Paradox of omega-3 PUFA oxidation

European Journal of Lipid Science and Technology

Volumn 116, Issue 10, 2014, Pages 1268-1279

  Miyashita, Kazuo ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

DHA; Emulsion; EPA; Liposome; Micelle; Oxidative stability

Indexed keywords

EID: 85027920513     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201400114     Document Type: Article

References (76)

1. Cho, S.-Y., Miyashita, K., Miyazawa, T., Fujimoto, K., Kaneda, T., Autoxidation of ethyl eicosapentaenoate and docosahexaenoate. J. Am. Oil Chem. Soc. 1987, 64, 876-879.
2. Cosgrove, J. P., Church, D. F., Pryor, W. A., The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids 1987, 22, 299-304.
3. Gunstone, F. D., Hilditch, T. P., The union gaseous oxygen with methyl oleate, linoleate, and linolenate. J. Chem. Soc. 1945, 836-841.
4. Holman, R. T., Elmer, O. C., The rates of oxidation of unsaturated fatty acids and esters. J. Am. Oil Chem. Soc. 1947, 24, 127-129.
5. Miyashita, K., Takagi, T., Study on the oxidative rate and prooxidant activity of free fatty acids. J. Am. Oil Chem. Soc. 1986, 63, 1380-1384.
6. Miyashita, K., Frankel, E. N., Neff, W. E., Awl, R. A., Autoxidation of polyunsaturated triacylglycerols. III. syntheytic triacylglycerols containing linoleate and linolenate. Lipids 1990, 25, 48-53.
7. Chen, B., McClements, D. J., Decker, E. A., Minor components in food oils: A critical review of their roles on lipid oxidation chemistry in bulk oils and emulsions. Crit. Rev. Food Sci. Nutr. 2011, 51, 901-916.
8. Coupland, J. N., McClements, D. J., Lipid oxidation in food emulsions. Trends Food Sci. Technol. 1996, 7, 83-91.
9. Frankel, E. N., Meyer, A. S., The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. J. Sci. Food Agric. 2000, 80, 1925-1941.
10. McClements, D. J., Decker, E. A., Lipid oxidation in oil-in-water emulsions: Impact of molecular environment on chemical reactions in heterogeneous food systems. J. Food Sci. 2000, 65, 1270-1282.
11. Sun, Y.-E., Wang, W.-D., Chen, H.-W., Li, C., Autoxidation of unsaturated lipids in food emulsion. Crit. Rev. Food Sci. Nutr. 2011, 51, 453-466.
12. Waraho, T., McClements, D. J., Decker, E. A., Mechanisms of lipid oxidation in food dispersions, Trends Food Sci. Technol. 2011, 22, 3-13.
13. Miyashita, K., Nara, E., Ota, T., Oxidative stability of polyunsaturated fatty acids in an aqueous solution. Biosci. Biotechnol. Biochem. 1993, 57, 1638-1640.
14. Miyashita, K., Polyunsaturated lipids in aqueous systems do not follow our preconceptions of oxidative stability. Lipid Technol. Newsletter 2002, 8, 35-41.
15. Miyashita, K., Effects of flexibility and permeability of polyunsaturated fatty acid molecules on their oxidative stability in aqueous systems. Lipid Technol. Newsletter 2004, 16, 197-202.
16. Kato, T., Hirukawa, T., Namiki, K., Selective terminal olefin oxidation of n-3 polyunsaturated fatty acids. Tetrahedron Lett. 1992, 33, 1475-1478.
17. Kobayashi, H., Yoshida, M., Maeda, I., Miyashita, K., Proton NMR relaxation times of polyunsaturated fatty acids in chloroform solutions and aqueous micelles. J. Oleo Sci. 2004, 56, 105-108.
18. Miyashita, K., Inukai, N., Ota, T., Effect of Tween 20 on the oxidative stability of sodium linoleate and sodium docosahexaenoate. Biosci. Biotechnol. Biochem. 1997, 61, 716-717.
19. Hirano, S., Miyashita, K., Ota, T., Nishikawa, M., et al., Aqueous oxidation of ethyl linoleate, ethyl linolenate, and ethyl docosahexaenoate. Biosci. Biotechnol. Biochem. 1997, 61, 281-285.
20. Kobayashi, H., Yoshida, M., Miyashita, K., Comparative study of the product components of lipid oxidation in aqueous and organic systems. Chem. Phys. Lipids 2003, 126, 111-120.
