International Archives of Allergy and Immunology

Review

Immunomodulation by Polyunsaturated Fatty Acids: Mechanisms and Effects

Stulnig T.M.

Author affiliations

Division of Endocrinology and Metabolism, Department of Internal Medicine III, University of Vienna, and Center of Molecular Medicine, Austrian Academy of Sciences, Vienna, Austria

Keywords: Polyunsaturated fatty acidsImmune responseLymphocytesMonocytesLipid mediatorsSignal transductionNuclear receptorsInflammatory disordersDiet

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Int Arch Allergy Immunol 2003;132:310–321
https://doi.org/10.1159/000074898

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Article / Publication Details

First-Page Preview
Abstract of Review

Received: October 28, 2003
Accepted: November 10, 2003
Published online: January 14, 2004
Issue release date: December 2003

Number of Print Pages: 12
Number of Figures: 2
Number of Tables: 1

ISSN: 1018-2438 (Print)
eISSN: 1423-0097 (Online)

For additional information: https://www.karger.com/IAA

Abstract

Polyunsaturated fatty acids (PUFAs) modulate immune responses, thereby exerting beneficial effects in a variety of inflammatory disorders. PUFAs of the n-3 series that are found in marine fish oils are particularly effective. A variety of molecular mechanisms have been found to explain how PUFAs could interfere with immune cell function. PUFAs alter eicosanoid (prostaglandin, leukotriene) synthesis, orphan nuclear receptor activation (e.g. peroxisome proliferator-activated receptors, liver X receptors) and T lymphocyte signaling by changing the molecular composition of special signaling platforms called lipid rafts. This review discusses these mechanisms in detail with respect to their probable relevance in vivo. In addition, the effects of PUFAs on the immune system in general are summarized, as are clinical effects in rheumatoid arthritis, inflammatory bowel disease and sepsis.

