The role of dietary fatty acids in lipoprotein oxidation and atherosclerosis

Current Opinion in Lipidology

Volumn 9, Issue 4, 1998, Pages 301-307

  Tsimikas, Sotirios ^a   Reaven, Peter D ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; FATTY ACID; LIPOPROTEIN; MONOUNSATURATED FATTY ACID; POLYUNSATURATED FATTY ACID; SATURATED FATTY ACID;

ARTICLE; ATHEROSCLEROSIS; CORONARY RISK; FAT INTAKE; HUMAN; ISCHEMIC HEART DISEASE; OXIDATION; PRIORITY JOURNAL;

ARTERIOSCLEROSIS; DIETARY FATS; FATTY ACIDS; INFLAMMATION; LIPOPROTEINS, LDL; OXIDATION-REDUCTION; RISK FACTORS; THROMBOSIS;

EID: 0031716862     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-199808000-00003     Document Type: Article

References (82)

1. Keys A. Coronary heart disease in seven countries. Circulation 1970; 41 (Suppl 1):1-195.
2. Mensink RP, Katan MB. Effect of dietary fatty acids on serum lipids and lipoproteins: a meta-analysis of 27 trials. Arterioscler Thromb 1992; 12:911-919.
3. Grundy SM, Bilheimer D, Blackburn H, Brown WV, Kwiterovich POJ, Mattson F, et al. Rationale of the diet-heart statement of the American Heart Association. Report of Nutrition Committee. Circulation 1982; 65:839A-854A.
4. Expert panel on population strategies for blood cholesterol reduction. National Cholesterol Education Program. Arch Intern Med 1991; 151:1071-1084.
5. Steinberg D, Lewis A. Conner Memorial Lecture. Oxidative modification of LDL and atherogenesis. Circulation 1997; 95:1062-1071.
6. Navab M, Berliner JA, Watson AD, Hama S, Territo MC, Lusis AJ, et al. The Yin and Yang of oxidation in the development of the fatty streak. Arterioscler Thromb Vasc Biol 1996; 16:831-842. This is a comprehensive review article outlining the role of minimally modified LDL in the early stages of atherosclerosis.
7. Berliner JA, Territo M, Almada L, Carter A, Shofonsky E, Fogelman AM. Monocyte chemotactic factor produced by endothelial cells. Arteriosclerosis 1986; 6:254-258.
8. Berliner JA, Territo MC, Sevanian A. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J Clin Invest 1990; 85:1260-1266.
9. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 1989; 320:915-924.
10. Reaven PD, Witztum JL. Oxidized low density lipoproteins in atherogenesis: role of dietary modification. Ann Rev Nutr 1996; 16:51-71.
11. Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, Witztum JL, et al. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem 1997; 272:13597-13560. This study identifies several degradation products of oxidized phospholipids present in minimally modified LDL that contain proinflammatory activity, and demonstrates that they are formed from arachidonic acid in the sn-2 position. The authors also suggest that these products may be relevant in vivo as they are recognized by endogenously produced autoantibodies cloned from apolipoprotein E -/-deficient mice.
12. Horkko S, Miller E, Dudl E, Reaven P, Curtiss LK, Zvaifler NJ, et al. Antiphospholipid antibodies are directed against epitopes of oxidized phospholipids. Recognition of cardiolipin by monoclonal antibodies to epitopes of oxidized low density lipoprotein. J Clin Invest 1996; 98:815-825.
13. Lee C, Barnett J, Reaven PD. Liposomes enriched in oleic acid are less susceptible to oxidation and have less proinflammatory activity when exposed to oxidative stress. J Lipid Res 1998; 39:1239-1244. This study uses liposomes containing synthetic phospholipids to demonstrate that 18:1 has direct antioxidant activity, independent of linoleic acid concentration. Additionally, 18:1 enriched liposomes generate less monocyle chemotaxis and adhesion when minimally oxidized.
14. Mata P, Alonso R, Lopez-Segura F, Ordovas JM, Lahoz C, Garces C, et al. Effect of dietary fat saturation on LDL oxidation and monocyte adhesion to human endothelial cells in vivo. Arterioscler Thromb Vasc Biol 1997; 16:1347-1355.
15. 1H-nuclear magnetic resonance analysis. Clin Chim Acta 1997; 258:193-200.
16. Dimitriadis E, Griffin M, Collins P, Johnson A, Owens D, Tomkin GH. Lipoprotein composition in NIDDM: effects of dietary oleic acid on the composition, oxidisabilily and function of low and high density lipoproteins. Diabetologia 1996; 39:667-676.
