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Interactive effects of increased intake of saturated fat and cholesterol on atherosclerosis in the Japanese quail (Coturnix japonica)

Published online by Cambridge University Press:  22 August 2007

Yvonne V. Yuan ,
David D. Kitts  and
David V. Godin
Yvonne V. Yuan*
Affiliation:
Department of Food Science, Faculty of Agricultural Sciences, University of British Columbia, 6650 NW Marine Drive, Vancouver, British Columbia, Canada V6T 1Z4
David D. Kitts
Affiliation:
Department of Food Science, Faculty of Agricultural Sciences, University of British Columbia, 6650 NW Marine Drive, Vancouver, British Columbia, Canada V6T 1Z4
David V. Godin
Affiliation:
Department of Pharmacology and Therapeutics, Faculty of Medicine, University of British Columbia, 2176 Health Sciences Mall, Vancouver, British Columbia, Canada V6T 1Z3
*
†Corresponding author: Dr David Kitts, fax +1 604 822 3959, email [email protected]
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Abstract

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Increasing the energy value of diets with dietary fat, particularly fats rich in saturated fatty acids, can result in the elevation of plasma total and lipoprotein cholesterol. In the present study, experimental diets were designed to examine the effects of increasing the energy content of diets with a saturated fat source and cholesterol in a non-purified diet on hyperlipoproteinaemia and aortic plaque composition in the atherosclerosis-susceptible Japanese quail (Coturnix japonica) model of human atherosclerosis. Commercial poultry diets containing two levels (i.e. 60 or 120 g/kg) of beef tallow as the primary source of saturated fat were balanced for endogenous cholesterol or supplemented with cholesterol (i.e. 0·5 or 5·0 g/kg) and fed to quail for 9 weeks to examine the effects on whole plasma, lipoprotein and aortic plaque lipid composition in relation to aortic plaque formation. Hypercholesterolaemia (P<0·001) was confirmed in birds fed on high-cholesterol (HC) diets only. An interaction (P=0·05) between dietary cholesterol and fat intake level was observed for plasma triacylglycerols (TG) and was specific to changes observed in VLDL composition. Diet-induced changes in lipoprotein total cholesterol, TG and phospholipid composition were greatest in the portomicron and VLDL fractions in birds fed on atherogenic diets. Hyperlipoproteinaemia induced by the 60 g/kg added beef tallow–HC diet resulted in significant (P<0·001) aortic plaque deposition, which was further enhanced in birds fed on the 120 g/kg beef tallow–HC diet. Quail fed on 120 g/kg beef tallow-HC diets exhibited the most severe aortic plaque formation, with marked increases in aortic tissue cholesterol content and quantifiable amounts of several cholesterol oxides (5,6α-epoxy-5α-cholesterol, 7β-hydroxycholesterol, cholestanetriol, 7-ketocholesterol and 25-hydroxycholesterol). In summary, hyperlipoproteinaemia associated with HC diets with a greater proportion of energy from saturated fat produced a combined effect in altering plasma and lipoprotein lipid composition as well as aortic tissue cholesterol and cholesterol oxide content in the Japanese quail.

Keywords

AtherosclerosisJapanese quailLipoproteinsCholesterol
Type
Research Article
Information
British Journal of Nutrition , Volume 80 , Issue 1 , July 1998 , pp. 89 - 100
Copyright
Copyright © The Nutrition Society 1998

