The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential

European Journal of Cancer

Volumn 45, Issue 12, 2009, Pages 2077-2086

  Spencer, Laura ^a   Mann, Christopher ^a   Metcalfe, Matthew ^a   Webb, M'Balu ^a   Pollard, Cristina ^a   Spencer, Daniel ^a   Berry, David ^a   Steward, William ^a   Dennison, Ashley ^a  

^a LEICESTER GENERAL HOSPITAL   (United Kingdom)

Author keywords

Angiogenesis inhibitor; Omega 3 fatty acids; Tumour angiogenesis

Indexed keywords

ANGIOGENESIS INHIBITOR; BETA CATENIN; CELECOXIB; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; ICOSAPENTAENOIC ACID; ICOSATETRAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LINOLENIC ACID; MATRIX METALLOPROTEINASE; NITRIC OXIDE; OMEGA 3 FATTY ACID; PLATELET DERIVED ENDOTHELIAL CELL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; PROSTAGLANDIN E2; STEARIDONIC ACID; VASCULOTROPIN;

ANTIANGIOGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CLINICAL TRIAL; COLON POLYP; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; HUMAN; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; DIET, MEDITERRANEAN; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RATS; TUMOR CELLS, CULTURED;

EID: 67650938102     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2009.04.026     Document Type: Article

References (109)

