Phytochemistry Reviews

, Volume 13, Issue 1, pp 223–244 | Cite as

Omega-3 fatty acids: physiology, biological sources and potential applications in supportive cancer care

  • L. Pottel
  • M. Lycke
  • T. Boterberg
  • I. Foubert
  • H. Pottel
  • F. Duprez
  • L. Goethals
  • P. R. DebruyneEmail author


The impact of the Western diet on chronic diseases, such as cancer, has been well recognized. Dietary saturated and trans fatty acids have been found to play a negative role in obesity, heart disease, diabetes and cancer, while the beneficial health effects of n-3 polyunsaturated fatty acids (n-3 PUFAs) have become widely accepted. Despite the current knowledge, n-3 PUFA intake is still under recommended daily intake levels in Europe. As wild fish, currently still the major source of n-3 PUFA, are facing a decline, alternative sources such as marine and plant (both natural and transgenic) sources are being explored. In this review we aim to provide an overview of the current biological sources of n-3 PUFAs, their part in normal physiology, as well as their emerging application in supportive cancer care, and more specifically in cancer cachexia, therapy-related neurocognitive dysfunction and distress. In addition, we provide a brief summary of currently ongoing clinical trials examining potential beneficial effects of n-3 PUFAs in reducing cancer(therapy)-related side effects, and describe future research directions.


Omega-3 fatty acids Plant sources Supportive cancer care 



Our work is supported by grants from the Belgian Federal Government, National Cancer Plan (NKP_CA_04 and NKP_2122c_044).

Conflict of interest

All authors declare that there are no known conflicts of interest associated with this publication.

Supplementary material

11101_2013_9309_MOESM1_ESM.doc (74 kb)
Supplementary Table 1: List of abbreviations (DOC 75 kb)
11101_2013_9309_MOESM2_ESM.doc (111 kb)
Supplementary Table 2: Clinical trials examining the role of n-3 PUFA on nutritional parameters in cachectic cancer patients (DOC 111 kb)
11101_2013_9309_MOESM3_ESM.doc (28 kb)
Supplementary Table 3: Clinical trials examining the role of n-3 PUFA on chemobrain (DOC 28 kb)
11101_2013_9309_MOESM4_ESM.doc (34 kb)
Supplementary Table 4: Clinical trials examining the role of n-3 PUFA on distress secondary to a cancer diagnosis (DOC 34 kb)
11101_2013_9309_MOESM5_ESM.doc (110 kb)
Supplementary Table 5: Clinical trials examining the role of n-3 PUFA for attenuation of cancer-related toxicities, as well as cancer prevention (Database entry date: November 2012) (DOC 110 kb)


  1. Abbadi A, Domergue F, Bauer J et al (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell 16:2734–2748PubMedCentralPubMedGoogle Scholar
  2. Anderson-Hanley C, Sherman ML, Riggs R et al (2003) Neuropsychological effects of treatments for adults with cancer: a meta-analysis and review of the literature. J Int Neuropsychol Soc 9:967–982PubMedGoogle Scholar
  3. Appleton KM, Rogers PJ, Ness AR (2010) Updated systematic review and meta-analysis of the effects of n-3 long-chain polyunsaturated fatty acids on depressed mood. Am J Clin Nutr 91:757–770PubMedGoogle Scholar
  4. Aronson W, 2008. Low-fat fish oil diet for prostate cancer prevention.
  5. Arterburn LM, Hall EB, Oken H (2006) Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr 83:1467S–1476SPubMedGoogle Scholar
  6. Arts MT, Ackman RG, Holub BJ (2001) Essential fatty acids’ in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137Google Scholar
  7. Astrup A, Dyerberg J, Elwood P et al (2011) The role of reducing intakes of saturated fat in the prevention of cardiovascular disease: where does the evidence stand in 2010? Am J Clin Nutr 93:684–688PubMedGoogle Scholar
  8. Baracos VE, Devivo C, Hoyle DH et al (1995) Activation of the ATP-ubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol 268:E996–E1006PubMedGoogle Scholar
  9. Barber MD, Ross JA, Voss AC et al (1999) The effect of an oral nutritional supplement enriched with fish oil on weight-loss in patients with pancreatic cancer. Br J Cancer 81:80–86PubMedCentralPubMedGoogle Scholar
  10. Bayram I, Erbey F, Celik N et al (2009) The use of a protein and energy dense eicosapentaenoic acid containing supplement for malignancy-related weight loss in children. Pediatr Blood Cancer 52:571–574PubMedGoogle Scholar