© 2003 S. Karger AG, Basel



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References

  1. Jump DB: The biochemistry of N3-polyunsaturated fatty acids. J Biol Chem 2002;277:8755–8758.
    External Resources
  2. Calder PC, Yaqoob P, Thies F, Wallace FA, Miles EA: Fatty acids and lymphocyte functions. Br J Nutr 2002;87(suppl 1):S31–S48.
  3. Mitchell JA, Warner TD: Cyclo-oxygenase-2:Pharmacology, physiology, biochemistry and relevance to NSAID therapy. Br J Pharmacol 1999;128:1121–1132.
    External Resources
  4. Goldyne ME: Lymphocytes and arachidonic acid metabolism. Prog Allergy 1988;44:140–152.
    External Resources
  5. Calder PC: n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann Nutr Metab 1997;41:203–234.
    External Resources
  6. 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; discussion 59–62.
  7. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN: Lipid mediator class switching during acute inflammation: Signals in resolution. Nat Immunol 2001;2:612–619.
    External Resources
  8. Malkowski MG, Thuresson ED, Lakkides KM, Rieke CJ, Micielli R, Smith WL, Garavito RM: Structure of eicosapentaenoic and linoleic acids in the cyclooxygenase site of prostaglandin endoperoxide H synthase-1. J Biol Chem 2001;276:37547–37555.
    External Resources
  9. Lee TH, Hoover RL, Williams JD, Sperling RI, Ravalese J 3rd, Spur BW, Robinson DR, Corey EJ, Lewis RA, Austen KF: Effect of dietary enrichment with eicosapentaenoic and docosahexaenoic acids on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N Engl J Med 1985;312:1217–1224.
    External Resources
  10. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ: The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr 1996;63:116–122.
    External Resources
  11. Sperling RI, Benincaso AI, Knoell CT, Larkin JK, Austen KF, Robinson DR: Dietary omega-3 polyunsaturated fatty acids inhibit phosphoinositide formation and chemotaxis in neutrophils. J Clin Invest 1993;91:651–660.
    External Resources
  12. Lee JY, Plakidas A, Lee WH, Heikkinen A, Chanmugam P, Bray G, Hwang DH: Differential modulation of Toll-like receptors by fatty acids: Preferential inhibition by n-3 polyunsaturated fatty acids. J Lipid Res 2003;44:479–486.
  13. Curtis CL, Rees SG, Little CB, Flannery CR, Hughes CE, Wilson C, Dent CM, Otterness IG, Harwood JL, Caterson B: Pathologic indicators of degradation and inflammation in human osteoarthritic cartilage are abrogated by exposure to n-3 fatty acids. Arthritis Rheum 2002;46:1544–1553.
    External Resources
  14. Curtis CL, Hughes CE, Flannery CR, Little CB, Harwood JL, Caterson B: n-3 fatty acids specifically modulate catabolic factors involved in articular cartilage degradation. J Biol Chem 2000;275:721–724.
    External Resources
  15. Fowler KH, Chapkin RS, McMurray DN: Effects of purified dietary n-3 ethyl esters on murine T lymphocyte function. J Immunol 1993;151:5186–5197.
    External Resources
  16. Jump DB: Dietary polyunsaturated fatty acids and regulation of gene transcription. Curr Opin Lipidol 2002;13:155–164.
    External Resources
  17. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ: Nuclear receptors and lipid physiology: Opening the X-files. Science 2001;294:1866–1865.
    External Resources
  18. Rosen ED, Spiegelman BM: PPARgamma: A nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 2001;276:37731–37734.
    External Resources
  19. Marx N, Kehrle B, Kohlhammer K, Grub M, Koenig W, Hombach V, Libby P, Plutzky J: PPAR activators as antiinflammatory mediators in human T lymphocytes: Implications for atherosclerosis and transplantation-associated arteriosclerosis. Circ Res 2002;90:703–710.
    External Resources
  20. Miyazaki Y, Tachibana H, Yamada K: Inhibitory effect of peroxisome proliferator-activated receptor-gamma ligands on the expression of IgE heavy chain germline transcripts in the human B cell line DND39. Biochem Biophys Res Commun 2002;295:547–552.
    External Resources