1. Folkman J. Tumor angiogenesis: therapeutic implications. New Engl J Med 285 (1971) 1182-1186
2. Folkman J., Cole P., and Zimmerman S. Tumor behavior in isolated perfused organs: in vitro growth and metastases of biopsy material in rabbit thyroid and canine intestinal segment. Ann Surg 164 (1966) 491-502
3. Folkman J. Biology of endothelial cells (1984), Martinus-Nijhoff, Boston
4. Gimbrone Jr. M.A., Leapman S.B., Cotran R.S., and Folkman J. Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 136 (1972) 261-276
5. Clark E.R., and Clark E.L. Microscopic observations on the growth of blood capillaries in the living mammal. Am J Anat 64 (1939) 251-301
6. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 25 (2004) 581-611
7. Ferrara N., and Kerbel R.S. Angiogenesis as a therapeutic target. Nature 438 (2005) 967-974
8. Philpott M., and Ferguson L.R. Immunonutrition and cancer. Mutat Res 551 (2004) 29-42
9. Hardman W.E. Omega-3 FA to augment cancer therapy. J Nutr 132 (2002) 3508S-3512S
10. Hardman W.E. N - 3 fatty acids and cancer therapy. J Nutr 134 (2004) 3427S-3430S
11. Ferrara N., and Henzel W.J. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161 (1989) 851-858
12. Muller Y.A., Li B., Christinger H.W., Wells J.A., Cunningham B.C., and de Vos A.M. Vascular endothelial growth factor: crystal structure and functional mapping of the kinase domain receptor binding site. Proc Natl Acad Sci USA 94 (1997) 7192-7197
13. Ellis L.M., Takahashi Y., Liu W., and Shaheen R.M. Vascular endothelial growth factor in human colon cancer: biology and therapeutic implications. Oncologist 5 Suppl. 1 (2000) 11-15
14. Nor J.E., Christensen J., Mooney D.J., and Polverini P.J. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of bcl-2 expression. Am J Pathol 154 (1999) 375-384
15. Takekoshi K., Isobe K., Yashiro T., et al. Expression of vascular endothelial growth factor (VEGF) and its cognate receptors in human pheochromocytomas. Life Sci 74 (2004) 863-871
16. Yang C.C., Chu K.C., and Yeh W.M. The expression of vascular endothelial growth factor in transitional cell carcinoma of urinary bladder is correlated with cancer progression. Urol Oncol 22 (2004) 1-6
17. Linderholm B.K., Lindh B., Beckman L., et al. Prognostic correlation of basic fibroblast growth factor and vascular endothelial growth factor in 1307 primary breast cancers. Clin Breast Cancer 4 (2003) 340-347
18. Loggini B., Boldrini L., Gisfredi S., et al. CD34 microvessel density and VEGF expression in basal and squamous cell carcinoma. Pathol Res Pract 199 (2003) 705-712
19. Wong C., Wellman T.L., and Lounsbury K.M. VEGF and HIF-1alpha expression are increased in advanced stages of epithelial ovarian cancer. Gynecol Oncol 91 (2003) 513-517
20. Giatromanolaki A., Koukourakis M.I., Simopoulos C., Polychronidis A., and Sivridis E. Vascular endothelial growth factor (VEGF) expression in operable gallbladder carcinomas. Eur J Surg Oncol 29 (2003) 879-883
21. Shiraishi A., Ishiwata T., Shoji T., and Asano G. Expression of PCNA, basic fibroblast growth factor, FGF receptor and vascular endothelial growth factor in adenomas and carcinomas of the human colon. Acta Histochem Cytochem 28 (1995) 21-29
22. Kimura H., Konishi K., Nukui T., et al. Prognostic significance of expression of thymidine phosphorylase and vascular endothelial growth factor in human gastric carcinoma. J Surg Oncol 76 (2001) 31-36
23. Tsuzuki T., Shibata A., Kawakami Y., Nakagawa K., and Miyazawa T. Conjugated eicosapentaenoic acid inhibits vascular endothelial growth factor-induced angiogenesis by suppressing the migration of human umbilical vein endothelial cells. J Nutr 137 (2007) 641-646
24. Yuan L., Yoshida M., and Davis P.F. Inhibition of pro-angiogenic factors by a lipid-rich shark extract. J Med Food 9 (2006) 300-306
25. Tsuji M., Murota S.I., and Morita I. Docosapentaenoic acid (22:5, n - 3) suppressed tube-forming activity in endothelial cells induced by vascular endothelial growth factor. Prostaglandins Leukot Essent Fatty Acids 68 (2003) 337-342