  11. Beaudoin F, Wilkinson BM, Stirling CJ et al (2000) In vivo targeting of a sunflower oil body protein in yeast secretory (sec) mutants. Plant J 23:159–170PubMedGoogle Scholar
  12. Beck SA, Smith KL, Tisdale MJ (1991) Anticachectic and antitumor effect of eicosapentaenoic acid and its effect on protein turnover. Cancer Res 51:6089–6093PubMedGoogle Scholar
  13. Behrens PW (2005) Photobioreactors and fermentors: the light and dark sides of growing algae. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, New York, pp 189–204Google Scholar
  14. Benatti P, Peluso G, Nicolai R et al (2004) Polyunsaturated fatty acids: biochemical, nutritional and epigenetic properties. J Am Coll Nutr 23:281–302PubMedGoogle Scholar
  15. Bonefeld-Jorgensen EC, Moller SM, Hansen JC (2001) Modulation of atherosclerotic risk factors by seal oil: a preliminary assessment. Int J Circumpolar Health 60:25–33PubMedGoogle Scholar
  16. Booker CS, Mann JI (2008) Trans fatty acids and cardiovascular health: translation of the evidence base. Nutr Metab Cardiovasc Dis 18:448–456PubMedGoogle Scholar
  17. Bossola M, Muscaritoli M, Costelli P et al (2003) Increased muscle proteasome activity correlates with disease severity in gastric cancer patients. Ann Surg 237:384–389PubMedGoogle Scholar
  18. Bruera E, Strasser F, Palmer JL et al (2003) Effect of fish oil on appetite and other symptoms in patients with advanced cancer and anorexia/cachexia: a double-blind, placebo-controlled study. J Clin Oncol 21:129–134PubMedGoogle Scholar
  19. Bukberg J, Penman D, Holland JC (1984) Depression in hospitalized cancer patients. Psychosom Med 46:199–212PubMedGoogle Scholar
  20. Burns A, Iliffe S (2009) Dementia. BMJ 338:b75PubMedGoogle Scholar
  21. Burns CP, Halabi S, Clamon G et al (2004) Phase II study of high-dose fish oil capsules for patients with cancer-related cachexia. Cancer 101:370–378PubMedGoogle Scholar
  22. Burstein HJ (2007) Cognitive side-effects of adjuvant treatments. Breast 16(Suppl 2):S166–S168PubMedGoogle Scholar
  23. Calder PC, Yaqoob P (2009) Omega-3 polyunsaturated fatty acids and human health outcomes. BioFactors 35:266–272PubMedGoogle Scholar
  24. Cariuk P, Lorite MJ, Todorov PT et al (1997) Induction of cachexia in mice by a product isolated from the urine of cachectic cancer patients. Br J Cancer 76:606–613PubMedCentralPubMedGoogle Scholar
  25. Carr D, Goudas L, Lawrence D, Pirl W, Lau J, DeVine D, Kupelnick B, Miller K (2002) Management of cancer symptoms: pain, depression, and fatigue. Evid Rep Technol Assess (Summ) (61):1–5Google Scholar
  26. Cavanaugh SA, Wettstein RM (1983) The relationship between severity of depression, cognitive dysfunction, and age in medical inpatients. Am J Psychiatry 140:495–496PubMedGoogle Scholar
  27. Cerchietti LC, Navigante AH, Castro MA (2007) Effects of eicosapentaenoic and docosahexaenoic n-3 fatty acids from fish oil and preferential Cox-2 inhibition on systemic syndromes in patients with advanced lung cancer. Nutr Cancer 59:14–20PubMedGoogle Scholar
  28. Chan JM, Weinberg V, Magbanua MJ, et al. (2011) Nutritional supplements, COX-2 and IGF-1 expression in men on active surveillance for prostate cancer. Cancer Causes Control 22:141–50 ( NCT00402285)Google Scholar
  29. Cheng B, Wu G, Vrinten P et al (2010) Towards the production of high levels of eicosapentaenoic acid in transgenic plants: the effects of different host species, genes and promoters. Transgenic Res 19:221–229PubMedGoogle Scholar
  30. Chia Seed Oil (2012). In.
  31. Clandinin MT, Chappell JE, Leong S et al (1980a) Extrauterine fatty acid accretion in infant brain: implications for fatty acid requirements. Early Hum Dev 4:131–138PubMedGoogle Scholar
  32. Clandinin MT, Chappell JE, Leong S et al (1980b) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum Dev 4:121–129PubMedGoogle Scholar
  33. Clandinin MT, Chappell JE, Heim T et al (1981) Fatty acid utilization in perinatal de novo synthesis of tissues. Early Hum Dev 5:355–366PubMedGoogle Scholar
  34. Colomer R, Moreno-Nogueira JM, Garcia-Luna PP et al (2007) N-3 fatty acids, cancer and cachexia: a systematic review of the literature. Br J Nutr 97:823–831PubMedGoogle Scholar