  21. Cunard R, Ricote M, DiCampli D, Archer DC, Kahn DA, Glass CK, Kelly CJ: Regulation of cytokine expression by ligands of peroxisome proliferator activated receptors. J Immunol 2002;168:2795–2802.
    External Resources
  22. Desvergne B, Wahli W: Peroxisome proliferator-activated receptors: Nuclear control of metabolism. Endocr Rev 1999;20:649–688.
    External Resources
  23. Mata de Urquiza A, Liu S, Sjoberg M, Zetterstrom RH, Griffiths W, Sjovall J, Perlmann T: Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 2000;290:2140–2144.
    External Resources
  24. Hertz R, Magenheim J, Berman I, Bar-Tana J: Fatty acyl-CoA thioesters are ligands of hepatic nuclear factor-4alpha. Nature 1998;392:512–516.
    External Resources
  25. Petrescu AD, Hertz R, Bar-Tana J, Schroeder F, Kier AB: Ligand specificity and conformational dependence of the hepatic nuclear factor-4alpha (HNF-4alpha). J Biol Chem 2002;277:23988–23999.
    External Resources
  26. Devchand PR, Keller H, Peters JM, Vazquez M, Gonzalez FJ, Wahli W: The PPARalpha-leukotriene B4 pathway to inflammation control. Nature 1996;384:39–43.
    External Resources
  27. Jiang C, Ting AT, Seed B: PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998;391:82–86.
    External Resources
  28. Jones DC, Ding X, Daynes RA: Nuclear receptor peroxisome proliferator-activated receptor alpha (PPARalpha) is expressed in resting murine lymphocytes. The PPARalpha in T and B lymphocytes is both transactivation and transrepression competent. J Biol Chem 2002;277:6838–6845.
    External Resources
  29. Huang JT, Welch JS, Ricote M, Binder CJ, Willson TM, Kelly C, Witztum JL, Funk CD, Conrad D, Glass CK: Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 1999;400:378–382.
    External Resources
  30. Yang XY, Wang LH, Chen T, Hodge DR, Resau JH, DaSilva L, Farrar WL: Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor gamma (PPARgamma) agonists. PPARgamma co-association with transcription factor NFAT. J Biol Chem 2000;275:4541–4544.
    External Resources
  31. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK: The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998;391:79–82.
    External Resources
  32. Clark RB, Bishop-Bailey D, Estrada-Hernandez T, Hla T, Puddington L, Padula SJ: The nuclear receptor PPAR gamma and immunoregulation: PPAR gamma mediates inhibition of helper T cell responses. J Immunol 2000;164:1364–1371.
    External Resources
  33. Petrova TV, Akama KT, Van Eldik LJ: Cyclopentenone prostaglandins suppress activation of microglia: Down-regulation of inducible nitric-oxide synthase by 15-deoxy-Delta12,14-prostaglandin J2. Proc Natl Acad Sci USA 1999;96:4668–4673.
    External Resources
  34. Vaidya S, Somers EP, Wright SD, Detmers PA, Bansal VS: 15-Deoxy-Delta12,1412,14-prostaglandin J2 inhibits the beta2 integrin-dependent oxidative burst: Involvement of a mechanism distinct from peroxisome proliferator-activated receptor gamma ligation. J Immunol 1999;163:6187–6192.
    External Resources
  35. Delerive P, Fruchart JC, Staels B: Peroxisome proliferator-activated receptors in inflammation control. J Endocrinol 2001;169:453–459.
    External Resources
  36. Pérez-Sala D, Cernuda-Morollón E, Cañada FJ: Molecular basis for the direct inhibition of AP-1 DNA binding by 15-deoxy-Delta(12,14)-prostaglandin J2. J Biol Chem, in press.
  37. Kondo M, Shibata T, Kumagai T, Osawa T, Shibata N, Kobayashi M, Sasaki S, Iwata M, Noguchi N, Uchida K: 15-Deoxy-Delta(12,14)-prostaglandin J(2): The endogenous electrophile that induces neuronal apoptosis. Proc Natl Acad Sci USA 2002;99:7367–7372.
    External Resources
  38. Shibata T, Kondo M, Osawa T, Shibata N, Kobayashi M, Uchida K: 15-Deoxy-delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes. J Biol Chem 2002;277:10459–10466.
    External Resources
  39. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA: Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 1999;5:698–701.
    External Resources