26. Yang S.P., Morita I., and Murota S.I. Eicosapentaenoic acid attenuates vascular endothelial growth factor-induced proliferation via inhibiting flk-1 receptor expression in bovine carotid artery endothelial cells. J Cell Physiol 176 (1998) 342-349
27. Calviello G., Di Nicuolo F., Gragnoli S., et al. N - 3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1alpha induction pathway. Carcinogenesis 25 (2004) 2303-2310
28. Rose D.P., and Connolly J.M. Antiangiogenicity of docosahexaenoic acid and its role in the suppression of breast cancer cell growth in nude mice. Int J Oncol 15 (1999) 1011-1015
29. Mukutmoni-Norris M., Hubbard N.E., and Erickson K.L. Modulation of murine mammary tumor vasculature by dietary n - 3 fatty acids in fish oil. Cancer Lett 150 (2000) 101-109
30. Tevar R., Jho D.H., Babcock T., Helton W.S., and Espat N.J. Omega-3 fatty acid supplementation reduces tumor growth and vascular endothelial growth factor expression in a model of progressive non-metastasizing malignancy. JPEN J Parenter Enteral Nutr 26 (2002) 285-289
31. Ambring A., Johansson M., Axelsen M., Gan L., Strandvik B., and Friberg P. Mediterranean-inspired diet lowers the ratio of serum phospholipid n - 6 to n - 3 fatty acids, the number of leukocytes and platelets, and vascular endothelial growth factor in healthy subjects. Am J Clin Nutr 83 (2006) 575-581
32. Ross R., Glomset J., Kariya B., and Harker L. A platelet-dependent serum factor that stimulates the proliferation of arterial smooth muscle cells in vitro. Proc Natl Acad Sci USA 71 (1974) 1207-1210
33. Heldin C.H., and Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79 (1999) 1283-1316
34. Ostman A., and Heldin C.H. Involvement of platelet-derived growth factor in disease: development of specific antagonists. Adv Cancer Res 80 (2001) 1-38
35. Cao R., Brakenhielm E., Li X., et al. Angiogenesis stimulated by PDGF-CC, a novel member in the PDGF family, involves activation of PDGFR-alphaalpha and -alphabeta receptors. FASEB J 16 (2002) 1575-1583
36. Li X., and Eriksson U. Novel PDGF family members: PDGFC and PDGF-D. Cytokine Growth Factor Rev 14 (2003) 91-98
37. Bergsten E., Uutela M., Li X., et al. PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat Cell Biol 3 (2001) 512-516
38. LaRochelle W.J., Jeffers M., McDonald W.F., et al. PDGF-D, a new protease-activated growth factor. Nat Cell Biol 3 (2001) 517-521
39. Crosby J.R., Tappan K.A., Seifert R.A., and Bowen-Pope D.F. Chimera analysis reveals that fibroblasts and endothelial cells require platelet-derived growth factor receptorbeta expression for participation in reactive connective tissue formation in adults but not during development. Am J Pathol 154 (1999) 1315-1321
40. Fox P.L., and DiCorleto P.E. Fish oils inhibit endothelial cell production of platelet-derived growth factor-like protein. Science 241 (1988) 453-456
41. Jendraschak E., Kaminski W.E., Hessel F., Kiefl R., and von Schacky C. Growth factor mRNA profiles in unstimulated human mononuclear cells: identification of genes which are constitutively and variably expressed. Biochem Biophys Res Commun 196 (1993) 25-31
42. Kaminski W.E., Jendraschak E., Kiefl R., and von Schacky C. Dietary omega-3 fatty acids lower levels of platelet-derived growth factor mRNA in human mononuclear cells. Blood 81 (1993) 1871-1879
43. Terano T., Shiina T., and Tamura Y. Eicosapentaenoic acid suppressed the proliferation of vascular smooth muscle cells through modulation of various steps of growth signals. Lipids 31 Suppl. (1996) S301-S304
44. Miyazono K., Okabe T., Urabe A., Takaku F., and Heldin C.H. Purification and properties of an endothelial cell growth factor from human platelets. J Biol Chem 262 (1987) 4098-4103
45. Ishikawa F., Miyazono K., Hellman U., et al. Identification of angiogenic activity and the cloning and expression of platelet-derived endothelial cell growth factor. Nature 338 (1989) 557-562