References

Austin, MA (1991) Plasma triglyceride and coronary heart disease. Arteriosclerosis and Thrombosis 11, 2–14.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Canadian Council of Animal Care (1993) Guide to the Care and Use of Experimental Animals, vol. 1, 2nd ed. [Olfert, ED, Cross, BM and MacWilliam, AA, editors]. Ottawa, ON: Canadian Council of Animal Care.Google Scholar
Castelli, WP (1986) The triglyceride issue: a view from Framingham. American Heart Journal 112, 432–437.Google Scholar
Clarkson, TB, Prichard, RW, Lofland, HB & Goodman, HO (1962) Interactions among dietary fat, protein and cholesterol in atherosclerosis-susceptible pigeons. Circulation Research 11, 400–404.Google Scholar
Faidley, TD, Luhman, CM, Galloway, ST, Foley, MR & Beitz, DC (1990) Effect of dietary fat source on lipoprotein composition and plasma lipid concentrations in pigs. Journal of Nutrition 120, 1126–1133.Google Scholar
Fernandez, ML & McNamara, DJ (1991) Regulation of cholesterol and lipoprotein metabolism in guinea pigs mediated by dietary fat quality and quantity. Journal of Nutrition 121, 934–943.CrossRefGoogle ScholarPubMed
Fernandez, ML & McNamara, DJ (1994) Dietary fat saturation and chain length modulate guinea pig hepatic cholesterol metabolism. Journal of Nutrition 124, 331–339.Google Scholar
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
Fungwe, TV, Cagen, LM, Cook, GA, Wilcox, HG & Heimberg, M (1993) Dietary cholesterol stimulates hepatic biosynthesis of triglyceride and reduces oxidation of fatty acids in the rat. Journal of Lipid Research 34, 933–941.Google Scholar
Fungwe, TV, Fox, JE, Cagen, LM, Wilcox, HG & Heimberg, M (1994) Stimulation of fatty acid biosynthesis by dietary cholesterol and of cholesterol synthesis by dietary fatty acid. Journal of Lipid Research 35, 311–318.Google Scholar
Godin, DV, Cheng, KM, Garnett, ME & Nichols, CR (1994) Anti-oxidant status of Japanese quail: comparison of atherosclerosis-susceptible and -resistant strains. Canadian Journal of Cardiology 10, 221–228.Google ScholarPubMed
Grundy, SM & Denke, MA (1990) Dietary influences on serum lipids and lipoproteins. Journal of Lipid Research 31, 1149–1172.CrossRefGoogle ScholarPubMed
Hayes, KC, Pronczuk, A & Khosla, P (1995) A rationale for plasma cholesterol modulation by dietary fatty acids: modulating of human response in animals. Journal of Nutritional Biochemistry 6, 188–194.CrossRefGoogle Scholar
Hunt, CE, Funk, GM & Vidmar, TJ (1992) Dietary polyunsaturated to saturated fatty acid ratio alters hepatic LDL transport in cynomolgus macaques fed low cholesterol diets. Journal of Nutrition 122, 1960–1970.Google Scholar
Keys, A, Anderson, JT, Mickelsen, O, Adelson, SF & Fidanza, F (1956) Diet and serum cholesterol in man: lack of effect of dietary cholesterol. Journal of Nutrition 59, 39–56.Google Scholar
Khosla, P & Hayes, KC (1993) Dietary palmitic acid raises plasma LDL cholesterol relative to oleic acid only at a high intake of cholesterol. Biochimica et Biophysica Acta 1210, 13–22.CrossRefGoogle Scholar
Kita, T, Brown, MS, Watanabe, Y & Goldstein, JL (1981) Deficiency of low density lipoprotein receptors in liver and adrenal gland of the WHHL rabbit, an animal model of familial hypercholester-olaemia. Proceedings of the National Academy of Sciences USA 78, 2268–2272.CrossRefGoogle Scholar
Kris-Etherton, PM, Derr, J, Mitchell, DC, Mustad, VA, Russell, ME, McDonnell, ET, Salabsky, D & Pearson, TA (1993) The role of fatty acid saturation on plasma lipids, lipoproteins, and apoli-poproteins: I. Effects of whole food diets high in cocoa butter, olive oil, soybean oil, dairy butter, and milk chocolate on the plasma lipids of young men. Metabolism 42, 121–129.Google Scholar
