterol, blood pressure and glucocorticoids in healthy overweight and obese subjects. Br. J. Nutr. 2010, 103, 842-850.
11. Baba, S., Natsume, M., Yasuda, A., Nakamura, Y. et al., Plasma LDL and HDL cholesterol and oxidized LDL concentrations are altered in normo- and hypercholesterolemic humans after intake of different levels of cocoa powder. J. Nutr. 2007, 137, 1436-1441.
12. Berry, N. M., Davison, K., Coates, A. M., Buckley, J. D. et al., Impact of cocoa flavanol consumption on blood pressure responsiveness to exercise. Br. J. Nutr. 2010, 103, 1480-1484.
13. Davison, K., Coates, A. M., Buckley, J. D., Howe, P. R. C., Effect of cocoa flavanols and exercise on cardiometabolic risk factors in overweight and obese subjects. Int. J. Obes. 2008, 32, 1289-1296.
14. Di Giuseppe, R., Di Castelnuovo, A., Centritto, F., Zito, F. et al., Regular consumption of dark chocolate is associated with low serum concentrations of C-reactive protein in a healthy Italian population. J. Nutr. 2008, 138, 1939-1945.
15. Engler, M. B., Engler, M. M., Chen, C. Y., Malloy, M. J. et al., Flavonoid-rich dark chocolate improves endothelial function and increases plasma epicatechin concentrations in healthy adults. J. Am. Coll. Nutr. 2004, 23, 197-204.
16. Fisher, N. D. L., Hughes, M., Gerhard-Herman, M., Hollenberg, N. K., Flavanol-rich cocoa induces nitric-oxide-dependent vasodilation in healthy humans. J. Hypertens. 2003, 21, 2281-2286.
17. Grassi, D., Desideri, G., Necozione, S., Lippi, C. et al., Blood pressure is reduced and insulin sensitivity increased in glucose-intolerant, hypertensive subjects after 15 days of consuming high-polyphenol dark chocolate. J. Nutr. 2008, 138, 1671-1676.
18. Grassi, D., Lippi, C., Necozione, S., Desideri, G. et al., Short-term administration of dark chocolate is followed by a significant increase in insulin sensitivity and a decrease in blood pressure in healthy persons. Am. J. Clin. Nutr. 2005, 81, 611-614.
19. Mellor, D. D., Sathyapalan, T., Kilpatrick, E. S., Beckett, S. et al., High-cocoa polyphenol-rich chocolate improves HDL cholesterol in type 2 diabetes patients. Diabet. Med. 2010, 27, 1318-1321.
20. Monagas, M., Khan, N., Andres-Lacueva, C., Casas, R. 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, 1144-1150.
21. Mursu, J., Voutilainen, S., Nurmi, T., Rissanen, T. H. et al., Dark chocolate consumption increases HDL cholesterol concentration and chocolate fatty acids may inhibit lipid peroxidation in healthy humans. Free Radic. Biol. Med. 2004, 37, 1351-1359.
22. Sudarma, V., Sukmaniah, S., Siregar, P., Effect of dark chocolate on nitric oxide serum levels and blood pressure in prehypertension subjects. Acta Med. Indones. 2011, 43, 224-228.
23. Vázquez-Agell, M., Urpi-Sarda, M., Sacanella, E., Camino-López, S., Chiva-Blanch, G. et al., Cocoa consumption reducesbbrk?> NF-κB activation in peripheral blood mononuclear cells in humans. Nutr. Metab. Cardiovasc. Dis. 2011, 23, 257-263.
24. Buitrago-Lopez, A., Sanderson, J., Johnson, L., Warnakula, S. et al., Chocolate consumption and cardiometabolic disorders: systematic review and meta-analysis. Br. Med. J. 2011, 343, d4488. DOI 10.1136/bmj.d4488.
25. Shrime, M. G., Bauer, S. R., Mcdonald, A. C., Chowdhury, N. H. et al., Flavonoid-rich cocoa consumption affects multiple cardiovascular risk factors in a meta-analysis of short-term studies. J. Nutr. 2011, 141, 1982-1988.