  40. Kohro T, Nakajima T, Wada Y, Sugiyama A, Ishii M, Tsutsumi S, Aburatani H, Imoto I, Inazawa J, Hamakubo T, Kodama T, Emi M: Genomic structure and mapping of human orphan receptor LXR alpha: Upregulation of LXRα mRNA during monocyte to macrophage differentiation. J Atheroscler Thromb 2000;7:145–151.
    External Resources
  41. Yoshikawa T, Shimano H, Yahagi N, Ide T, Amemiya-Kudo M, Matsuzaka T, Nakakuki M, Tomita S, Okazaki H, Tamura Y, Iizuka Y, Ohashi K, Takahashi A, Sone H, Osuga Ji J, Gotoda T, Ishibashi S, Yamada N: Polyunsaturated fatty acids suppress sterol regulatory element-binding protein-1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J Biol Chem 2002;277:1705–1711.
    External Resources
  42. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P: Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat Med 2003;9:213–219.
    External Resources
  43. Stulnig TM, Huber J, Leitinger N, Imre E-M, Angelisová P, Nowotny P, Waldhäusl W: Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J Biol Chem 2001;276:37335–37340.
    External Resources
  44. Simons K, Ikonen E: Functional rafts in cell membranes. Nature 1997;387:569–572.
    External Resources
  45. Brown DA, London E: Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111–136.
    External Resources
  46. Stulnig TM, Berger M, Sigmund T, Raederstorff D, Stockinger H, Waldhäusl W: Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. J Cell Biol 1998;143:637–644.
    External Resources
  47. Fan YY, McMurray DN, Ly LH, Chapkin RS: Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J Nutr 2003;133:1913–1920.
  48. Webb Y, Hermida-Matsumoto L, Resh MD: Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J Biol Chem 2000;275:261–270.
    External Resources
  49. Lindwasser OW, Resh MD: Myristoylation as a target for inhibiting HIV assembly: Unsaturated fatty acids block viral budding. Proc Natl Acad Sci USA 2002;99:13037–13042.
    External Resources
  50. Liang X, Nazarian A, Erdjument-Bromage H, Bornmann W, Tempst P, Resh MD: Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J Biol Chem 2001;276:30987–30994.
    External Resources
  51. Zeyda M, Staffler G, Horejsi V, Waldhausl W, Stulnig TM: LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J Biol Chem 2002;277:28418–28423.
    External Resources
  52. Zeyda M, Szekeres AB, Säemann MD, Geyeregger R, Stockinger H, Zlabinger GJ, Waldhäusl W, Stulnig TM: Suppression of T cell signaling by polyunsaturated fatty acids: Selectivity in inhibition of mitogen-activated protein kinase and nuclear factor activation. J Immunol 2003;170:6033–6039.
    External Resources
  53. Meydani SN, Endres S, Woods MM, Goldin BR, Soo C, Morrill-Labrode A, Dinarello CA, Gorbach SL: Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: Comparison between young and older women. J Nutr 1991;121:547–555.
    External Resources
  54. Petroni A, Blasevich M, Papini N, Salami M, Sala A, Galli C: Inhibition of leukocyte leukotriene B4 production by an olive oil-derived phenol identified by mass-spectrometry. Thromb Res 1997;87:315–322.
    External Resources
  55. Belluzzi A: N-3 fatty acids for the treatment of inflammatory bowel diseases. Proc Nutr Soc 2002;61:391–395.
    External Resources
  56. Simopoulos AP: The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 2002;56:365–379.
    External Resources
  57. Gassull MA, Fernandez-Banares F, Cabre E, Papo M, Giaffer MH, Sanchez-Lombrana JL, Richart C, Malchow H, Gonzalez-Huix F, Esteve M: Fat composition may be a clue to explain the primary therapeutic effect of enteral nutrition in Crohn’s disease: Results of a double blind randomised multicentre European trial. Gut 2002;51:164–168.
    External Resources
  58. Jolly CA, Jiang YH, Chapkin RS, McMurray DN: Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide. J Nutr 1997;127:37–43.
    External Resources