21. Miyashita, K., Hirano, S., Itabashi, Y., Ota, T., et al., Oxidative stability of polyunsaturated monoacylglycerol and triacylglycerol in aqueous micelles. J. Jpn. Oil Chem. Soc. 1997, 46, 205-208.
22. Miyashita, K., Hirao, M., Nara, E., Ota, T., Oxidative stability of triglycerides from orbital fat of tuna and soybean oil in an emulsion. Fisheries Sci. 1995, 61, 273-275.
23. Lethuaut, L., Métro, F., Genot, C., Effect of droplet size on lipid oxidation rates of oil-in-water emulsions stabilized by protein. J. Am. Oil. Chem. Soc. 2002, 79, 425-430.
24. Azuma, G., Kimura, N., Hosokawa, M., Miyashita, K., Effect of droplet size on the oxidative stability of soybean oil TAG and fish oil TAG in oil-in-water emulsion. J. Oleo Sci. 2009, 58, 329-338.
25. Araseki, M., Yamamoto, K., Miyashita, K., Oxidative stability of polyunsaturated fatty acid in phosphatidylcholine liposomes. Biosci. Biotechnol. Biochem. 2002, 66, 2573-2577.
26. Miyashita, K., Nara, E., Ota, T., Comparative study on the oxidative stability of phosphatidylcholines from salmon egg and soybean in an aqueous solution. Biosci. Biotechnol. Biochem. 1994, 58, 1772-1775.
27. Nara, E., Miyashita, K., Ota, T., Oxidative stability of liposomes prepared from soybean PC, chicken egg PC, and salmon egg PC. Biosci. Biotechnol. Biochem. 1997, 61, 1736-1738.
28. Nara, E., Miyashita, K., Ota, T., Nadachi, Y., The oxidative stabilities of polyunsaturated fatty acids in salmon egg phosphatidylcholine liposomes. Fisheries Sci. 1998, 64, 282-286.
29. Applegate, K. R., Glomset, J. A., Computer-based modeling of the conformation and packing properties of docosahexaenoic acid. J. Lipid Res. 1986, 27, 658-680.
30. Applegate, K. R., Glomset, J. A., Effect of acyl chain unsaturation on the conformation of model diacylglycerols-a computer modeling study. J. Lipid Res. 1991a, 32, 1635-1644.
31. Applegate, K. R., Glomset, J. A., Effect of acyl chain unsaturation on the packing of model diacylglycerols in simulated monolayers. J. Lipid Res. 1991b, 32, 1645-1655.
32. Albrand, M., Pageaux, J. F., Lagarde, M., Dolmazon, R., Conformational-analysis of isolated docosahexaenoic acid (22/6N-3) and its 14-(S) and 11-(S) hydroxyl derivatives by force-field calculations. Chem. Phys. Lipids 1994, 72, 7-17.
33. Brockman, H. L., Applegate, K. R., Momsen, M. M., King, W. C., Glomset, J. A., Packing and electrostatic behavior of sn-2 docosahexaenoyl and -arachidonoyl phosphoglycerides. Biophys. J. 2003, 85, 2384-2396.
34. Feng, S. S., Brockman, H. L., Macdonald, R. C., On osmotictype equations of state for liquid-expanded monolayers of lipids at the air-water-interface. Langmuir 1994, 10, 3188-3194.
35. 13C NMR of multilamellar dispersions of polyunsaturated (22:6) phospholipids. Biophys. J. 2000, 79, 885-897.
36. Feller, S. E., Garwrish, K., MacKerell, A. D. Jr., Polyunsaturated fatty acids in lipid bilayers intrinsic and environmental contributions to their unique physical properties. J. Am. Chem. Soc. 2002, 124, 318-326.
37. 2H NMR and molecular dynamics simulations. J. Am. Chem. Soc. 2002, 124, 298-309.
38. Saiz, L., Klein, M. L., Structural properties of a highly polyunsaturated lipid bilayer from molecular dynamics simulations. Biophys. J. 2001, 81, 204-216.
39. 17O NMR. Biophys. J. 1997, 73, 855-864.
40. Olbrich, K., Rawicz, W., Needham, D., Evans, E., Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 2000, 79, 321-327.
41. Coxon, D. T., Proce, K. R., Chan, H. W.-S., Formation, isolation and structure dtermination of methyl linolenate diperoxides. Chem. Phys. Lipids 1981, 28, 365-378.
42. Neff, W. E., Frankel, E. N., Weisleder, D., High pressure liquid chromatography of autoxidized lipids: II. hydroperoxy-cyclic peroxides and other secondary products from methyl linolenate. Lipids 1981, 16, 439-448.