26. Hooper, L., Kay, C., Abdelhamid, A., Kroon, P. A. et al., Effects of chocolate, cocoa, and flavan-3-ols on cardiovascular health: a systematic review and meta-analysis of randomized trials. Am. J. Clin. Nutr. 2012, 95, 740-751.
27. Tokede, O. A., Gaziano, J. M., Djoussé, L., Effects of cocoa products/dark chocolate on serum lipids: a meta-analysis. Eur. J. Clin. Nutr. 2011, 65, 879-886.
28. Bauer, S. R., Ding, E. L., Smit, L. A., Cocoa consumption, cocoa flavonoids, and effects on cardiovascular risk factors: an evidence-based review. Curr. Cardiovasc. Risk Rep. 2011, 5, 120-127.
29. Jia, L., Liu, X., Bai, Y. Y., Li, S. H. et al., Short-term effect of cocoa product consumption on lipid profile: a meta-analysis of randomized controlled trial. Am. J. Clin. Nutr. 2010, 92, 218-225.
30. Scheid, L., Reusch, A., Stehle, P., Ellinger, S., Antioxidant effects of cocoa and cocoa products ex vivo and in vivo: is there evidence from controlled intervention studies? Curr. Opin. Clin. Nutr. Metab. Care. 2010, 13, 737-742.
31. Tokede, O. A., Ellison, C. R., Pankow, J. S., North, K. E. et al., Chocolate consumption and prevalence of metabolic syndrome in the NHLBI family heart study. e-SPEN J. 2012, 7, e139-e143.
32. Devaraj, S., Goyal, R., Jialal, I., Inflammation, oxidative stress, and the metabolic syndrome. Diabetes Pathophysiol. 2008, 32-37.
33. Ford, E. S., Prevalence of the metabolic syndrome defined by the International Diabetes Federation among adults in the U.S. Diabetes Care 2005, 28, 2745-2749.
34. Cherniack, E. P., Polyphenols: planting the seeds of treatment for the metabolic syndrome. Nutrition 2011, 27, 617-623.
35. Ford, E. S., Li, C., Zhao, G., Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US. J. Diabetes 2010, 2, 180-193.
36. Crist, L. A., Champagne, C. M., Corsino, L., Lien, L. F. et al., Influence of change in aerobic fitness and weight on prevalence of metabolic syndrome. Prev. Chronic Dis. 2012, 9, E68.
37. Das, U. N., Is metabolic syndrome X an inflammatory condition? Exp. Biol. Med. 2002, 227, 989-997.
38. Esposito, K., Giugliano, D., The metabolic syndrome and inflammation: association or causation? Nutr. Metab. Cardiovasc. Dis. 2004, 14, 228-232.
39. Després, J-P., Lemieux, I., Abdominal obesity and metabolic syndrome. Nature 2006, 444, 881-887.
40. Laclaustra, M., Corella, D., Ordovas, J. M., Metabolic syndrome pathophysiology: the role of adipose tissue. Nutr. Metab. Cardiovasc. Dis. 2007, 17, 125-139.
41. De Ferranti, S., Mozaffarian, D., The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin. Chem. 2008, 54, 945-955.
42. Sharma, P., Inflammation and the metabolic syndrome. Ind. J. Clin. Biochem. 2011, 26, 317-318.
43. Maury, E., Brichard, S. M., Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol. Cell. Endocrinol. 2010, 314, 1-16.
44. Elks, C. M., Francis, J., Central adiposity, systemic inflammation, and the metabolic syndrome. Curr. Hypertens. Rep. 2010, 12, 99-104.
45. Balistreri, C. R., Caruso, C., Candore, G., The role of adipose tissue and adipokines in obesity-related inflammatory diseases. Mediators Inflamm. 2010, 2010, 1-9.
46. Kershaw, E. E., Flier, J. S., Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 2004, 89, 2548-2556.
47. Wellen, K. E., Hotamisligil, G. S., Obesity-induced inflammatory changes in adipose tissue. J. Clin. Invest. 2003, 112, 1785-1788.
48. Eder, K., Baffy, N., Falus, A., The major inflammatory mediator interleukin-6 and obesity. Inflamm. Res. 2009, 58, 727-736.
49. Pompeia, C., Lima, T., Curi, R., Arachidonic acid cytotoxicity: can arachidonic acid be a physiological mediator of cell death? Cell Biochem. Funct. 2003, 21, 97-104.