  59. Peterson LD, Jeffery NM, Thies F, Sanderson P, Newsholme EA, Calder PC: Eicosapentaenoic and docosahexaenoic acids alter rat spleen leukocyte fatty acid composition and prostaglandin E2 production but have different effects on lymphocyte functions and cell-mediated immunity. Lipids 1998;33:171–180.
    External Resources
  60. Peterson LD, Thies F, Sanderson P, Newsholme EA, Calder PC: Low levels of eicosapentaenoic and docosahexaenoic acids mimic the effects of fish oil upon rat lymphocytes. Life Sci 1998;62:2209–2217.
    External Resources
  61. Prickett JD, Robinson DR, Steinberg AD: Dietary enrichment with the polyunsaturated fatty acid eicosapentaenoic acid prevents proteinuria and prolongs survival in NZB x NZW F1 mice. J Clin Invest 1981;68:556–559.
    External Resources
  62. Cleland LG, James MJ: Fish oil and rheumatoid arthritis: Antiinflammatory and collateral health benefits. J Rheumatol 2000;27:2305–2307.
    External Resources
  63. Calder PC: Dietary fatty acids and the immune system. Nutr Rev 1998;56:S70–S83.
  64. Calder PC: Dietary fatty acids and lymphocyte functions. Proc Nutr Soc 1998;57:487–502.
    External Resources
  65. Hughes DA, Southon S, Pinder AC: (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro. J Nutr 1996;126:603–610.
    External Resources
  66. Hughes DA, Pinder AC: N-3 polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes and inhibit antigen-presentation in vitro. Clin Exp Immunol 1997;110:516–523.
    External Resources
  67. Prickett JD, Robinson DR, Bloch KJ: Enhanced production of IgE and IgG antibodies associated with a diet enriched in eicosapentaenoic acid. Immunology 1982;46:819–826.
    External Resources
  68. Meydani SN, Lichtenstein AH, Cornwall S, Meydani M, Goldin BR, Rasmussen H, Dinarello CA, Schaefer EJ: Immunologic effects of national cholesterol education panel step-2 diets with and without fish-derived N-3 fatty acid enrichment. J Clin Invest 1993;92:105–113.
    External Resources
  69. van der Heide JJ, Bilo HJ, Donker JM, Wilmink JM, Tegzess AM: Effect of dietary fish oil on renal function and rejection in cyclosporine-treated recipients of renal transplants. N Engl J Med 1993;329:769–773.
    External Resources
  70. Mayser P, Grimm H, Grimminger F: n-3 fatty acids in psoriasis. Br J Nutr 2002;87(suppl 1):S77–S82.
  71. Leiba A, Amital H, Gershwin ME, Shoenfeld Y: Diet and lupus. Lupus 2001;10:246–248.
    External Resources
  72. Simopoulos AP: Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr 2002;21:495–505.
    External Resources
  73. Calder PC: N-3 polyunsaturated fatty acids and inflammation: From molecular biology to the clinic. Lipids 2003;38:343–352.
    External Resources
  74. Feldmann M, Brennan FM, Maini RN: Role of cytokines in rheumatoid arthritis. Annu Rev Immunol 1996;14:397–440.
    External Resources
  75. Sperling RI: Eicosanoids in rheumatoid arthritis. Rheum Dis Clin North Am 1995;21:741–758.
    External Resources
  76. Feldmann M, Maini RN: The role of cytokines in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 1999;38(suppl 2):3–7.
  77. Calder PC, Zurier RB: Polyunsaturated fatty acids and rheumatoid arthritis. Curr Opin Clin Nutr Metab Care 2001;4:115–121.
    External Resources
  78. Rennie KL, Hughes J, Lang R, Jebb SA: Nutritional management of rheumatoid arthritis: A review of the evidence. J Hum Nutr Diet 2003;16:97–109.
    External Resources
  79. Fortin PR, Lew RA, Liang MH, Wright EA, Beckett LA, Chalmers TC, Sperling RI: Validation of a meta-analysis: The effects of fish oil in rheumatoid arthritis. J Clin Epidemiol 1995;48:1379–1390.
    External Resources
  80. Symmons DP, Jones MA, Scott DL, Prior P: Longterm mortality outcome in patients with rheumatoid arthritis: Early presenters continue to do well. J Rheumatol 1998;25:1072–1077.
    External Resources
  81. Wolfe F, Mitchell DM, Sibley JT, Fries JF, Bloch DA, Williams CA, Spitz PW, Haga M, Kleinheksel SM, Cathey MA: The mortality of rheumatoid arthritis. Arthritis Rheum 1994;37:481–494.
    External Resources
  82. 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.
    External Resources
