Effects of chocolate supplementation on metabolic and cardiovascular parameters in ApoE3L mice fed a high-cholesterol atherogenic diet

Molecular Nutrition and Food Research

Volumn 57, Issue 11, 2013, Pages 2039-2048

  Yakala, Gopala K ^a,b   Wielinga, Peter Y ^b,c   Suarez, Manuel ^d,e   Bunschoten, Annelies ^f   van Golde, Jolanda M ^b   Arola, Lluis ^d,e   Keijer, Jaap ^b,f   Kleemann, Robert ^b,c   Kooistra, Teake ^b,c   Heeringa, Peter ^a,b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^c TNO   (Netherlands)

^d UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^e TECNIO   (Spain)

^f WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Atherosclerosis; Cardiovascular disease; Inflammation; Liver injury; Renal inflammation

Indexed keywords

APOLIPOPROTEIN E3; APOLIPOPROTEIN E3 (LEIDEIN); ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; PLANT EXTRACT; POLYPHENOL; SERUM AMYLOID A; SUGAR; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL; ARTICLE; ATHEROGENIC DIET; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD; CACAO; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CHEMISTRY; CHOLESTEROL INTAKE; DIET SUPPLEMENTATION; DIETARY FIBER; FEMALE; GENETICS; INFLAMMATION; LIVER; LIVER INJURY; METABOLISM; MOUSE; NEPHRITIS; PATHOLOGY;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; INFLAMMATION; LIVER INJURY; RENAL INFLAMMATION;

ANIMALS; APOLIPOPROTEIN E3; ATHEROSCLEROSIS; CACAO; CANDY; CARDIOVASCULAR SYSTEM; CHOLESTEROL, DIETARY; DIET, ATHEROGENIC; DIETARY FIBER; DIETARY SUPPLEMENTS; E-SELECTIN; FEMALE; INFLAMMATION; LIVER; MICE; PLANT EXTRACTS; PLAQUE, ATHEROSCLEROTIC; POLYPHENOLS; SERUM AMYLOID A PROTEIN; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84886772717     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200858     Document Type: Article

References (47)

