Fatty acids from fish: The anti-inflammatory potential of long-chain omega-3 fatty acids

Nutrition Reviews

Volumn 68, Issue 5, 2010, Pages 280-289

  Wall, Rebecca ^a   Ross, R Paul ^a,b   Fitzgerald, Gerald F ^c   Stanton, Catherine ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Anti inflammatory; DHA; EPA; Fish oil; Omega 3

Indexed keywords

ADRENIC ACID; ALPHA TOCOPHEROL; ARACHIDONIC ACID; DIHOMO GAMMA LINOLENIC ACID; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; FATTY ACID DERIVATIVE; FISH OIL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; ICOSANOID; ICOSAPENTAENOIC ACID; ICOSATETRAENOIC ACID; LIGNOCERIC ACID; LINOLEIC ACID; LONG CHAIN FATTY ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PLACEBO; POLYUNSATURATED FATTY ACID; STEARIDONIC ACID;

ANTIINFLAMMATORY ACTIVITY; CARDIOVASCULAR DISEASE; CHRONIC INFLAMMATION; DIETARY INTAKE; ENTERITIS; FISH; FOOD INTAKE; GENE EXPRESSION; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; MARINE BACTERIUM; MENTAL DISEASE; NEOPLASM; NERVE DEGENERATION; NONHUMAN; REVIEW; RHEUMATOID ARTHRITIS; SUPPLEMENTATION; ANIMAL; CHRONIC DISEASE; INFLAMMATION; METABOLISM; NUTRITIONAL VALUE; SEA FOOD;

ANIMALS; CHRONIC DISEASE; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FISHES; HUMANS; INFLAMMATION; NUTRITIVE VALUE; SEAFOOD;

EID: 77953904162     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1111/j.1753-4887.2010.00287.x     Document Type: Review

References (117)

1. Das UN. Biological significance of essential fatty acids. J Assoc Physicians India. 2006;54:309-319.
2. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr. 2006;83:1505-1519.
3. Simopoulos AP. Importance of the ratio of omega-6/ omega-3 essential fatty acids: Evolutionary aspects. World Rev Nutr Diet. 2003;92:1-22.
4. Sanders TA. Polyunsaturated fatty acids in the food chain in Europe. Am J Clin Nutr. 2000;71(Suppl):S176-S178.
5. Simopoulos AP, Leaf A, Salem N. Workshop statement on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2000;63:119-121.
6. James MJ, Gibson RA, Cleland LG. Dietary polyunsaturated fatty acids and inflammatory mediator production. Am J Clin Nutr. 2000;71(Suppl):S343-S348.
7. Simopoulos AP. Essential fatty acids in health and chronic diseases. Forum Nutr. 2003;56:67-70.
8. Shahidi F,Miraliakbari H. Omega-3 (n-3) fatty acids in health and disease: Part 1 - cardiovascular disease and cancer. J Med Food. 2004;7:387-401.
9. Sprecher H. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta. 2000;1486:219-231.
10. Simopoulos AP. n-3 fatty acids and human health: Defining strategies for public policy. Lipids. 2001;36(Suppl):S83-S89.
11. Kris-Etherton P, Hecker M, Binkoski KD. Polyunsaturated fatty acids and cardiovascular health. Nutr Rev. 2004;62:414-426.
12. Mantzioris E, James MJ, Gibson RA, Cleland LG. Dietary substitution with an alpha-linolenic acid rich vegetable oil increases eicosapentaenoic acid concentrations in tissues. Am J Clin Nutr. 1994;59:1304-1309.
13. Wallace FA,Miles EA, Calder PC. Comparison of the effects of linseed oil and different doses of fish oil on mononuclear cell function in healthy human subjects. Br J Nutr. 2003;89:679-689.
14. Finnegan YE, Minihane AM, Leigh-Firbank EC, et al. Plantand marine-derived n-3 polyunsaturated fatty acids have differential effects on fasting and postprandial blood lipid concentrations and on the susceptibility of LDL to oxidative modification in moderately hyperlipidemic subjects. Am J Clin Nutr. 2003;77:783-795.