  35. Darbani B, Eimanifar A, Stewart CN Jr et al (2007) Methods to produce marker-free transgenic plants. Biotechnol J 2:83–90PubMedGoogle Scholar
  36. de Luis DA, Izaola O, Aller R et al (2008) A randomized clinical trial with two omega 3 fatty acid enhanced oral supplements in head and neck cancer ambulatory patients. Eur Rev Med Pharmacol Sci 12:177–181PubMedGoogle Scholar
  37. De Miranda Torrinhas RS, Santana R, Garcia T, et al. (2012) Parenteral fish oil as a pharmacological agent to modulate post-operative immune response: a randomized, double-blind, and controlled clinical trial in patients with gastrointestinal cancer. Clin Nutr ( NCT01218841)Google Scholar
  38. Debruyne PR, Witek M, Gong L et al (2006) Bile acids induce ectopic expression of intestinal guanylyl cyclase C Through nuclear factor-kappaB and Cdx2 in human esophageal cells. Gastroenterology 130:1191–1206PubMedGoogle Scholar
  39. Debruyne PR, Pottel L, Nutriom TMG (2012) Influence of oral echium oil (omega-3 fatty acid) supplementation on weight loss in (pre)cachectic head and neck cancer patients: the nutriom trial. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 156:S1–S100 (P-17)Google Scholar
  40. Decsi T, Kennedy K (2011) Sex-specific differences in essential fatty acid metabolism. Am J Clin Nutr 94:1914S–1919SPubMedGoogle Scholar
  41. Delpal S, Pauloin A, Hue-Beauvais C et al (2013) Effects of dietary fish oil and corn oil on rat mammary tissue. Cell Tissue Res 351:453–464PubMedGoogle Scholar
  42. Demark-Wahnefried W, Robertson CN, Walther PJ, et al. (2004) Pilot study to explore effects of low-fat, flaxseed-supplemented diet on proliferation of benign prostatic epithelium and prostate-specific antigen. Urology 63:900–904 ( NCT000049309)Google Scholar
  43. Dewey A, Baughan C, Dean T, et al. (2007) Eicosapentaenoic acid (EPA, an omega-3 fatty acid from fish oils) for the treatment of cancer cachexia. Cochrane Database Syst Rev 24:CD004597Google Scholar
  44. Di Giuseppe R, De Lorgeril M, Salen P et al (2009) Alcohol consumption and n-3 polyunsaturated fatty acids in healthy men and women from 3 European populations. Am J Clin Nutr 89:354–362PubMedGoogle Scholar
  45. Dowell P, Hu Z, Lane MD (2005) Monitoring energy balance: metabolites of fatty acid synthesis as hypothalamic sensors. Annu Rev Biochem 74:515–534PubMedGoogle Scholar
  46. Eaton SB, Eaton SB 3rd, Sinclair AJ et al (1998) Dietary intake of long-chain polyunsaturated fatty acids during the paleolithic. World Rev Nutr Diet 83:12–23PubMedGoogle Scholar
  47. El Hafid R, Blade SF, Hoyano Y (2002) Seeding date and nitrogen fertilization effects on the performance of borage (Borago officinalis L.). Ind Crops Prod 16:193–199Google Scholar
  48. Fabian C (2011) Prevention strategy for pre-menopausal women at high risk for development of breast cancer.
  49. Farhady P (2008) Investigation of the usefulness of Omega 3 vitamins in the relief of hot flashes in menopausal women.
  50. Fearon KC, Von Meyenfeldt MF, Moses AG et al (2003) Effect of a protein and energy dense N-3 fatty acid enriched oral supplement on loss of weight and lean tissue in cancer cachexia: a randomised double blind trial. Gut 52:1479–1486PubMedGoogle Scholar
  51. Fearon KC, Barber MD, Moses AG et al (2006) Double-blind, placebo-controlled, randomized study of eicosapentaenoic acid diester in patients with cancer cachexia. J Clin Oncol 24:3401–3407PubMedGoogle Scholar
  52. Fearon K, Strasser F, Anker SD et al (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12:489–495PubMedGoogle Scholar
  53. Fedorova I, Hussein N, Di Martino C et al (2007) An n-3 fatty acid deficient diet affects mouse spatial learning in the Barnes circular maze. Prostaglandins Leukot Essent Fatty Acids 77:269–277PubMedCentralPubMedGoogle Scholar
  54. Fedorova I, Hussein N, Baumann MH et al (2009) An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze. Behav Neurosci 123:196–205PubMedGoogle Scholar
  55. Ferlay J, Parkin DM, Steliarova-Foucher E (2010) Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 46:765–781PubMedGoogle Scholar
  56. Flider FJ (2005) GLA: uses and new sources. INFORM 16:279–282Google Scholar
  57. Fraeye I, Bruneel C, Lemahieu C et al (2012) Dietary enrichment of eggs with omega-3 fatty acids: a review. Food Res Int 48:961–969Google Scholar