43. Porter, N. A., Galdwell, S. E., Mills, K. A., Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995, 30, 277-290.
44. Allayee, H., Roth, N., Hodis, H. N., Polyunsaturated fatty acids and cardiovascular disease: implications for nutrigenetics. J. Nutrigenet. Nutrigenomics 2009, 2, 140-148.
45. Calder, P. C., n-3 Fatty acids and cardiovascular disease: Evidence explained and mechanisms explored. Clin. Sci. 2004, 107, 1-11.
46. Kris-Etherton, P. M., Harris, W. S., Appel, L. J., Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002, 106, 2747-2757.
47. Leaf, A., Kang, J. X., Xiao, Y.-F., Fish oil fatty acids as cardiovascular drugs. Curr. Vasc. Pharmacol. 2008, 6, 1-12.
48. Russo, G. L., Dietary n-6 and n-3 polyunsaturated fatty acids: From biochemistry to clinical implications in cardiovascular prevention. Biochem. Pharmacol. 2009, 77, 937-946.
49. Wang, C., Harris, W. S., Chung, M., Lichtenstein, A. H., et al., Fatty acids from fish or fish-oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary prevention studies: A systematic review. Am. J. Clin. Nutr. 2006, 84, 5-17.
50. Hoffman, D. R., Boettcher, J. A., Diersen-Schade, D. A., Toward optimizing vision and cognition in term infants by dietary docosahexaenoic and arachidonic acid supplementation: A review of randomized controlled trials. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81, 151-158.
51. Le, H. D., Meisel, J. A., de Meijer, V. E., Gura, K. M., Puder, M., The essentiality of arachidonic acid and docosahexaenoic acid. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81, 165-170.
52. Davis-Bruno, K., Tassinari, M. S., Essential fatty acid supplementation of DHA and ARA and effects on neurodevelopment across animal species: A review of the literature. Birth Defects Res. B 2011, 92, 240-250.
53. Araseki, M., Kobayashi, H., Hosokawa, M., Miyashita, K., Lipid peroxidation of a human hepatoma cell line (HepG2) after incorporation of linoleic acid, arachidonic acid, and docosahexaenoic acid. Biosci. Biotechnol. Biochem. 2005, 69, 483-490.
54. Kubo, K., Saito, M., Tadokoro, T., Maekawa, A., Changes in susceptibility of tissues to lipid peroxidation after ingestion of various levels of docosahexaenoic acid and vitamin E. Br. J. Nutr. 1997, 78, 655-669.
55. Kubo, K., Saito, M., Tadokoro, T., Maekawa, A., Dietary docosahexaenoic acid does not promote lipid peroxidation in rat tissue to the extent expected from peroxidizability index of the lipids. Biosci. Biotechnol. Biochem. 1998, 62, 1698-1706.
56. Kubo, K., Saito, M., Tadokoro, T., Maekawa, A., Preferential incorporation of docosahexaenoic acid into nonphosphorus lipids and phosphatidylethanolamine protects rats from dietary DHA-stimulated lipid peroxidation. J. Nutr. 2000, 130, 1749-1759.
57. Ando, K., Nagata, K., Yoshida, R., Kikugawa, K., Suzuki, M., Effect of n-3 polyunsaturated fatty acid supplementation on lipid peroxidation of rat organs. Lipids 2000, 35, 401-407.
58. Wander, R. C., Du, S.-H., Oxidation of plasma proteins is not increased after supplementation with eicosapentaenoic and docosahexaenoic acids. Am. J. Clin. Nutr. 2000, 72, 731-737.
59. Wander, R. C., Du, S.-H., Thomas, D. R., Influence of long-chain polyunsaturated fatty acids on oxidation of low density lipoprotein. Prostaglandins Leukot. Essent. Fatty Acids 1998, 59, 143-151.
60. Eritsland, J., Arnesen, H., Seljeflot, I., Høstmark, A. T., Long-term metabolic effects of n-3 polyunsaturated fatty acids in patients with coronary artery disease. Am. J. Clin. Nutr. 1995, 61, 831-836.