15. Liou YA, King DJ, Zibrik D, Innis SM. Decreasing linoleic acid with constant alpha-linolenic acid in dietary fats increases (n-3) eicosapentaenoic acid in plasma phospholipids in healthy men. J Nutr. 2007;137:945-952.
16. Burdge GC. Metabolism of alpha-linolenic acid in humans. Prostaglandins Leukot Essent Fatty Acids. 2006;75:161-168.
17. DeFilippis AP, Sperling LS. Understanding omega-3s. Am Heart J. 2006;151:564-570.
18. Kris-Etherton PM, Griegera JA, Etherton TB. Dietary reference intakes for DHA, EPA. Prostaglandins Leukot Essent Fatty Acids. 2009;81:99-104.
19. Erwin J, Bloch K. Biosynthesis of unsaturated fatty acids in microorganisms. Science. 1964;143:1006-1012.
20. Wirsen CO, Jannaschm HW, Waleham SG, Canuel EA. Membrane lipids of a psychrophilic and barophilic deep-sea bacterium. Curr Microbiol. 1987;14:312-322.
21. Singh A,Ward OP.Microbial production of docosahexaenoic acid (DHA, C22:6). Adv Appl Microbiol. 1997;45:271-312.
22. Yanu Y, Nakayama A, Saito H, Ishihara K. Production of docosahexaenoic acid by marine bacteria isolated from deep-sea fish. Lipids. 1994;29:527-528.
23. Metz JG, Roessler P, Facciotti D, et al. Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science. 2001;293:290-293.
24. Ootaki M, Morita N, Nishida T, et al. Genes and pathways involved in biosynthesis of eicosapentaenoic and docosahexaenoic acids in bacteria. In: Murata N, Yamada M, Nishida I, Okuyama H, Sekiya J, Wada H, eds. Advanced Research on Plant Lipids. Dordrecht, The Netherlands: Kluwer Academic Publishers; 2003:49-52.
25. Orikasa Y, Yamada A, Yu R, et al. Characterisation of the eicosapentaenoic acid biosynthesis gene cluster from Shewanella sp. Strain SCRC-2738. Cell Mol Biol. 2004;50:625-630.
26. Morita N, Nishida T, Tanaka N, Yano Y, Okuyama H. Enhancement of polyunsaturated fatty acid production by cerulenin treatment in polyunsaturated fatty acid-producing bacteria. Biotechnol Lett. 2005;27:389-393.
27. Amiri-Jami M, Wang H, Kakuda Y, Griffiths MW. Enhancement of polyunsaturated fatty acid production by Tn5 transposon in Shewanella baltica. Biotechnol Lett. 2006;28: 1187-1192.
28. Orikasa Y, Nishida T, Yamada A, et al. Recombinant production of docosahexaenoic acid in a polyketide biosynthesis mode in Escherichia coli. Biotechnol Lett. 2006;28:1841-1847.
29. Lee SJ, Kim CH, Seo PS, Kwon O, Hur BK, Seo JW. Enhancement of heterologous production of eicosapentaenoic acid in Escherichia coli by substitution of promoter sequences within the biosynthesis gene cluster. Biotechnol Lett. 2008;30:2139-2142.
30. Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A. Dietary long-chain n-3 fatty acids for the prevention of cancer: A review of potential mechanisms. Am J Clin Nutr. 2004;79:935-945.
31. Brittish Nutrition Foundation. Briefing Paper: N-3 Fatty Acids and Health. London: British Nutrition Foundation; 1999.
32. Calder PC, Burdge GC. Fatty acids. In: Nicolaou A, Kokotos G, eds. Bioactive Lipids. Bridgewater, UK: The Oily Press; 2004: 1-36.