  58. Garcia A (2005) Omega-3 fatty acids in preventing breast cancer in women at high risk of developing breast cancer.
  59. Gerster H (1998) Can adults adequately convert alpha-linolenic acid (18:3n–3) to eicosapentaenoic acid (20:5n–3) and docosahexaenoic acid (22:6n–3)? Int J Vitam Nutr Res 68:159–173PubMedGoogle Scholar
  60. Ghoreishi Z, Esfahani A, Djazayeri A, et al. (2012) Omega-3 fatty acids are protective against paclitaxel-induced peripheral neuropathy: a randomized double-blind placebo controlled trial. BMC Cancer 12:355 ( NCT01049295)Google Scholar
  61. Glatz JF, Borchers T, Spener F et al (1995) Fatty acids in cell signalling: modulation by lipid binding proteins. Prostaglandins Leukot Essent Fatty Acids 52:121–127PubMedGoogle Scholar
  62. Gogus U, Smith C (2010) N-3 omega fatty acids: a review of current knowledge. Int J Food Sci Technol 45:417–436Google Scholar
  63. Grassi L, Gritti P, Rigatelli M et al (2000) Psychosocial problems secondary to cancer: an Italian multicentre survey of consultation-liaison psychiatry in oncology. Italian Consultation-Liaison Group. Eur J Cancer 36:579–585PubMedGoogle Scholar
  64. Green TG, Hilditch TP (1935) The identification of linoleic and linolenic acids. Biochem J 29:1552–1563PubMedGoogle Scholar
  65. Guarcello M, Riso S, Andrea FD (2006) EPA-enriched oral nutritional support in patients with lung cancer: effects on nutritional status and quality of life. Nutr Ther Metab 24:168–175Google Scholar
  66. Guest DD, Evans EM, Rogers LQ (2013) Diet components associated with perceived fatigue in breast cancer survivors. Eur J Cancer Care (Engl) 22:51–59Google Scholar
  67. Guil-Guerrero JL (2007) Stearidonic acid (18:4n–3): metabolism, nutritional importance, medical uses and natural sources. Eur J Lipid Sci Technol 109:1226–1236Google Scholar
  68. Hennebelle M, Balasse L, Latour A et al (2012) Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress. PLoS ONE 7:e42142PubMedCentralPubMedGoogle Scholar
  69. Hershman D (2009) Omega-3-fatty acid on joint symptoms inducted by aromatase inhibitors. Available from:
  70. Hershman D, Baker LH (2011) Omega-3-fatty acid supplements in treating muscle and bone pain and stiffness in patients with stage I, stage II, or stage III breast cancer receiving hormone therapy. Available from:
  71. Hilbert G, Lillemark L, Balchen S et al (1998) Reduction of organochlorine contaminants from fish oil during refining. Chemosphere 37:1241–1252PubMedGoogle Scholar
  72. Hoffmann M, Wagner M, Abbadi A et al (2008) Metabolic engineering of omega3-very long chain polyunsaturated fatty acid production by an exclusively acyl-CoA-dependent pathway. J Biol Chem 283:22352–22362PubMedGoogle Scholar
  73. Hooijmans CR, Pasker-De Jong PC, De Vries RB et al (2012) The effects of long-term omega-3 fatty acid supplementation on cognition and Alzheimer’s pathology in animal models of Alzheimer’s disease: a systematic review and meta-analysis. J Alzheimers Dis 28:191–209PubMedGoogle Scholar
  74. Huang YS, Pereira SL, Leonard AE (2004) Enzymes for transgenic biosynthesis of long-chain polyunsaturated fatty acids. Biochimie 86:793–798PubMedGoogle Scholar
  75. James MJ, Ursin VM, Cleland LG (2003) Metabolism of stearidonic acid in human subjects: comparison with the metabolism of other n-3 fatty acids. Am J Clin Nutr 77:1140–1145PubMedGoogle Scholar
  76. Janick J, Simon JE, Quinn J et al (1989) Borage: a source of gamma linolenic acid. Herbs Spices Med Plants Recent Adv Bot Hortic Pharmacol 4:145–168Google Scholar
  77. Jatoi A, Rowland K, Loprinzi CL et al (2004) An eicosapentaenoic acid supplement versus megestrol acetate versus both for patients with cancer-associated wasting: a North Central Cancer Treatment Group and National Cancer Institute of Canada collaborative effort. J Clin Oncol 22:2469–2476PubMedGoogle Scholar
  78. Jenkins D (2006) ALA and Prostate Cancer.
  79. Kaplan B (2010) A double-blind study to evaluate the effect of femarelle® on menopausal on vasomotor symptoms.
  80. Kapoor R, Huang YS (2006) Gamma linolenic acid: an antiinflammatory omega-6 fatty acid. Curr Pharm Biotechnol 7:531–534PubMedGoogle Scholar
  81. Karr JE, Alexander JE, Winningham RG (2011) Omega-3 polyunsaturated fatty acids and cognition throughout the lifespan: a review. Nutr Neurosci 14:216–225PubMedGoogle Scholar
  82. Kavraal S, Oncu SK, Bitiktas S et al (2012) Maternal intake of Omega-3 essential fatty acids improves long term potentiation in the dentate gyrus and Morris water maze performance in rats. Brain Res 1482:32–39PubMedGoogle Scholar
  83. Kiecolt-Glaser JK, Belury MA, Porter K et al (2007) Depressive symptoms, omega-6:omega-3 fatty acids, and inflammation in older adults. Psychosom Med 69:217–224PubMedCentralPubMedGoogle Scholar
  84. Kim J, Li Y, Watkins BA (2011) Endocannabinoid signaling and energy metabolism: a target for dietary intervention. Nutrition 27:624–632PubMedGoogle Scholar
  85. Kinney AJ, Cahoon EB, Damude HG, Hitz WD, Kolar CW, Liu ZB (2004) Production of very long chain polyunsaturated fatty acids in oilseed plants. E.I. Dupont De Nemours and Company. International Patent Publication WO2004071467Google Scholar
  86. Kobayakawa M, Yamawaki S, Hamazaki K et al (2005) Levels of omega-3 fatty acid in serum phospholipids and depression in patients with lung cancer. Br J Cancer 93:1329–1333PubMedCentralPubMedGoogle Scholar
  87. Kramer JK, Cruz-Hernandez C, Or-Rashid M, et al. (2004) The use of total trans-11 containing FA, rather than total “n-7” FA, is recommended to assess the content of FA with a positive health image in rumiant fats. Lipids 39:693–5 (author reply 5–6)Google Scholar