46. Moghaddam A., and Bicknell R. Expression of platelet-derived endothelial cell growth factor in escherichia coli and confirmation of its thymidine phosphorylase activity. Biochemistry 31 (1992) 12141-12146
47. Moghaddam A., Zhang H.T., Fan T.P., et al. Thymidine phosphorylase is angiogenic and promotes tumor growth. Proc Natl Acad Sci USA 92 (1995) 998-1002
48. Takahashi Y., Bucana C.D., Akagi Y., et al. Significance of platelet-derived endothelial cell growth factor in the angiogenesis of human gastric cancer. Clin Cancer Res 4 (1998) 429-434
49. Takahashi Y., Bucana C.D., Liu W., et al. Platelet-derived endothelial cell growth factor in human colon cancer angiogenesis: role of infiltrating cells. J Natl Cancer Inst 88 (1996) 1146-1151
50. Takebayashi Y., Akiyama S., Akiba S., et al. Clinicopathologic and prognostic significance of an angiogenic factor, thymidine phosphorylase, in human colorectal carcinoma. J Natl Cancer Inst 88 (1996) 1110-1117
51. Ikeda N., Adachi M., Taki T., et al. Prognostic significance of angiogenesis in human pancreatic cancer. Brit J Cancer 79 (1999) 1553-1563
52. Auguste P., Javerzat S., and Bikfalvi A. Regulation of vascular development by fibroblast growth factors. Cell Tissue Res 314 (2003) 157-166
53. Bikfalvi A., Klein S., Pintucci G., and Rifkin D.B. Biological roles of fibroblast growth factor-2. Endocr Rev 18 (1997) 26-45
54. Gospodarowicz D., Moran J.S., and Braun D.L. Control of proliferation of bovine vascular endothelial cells. J Cell Physiol 91 (1977) 377-385
55. Gospodarowicz D., and Bialecki H. Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology 104 (1979) 757-764
56. Lafleur M.A., Handsley M.M., Knauper V., Murphy G., and Edwards D.R. Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs). J Cell Sci 115 (2002) 3427-3438
57. Pardo O.E., Lesay A., Arcaro A., et al. Fibroblast growth factor 2-mediated translational control of IAPs blocks mitochondrial release of Smac/DIABLO and apoptosis in small cell lung cancer cells. Mol Cell Biol 23 (2003) 7600-7610
58. Udayakumar T.S., Nagle R.B., and Bowden G.T. Fibroblast growth factor-1 transcriptionally induces membrane type-1 matrix metalloproteinase expression in prostate carcinoma cell line. Prostate 58 (2004) 66-75
59. Kuwahara K., Sasaki T., Kuwada Y., Murakami M., Yamasaki S., and Chayama K. Expressions of angiogenic factors in pancreatic ductal carcinoma: a correlative study with clinicopathologic parameters and patient survival. Pancreas 26 (2003) 344-349
60. Netzer P., Domek M., Pai R., Halter F., and Tarnawski A. Inhibition of human colon cancer cell growth by antisense oligodeoxynucleotides targeted at basic fibroblast growth factor. Aliment Pharmacol Ther 15 (2001) 1673-1679
61. George M.L., Tutton M.G., Abulafi A.M., Eccles S.A., and Swift R.I. Plasma basic fibroblast growth factor levels in colorectal cancer: a clinically useful assay?. Clin Exp Metastasis 19 (2002) 735-738
62. Yang S.P., Morita I., and Murota S.I. Eicosapentaenoic acid attenuates vascular endothelial growth factor-induced proliferation via inhibiting flk-1 receptor expression in bovine carotid artery endothelial cells. J Cell Physiol 176 (1998) 342-349
63. Morita I. Regulation of angiogenesis-expression of VEGF receptors. Hum Cell 11 (1998) 215-220
64. Milkiewicz M., Ispanovic E., Doyle J.L., and Haas T.L. Regulators of angiogenesis and strategies for their therapeutic manipulation. Int J Biochem Cell Biol 38 (2006) 333-357
65. Sengupta S., Gherardi E., Sellers L.A., Wood J.M., Sasisekharan R., and Fan T.P. Hepatocyte growth factor/scatter factor can induce angiogenesis independently of vascular endothelial growth factor. Arterioscler Thromb Vasc Biol 23 (2003) 69-75
66. Barnes C.J., and Kumar R. Epidermal growth factor receptor family tyrosine kinases as signal integrators and therapeutic targets. Cancer Metastasis Rev 22 (2003) 301-307
67. Laughner E., Taghavi P., Chiles K., Mahon P.C., and Semenza G.L. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 21 (2001) 3995-4004