33. Surette ME. The science behind omega-3 fatty acids. Can Med Assoc J. 2008;178:177-180.
34. Calder PC, Yaqoob P. Omega-3 polyunsaturated fatty acids and human health outcomes. Biofactors. 2009;35:266-272.
35. Tilley SL, Coffman TM, Koller BH. Mixed messages: Modulation of inflammation and immune responses by prostaglandins and thromboxanes. J Clin Invest. 2001;108:15-23.
36. Kinsella JE, Lokesh B, Broughton S, Whelan J. Dietary polyunsaturated fatty acids and eicosanoids: Potential effects on the modulation of inflammatory and immune cells: An overview. Nutrition. 1990;6:24-44.
37. Calder PC. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res. 2008;52:885-897.
38. Calder PC. Polyunsaturated fatty acids, inflammation, and immunity. Lipids. 2001;36:1007-1024.
39. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21:495-505.
40. Bagga D, Wang L, Farias-Eisner R, Glaspy JA, Reddy ST. Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc Natl Acad Sci USA. 2003;100:1751-1756.
41. Wallace JL. Prostaglandin biology in inflammatory bowel disease. Gastroenterol Clin North Am. 2001;30:971-980.
42. Jupp J, Hillier K, Elliott DH, et al. Colonic expression of leukotriene-pathway enzymes in inflammatory bowel diseases. Inflamm Bowel Dis. 2007;13:537-546.
43. Robinson JG, Stone NJ. Antiatherosclerotic and antithrombotic effects of omega-3 fatty acids. Am J Cardiol. 2006;98:39-49.
44. Goldman DW, Pickett WC, Goetzl EJ. Human neutrophil chemotactic and degranulating activities of leukotriene B5 (LTB5) derived from eicosapentaenoic acid. Biochem Biophys Res Commun. 1983;117:282-288.
45. Lee TH, Mencia-Huerta JM, Shih C, Corey EJ, Lewis RA, Austen KF. Characterization and biologic properties of 5,12- dihydroxy derivatives of eicosapentaenoic acid, including leukotriene-B5 and the double lipoxygenase product. J Biol Chem. 1984;259:2383-2389.
46. Hong S, Gronert K, Devchand PR, Moussignac RL, Serhan CN. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem. 2003;278:14677-14687.
47. Serhan CN, Hong S, Gronert K, et al. Resolvins: A family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025-1037.
48. Serhan CN, Lu Y, Hong S, Yang R. Mediator lipidomics: Search algorithms for eicosanoids, resolvins, and protectins. Meth Enzymol. 2007;432:275-317.
49. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature. 2007;447:869-874.
50. Serhan CN, Clish CB, Brannon J, Colgan SP, Chiang N, Gronert K. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med. 2000;192:1197-1204.
51. Weylandt KH, Kang JX, Wiedenmann B, Baumgart DC. Lipoxins and resolvins in inflammatory bowel disease. Inflamm Bowel Dis. 2007;13:797-799.
52. Endres S, Ghorbani R, Kelley VE, et al. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med. 1989;320:265-271.
53. Yaqoob P, Pala HS, Cortina-Borja M, Newsholme EA, Calder PC. Encapsulated fish oil enriched in a-tocopherol alters plasma phospholipid and mononuclear cell fatty acid compositions but not mononuclear cell functions. Eur J Clin Invest. 2000;30:260-274.
54. Healy DA, Wallace FA, Miles EA, Calder PC, Newsholm P. Effect of low-to-moderate amounts of dietary fish oil on neutrophil lipid composition and function. Lipids. 2000;35:763-768.
55. Rees D, Miles EA, Banerjee T, et al. Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: A comparison of young and older men. Am J Clin Nutr. 2006;83:331-342.
56. Gibney MJ, Hunter B. The effects of short- and long-term supplementation with fish oil on the incorporation of n-3 polyunsaturated fatty acids into cells of the immune system in healthy volunteers. Eur J Clin Nutr. 1993;47:255-259.
57. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ. The effect on human tumor necrosis factor a and interleukin 1b production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr. 1996;63:116-122.