17. O'Byrne DJ, O'Keefe SF, Shireman RB. Low-fat, monounsaturate-rich diets reduce susceptibility of low density lipoproteins to peroxidation ex vivo. Lipids 1998; 33:149-157.
18. Sola R, La Ville AE, Richard JL, Motta C, Bargallo MT, Girona J, et al. Oleic acid rich diet protects against the oxidative modification of high density lipoprotein. Free Rad Biol Med 1997; 22:1037-1045.
19. Gumbiner B, Low CC, Reaven PD. Effects of a monounsaturated fatty acid-enriched hypocaloric diet on cardiovascular risk factors in obese patients with type 2 diabetes. Diabetes Care 1998; 21:9-15.
20. Karman RJ, Garcia JG, Hart CM. Endothelial cell monolayer dysfunction caused by oxidized low density lipoprotein: attenuation by oleic acid. Prostagland Leukot Essent Fatty Acids 1997; 56:345-353.
21. Mata P, Varela O, Alonso R, Lahoz C, de Oya M, Badimon L. Monounsaturated and polyunsaturated n-6 fatty acid-enriched diets modify LDL oxidation and decrease human coronary smooth muscle cell DNA synthesis. Arterioscler Thromb Vasc Biol 1997; 17:2088-2095. This manuscript demonstrates that an oleic acid-rich, Mediterranean type diet protects LDL from oxidation better than n-3 or n-6 PUFA-enriched diets. MUFA and n-6 PUFA diets also resulted in reduced indices of coronary smooth muscle cell proliferation in vitro when they were exposed to human serum from these patients.
22. Reaven PD, Parthasarathy S, Grasse BJ, Miller E, Almazan F, Mattson FH, et al. Feasibility of using an oleate-rich diet to reduce the susceptibility of low-density lipoprotein to oxidative modification in humans. Am J Clin Nutr 1991; 54:701-706.
23. Reaven PD, Grasse BJ, Tribble DL. Effects of linoleate-enriched and oleate-enriched diets in combination with α-tocopherol on the susceptibility of LDL and LDL subfractions to oxidative modification in humans. Arterioscler Thromb Vasc Biol 1994; 14:557-566.
24. Thomas MJ, Rudel LL. Dietary fatty acids, low density lipoprotein composition and oxidation and primate atherosclerosis. J Nutr 1996; 126:1058S-1062S.
25. Suzukawa M, Abbey M, Clifton P, Nestel PJ. Enhanced capacity of n-3 fatty acid-enriched macrophages to oxidize low density lipoprotein mechanisms and effects of antioxidant vitamins. Atherosclerosis 1996; 124:157-169.
26. Louheranta AM, Porkkala-Sarataho EK, Nyyssonen MK, Salonen RM, Salonen JT. Linoleic acid intake and susceptibility of very-low-density and low density lipoproteins to oxidation in men. Am J Clin Nutr 1996; 63:698-703.
27. Jira W, Spiteller G, Carson W, Schramm A. Strong increase in hydroxy fatty acids derived from linoleic acid in human low density lipoproteins of atherosclerotic patients. Chem Phys Lipids 1998; 91:1-11.
28. Connor WE, Connor SL. Should a low-fat, high-carbohydrate diet be recommended for everyone? The case for a low-fat, high-carbohydrate diet. N Engl J Med 1997; 337:562-567.
29. Knapp HR. Dietary fatty acids in human thrombosis and hemostasis. Am J Clin Nutr 1997; 65:16875-16983.
30. Lopez-Segura F, Velasco F, Lopez-Miranda J, Castro P, Lopez-Pedrera R, Blanco A, et al. Monounsaturated fatty acid-enriched diet decreases plasma plasminogen activator inhibitor type 1. Arterioscler Thromb Vasc Biol 1996; 16:82-88.
31. De La Cruz JP, Martin-Romero M, Carmona JA, Villalobos MA, Sanchez de la Cuesta F. Effect of evening primrose oil on platelet aggregation in rabbits fed an atherogenic diet. Thromb Res 1997; 87:141-149.
32. Connor SL, Connor WE. Are fish oils beneficial in the prevention and treatment of coronary artery disease? Am J Clin Nutr 1997; 66:1020S-1031S.
33. Berrettini M, Parise P, Ricotta S, Iorio A, Peirone C, Nenci GG. Increased plasma levels of tissue factor pathway inhibitor (TFPI) after n-3 polyunsaturated fatty acids supplementation in patients with chronic atherosclerotic disease. Thromb Haemost 1996; 75:395-400.