68. Murphy L.C., Dotzlaw H., Wong M.S., et al. Epidermal growth factor: receptor and ligand expression in human breast cancer. Semin Cancer Biol 1 (1990) 305-315
69. Cohen R.B. Epidermal growth factor receptor as a therapeutic target in colorectal cancer. Clin Colorectal Cancer 2 (2003) 246-251
70. Ozawa F., Friess H., Tempia-Caliera A., Kleeff J., and Buchler M.W. Growth factors and their receptors in pancreatic cancer. Teratog Carcinog Mutagen 21 (2001) 27-44
71. Brand F.X., Ravanel N., Gauchez A.S., et al. Prospect for anti-her2 receptor therapy in breast cancer. Anticancer Res 26 (2006) 715-722
72. Ciardiello F. Epidermal growth factor receptor inhibitors in cancer treatment. Future Oncol 1 (2005) 221-234
73. Dimmeler S., Hermann C., Galle J., and Zeiher A.M. Upregulation of superoxide dismutase and nitric oxide synthase mediates the apoptosis-suppressive effects of shear stress on endothelial cells. Arterioscler Thromb Vasc Biol 19 (1999) 656-664
74. Rossig L., Fichtlscherer B., Breitschopf K., et al. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 274 (1999) 6823-6826
75. Cianchi F., Cortesini C., Bechi P., et al. Up-regulation of cyclooxygenase 2 gene expression correlates with tumor angiogenesis in human colorectal cancer. Gastroenterology 121 (2001) 1339-1347
76. Cianchi F., Cortesini C., Fantappie O., et al. Cyclooxygenase-2 activation mediates the proangiogenic effect of nitric oxide on colorectal cancer. Clin Cancer Res 10 (2004) 2694-2704
77. Ziche M., Morbidelli L., Choudhuri R., et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99 (1997) 2625-2634
78. Ren J., and Chung S.H. Anti-inflammatory effect of alpha-linolenic acid and its mode of action through the inhibition of nitric oxide production and inducible nitric oxide synthase gene expression via NF-kappaB and mitogen-activated protein kinase pathways. J Agric Food Chem 55 (2007) 5073-5080
79. Komatsu W., Ishihara K., Murata M., Saito H., and Shinohara K. Docosahexaenoic acid suppresses nitric oxide production and inducible nitric oxide synthase expression in interferon-gamma plus lipopolysaccharide-stimulated murine macrophages by inhibiting the oxidative stress. Free Radic Biol Med 34 (2003) 1006-1016
80. Jeyarajah D.R., Kielar M., Penfield J., and Lu C.Y. Docosahexaenoic acid, a component of fish oil, inhibits nitric oxide production in vitro. J Surg Res 83 (1999) 147-150
81. Ohata T., Fukuda K., Takahashi M., Sugimura T., and Wakabayashi K. Suppression of nitric oxide production in lipopolysaccharide-stimulated macrophage cells by omega 3 polyunsaturated fatty acids. Jpn J Cancer Res 88 (1997) 234-237
82. Boutard V., Fouqueray B., Philippe C., Perez J., and Baud L. Fish oil supplementation and essential fatty acid deficiency reduce nitric oxide synthesis by rat macrophages. Kidney Int 46 (1994) 1280-1286
83. Narayanan B.A., Narayanan N.K., Simi B., and Reddy B.S. Modulation of inducible nitric oxide synthase and related proinflammatory genes by the omega-3 fatty acid docosahexaenoic acid in human colon cancer cells. Cancer Res 63 (2003) 972-979
84. Nowak J., Weylandt K.H., Habbel P., et al. Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n - 3 fatty acids. Carcinogenesis 28 (2007) 1991-1995
85. Stein-Werblowski R. Prostaglandins and cancer. Oncology 30 (1974) 169-176
86. Karmali R.A. Review: prostaglandins and cancer. Prostaglandins Med 5 (1980) 11-28
87. Williams C.S., Luongo C., Radhika A., et al. Elevated cyclooxygenase-2 levels in min mouse adenomas. Gastroenterology 111 (1996) 1134-1140
88. Steinbach G., Lynch P.M., Phillips R.K., et al. The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. New Engl J Med 342 (2000) 1946-1952
89. Gottlieb S. COX 2 inhibitors might be useful in cancer prevention. BMJ 319 (1999) 1155
90. Vinogradova Y., Hippisley-Cox J., Coupland C., and Logan R.F. Risk of colorectal cancer in patients prescribed statins, nonsteroidal anti-inflammatory drugs, and cyclooxygenase-2 inhibitors: nested case-control study. Gastroenterology 133 (2007) 393-402