58. Trebble TM, Wootton SA, Miles EA, et al. Prostaglandin E2 production and T cell function after fish-oil supplementation: Response to antioxidant cosupplementation. Am J Clin Nutr. 2003;78:376-382.
59. Kelley DS, Taylor PC, Nelson GJ, et al. Docosahexaenoic acid ingestion inhibits natural killer cell activity and production of inflammatory mediators in young healthy men. Lipids. 1999;34:317-324.
60. von Schacky C, Kiefl R, Jendraschak E, KaminskiWE. n-3 fatty acids and cysteinyl-leukotriene formation in humans in vitro, ex vivo, and in vivo. J Lab Clin Med. 1993;121:302-309.
61. Calder PC. Dietary modification of inflammation with lipids. Proc Nutr Soc. 2002;61:345-358.
62. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell. 2002;109(Suppl):S81-S96.
63. Lo CJ, Chiu KC, Fu M, Lo R, Helton S. Fish oil decreases macrophage tumor necrosis factor gene transcription by altering the NF kappa B activity. J Surg Res. 1999;82:216-221.
64. Novak TE, Babcock TA, Jho DH, Helton WS, Espat NJ. NF-kB inhibition by w-3 fatty acids modulates LPS-stimulated macrophage TNF-a transcription. Am J Physiol. 2003;284:L84-L89.
65. Zhao Y, Joshi-Barve S, Barve S, Chen LH. Eicosapentaenoic acid prevents LPS-induced TNF-a expression by preventing NF-kB activation. J Am Coll Nutr. 2004;23:71-78.
66. Hudert CA, Weylandt KH, Lu Y, et al. Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc Natl Acad Sci USA. 2006;103:11276-11281.
67. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ. Nuclear receptors and lipid physiology: Opening the X-files. Science. 2001;294:1866-1870.
68. Kota BP, Huang TH, Roufogalis BD. An overview on biological mechanisms of PPARs. Pharmacol Res. 2005;51:85-94.
69. Poynter ME, Daynes RA. Peroxisome proliferator-activated receptor alpha activation modulates cellular redox status, represses nuclear factor-kappaB signaling, and reduces inflammatory cytokine production in aging. J Biol Chem. 1998;273:32833-32841.
70. Ricote M, Huang JT, Welch JS, Glass CK. The peroxisome proliferator-activated receptor (PPARgamma) as a regulator of monocyte/macrophage function. J Leukoc Biol. 1999;66:733-739.
71. Li H, Ruan XZ, Powis SH, et al. EPA and DHA reduce LPSinduced inflammation responses in HK-2 cells: Evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 2005;67:867-874.
72. Calder PC. Session 3: Joint Nutrition Society and Irish Nutrition and Dietetic Institute Symposium on "Nutrition and autoimmune disease" PUFA, inflammatory processes and rheumatoid arthritis. Proc Nutr Soc. 2008;67:409-418.
73. Sijben JWC, Calder PC. Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease. Proc Nutr Soc. 2007;66:237-259.
74. Shoda R, Matsueda K, Yamato S, Umeda N. Epidemiologic analysis of Crohn disease in Japan: Increased dietary intake of n-6 polyunsaturated fatty acids and animal protein relates to the increased incidence of Crohn disease in Japan. Am J Clin Nutr. 1996;63:741-745.
75. Sakamoto N, Kono S, Wakai K, et al. Dietary risk factors for inflammatory bowel disease: A multicenter case-control study in Japan. Inflamm Bowel Dis. 2005;11:154-163.
76. Shimizu T, Fujii T, Suzuki R, et al. Effects of highly purified eicosapentaenoic acid on erythrocyte fatty acid composition and leukocyte and colonic mucosa leukotriene B4 production in children with ulcerative colitis. J Pediatr Gastroenterol Nutr. 2003;37:581-585.
77. Hawthorne AB, Daneshmend TK, Hawkey CJ. Treatment of ulcerative colitis with fish oil supplementation: A prospective 12 month randomised controlled trial. Gut. 1992;33:922-928.