  88. Krill Oil Novel Food Approval (2009) Krill oil novel food approval, decision 2009/752/EC.
  89. Kris-Etherton PM (1999) AHA science advisory. Monounsaturated fatty acids and risk of cardiovascular disease. American Heart Association. Nutrition Committee. Circulation 100:1253–1258PubMedGoogle Scholar
  90. Kris-Etherton PM, Harris WS, Appel LJ et al (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747–2757PubMedGoogle Scholar
  91. Krul ES, Lemke SL, Mukherjea R et al (2012) Effects of duration of treatment and dosage of eicosapentaenoic acid and stearidonic acid on red blood cell eicosapentaenoic acid content. Prostaglandins Leukot Essent Fatty Acids 86:51–59PubMedGoogle Scholar
  92. Kuhnt K, Degen C, Jaudszus A et al (2012) Searching for health beneficial n-3 and n-6 fatty acids in plant seeds. Eur J Lipid Sci Technol 114:153–160PubMedCentralPubMedGoogle Scholar
  93. Languille S, Aujard F, Pifferi F (2012) Effect of dietary fish oil supplementation on the exploratory activity, emotional status and spatial memory of the aged mouse lemur, a non-human primate. Behav Brain Res 235:280–286PubMedGoogle Scholar
  94. Larque E, Gil-Sanchez A, Prieto-Sanchez MT et al (2012) Omega 3 fatty acids, gestation and pregnancy outcomes. Br J Nutr 107(Suppl 2):S77–S84PubMedGoogle Scholar
  95. Lazarus DD, Destree AT, Mazzola LM et al (1999) A new model of cancer cachexia: contribution of the ubiquitin-proteasome pathway. Am J Physiol 277:E332–E341PubMedGoogle Scholar
  96. Lee KW, Lip GYH (2003) The role of omega-3 fatty acids in the secondary prevention of cardiovascular disease. Q J Med 96:465–480Google Scholar
  97. Li N, Xia Q, Ruan J et al (2011) Hepatotoxicity and tumorigenicity induced by metabolic activation of pyrrolizidine alkaloids in herbs. Curr Drug Metab 12:823–834PubMedGoogle Scholar
  98. Lin PY, Chiu CC, Huang SY et al (2012) A meta-analytic review of polyunsaturated fatty acid compositions in dementia. J Clin Psychiatry 73:1245–1254PubMedGoogle Scholar
  99. Lucas M, Asselin G, Merette C et al (2009) Ethyl-eicosapentaenoic acid for the treatment of psychological distress and depressive symptoms in middle-aged women: a double-blind, placebo-controlled, randomized clinical trial. Am J Clin Nutr 89:641–651PubMedGoogle Scholar
  100. Luchtman DW, Song C (2012) Cognitive enhancement by omega-3 fatty acids from child-hood to old age: findings from animal and clinical studies. Neuropharmacology 64:550–565PubMedGoogle Scholar
  101. Lustberg M (2011) Omega-3 fatty acids in preventing joint symptoms in patients with stage I-III breast cancer receiving anastrozole, exemestane, or letrozole.
  102. Mahaffey KR, Sunderland EM, Chan HM et al (2011) Balancing the benefits of n-3 polyunsaturated fatty acids and the risks of methylmercury exposure from fish consumption. Nutr Rev 69:493–508PubMedCentralPubMedGoogle Scholar
  103. Maki KC, Reeves MS, Farmer M et al (2009) Krill oil supplementation increases plasma concentrations of eicosapentaenoic and docosahexaenoic acids in overweight and obese men and women. Nutr Res 29:609–615PubMedGoogle Scholar
  104. Makrides M, Neumann M, Simmer K et al (1995) Are long-chain polyunsaturated fatty acids essential nutrients in infancy? Lancet 345:1463–1468PubMedGoogle Scholar
  105. Malerba G, Schaeffer L, Xumerle L et al (2008) SNPs of the FADS gene cluster are associated with polyunsaturated fatty acids in a cohort of patients with cardiovascular disease. Lipids 43:289–299PubMedGoogle Scholar
  106. Mann NJ, O’connell SL, Baldwin KM et al (2010) Effects of seal oil and tuna-fish oil on platelet parameters and plasma lipid levels in healthy subjects. Lipids 45:669–681PubMedGoogle Scholar
  107. Mantovani G, Maccio A, Madeddu C et al (2006) A phase II study with antioxidants, both in the diet and supplemented, pharmaconutritional support, progestagen, and anti-cyclooxygenase-2 showing efficacy and safety in patients with cancer-related anorexia/cachexia and oxidative stress. Cancer Epidemiol Biomarkers Prev 15:1030–1034PubMedGoogle Scholar
  108. Marangell LB, Martinez JM, Zboyan HA et al (2003) A double-blind, placebo-controlled study of the omega-3 fatty acid docosahexaenoic acid in the treatment of major depression. Am J Psychiatry 160:996–998PubMedGoogle Scholar
  109. Mazzotta P, Jeney CM (2009) Anorexia-cachexia syndrome: a systematic review of the role of dietary polyunsaturated Fatty acids in the management of symptoms, survival, and quality of life. J Pain Symptom Manage 37:1069–1077PubMedGoogle Scholar
  110. Mccann SE, Hootman KC, Weaver AM, et al. (2012) Dietary intakes of total and specific lignans are associated with clinical breast tumor characteristics. J Nutr 142:91–8 ( NCT00794989)Google Scholar
  111. Meijer A, Roseman M, Milette K et al (2011) Depression screening and patient outcomes in cancer: a systematic review. PLoS ONE 6:e27181PubMedCentralPubMedGoogle Scholar
  112. Meyer BJ, Mann NJ, Lewis JL et al (2003) Dietary intakes and food sources of omega-6 and omega-3 polyunsaturated fatty acids. Lipids 38:391–398PubMedGoogle Scholar
  113. Miller MR, Nichols PD, Carter CG (2008) n-3 Oil sources for use in aquaculture–alternatives to the unsustainable harvest of wild fish. Nutr Res Rev 21:85–96PubMedGoogle Scholar