34. Abbate R, Gori AM, Martini F, Brunelli T, Filippini M, Francalanci I, et al. n-3 PUFA supplementation, monocyte PCA expression and interleukin-6 production. Prostagland Leukot Essent Fatty Acids 1996; 54:439-444.
35. Poston RN, Haskard DO, Coucher JR, Gall NP, Johnson-Tidey RR. Expression of intercellular adhesion molecule-1 in atherosclerotic plaques. Am J Pathol 1992; 140:665-673.
36. Yaqoob P, Knapper JA, Webb DH, Williams CM, Newsholme EA, Calder PC. Effect of olive oil on immune function in middle-aged men. Am J Clin Nutr 1998; 67:129-135.
37. Hardwick SJ, Carpenter KL, Law NS, Van Der Veen C, Marchant CE, et al. Toxicity of polyunsaturated fatty acid esters for human monocyte-macrophages: the anomalous behaviour of cholesteryl linolenate. Free Rad Res 1997; 26:351-362. This manuscript demonstrates that the toxicity of PUFAs (in the form of cholesterol esters and triglycerides) to human monocyte-macrophages is directly proportional to the increasing unsaturation of the fatty acids, which correlates with increasing susceptibility to oxidation. Cholesterol linolenate was unusual in that it oxidized easily but did not appear to be toxic.
38. Renaud S, De Lorgeril M, Delaye J, Guidollet J, Jacquard F, Mamelle N, et al. Cretan Mediterranean diet for prevention of coronary heart disease. Am J Clin Nutr 1995; 61:13605-13703.
39. De Lorgeril M, Renaud S, Mamelle N, Salen P, Martin JL, Monjaud I, et al. Mediterranean alpha-linolenic acid-rich diet in secondary prevention of coronary heart disease. Lancet 1994; 343:1454-1459.
40. De Lorgeril M, Salen P, Martin JL, Mamelle N, Monjaud I, Touboul P, Delaye J. Effect of a Mediterranean type of diet on the rate of cardiovascular complications in patients with coronary artery disease. Insights into the cardioprotective effect of certain nutriments. J Am Coll Cardiol 1996; 28:1103-1108. This prospective, secondary prevention study in 605 patients showed that a Mediterranean type diet that was enriched in oleic and linolenic acids reduced the incidence of CHD events by 76% after approximately 2 years. The benefit was independent of changes in cholesterol levels.
41. Fincham JE, Benade AJ, Kruger M, Smuts CM, Gobregts E, Chalton DO, Kritchevsky D. Atherosclerosis: aortic lipid changes induced by diets suggest diffuse disease with focal severity in primates that model human atheromas. Nutrition 1998; 14:17-22.
42. Barbeau ML, Klemp KF, Guyton JR, Rogers KA. Dietary fish oil. Influence on lesion regression in the porcine model of atherosclerosis. Arterioscler Thromb Vasc Biol 1997; 17:688-694
43. Boerboom LE, Olinger GN, Almassi GH, Skrinska VA. Both dietary fish-oil supplementation and aspirin fail to inhibit atherosclerosis in long-term bypass grafts in moderately hypercholesterolemic nonhuman primates. Circulation 1997; 96:968-974.
44. Whitman SC, Fish JR, Rand ML, Rogers KA. n-3 fatty acid incorporation into LDL particles renders them more susceptible to oxidation in vitro but not necessarily more atherogenic in vivo. Arterioscler Thromb 1994; 14:1170-1176.
45. Rudel LL, Parks JS, Sawyer JK. Compared with dietary monounsaturated and saturated fat, polyunsaturated tat protects African green monkeys from coronary artery atherosclerosis. Arterioscler Thromb Vasc Biol 1995; 15:2101-2110.
46. Wolfe MS, Sawyer JK, Morgan TM, Bullock BC, Rudel LL. Dietary polyunsaturated fat decreases coronary artery atherosclerosis in a pediatric-aged population of African green monkeys. Arterioscler Thromb 1994; 14:587-597.
47. Rudel LL, Haines J, Sawyer JK, Shah R, Wilson MS, Carr TP. Hepatic origin of cholesteryl oleate in coronary artery atherosclerosis in African green monkeys. Enrichment by dietary monounsaturaled fat. J Clin Invest 1997; 100:74-83.
48. Nielsen LB, Leth-Espensen P, Nordestgaard BG, Foged E, Kjeldsen K, Stender S. Replacement of dietary saturated fat with monounsaturated fat: effect on atherogenesis in cholesterol-fed rabbits clamped at the same plasma cholesterol level. Br J Nutr 1995; 74:509-521.