61. Bonanome, A., Biasia, F., De Luca, M., Munaretto, G., et al., n-3 Fatty acids do not enhance LDL susceptibility to oxidation in hypertriacylglycerolemic hemodialyzed subjects. Am. J. Clin. Nutr. 1996, 63, 261-266.
62. Brude, I. R., Drevon, C. A., Hjermann, I., Seljeflot, I., et al., Sandstad, B., Solvoll, K., Halvorsen, B., Arnesen, H., Nenseter, M.S., Peroxidation of LDL from combined-hyperlipidemic male smokers supplied with ω-3 fatty acids and antioxidants. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 2576-2588.
63. Frankel, E. N., Parks, E. J., Xu, R., Schneeman, B. O., et al., Effect of n-3 fatty acid-rich fish oil supplementation on the oxidation of low density lipoproteins. Lipids 1994, 29, 233-236.
64. Hansen, J. B., Berge, R. K., Nordøy, A., Bønaa, K. H., Lipid plasma after intake of highly purified eicosapentaenoic or docosahexaenoic acids. Lipids 1998, 33, 1123-1129.
65. Higdon, J. V., Du, S. H., Lee, Y. S., Wu, T., Wander, R. C., Supplementation of postmenopausal women with fish oil does not increase overall oxidation of LDL ex vivo compared to dietary oils rich in oleate and linoleate. J. Lipid Res. 2001, 42, 407-418.
66. Higgins, S., Carrol, Y. L., McCarthy, S. N., Corridan, B. M., et. al., Susceptibility of LDL to oxidative modification in healthy volunteers supplemented with low doses of n-3 polyunsaturated fatty acids. Br. J. Nutr. 2001, 85, 23-31.
67. Nenseter, M. S., Rustan, A. C., Lund-Katz, S., Soyland, E., et. al., Effects of dietary supplementation with n-3 polyunsaturated fatty acids on physical properties and metabolism of low density lipoproteins in humans. Arterioscl. Thromb. 1992, 12, 369-379.
68. Ottestad, I., Vogt, G., Retterstøl, K., Myhrstad, M. C., et. al., Oxidised fish oil does not influence established markers of oxidative stress in healthy hum an subject s: A randomised controlled trial. Br. J. Nutr. 2012, 108, 315-326.
69. Egert, S., Somoza, V., Kannenberg, F., Fobker, M., et. al., Influence of three rapeseed oil-rich diets, fortified with α-linolenic acid, eicosapentaenoic acid or docosahexaenoic acid on the composition and oxidizability of low-density lipoproteins: Results of a controlled study in healthy volunteers. Eur. J. Clin. Nutr. 2007, 61, 314-325.
70. Grundt, H., Nilsen, D. W. T., Mansoor, M. A., Nordøy, A., Increased lipid peroxidation during long-term intervention with high doses of n-3 fatty acids (PUFA s) following an acute myocardial infarction. Eur. J. Clin. Nutr. 2003, 57, 793-800.
71. Harats, D., Dabach, Y., Hollander, G., Ben-Naim, M., et. al., (1991): Fish oil ingestion in smokers and nonsmokers enhances peroxidation of plasma lipoproteins. Atherosclerosis 1991, 90, 127-139.
72. Meydani, M., Natiello, F., Goldin, B., Free, N., et al., Effect of long -term fish oil supplementation on vitamin E status and lipid peroxidation in women. J. Nutr. 1991, 121, 484-491.
73. Oostenbrug, G. S., Mensink, R. P., Hornstra, G., Effects of fish oil and vitamin E supplementation on copper-catalysed oxidation of human low density lipoprotein in vitro. Eur. J. Clin. Nutr. 1994, 48, 895-898.
74. Roberts, W. G., Gordon, M. H., Walker, A. F., Effects of enhanced consumption of fruit and vegetables on plasma antioxidant status and oxidative resistance of LDL in smokers supplemented with fish oil. Eur. J. Clin. Nutr. 2003, 57, 1303-1310.
75. Suzukawa, M., Abbey, M., Howe, P. R. C., Nestel, P. J., Effects of fish oil fatty acids on low density lipoprotein size, oxidizability, and uptake by macrophages. J. Lipid Res. 1995, 36, 473-484.
76. Turini, M. E., Crozier, G. L., Donnet-Hughes, A., Richelle, M. A., Short term fish oil supplementation improved innate immunity, but increased ex vivo oxidation of LDL in man-a pilot study. Eur. J. Nutr. 2001, 40, 56-65.