  114. Mirzazadeh M (2009) Omega-3 fatty acids in treating patients with advanced prostate cancer.
  115. Mizock BA (2010) Immunonutrition and critical illness: an update. Nutrition 26:701–707PubMedGoogle Scholar
  116. Monteiro J, Li FJ, Maclennan M et al (2012) Menhaden oil, but not safflower or soybean oil, aids in restoring the polyunsaturated fatty acid profile in the novel delta-6-desaturase null mouse. Lipids Health Dis 11:60PubMedCentralPubMedGoogle Scholar
  117. Moranis A, Delpech JC, De Smedt-Peyrusse V et al (2012) Long term adequate n-3 polyunsaturated fatty acid diet protects from depressive-like behavior but not from working memory disruption and brain cytokine expression in aged mice. Brain Behav Immun 26:721–731PubMedGoogle Scholar
  118. Morimoto KC, Van Eenennaam AL, Depeters EJ et al (2005) Endogenous production of n-3 and n-6 fatty acids in mammalian cells. J Dairy Sci 88:1142–1146PubMedGoogle Scholar
  119. Moses AW, Slater C, Preston T et al (2004) Reduced total energy expenditure and physical activity in cachectic patients with pancreatic cancer can be modulated by an energy and protein dense oral supplement enriched with n-3 fatty acids. Br J Cancer 90:996–1002PubMedCentralPubMedGoogle Scholar
  120. Mozaffari-Khosravi H, Yassini-Ardakani M, Karamati M, Shariati-Bafghi SE (2013) Eicosapentaenoic acid versus docosahexaenoic acid in mild-to-moderate depression: a randomized, double-blind, placebo-controlled trial. Eur Neuropsychopharmacol 23(7):636–644Google Scholar
  121. Murff HJ (2012) Fish oil supplementation, nutrigenomics and colorectal cancer prevention.
  122. Murphy RA, Mourtzakis M, Chu QS et al (2010a) Supplementation with fish oil increases first-line chemotherapy efficacy in patients with advanced nonsmall cell lung cancer. Cancer 117:3774–3780Google Scholar
  123. Murphy RA, Mourtzakis M, Chu QS et al (2010b) Skeletal muscle depletion is associated with reduced plasma (n-3) fatty acids in non-small cell lung cancer patients. J Nutr 140:1602–1606PubMedGoogle Scholar
  124. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283PubMedGoogle Scholar
  125. Myers JS, Pierce J, Pazdernik T (2008) Neurotoxicology of chemotherapy in relation to cytokine release, the blood-brain barrier, and cognitive impairment. Oncol Nurs Forum 35:916–920PubMedGoogle Scholar
  126. Napier JA (2007) The production of unusual fatty acids in transgenic plants. Annu Rev Plant Biol 58:295–319PubMedGoogle Scholar
  127. Nichols PD, Petrie J, Singh S (2010) Long-chain omega-3 oils—an update on sustainable sources. Nutrients 2:572–585PubMedCentralPubMedGoogle Scholar