49. Staprans I, Rapp JH, Pan XM, Hardman DA, Feingold KR. Oxidized lipids in the diet accelerate the development of fatty streaks in cholesterol-fed rabbits. Arterioscler Thromb Vasc Biol 1996; 16:533-538. This unique study demonstrates that oxidized lipids present in the diet predispose to a higher risk of atherosclerosis in the rabbit model, suggesting a novel risk factor for the development of atherosclerosis.
50. Stephens NG, Parsons A, Schofield PM, Kelly F, Cheeseman K, Mitchinson MJ. Randomised controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet 1996; 347:781-786.
51. Kushi LH, Lew RA, Stare FJ, Ellison CR, el Lozy M, Bourke G, et al. Diet and 20-year mortality from coronary heart disease. The Ireland-Boston Diet-Heart Study. N Engl J Med 1985; 312:811-818.
52. McGee DL, Reed DM, Yano K, Kagan A, Tillotson J. Ten-year incidence of coronary heart disease in the Honolulu Heart Program. Relationship to nutrient intake. Am J Epidemiol 1984; 119:667-676.
53. Hu FB, Stampfer MJ, Manson JE, Rimm E, Colditz GA, Rosner BA, et al. Dietary fat intake and the risk of coronary heart disease in women. N Engl J Med 1997; 337:1491-1499. This large, prospective cohort study of 80 082 nurses using dietary questionnaires showed at follow-up after 14 years that dietary intake of saturated and trans unsaturated fat was associated with an increased CHD risk while higher intake of MUFA and PUFA fat was associated with reduced risk. Total fat intake by itself was not associated with any risk or benefit.
54. Ohrvall M, Berglund L, Salminen I, Lithell H, Aro A, Vessby B. The serum cholesterol ester fatty acid composition but not the serum concentration of alpha tocopherol predicts the development of myocardial infarction in 50-year-old men: 19 years follow-up. Atherosclerosis 1996; 127:65-71.
55. Watts GF, Jackson P, Mandalia S, Brunt JN, Lewis ES, Coltart DJ, Lewis B. Nutrient intake and progression of coronary artery disease. Am J Cardiol 1994; 73:328-332.
56. Haskell WL, Alderman EL, Fair JM, Maron DJ, Mackey SF, Superko HR, et al. Effects of intensive multiple risk factor reduction on coronary atherosclerosis and clinical cardiac events in men and women with coronary artery disease. The Stanford Coronary Risk Intervention Project (SCRIP). Circulation 1994; 89:975-990.
57. Ornish D, Brown SE, Scherwitz LW, Billings JH, Armstrong WT, Ports TA, et al. Can lifestyle changes reverse coronary heart disease? The Lifestyle Heart Trial. Lancet 1990; 336:129-133.
58. Schuler G, Hambrecht R, Schlierf G, Niebauer J, Hauer K, Neumann J, et al. Regular physical exercise and low-fat diet. Effects on progression of coronary artery disease. Circulation 1992; 86:1-11.
59. Arntzenius AC, Kromhout D, Barth JD, Reiber JH, Bruschke AV, Buis B, et al. Diet, lipoproteins, and the progression of coronary atherosclerosis. The Leiden Intervention Trial. N Engl J Med 1985; 312:805-811.
60. Watts GF, Jackson P, Burke V, Lewis B. Dietary fatty acids and progression of coronary artery disease in men. Am J Clin Nutr 1996; 64:202-209.
61. Blankenhorn DH, Johnson RL, Mack WJ, Zein HA, Vailas LI. The influence of diet on the appearance of new lesions in coronary human arteries. JAMA 1990; 263:318-324.
62. Tell GS, Evans GW, Folsom AR, Shimakawa T, Carpenter MA, Heiss G. Dietary fat intake and carotid artery wall thickness: the Atherosclerosis Risk in Communities (ARIC) Study. Am J Epidemiol 1994; 139:979-989.
63. Trichopoulou A, Kouris-Blazos A, Wahlqvist ML, Gnardellis C, Lagiou P, Polychronopoulous E, et al. Diet and overall survival in elderly peoole. BMJ 1995; 311:1457-1460.
64. Shekelle RB, Shryock AM, Paul O, Lepper M, Stamler J, Liu S, Raynor WJJ. Diet, serum cholesterol, and death from coronary heart disease. The Western Electric study. N Engl J Med 1981; 304:65-70.
65. Albert CM, Hennekens CH, O'Donnell CJ, Ajani UA, Carey VJ, Willett WC, et al. Fish consumption and risk of sudden cardiac death. JAMA 1998; 279:23-28.