Kritchevsky, D (1970) Role of cholesterol vehicle in experimental atherosclerosis. American Journal of Clinical Nutrition 23, 1105–1110.CrossRefGoogle ScholarPubMed
Lin, ECK, Fernandez, ML & McNamara, DJ (1992) Dietary fat type and cholesterol quantity interact to affect cholesterol metabolism in guinea pigs. Journal of Nutrition 122, 2019–2029.Google Scholar
Lindsey, S, Benattar, J, Pronczuk, A & Hayes, KC (1990) Dietary palmitic acid (C16:0) enhances high density lipoprotein cholesterol and low density lipoprotein receptor mRNA abundance in hamsters. Proceedings of the Society for Experimental Biology and Medicine 195, 261–269.CrossRefGoogle Scholar
Lipid Research Clinics Program (1984) The lipid research clinics coronary primary prevention trial results. I: Reduction in incidence of coronary heart disease. Journal of the American Medical Association 251, 351–364.CrossRefGoogle Scholar
Liu, CH, Huang, M & Huang, P-C (1995) Sources of triacylglycerol accumulation in livers of rats fed on cholesterol-supplemented diets. Lipids 30, 527–531.CrossRefGoogle Scholar
Mattson, FH & Grundy, SM (1985) Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. Journal of Lipid Research 26, 194–202.Google Scholar
Miller, DS & Payne, PR (1959) A ballistic bomb calorimeter. British Journal of Nutrition 13, 501–508.CrossRefGoogle ScholarPubMed
Mott, GE, Jackson, EM, McMahan, CA & McGill, HC Jr (1992) Dietary cholesterol and type of fat differentially affect cholesterol metabolism and atherosclerosis in baboons. Journal of Nutrition 122, 1397–1406.Google Scholar
Mustad, VA, Ellsworth, JL, Cooper, AD, Kris-Etherton, PM & Etherton, TD (1996) Dietary linoleic acid increases and palmitic acid decreases LDL receptor protein and mRNA abundance in young pigs. Journal of Lipid Research 37, 2310–2323.CrossRefGoogle ScholarPubMed
Mustad, VA, Etherton, TD, Cooper, AD, Mastro, AM, Pearson, TA, Jonnalagadda, SS & Kris-Etherton, PM (1997) Reducing saturated fat intake is associated with increased levels of LDL receptors on mononuclear cells in healthy men and women. Journal of Lipid Research 38, 459–468.CrossRefGoogle ScholarPubMed
Nishina, PM, Lowe, S, Verstuyft, J, Naggert, JK, Kuypers, FA & Paigen, B (1993) Effects of dietary fats from animal and plant sources on diet-induced fatty streak lesions in C57BL/6J mice. Journal of Lipid Research 34, 1413–1422.CrossRefGoogle ScholarPubMed
Nwokolo, E & Kitts, DD (1988) Growth parameters and plasmatissue fatty acid profiles of rats fed rubber seed oil. Food Chemistry 30, 219–229.CrossRefGoogle Scholar
Ohtani, H, Hayashi, K, Hirata, Y, Dojo, S, Nakashima, K, Nishio, E, Kurushima, H, Sacki, M & Kajiyama, G (1990) Effects of dietary cholesterol and fatty acids on plasma cholesterol level and hepatic lipoprotein metabolism. Journal of Lipid Research 31, 1413–1422.Google Scholar
Patsch, JR, Miesenboeck, G, Hopferwieser, T, Muehlberger, V, Knapp, E, Dunn, JK, Gotto, AM Jr & Patsch, W (1992) Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arteriosclerosis and Thrombosis 12, 1336–1345.CrossRefGoogle ScholarPubMed
Peng, S-K, Taylor, CB, Hill, JC & Morin, RJ (1985) Cholesterol oxidation derivatives and arterial endothelial damage. Atherosclerosis 54, 121–133.CrossRefGoogle ScholarPubMed
Pronczuk, A, Khosla, P & Hayes, KC (1994) Dietary myristic, palmitic and linoleic acids modulate cholesterolemia in gerbils. FASEB Journal 8, 1191–1200.CrossRefGoogle ScholarPubMed
Radcliffe, JD & Tromposch, TS (1988) The effect of dietary cholesterol level on lipid status and initiation of atherosclerosis in Japanese quail. Nutrition Research 8, 1021–1027.Google Scholar
Randolph, RK & St Clair, RW (1994) Pigeon aortic smooth muscle cells lack a functional low density lipoprotein receptor pathway. Journal of Lipid Research 25, 903–912.CrossRefGoogle Scholar