  128. Novel Food Approval (2007) Echium Plantagineum novel food approval.
  129. O’connor TL (2008) Flaxseed, aromatase inhibitors and breast tumor characteristics (FABrC).
  130. Okada T, Furuhashi N, Kuromori Y et al (2005) Plasma palmitoleic acid content and obesity in children. Am J Clin Nutr 82:747–750PubMedGoogle Scholar
  131. Olendzki BC, Leung K, Van Buskirk S et al (2011) Treatment of rheumatoid arthritis with marine and botanical oils: influence on serum lipids. Evid Based Complement Alternat Med 2011:827286PubMedCentralPubMedGoogle Scholar
  132. Oomah BD, Busson M, Godfrey DV et al (2002) Characteristics of hemp (Cannabis Sativa L.) seed oil. Food Chem 76:33–43Google Scholar
  133. Osman H, Suriah AR, Law EC (2001) Fatty acid composition and cholesterol content of selected marine fish in Malaysian waters. Food Chem 73:55–60Google Scholar
  134. Pace TW, Hu F, Miller AH (2007) Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav Immun 21:9–19PubMedCentralPubMedGoogle Scholar
  135. Palacios G, Lovoll M, Tengs T et al (2010) Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS ONE 5:e11487PubMedCentralPubMedGoogle Scholar
  136. Park JS, Chyun JH, Kim YK et al (2010) Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutr Metab (Lond) 7:18Google Scholar
  137. Pedersen B, Koktved DP, Nielsen LL (2012) Living with side effects from cancer treatment—a challenge to target information. Scand J Caring Sci. doi: 10.1111/j.1471-6712.2012.01085.x
  138. Persson C, Glimelius B, Ronnelid J et al (2005) Impact of fish oil and melatonin on cachexia in patients with advanced gastrointestinal cancer: a randomized pilot study. Nutrition 21:170–178PubMedGoogle Scholar
  139. Petrie JR, Shrestha P, Mansour MP et al (2010) Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Delta6-desaturase with omega3-preference from the marine microalga Micromonas pusilla. Metab Eng 12:233–240PubMedGoogle Scholar
  140. Pruthi S, Thompson SL, Novotny PJ, et al. (2007) Pilot evaluation of flaxseed for the management of hot flashes. J Soc Integr Oncol 5:106–112 ( NCT00275704)Google Scholar
  141. Pruthi S, Qin R, Terstreip SA, et al. (2012) A phase III, randomized, placebo-controlled, double-blind trial of flaxseed for the treatment of hot flashes: North Central Cancer Treatment Group N08C7. Menopause 19:48–53 ( NCT00956813)Google Scholar
  142. Qi B, Fraser T, Mugford S et al (2004) Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants. Nat Biotechnol 22:739–745PubMedGoogle Scholar
  143. Quinn JF, Raman R, Thomas RG et al (2010) Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 304:1903–1911PubMedCentralPubMedGoogle Scholar
  144. Raff M, Tholstrup T, Basu S et al (2008) A diet rich in conjugated linoleic acid and butter increases lipid peroxidation but does not affect atherosclerotic, inflammatory, or diabetic risk markers in healthy young men. J Nutr 138:509–514PubMedGoogle Scholar
  145. Raison CL, Capuron L, Miller AH (2006) Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 27:24–31PubMedCentralPubMedGoogle Scholar
  146. Read JA, Beale PJ, Volker DH et al (2007) Nutrition intervention using an eicosapentaenoic acid (EPA)-containing supplement in patients with advanced colorectal cancer. Effects on nutritional and inflammatory status: a phase II trial. Support Care Cancer 15:301–307PubMedGoogle Scholar
  147. Rhodes LE (2009) An immunonutritional approach to the prevention of skin cancer.
  148. Ries A, Trottenberg P, Elsner F et al (2012) A systematic review on the role of fish oil for the treatment of cachexia in advanced cancer: an EPCRC cachexia guidelines project. Palliat Med 26:294–304PubMedGoogle Scholar
  149. Robert SS, Singh SP, Zhou XR et al (2005) Metabolic engineering of Arabidopsis to produce nutritionally important DHA in seed oil. Funct Plant Bio 32:473–479Google Scholar
  150. Rojas CV, Martinez JI, Flores I et al (2003) Gene expression analysis in human fetal retinal explants treated with docosahexaenoic acid. Invest Ophthalmol Vis Sci 44:3170–3177PubMedGoogle Scholar
  151. Ros E (2003) Dietary cis-monounsaturated fatty acids and metabolic control in type 2 diabetes. Am J Clin Nutr 78:617S–625SPubMedGoogle Scholar
  152. Ross JA, Fearon KC (2002) Eicosanoid-dependent cancer cachexia and wasting. Curr Opin Clin Nutr Metab Care 5:241–248PubMedGoogle Scholar
  153. Ross JA, Moses AG, Fearon KC (1999) The anti-catabolic effects of n-3 fatty acids. Curr Opin Clin Nutr Metab Care 2:219–226PubMedGoogle Scholar
  154. Rubio-Rodríguez N, Beltrán S, Jaime I, et al. (2010) Production of omega-3 polyunsaturated fatty acid concentrates: a review. Innov Food Sci Emerg Technol 11:1–12Google Scholar
  155. Ruiz-Lopez N, Haslam RP, Venegas-Caleron M et al (2009) The synthesis and accumulation of stearidonic acid in transgenic plants: a novel source of ‘heart-healthy’ omega-3 fatty acids. Plant Biotechnol J 7:704–716PubMedGoogle Scholar
  156. Ruiz-Lopez N, Sayanova O, Napier JA et al (2012) Metabolic engineering of the omega-3 long chain polyunsaturated fatty acid biosynthetic pathway into transgenic plants. J Exp Bot 63:2397–2410PubMedGoogle Scholar
  157. Ryan AM, Reynolds JV, Healy L, et al. (2009a) Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial. Ann Surg 249:355–363 ( NCT00790140)Google Scholar
  158. Ryan AM, Reynolds JV, Healy L et al (2009b) Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial. Ann Surg 249:355–363PubMedGoogle Scholar
  159. Ryckebosch E, Bruneel C, Muylaert K, et al. (2012) Microalgae as an alternative source of omega-3 long chain polyunsaturated fatty acids. Lipid Technol 24:128–130Google Scholar
  160. Sangiovanni JP, Parra-Cabrera S, Colditz GA et al (2000) Meta-analysis of dietary essential fatty acids and long-chain polyunsaturated fatty acids as they relate to visual resolution acuity in healthy preterm infants. Pediatrics 105:1292–1298PubMedGoogle Scholar
  161. Sato S, Xing A, Ye X et al (2004) Production of gamma-linolenic acid and stearidonic acid in seeds of marker-free transgenic soybean. Crop Sci 44:646–652Google Scholar
  162. Sayanova O, Haslam R, Venegas Caleron M et al (2007) Cloning and characterization of unusual fatty acid desaturases from Anemone leveillei: identification of an acyl-coenzyme A C20 Delta5-desaturase responsible for the synthesis of sciadonic acid. Plant Physiol 144:455–467PubMedCentralPubMedGoogle Scholar
  163. Saykin AJ, Ahles TA, Mcdonald BC (2003) Mechanisms of chemotherapy-induced cognitive disorders: neuropsychological, pathophysiological, and neuroimaging perspectives. Semin Clin Neuropsychiatry 8:201–216PubMedGoogle Scholar
  164. Scheltens P, Twisk JW, Blesa R et al (2012) Efficacy of souvenaid in mild Alzheimer’s disease: results from a randomized, controlled trial. J Alzheimers Dis 31:225–236PubMedGoogle Scholar