78. Trebble TM, Arden NK, Wootton SA, et al. Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn disease. Am J Clin Nutr. 2004;80:1137-1144.
79. Chapkin RS, Davidson LA, Ly L, Weeks BR, Lupton JR, McMurray DN. Immunomodulatory effects of (n-3) fatty acids: Putative link to inflammation and colon cancer. J Nutr. 2007;137:200-204.
80. Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med. 1996;334:1557-1560.
81. Ferrucci L, Cherubini A, Bandinelli S, et al. Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. J Clin Endocrinol Metab. 2006;91:439-446.
82. Serhan CN, Savill J. Resolution of inflammation: The beginning programs the end. Nat Immunol. 2005;6:1191-1197.
83. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med. 1999;340:115-126.
84. Bang HO, Dyerberg J. Lipid metabolism and ischemic heart disease in Greenland Eskimos. Acta Med Scand. 1976;200:69-73.
85. Menotti A, Kromhout D, Blackburn H, Fidanza F, Buzina R, Nissinen A. Food intake patterns and 25-year mortality from coronary heart disease: Cross-cultural correlations in the Seven Countries Study. The Seven Countries Study Research Group. Eur J Epidemiol. 1999;15:507-515.
86. Holub BJ. Clinical nutrition: 4. Omega-3 fatty acids in cardiovascular care. CMAJ. 2002;166:608-615.
87. Lemaitre RN, King IB, Mozaffarian D, Kuller LH, Tracy RP, Siscovick DS. n-3 polyunsaturated fatty acids, fatal ischemic heart disease, and nonfatal myocardial infarction in older adults: The Cardiovascular Health Study. Am J Clin Nutr. 2003;77:279-280.
88. He K, Song Y, Daviglus ML, et al. Accumulated evidence on fish consumption and coronary heart disease mortality: A meta-analysis of cohort studies. Circulation. 2004;109:2705-2711.
89. Mozaffarian D, Geelen A, Brouwer IA, Geleijnse JM, Zock PL, Katan MB. Effect of fish oil on heart rate in humans: A metaanalysis of randomized controlled trials. Circulation. 2005;112:1945-1952.
90. Yokoyama M, Origasa H, MatsuzakiM, et al. Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): A randomised open-label, blinded endpoint analysis. Lancet. 2007;369:1090-1098.
91. Gissi HF, Tavazzi L, Maggioni A, et al. Effect on n-3 polyunsaturated fatty acids in patients with chronic heart failure (the GISSI-HF trial): A randomised, double-blind, placebocontrolled trial. Lancet. 2008;372:1223-1230.
92. Folsom AR, Demissie Z. Fish intake, marine omega-3 fatty acids, and mortality in a cohort of postmenopausal women. Am J Epidemiol. 2004;160:1005-1010.
93. Streppel MT, Ocké MC, Boshuizen HC, Kok FJ, Kromhout D. Long-term fish consumption and n-3 fatty acid intake in relation to (sudden) coronary heart disease death: The Zutphen study. Eur Heart J. 2008;29:2024-2030.
94. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardio (GISSI) (Italian Group for the Study of the Survival of Myocardial Infarction). Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: Results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico. Lancet. 1999;354:447-455.
95. MatsuzakiM, YokoyamaM, Saito Y, et al. Incremental effects of eicosapentaenoic acid on cardiovascular events instatin-treated patients with coronary artery disease. Circ J. 2009;73:1283-1290.
96. He K. Fish, long-chain omega-3 polyunsaturated fatty acids and prevention of cardiovascular disease - eat fish or take fish oil supplements? Prog Cardiovasc Dis. 2009;52:95-114.
97. Van de Werf F, Bax J, Betriu A, et al. Management of acute myocardial infarction in patients presenting with persistent ST-segment elevation: The Task Force on the Management of ST-Segment Elevation Acute Myocardial Infarction of the European Society of Cardiology. Eur Heart J. 2008;29:2909-2945.