50. Sears, B., Ricordi, C., Anti-inflammatory nutrition as a pharmacological approach to treat obesity. J. Obes. 2011, 2011, pii: 431985. DOI 10.1155/2011/431985.
51. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M. et al., Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112, 1796-1808.
52. Xu, H., Barnes, G. T., Yang, Q., Tan, G. et al., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112, 1821-1830.
53. Sears, B., Anti-inflammatory diets for obesity and diabetes. J. Am. Coll. Nutr. 2009, 28 (Suppl), 482S-491S.
54. Khandekar, M. J., Cohen, P., Spiegelman, B. M., Molecular mechanisms of cancer development in obesity. Nat. Rev. Cancer 2011, 11, 886-895.
55. Stote, K. S., Clevidence, B. A., Novotny, J. A., Henderson, T. et al., Effect of cocoa and green tea on biomarkers of glucose regulation, oxidative stress, inflammation and hemostasis in obese adults at risk for insulin resistance. Eur. J. Clin. Nutr. 2012, 66, 1153-1159.
56. Schramm, D. D., Wang, J. F., Holt, R. R., Ensunsa, J. L. et al., Chocolate procyanidins decrease the leukotriene-prostacyclin ratio in humans and human aortic endothelial cells. Am. J. Clin. Nutr. 2001, 73, 36-40.
57. Tzounis, X., Rodriguez-mateos, A., Vulevic, J., Gibson, G. R. et al., Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am. J. Clin. Nutr. 2011, 93, 62-72.
58. Mathur, S., Devaraj, S., Grundy, S. M., Jialal, I., Cocoa products decrease low density lipoprotein oxidative susceptibility but do not affect biomarkers of inflammation in humans. J. Nutr. 2002, 132, 3663-3667.
59. Muniyappa, R., Hall, G., Kolodziej, T. L., Karne, R. J. et al., Cocoa consumption for 2 wk enhances insulin-mediated vasodilatation without improving blood pressure or insulin resistance in essential hypertension. Am. J. Clin. Nutr. 2008, 88, 1685-1696.
60. Yamashita, Y., Okabe, M., Natsume, M., Ashida, H., Prevention mechanisms of glucose intolerance and obesity by cacao liquor procyanidin extract in high-fat diet-fed C57BL/6 mice. Arch. Biochem. Biophys. 2012, 527, 95-104.
61. Tomaru, M., Takano, H., Osakabe, N., Yasuda, A. et al., Dietary supplementation with cacao liquor proanthocyanidins prevents elevation of blood glucose levels in diabetic obese mice. Nutrition 2007, 23, 351-355.
62. Min, S. Y., Yang, H., Seo, S. G., Shin, S. H. et al., Cocoa polyphenols suppress adipogenesis in vitro and obesity in vivo by targeting insulin receptor. Int. J. Obes. 2013, 37, 584-592.
63. Matsui, N., Ito, R., Nishimura, E., Yoshikawa, M. et al., Ingested cocoa can prevent high-fat diet-induced obesity by regulating the expression of genes for fatty acid metabolism. Nutrition 2005, 21, 594-601.
64. Yasuda, A., Natsume, M., Sasaki, K., Baba, S. et al., Cacao procyanidins reduce plasma cholesterol and increase fecal steroid excretion in rats fed a high-cholesterol diet. BioFactors 2008, 33, 211-223.
65. Ramos-Romero, S., Pérez-Cano, F. J., Pérez-Berezo, T., Castellote, C. et al., A seven-day high cocoa diet decreases oxidant and inflammatory properties of peritoneal macrophages in rats. Proc. Nutr. Soc. 2010, 69, E253.
66. Jalil, A. M. M., Ismail, A., Pei, C. P., Hamid, M. et al., Effects of cocoa extract on glucometabolism, oxidative stress, and antioxidant enzymes in obese-diabetic (Ob-db) rats. J. Agric. Food Chem. 2008, 56, 7877-7884.
67. Jalil, A. M. M., Ismail, A., Pei, C. P., Hamid, M. et al., Effects of cocoa extract containing polyphenols and methylxanthines on biochemical parameters of obese-diabetic rats. J. Sci. Food Agric. 2009, 89, 130-137.