66. Daviglus ML, Stamler J, Orencia AJ, Dyer AR, Liu K, Greenland P, et al. Fish consumption and the 30-year risk of fatal myocardial infarction. N Engl J Med 1997; 336:1046-1053. This epidemiologic study in men showed an inverse association between the risk of CHD (especially fatal myocardial infarction) and consumption of as little as one fish meal per week.
67. Siscovick DS, Raghunathan TE, King I, Weinmann S, Wicklund KG, Albright J, et al. Dietary intake and cell membrane levels of long-chain n-3 polyunsaturated fatty acids and the risk of primary cardiac arrest. JAMA 1995; 274:1363-1367.
68. Kromhout D, Bosschieter EB, de Lezenne C. The inverse relation between fish consumption and 20-year mortality from coronary heart disease. N Engl J Med 1985; 312:1205-1209.
69. Burr ML, Fehily AM, Gilbert JF, Rogers S, Holliday RM, Sweenam PM, et al. Effects of changes in fat, fish, and fibre intakes on death and myocardial reinfarction: Diet and Reinfarction Study (DART). Lancet 1989; 10:757-761.
70. Sacks FM, Stone PH, Gibson CM, Silverman DI, Rosner B, Pasternak RC. Controlled trial of fish oil for regression of human coronary atherosclerosis. HARP Research Group. J Am Coll Cardiol 1995; 25:1492-1498.
71. Goode GK, Garcia S, Heagerty AM. Dietary supplementation with marine fish oil improves in vitro small artery endothelial function in hypercholesterolemic patients: a double-blind placebo-controlled study. Circulation 1997; 96:2802-2807.
72. Pietinen P, Ascherio A, Korhonen P, Hartman AM, Willett WC, Albanes D, Virtamo J. Intake of fatty acids and risk of coronary heart disease in a cohort of Finnish men. The Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Am J Epidemiol 1997; 145:876-887.
73. Yam D, Eliraz A, Berry EM. Diet and disease - the Israeli paradox: possible dangers of a high omega-6 polyunsaturated fatty acid diet. Israel J Med Sci 1996; 32:1134-1143
74. Griffin ME, McInerney D, Fraser A, Johnson AH, Collins PB, Owens D, Tomkin GH. Autoantibodies to oxidized low density lipoprotein: the relationship to low density lipoprotein fatty acid composition in diabetes. Diabet Med 1997; 14:741-747.
75. Suarna C, Dean RT, Southwell-Keeley PT, Moore DE, Stocker R. Separation and characterization of cholesteryl oxo- and hydroxy-linoleate isolated from human atherosclerotic plaque. Free Radic Res 1997; 27:397-408. This study demonstrates that human carotid plaques contain extensive oxidation byproducts of linoleic acid, and also confirms observations from previous studies that oxidation of PUFA occurs in vivo in human arteries.
76. Felton CV, Crook D, Davies MJ, Oliver MF. Relation of plaque lipid composition and morphology to the stability of human aortic plaques. Arterioscler Thromb Vasc Biol 1997; 17:1337-1345. This pathology and biochemical study of human aortic plaques revealed that the edges of disrupted plaques contain increased amounts of cholesterol esters. These findings correlated with thin fibrous caps and the presence of macrophages, suggesting that these cholesterol esters may influence lesion compostion.
77. Staprans I, Rapp JH, Pan XM, Kim KY, Feingold KR. Oxidized lipids in the diet are a source of oxidized lipid in chylomicrons of human serum. Arterioscler Thromb 1994; 14:1900-1905.
78. Rapp JH, Connor WE, Lin DS, Porter JM. Dietary eicosapentaenoic acid and docosahexaenoic acid from fish oil. Their incorporation into advanced human atherosclerotic plaques. Arterioscler Thromb 1991; 11:903-911.
79. Zock PL, Mensink RP. Dietary trans-fatty acids and serum lipoproteins in humans. Curr Opin Lipidol 1996; 7:34-37.
80. Mensink RP, Katan MB. Effect of dietary trans fatty acids on high-density and low-density lipoprotein cholesterol levels in healthy subjects. N Engl J Med 1990; 323:439-445.
81. Lichtenstein AH. Trans fatty acids, plasma lipid levels, and risk of developing cardiovascular disease. A statement for healthcare professionals from the American Heart Association. Circulation 1997; 95:2588-2590. This is a succinct review summarizing the role of trans fatty acids in CHD.
82. Willett WC. Diet and health: what should we eat? Science 1994; 264:532-537.