Reagen, JW Jr, Miller, LR & St Clair, RW (1990) In vivo clearance of low-density lipoprotein in pigeons occurs by a receptor-like mechanism that is not down-regulated by cholesterol feeding. Journal of Biological Chemistry 265, 9381–9391.Google Scholar
Rokosova, B, Rapp, JH, Porter, JM & Bentley, JP (1986) Composition and metabolism of symptomatic distal aortic plaque. Journal of Vascular Surgery 3, 617–622.Google Scholar
Schaefer, EJ, Levy, RI, Ernst, ND, van Sant, FD & Brewer, BH (1981) The effects of low cholesterol, high polyunsaturated fat, and low-fat diets on plasma lipid and lipoprotein cholesterol levels in normal and hypercholesterolemic subjects. American Journal of Clinical Nutrition 34, 1758–1763.CrossRefGoogle ScholarPubMed
Seppanen-Laakson, T, Vanhanen, H, Laaksom, I, Kohtamaki, H & Viikari, J (1992) Replacement of butter on bread by rapeseed oil and rapeseed oil-containing margarine: effects on plasma fatty acid composition and serum cholesterol. British Journal of Nutrition 68, 639–654.Google Scholar
Shepherd, J, Packard, CJ, Grundy, SM, Yeshurun, A, Gotto, M & Taunton, OD (1980) Effects of saturated and polyunsaturated fat diets on the chemical composition and metabolism of low density lipoproteins in man. Journal of Lipid Research 21, 91–99.CrossRefGoogle ScholarPubMed
Shih, JCH, Pullman, EP & Kao, KJ (1983) Genetic selection, general characterization, and histology of atherosclerosis-susceptible and -resistant Japanese quail. Atherosclerosis 49, 41–53.CrossRefGoogle ScholarPubMed
Siedel, J, Hagele, EO, Ziegenhorn, J & Wahlefeld, AW (1983) Reagent for the enzymatic determination of serum cholesterol with improved lipolytic efficiency. Clinical Chemistry 29, 1075–1080.CrossRefGoogle ScholarPubMed
Spady, DK & Dietschy, JM (1985) Dietary saturated triacylglycerols suppress hepatic low density lipoprotein receptor activity in the hamster. Proceedings of the National Academy of Sciences USA 82, 4526–4530.CrossRefGoogle ScholarPubMed
Spady, DK & Dietschy, JM (1988) Interaction of dietary cholesterol and triacylglycerides on the regulation of hepatic low density lipoprotein transport in the hamster. Journal of Clinical Investigation 81, 300–309.Google Scholar
Steinbrecher, UP & Lougheed, M (1992) Scavenger receptor independent stimulation of cholesterol esterification in macrophages by low density lipoprotein extracted from human aortic intima. Arteriosclerosis and Thrombosis 12, 608–625.Google Scholar
Sundram, K, Hayes, KC & Siru, OH (1995) Both dietary 18 : 2 and 16 : 0 may be required to improve the serum LDL/HDL cholesterol ratio in normocholesterolemic men. Journal of Nutritional Biochemistry 6, 179–187.Google Scholar
Takayama, M, Itoh, S, Nagasaki, T & Tanimizu, I (1977) A new enzymatic method for determination of serum choline-containing phospholipids. Clinica Chimica Acta 79, 93–98.Google ScholarPubMed
Terpstra, AHM, Sanchez-Muniz, FJ, West, CE & Woodward, CJH (1982) The density profile and cholesterol concentration of serum lipoproteins in domestic and laboratory animals. Comparative Biochemistry and Physiology 71B, 669–763.Google Scholar
Thompson, GR, Souter, AK, Spengel, FA, Jadhav, A, Gavigan, SJP & Myant, NB (1981) Defects of receptor-mediated low density lipoprotein catabolism in homozygous familial hypercholesterolaemia and hyperthyroidism in vivo. Proceedings of the National Acadamy of Sciences USA 78, 25911–25915.Google Scholar
Yuan, YV, Kitts, DD & Godin, DV (1997) Influence of dietary cholesterol and fat source on atherosclerosis in the Japanese quail (Coturnix japonica). British Journal of Nutrition 78, 993–1014.CrossRefGoogle ScholarPubMed
Ziegenhorn, J (1975) Improved method for enzymatic determination of serum triglycerides. Clinical Chemistry 21, 1627–1629.CrossRefGoogle ScholarPubMed