68. Cienfuegos-Jovellanos, E., Quiñones, M. D. M., Muguerza, B., Moulay, L. et al., Antihypertensive effect of a polyphenol-rich cocoa powder industrially processed to preserve the original flavonoids of the cocoa beans. J. Agric. Food Chem. 2009, 57, 6156-6162.
69. Sánchez, D., Moulay, L., Muguerza, B., Quiñones, M. et al., Effect of a soluble cocoa fiber-enriched diet in Zucker fatty rats. J. Med. Food 2010, 13, 621-628.
70. Gu, Y., Hurst, W. J., Stuart, D. A., Lambert, J. D., Inhibition of key digestive enzymes by cocoa extracts and procyanidins. J. Agric. Food Chem. 2011, 59, 5305-5311.
71. Yamashita, Y., Okabe, M., Natsume, M., Ashida, H., Cacao liquor procyanidin extract improves glucose tolerance by enhancing GLUT4 translocation and glucose uptake in skeletal muscle. J. Nutr. Sci. 2012, 1, 1-9.
72. Tucci, S. A., Boyland, E. J., Halford, J. C., The role of lipid and carbohydrate digestive enzyme inhibitors in the management of obesity: a review of current and emerging therapeutic agents. Diabetes Metab. Syndr. Obes. 2010, 3, 125-143.
73. Schewe, T., Sadik, C., Klotz, L O., Yoshimoto, T. et al., Polyphenols of cocoa: inhibition of mammalian 15-lipoxygenase. Biol. Chem. 2001, 382, 1687-1696.
74. Schewe, T., Ku, H., Flavonoids of cocoa inhibit recombinant human 5-lipoxygenase. J. Nutr. 2002, 132, 1825-1829.
75. Mao, T. K., Powell, J., Water, J. V. D., Keen, C. L. et al., The effect of cocoa procyanidins on the transcription and secretion of interleukin 1beta in peripheral blood mononuclear cells. Life Sci. 2000, 66, 1377-1386.
76. Mao, T. K., Van de Water, J., Keen, C. L., Schmitz, H. H. et al., Modulation of TNF-α secretion in peripheral blood mononuclear cells by cocoa flavanols and procyanidins. Dev. Immunol. 2002, 9, 135-141.
77. Ramiro, E., Franch, A., Castellote, C., Pérez-Cano, F. et al., Flavonoids from Theobroma cacao down-regulate inflammatory mediators. J. Agric. Food Chem. 2005, 53, 8506-8511.
78. Recio, M. C., Giner, R. M., Cienfuegos-jovellanos, E., Laghi, S. et al., Inhibition of ulcerative colitis in mice after oral administration of a polyphenol-enriched cocoa extract is mediated by the inhibition of STAT1 and STAT3 phosphorylation in colon cells. J. Agric. Food Chem. 2011, 59, 6474-6483.
79. Vazquez-prieto, M. A., Bettaieb, A., Haj, F. G., Fraga, C. G. et al., (-)-Epicatechin prevents TNFa-induced activation of signaling cascades involved in inflammation and insulin sensitivity in 3T3-L1 adipocytes. Arch. Biochem. Biophys. 2012, 527, 113-118.
80. Zhang, W., Liu, H., Xie, K., Yin, L. et al., Procyanidin dimer B2 [epicatechin-(4beta-8)-epicatechin] suppresses the expression of cyclooxygenase-2 in endotoxin-treated monocytic cells. Biochem. Biophys. Res. Commun. 2006, 345, 508-515.
81. Ono, K., Takahashi, T., Kamei, M., Mato, T. et al., Effects of an aqueous extract of cocoa on nitric oxide production of macrophages activated by lipopolysaccharide and interferon-γ. Nutrition 2003, 19, 681-685.
82. Ramirez-Sanchez, I., Maya, L., Ceballos, G., Villarreal, F., (-)-Epicatechin activation of endothelial cell eNOS, NO and related signaling pathways. Hypertension 2010, 55, 1398-1405.