91. Hendrickse C.W., Kelly R.W., Radley S., Donovan I.A., Keighley M.R., and Neoptolemos J.P. Lipid peroxidation and prostaglandins in colorectal cancer. Brit J Surg 81 (1994) 1219-1223
92. Gullino P.M. Prostaglandins and gangliosides of tumor microenvironment: their role in angiogenesis. Acta Oncol 34 (1995) 439-441
93. Pai R., Szabo I.L., Soreghan B.A., Atay S., Kawanaka H., and Tarnawski A.S. PGE(2) stimulates VEGF expression in endothelial cells via ERK2/JNK1 signaling pathways. Biochem Biophys Res Commun 286 (2001) 923-928
94. Majima M., Hayashi I., Muramatsu M., Katada J., Yamashina S., and Katori M. Cyclo-oxygenase-2 enhances basic fibroblast growth factor-induced angiogenesis through induction of vascular endothelial growth factor in rat sponge implants. Brit J Pharmacol 130 (2000) 641-649
95. Bommareddy A., Arasada B.L., Mathees D.P., and Dwivedi C. Chemopreventive effects of dietary flaxseed on colon tumor development. Nutr Cancer 54 (2006) 216-222
96. Reddy B.S., Patlolla J.M., Simi B., Wang S.H., and Rao C.V. Prevention of colon cancer by low doses of celecoxib, a cyclooxygenase inhibitor, administered in diet rich in omega-3 polyunsaturated fatty acids. Cancer Res 65 (2005) 8022-8027
97. Narayanan N.K., Narayanan B.A., and Reddy B.S. A combination of docosahexaenoic acid and celecoxib prevents prostate cancer cell growth in vitro and is associated with modulation of nuclear factor-kappaB, and steroid hormone receptors. Int J Oncol 26 (2005) 785-792
98. Chiu L.C., Tong K.F., and Ooi V.E. Cytostatic and cytotoxic effects of cyclooxygenase inhibitors and their synergy with docosahexaenoic acid on the growth of human skin melanoma A-375 cells. Biomed Pharmacother 59 Suppl. 2 (2005) S293-S297
99. Garcea G., Lloyd T.D., Gescher A., Dennison A.R., Steward W.P., and Berry D.P. Angiogenesis of gastrointestinal tumours and their metastases - a target for intervention?. Eur J Cancer 40 (2004) 1302-1313
100. Jung Y.J., Isaacs J.S., Lee S., Trepel J., and Neckers L. IL-1beta-mediated up-regulation of HIF-1alpha via an NFkappaB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J 17 (2003) 2115-2117
101. Narayanan B.A., Narayanan N.K., Desai D., Pittman B., and Reddy B.S. Effects of a combination of docosahexaenoic acid and 1,4-phenylene bis(methylene) selenocyanate on cyclooxygenase 2, inducible nitric oxide synthase and beta-catenin pathways in colon cancer cells. Carcinogenesis 25 (2004) 2443-2449
102. Calviello G., Resci F., Serini S., et al. Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2. Carcinogenesis 28 (2007) 1202-1209
103. Morlion B.J., Torwesten E., Lessire H., et al. The effect of parenteral fish oil on leukocyte membrane fatty acid composition and leukotriene-synthesizing capacity in patients with postoperative trauma. Metabolism 45 (1996) 1208-1213
104. Roulet M., Frascarolo P., Pilet M., and Chapuis G. Effects of intravenously infused fish oil on platelet fatty acid phospholipid composition and on platelet function in postoperative trauma. JPEN J Parenter Enteral Nutr 21 (1997) 296-301
105. Mayer K., Fegbeutel C., Hattar K., et al. Omega-3 vs. omega-6 lipid emulsions exert differential influence on neutrophils in septic shock patients: impact on plasma fatty acids and lipid mediator generation. Intensive Care Med 29 (2003) 1472-1481
106. Grecu I., Mirea L., and Grintescu I. Parenteral fish oil supplementation in patients with abdominal sepsis. Clin Nutr 22 (2003) S23
107. Heller A.R., Rossler S., Litz R.J., et al. Omega-3 fatty acids improve the diagnosis-related clinical outcome. Crit Care Med 34 (2006) 972-979
108. Tsekos E., Reuter C., Stehle P., and Boeden G. Perioperative administration of parenteral fish oil supplements in a routine clinical setting improves patient outcome after major abdominal surgery. Clin Nutr 23 (2004) 325-330
109. Weiss G., Meyer F., Matthies B., Pross M., Koenig W., and Lippert H. Immunomodulation by perioperative administration of n - 3 fatty acids. Brit J Nutr 87 (2002) S89-S94