98. British Cardiac Society, British Hypertension Society, Diabetes UK, and HEART UK. Primary Care Cardiovascular Society, and Stroke Association. JBS 2: Joint British Societies' guidelines on prevention of cardiovascular disease in clinical practice. Heart. 2005;91:v1-v52.
99. Julien C, Berthiaume L, Hadj-Tahar A, et al. Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and Parkinsonian monkeys. Neurochem Int. 2006;48:404-414.
100. Salem N, Wegher B, Mena P, Uauy R. Arachidonic and docosahexaenoic acids are biosynthesized from their 18-carbon precursors in human infants. Proc Natl Acad Sci USA. 1996;93:49-54.
101. Fedorova I, Salem N Jr. Omega-3 fatty acids and rodent behaviour. Prostaglandins Leukot Essent Fatty Acids. 2006;75:271-289.
102. Pawlosky RJ, Bacher J, Salemn N Jr. Ethanol consumption alters electroretinograms and depletes neural tissues of docosahexaenoic acid in rhesus monkeys: Nutritional consequences of a low n-3 fatty acid diet. Alcohol Clin Exp Res. 2001;25:1758-1765.
103. Murthy M, Hamilton J, Greiner RS, Moriguchi T, Salem N Jr, Kim HY. Differential effects of n-3 fatty acid deficiency on phospholipid molecular species composition in the rat hippocampus. J Lipid Res. 2002;43:611-617.
104. Levant B, Ozias MK, Carlson SE. Specific brain regions of female rats are differentially depleted of docosahexaenoic acid by reproductive activity and an (n-3) fatty aciddeficient diet. J Nutr. 2007;137:130-134.
105. Heude B, Ducimetière P, Berr C. Cognitive decline and fatty acid composition of erythrocyte membranes - The EVA Study. Am J Clin Nutr. 2003;77:803-808.
106. Schaefer EJ, Bongard V, Beiser AS, et al. Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: The Framingham Heart Study. Arch Neurol. 2006;63:1545-1550.
107. Hashimoto M, Hossain S, Shimada T, et al. Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats. J Neurochem. 2002;81:1084-1091.
108. Lim GP, Calon F, Morihara T, et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci. 2005;25:3032-3040.
109. Hashimoto M, Hossain S, Agdul H, Shido O. Docosahexaenoic acid-induced amelioration on impairment of memory learning in amyloid beta-infused rats relates to the decreases of amyloid beta and cholesterol levels in detergent-insoluble membrane fractions. Biochim Biophys Acta. 2005;1738:91-98.
110. Barberger-Gateau P, Letenneur L, Deschamps V, Pérès K, Dartigues JF, Renaud S. Fish, meat, and risk of dementia: Cohort study. BMJ. 2002;325:932-933.
111. Morris MC, Evans DA, Bienias JL, et al. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch Neurol. 2003;60:940-946.
112. Kalmijn S, van Boxtel MP, Ocke M, et al. Dietary intake of fatty acids and fish in relation to cognitive performance at middle age. Neurology. 2004;62:275-280.
113. van Gelder BM, Tijhuis M, Kalmijn S, Kromhout D. Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: The Zutphen Elderly Study. Am J Clin Nutr. 2007;85:1142-1147.
114. Waitzberg DL, Torrinhas RS. Fish oil lipid emulsions and immune response: what clinicians need to know. Nutr Clin Pract. 2009;24:487-499.
115. Grimm H,Mertes N, Goeters C, et al. Improved fatty acid and leukotriene pattern with a novel lipid emulsion in surgical patients. Eur J Nutr. 2006;45:55-60.
116. Liang B, Wang S, Ye YJ, et al. Impact of postoperative omega-3 fatty acid-supplemented parenteral nutrition on clinical outcomes and immunomodulations in colorectal cancer patients. World J Gastroenterol. 2008;14:2434-2439.
117. Kris-Etherton PM. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 2002; 106:2747-2757.