83. Persson, I. A, Persson, K., Hägg, S., Andersson, R.G., Effects of cocoa extract and dark chocolate on angiotensin-converting enzyme and nitric oxide in human endothelial cells and healthy volunteers-a nutrigenomics perspective. J. Cardiovasc. Pharmacol. 2011, 57, 44-50.
84. Holt, R. R., Lazarus, S. A., Sullards, M. C., Zhu, Q. Y. et al., Procyanidin dimer B2 [epicatechin-(4beta-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa. Am. J. Clin. Nutr. 2002, 76, 798-804.
85. Sae-tan, S., Grove, K. A., Lambert, J. D., Weight control and prevention of metabolic syndrome by green tea. Pharmacol. Res. 2011, 64, 146-154.
86. Ruzaidi, A., Amin, I., Nawalyah, A. G., Hamid, M. et al., The effect of Malaysian cocoa extract on glucose levels and lipid profiles in diabetic rats. J. Ethnopharmacol. 2005, 98, 55-60.
87. Vinson, J. A., Proch, J., Bose, P., Muchler, S. et al., Chocolate is a powerful ex vivo and in vivo antioxidant, an antiatherosclerotic agent in an animal model, and a significant contributor to antioxidants in the European and American diets. J. Agric. Food Chem. 2006, 54, 8071-8076.
88. Hamed, M. S., Gambert, S., Bliden, K. P., Bailon, O. et al., Dark chocolate effect on platelet activity, C-reactive protein and lipid profile: a pilot study. South. Med. J. 2008, 101, 1203-1208.
89. Wan, Y., Vinson, J. A., Etherton, T. D., Proch, J. et al., Effects of cocoa powder and dark chocolate on LDL oxidative susceptibility and prostaglandin concentrations in humans. Am. J. Clin. Nutr. 2001, 74, 596-602.
90. Murphy, K. J., Chronopoulos, A. K., Singh, I., Francis, M. A. et al., Dietary flavanols and procyanidin oligomers from cocoa (Theobroma cacao) inhibit platelet function. Am. J. Clin. Nutr. 2003, 77, 1466-1473.
91. Taubert, D., Roesen, R., Lehmann, C., Jung, N. et al., Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide. JAMA 2007, 298, 49-60.
92. Grassi, D., Necozione, S., Lippi, C., Croce, G. et al., Cocoa reduces blood pressure and insulin resistance and improves endothelium-dependent vasodilation in hypertensives. Hypertension 2005, 46, 398-405.
93. Barrios-Ramos, J. P., Garduño-Siciliano, L., Loredo, M., Chamorro-Cevallos, G. et al., The effect of cocoa, soy, oats and fish oil on metabolic syndrome in rats. J. Sci. Food Agric. 2012, 92, 2349-2357.
94. Quiñones, M., Muguerza, B., Miguel, M., Aleixandre, A., Evidence that nitric oxide mediates the blood pressure lowering effect of a polyphenol-rich cocoa powder in spontaneously hypertensive rats. Pharmacol. Res. 2011, 64, 478-481.
95. Mao, T., Water, J. V. D., Keen, C. L., Schmitz, H. H. et al., Cocoa procyanidins and human cytokine transcription and secretion. J. Nutr. 2000, 130, 2093S-2039S.
96. Kenny, T. P., Keen, C. L., Schmitz, H. H., Gershwin, M. E., Immune effects of cocoa procyanidin oligomers on peripheral blood mononuclear cells. Exp. Biol. Med. 2007, 232, 293-300.
97. Zeng, H., Locatelli, M., Bardelli, C., Amoruso, A. et al., Anti-inflammatory properties of clovamide and Theobroma cacao phenolic extracts in human monocytes: evaluation of respiratory burst, cytokine release, NF-kB activation, and PPARγ modulation. J. Agric. Food Chem. 2011, 59, 5342-5350.
98. Mackenzie, G. G., Carrasquedo, F., Delfino, J. M., Keen, C. L. et al., Epicatechin, catechin, and dimeric procyanidins inhibit PMA-induced NF-kappaB activation at multiple steps in Jurkat T cells. FASEB J. 2004, 18, 167-169.
99. Karim, M., McCormick, K., Kappagoda, C. T., Effects of cocoa extracts on endothelium-dependent relaxation. J. Nutr. 2000, 130, 2105S-2108S.