  83. Haagsma CJ, Blom HJ, van Riel PL, van’t Hof MA, Giesendorf BA, van Oppenraaij-Emmerzaal D, van de Putte LB: Influence of sulphasalazine, methotrexate, and the combination of both on plasma homocysteine concentrations in patients with rheumatoid arthritis. Ann Rheum Dis 1999;58:79–84.
    External Resources
  84. Landewe RB, van den Borne BE, Breedveld FC, Dijkmans BA: Methotrexate effects in patients with rheumatoid arthritis with cardiovascular comorbidity. Lancet 2000;355:1616–1617.
    External Resources
  85. Donadio JV, Grande JP: IgA nephropathy. N Engl J Med 2002;347:738–748.
    External Resources
  86. Donadio JV Jr, Bergstralh EJ, Offord KP, Spencer DC, Holley KE: A controlled trial of fish oil in IgA nephropathy. Mayo Nephrology Collaborative Group. N Engl J Med 1994;331:1194–1199.
    External Resources
  87. Donadio JV Jr, Grande JP, Bergstralh EJ, Dart RA, Larson TS, Spencer DC: The long-term outcome of patients with IgA nephropathy treated with fish oil in a controlled trial. Mayo Nephrology Collaborative Group. J Am Soc Nephrol 1999;10:1772–1777.
    External Resources
  88. Hogg RJ: A randomized, placebo-controlled, multicenter trial evaluating alternate-day prednisone and fish oil supplements in young patients with immunoglobulin A nephropathy. Scientific Planning Committee of the IgA Nephropathy Study. Am J Kidney Dis 1995;26:792–796.
    External Resources
  89. 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.
    External Resources
  90. Lorenz-Meyer H, Bauer P, Nicolay C, Schulz B, Purrmann J, Fleig WE, Scheurlen C, Koop I, Pudel V, Carr L: Omega-3 fatty acids and low carbohydrate diet for maintenance of remission in Crohn’s disease. A randomized controlled multicenter trial. Study Group Members (German Crohn’s Disease Study Group). Scand J Gastroenterol 1996;31:778–785.
    External Resources
  91. Hawthorne AB, Daneshmend TK, Hawkey CJ, Belluzzi A, Everitt SJ, Holmes GK, Malkinson C, Shaheen MZ, Willars JE: Treatment of ulcerative colitis with fish oil supplementation: A prospective 12 month randomised controlled trial. Gut 1992;33:922–928.
    External Resources
  92. Stenson WF, Cort D, Rodgers J, Burakoff R, DeSchryver-Kecskemeti K, Gramlich TL, Beeken W: Dietary supplementation with fish oil in ulcerative colitis. Ann Intern Med 1992;116:609–614.
    External Resources
  93. Loeschke K, Ueberschaer B, Pietsch A, Gruber E, Ewe K, Wiebecke B, Heldwein W, Lorenz R: n-3 fatty acids only delay early relapse of ulcerative colitis in remission. Dig Dis Sci 1996;41:2087–2094.
    External Resources
  94. Dinarello CA: Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 1997;112:321S–329S.
  95. Mayer K, Grimm H, Grimminger F, Seeger W: Parenteral nutrition with n-3 lipids in sepsis. Br J Nutr 2002;87(suppl 1):S69–S75.
  96. Mayer K, Gokorsch S, Fegbeutel C, Hattar K, Rosseau S, Walmrath D, Seeger W, Grimminger F: Parenteral nutrition with fish oil modulates cytokine response in patients with sepsis. Am J Respir Crit Care Med 2003;167:1321–1328.
    External Resources
  97. Weiss G, Meyer F, Matthies B, Pross M, Koenig W, Lippert H: Immunomodulation by perioperative administration of n-3 fatty acids. Br J Nutr 2002;87(suppl 1):S89–S94.
  98. Gadek JE, DeMichele SJ, Karlstad MD, Pacht ER, Donahoe M, Albertson TE, Van Hoozen C, Wennberg AK, Nelson JL, Noursalehi M: Effect of enteral feeding with eicosapentaenoic acid, gamma-linolenic acid, and antioxidants in patients with acute respiratory distress syndrome. Enteral Nutrition in ARDS Study Group. Crit Care Med 1999;27:1409–1420.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Review

Received: October 28, 2003
Accepted: November 10, 2003
Published online: January 14, 2004
Issue release date: December 2003

Number of Print Pages: 12
Number of Figures: 2
Number of Tables: 1

ISSN: 1018-2438 (Print)
eISSN: 1423-0097 (Online)

For additional information: https://www.karger.com/IAA

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