1. Rosamond, W., Flegal, K., Friday, G., Furie, K. et al., Heart disease and stroke statistics-2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2007, 115, e69-e171.
2. Rosamond, W., Flegal, K., Furie, K., Go, A. et al., Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2008, 117, e25-e146.
3. Ballantyne, C., Arroll, B., Shepherd, J., Lipids and CVD management: towards a global consensus. Eur Heart J. 2005, 26, 2224-2231.
4. Wielinga, P. Y., Yakala, G. K., Heeringa, P., Kleemann, R. et al., Beneficial effects of alternate dietary regimen on liver inflammation, atherosclerosis and renal activation. PloS One 2011, 6, e18432.
5. Hu, F. B., Willett, W. C., Optimal diets for prevention of coronary heart disease. JAMA 2002, 288, 2569-2578.
6. Ding, E. L., Mozaffarian, D., Optimal dietary habits for the prevention of stroke. Semin. Neurol. 2006, 26, 11-23.
7. Stampfer, M. J., Hu, F. B., Manson, J. E., Rimm, E. B. et al., Primary prevention of coronary heart disease in women through diet and lifestyle. N. Eng. J. Med. 2000, 343, 16-22.
8. Hertog, M. G., Feskens, E. J., Hollman, P. C., Katan, M. B. et al., Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen elderly study. Lancet 1993, 342, 1007-1011.
9. Scalbert, A., Johnson, I. T., Saltmarsh, M., Polyphenols: antioxidants and beyond. Am. J. Clin. Nutr. 2005, 81, 215S-217S.
10. Manach, C., Mazur, A., Scalbert, A., Polyphenols and prevention of cardiovascular diseases. Curr. Opin. Lipidol. 2005, 16, 77-84.
11. Arts, I. C., Hollman, P. C., Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr. 2005, 81, 317S-325S.
12. Corti, R., Flammer, A. J., Hollenberg, N. K., Luscher, T. F., Cocoa and cardiovascular health. Circulation 2009, 119, 1433-1441.
13. Fernandez-Murga, L., Tarin, J. J., Garcia-Perez, M. A., Cano, A., The impact of chocolate on cardiovascular health. Maturitas 2011, 69, 312-321.
14. Buitrago-Lopez, A., Sanderson, J., Johnson, L., Warnakula, S. et al., Chocolate consumption and cardiometabolic disorders: systematic review and meta-analysis. BMJ 2011, 343, d4488.
15. Erdman, J. W., Jr, Carson, L., Kwik-Uribe, C., Evans, E. M. et al., Effects of cocoa flavanols on risk factors for cardiovascular disease. Asia Pacific J. Clin. Nutr. 2008, 17(Suppl 1), 284-287.
16. Kurosawa, T., Itoh, F., Nozaki, A., Nakano, Y. et al., Suppressive effects of cacao liquor polyphenols (CLP) on LDL oxidation and the development of atherosclerosis in Kurosawa and Kusanagi hypercholesterolemic rabbits. Atherosclerosis 2005, 179, 237-246.
17. Loke, W. M., Proudfoot, J. M., Hodgson, J. M., McKinley, A. J. et al., Specific dietary polyphenols attenuate atherosclerosis in apolipoprotein E-knockout mice by alleviating inflammation and endothelial dysfunction. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 749-757.
18. Osakabe, N., Yamagishi, M., Procyanidins in Theobroma cacao reduce plasma cholesterol levels in high cholesterol-fed rats. J. Clin. Biochem. Nutr. 2009, 45, 131-136.
19. 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.
20. van den Maagdenberg, A. M., Hofker, M. H., Krimpenfort, P. J., de Bruijn, I. et al., Transgenic mice carrying the apolipoprotein E3-leiden gene exhibit hyperlipoproteinemia. J. Biol. Chem. 1993, 268, 10540-10545
21. Verschuren, L., Kleemann, R., Offerman, E. H., Szalai, A. J. et al., Effect of low dose atorvastatin versus diet-induced cholesterol lowering on atherosclerotic lesion progression and inflammation in apolipoprotein E*3-leiden transgenic mice. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 161-167.
22. Kleemann, R., Princen, H. M., Emeis, J. J., Jukema, J. W. et al., Rosuvastatin reduces atherosclerosis development beyond and independent of its plasma cholesterol-lowering effect in APOE*3-leiden transgenic mice: evidence for antiinflammatory effects of rosuvastatin. Circulation 2003, 108, 1368-1374.
23. Post, S. M., de Roos, B., Vermeulen, M., Afman, L. et al., Cafestol increases serum cholesterol levels in apolipoprotein E*3-leiden transgenic mice by suppression of bile acid synthesis. Arterioscler. Thromb. Vasc. Biol. 2000, 20, 1551-1556.
24. van Vlijmen, B. J., Mensink, R. P., van 't Hof, H. B., Offermans, R. F. et al., Effects of dietary fish oil on serum lipids and VLDL kinetics in hyperlipidemic apolipoprotein E*3-leiden transgenic mice. J. Lipid Res. 1998, 39, 1181-1188.
25. van der Hoogt, C. C., de Haan, W., Westerterp, M., Hoekstra, M. et al., Fenofibrate increases HDL-cholesterol by reducing cholesteryl ester transfer protein expression. J. Lipid Res. 2007, 48, 1763-1771.
26. Kleemann, R., Verschuren, L., Morrison, M., Zadelaar, S. et al., Anti-inflammatory, anti-proliferative and anti-atherosclerotic effects of quercetin in human in vitro and in vivo models. Atherosclerosis 2011, 218, 44-52.
27. Monahan, K. D., Effect of cocoa/chocolate ingestion on brachial artery flow-mediated dilation and its relevance to cardiovascular health and disease in humans. Arch. Biochem. Biophys. 2012, 527, 90-94.
28. Rimbach, G., Melchin, M., Moehring, J., Wagner, A. E., Polyphenols from cocoa and vascular health: a critical review. Internat. J. Mol. Sci. 2009, 10, 4290-4309.
29. Vitaglione, P., Barone Lumaga, R., Ferracane, R., Sellitto, S. et al., Human bioavailability of flavanols and phenolic acids from cocoa-nut creams enriched with free or microencapsulated cocoa polyphenols. Br. J. Nutr. 2012, 10, 1-12.
30. Hollman, P. C., Cassidy, A., Comte, B., Heinonen, M. et al., The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J. Nutr. 2011, 141, 989S-1009S.
31. Wielinga, P. Y., Harthoorn, L. F., Verschuren, L., Schoemaker, M. H. et al., Arachidonic acid/docosahexaenoic acid-supplemented diet in early life reduces body weight gain, plasma lipids, and adiposity in later life in ApoE*3Leiden mice. Mol. Nutr. Food Res. 2012, 56, 1081-1089.
32. Serra, A., Macià, A., Romero, M.-P., Piñol, C. et al., Rapid methods to determine procyanidins, anthocyanins, theobromine and caffeine in rat tissues by liquid chromatography-tandem mass spectrometry. J. Chromatogr. B 2011, 879, 1519-1528
33. Yakala, G. K., van der Heijden, R., Molema, G., Schipper, M. et al., Beneficial effects of an alternating high- fat dietary regimen on systemic insulin resistance, hepatic and renal inflammation and renal function. PloS One 2012, 7, e45866.
34. Schulz, T. J., Thierbach, R., Voigt, A., Drewes, G. et al., Induction of oxidative metabolism by mitochondrial frataxin inhibits cancer growth: Otto Warburg revisited. J. Biol. Chem. 2006, 281, 977-981.
35. Visioli, F., Bernaert, H., Corti, R., Ferri, C. et al., Chocolate, lifestyle, and health. Crit. Rev. Food Sci. Nutr. 2009, 49, 299-312.
36. Galleano, M., Oteiza, P. I., Fraga, C. G., Cocoa, chocolate, and cardiovascular disease. J. Cardiovasc. Pharmacol. 2009, 54, 483-490.
37. Araujo, J. A., Zhang, M., Yin, F., Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front. Pharmacol. 2012, 3, 119.
38. Ding, E. L., Hutfless, S. M., Ding, X., Girotra, S., Chocolate and prevention of cardiovascular disease: a systematic review. Nutr. Metabol. 2006, 3, 2.
39. Kurosawa, T., Itoh, F., Nozaki, A., Nakano, Y. et al., Suppressive effect of cocoa powder on atherosclerosis in Kurosawa and Kusanagi hypercholesterolemic rabbits. J. Atheroscler. Thromb. 2005, 12, 20-28.
40. 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. Agricultural Food Chem. 2006, 54, 8071-8076.
41. Desch, S., Schmidt, J., Kobler, D., Sonnabend, M. et al., Effect of cocoa products on blood pressure: systematic review and meta-analysis. Am. J. Hypertens. 2010, 23, 97-103.
42. Jain, A., Soni, M., Deb, L., Jain, A. et al., Antioxidant and hepatoprotective activity of ethanolic and aqueous extracts of momordica dioica roxb. leaves. J. Ethnopharmacol. 2008, 115, 61-66.
43. Waddington, E., Puddey, I. B., Croft, K. D., Red wine polyphenolic compounds inhibit atherosclerosis in apolipoprotein E-deficient mice independently of effects on lipid peroxidation. Am. J. Clin. Nutr. 2004, 79, 54-61.
44. Stocker, R., O'Halloran, R. A., Dealcoholized red wine decreases atherosclerosis in apolipoprotein E gene-deficient mice independently of inhibition of lipid peroxidation in the artery wall. Am. J. Clin. Nutr. 2004, 79, 123-130.
45. Libby, P., Inflammation in atherosclerosis. Nature 2002, 420, 868-874.
46. Katz, D. L., Doughty, K., Ali, A., Antiox. Redox Signal. 2011, 15, 2779-2811.
47. Brown, L., Rosner, B., Willett, W. W., Sacks, F. M., Cholesterol-lowering effects of dietary fiber: a meta-analysis. Am. J. Clin. Nutr. 1999, 69, 30-42.