  165. Schmidt E (2007) Omega-3 fatty acids and postoperative complications after colorectal surgery (omega3).
  166. Schwab JJ, Bialow M, Brown JM et al (1967) Diagnosing depression in medical inpatients. Ann Intern Med 67:695–707PubMedGoogle Scholar
  167. Shannon J (2005) Fish oil and green tea extract in preventing prostate cancer in patients who are at risk for developing prostate cancer.
  168. Siddiqui R, Pandya D, Harvey K et al (2006) Nutrition modulation of cachexia/proteolysis. Nutr Clin Pract 21:155–167PubMedGoogle Scholar
  169. Signori C, Dubrock C, Richie JP, et al. (2012) Administration of omega-3 fatty acids and Raloxifene to women at high risk of breast cancer: interim feasibility and biomarkers analysis from a clinical trial. Eur J Clin Nutr 66:878–884 ( NCT00723398)Google Scholar
  170. Sijben JW, Calder PC (2007) Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease. Proc Nutr Soc 66:237–259PubMedGoogle Scholar
  171. Simopoulos AP (2002) Omega-3 fatty acids in wild plants, nuts and seeds. Asia Pac J Clin Nutr 11:S163–S173Google Scholar
  172. Simopoulos AP (2010) Genetic variants in the metabolism of omega-6 and omega-3 fatty acids: their role in the determination of nutritional requirements and chronic disease risk. Exp Biol Med (Maywood) 235:785–795Google Scholar
  173. Simopoulos AP, Leaf A, Salem N Jr (1999) Essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. Ann Nutr Metab 43:127–130PubMedGoogle Scholar
  174. Singer S, Kuhnt S, Gotze H et al (2009) Hospital anxiety and depression scale cutoff scores for cancer patients in acute care. Br J Cancer 100:908–912PubMedCentralPubMedGoogle Scholar
  175. Sioen I, De Henauw S, Van Camp J et al (2009) Comparison of the nutritional-toxicological conflict related to seafood consumption in different regions worldwide. Regul Toxicol Pharmacol 55:219–228PubMedGoogle Scholar
  176. Smith HJ, Lorite MJ, Tisdale MJ (1999) Effect of a cancer cachectic factor on protein synthesis/degradation in murine C2C12 myoblasts: modulation by eicosapentaenoic acid. Cancer Res 59:5507–5513PubMedGoogle Scholar
  177. Song C, Li X, Leonard BE et al (2003) Effects of dietary n-3 or n-6 fatty acids on interleukin-1beta-induced anxiety, stress, and inflammatory responses in rats. J Lipid Res 44:1984–1991PubMedGoogle Scholar
  178. Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486:219–231PubMedGoogle Scholar
  179. Sternfeld B, Lacroix A, Caan BJ, et al. (2013) Design and methods of a multi-site, multi-behavioral treatment trial for menopausal symptoms: The MsFLASH experience. Contemp Clin Trials 35:25–34 ( NCT01178892)Google Scholar
  180. Suzuki S, Akechi T, Kobayashi M et al (2004) Daily omega-3 fatty acid intake and depression in Japanese patients with newly diagnosed lung cancer. Br J Cancer 90:787–793PubMedCentralPubMedGoogle Scholar
  181. Sydenham E, Dangour AD, Lim WS (2012) Omega 3 fatty acid for the prevention of cognitive decline and dementia. Cochrane Database Syst Rev 6:CD005379Google Scholar
  182. Tajalizadekhoob Y, Sharifi F, Fakhrzadeh H et al (2011) The effect of low-dose omega 3 fatty acids on the treatment of mild to moderate depression in the elderly: a double-blind, randomized, placebo-controlled study. Eur Arch Psychiatry Clin Neurosci 261:539–549PubMedGoogle Scholar
  183. Tam O, Innis SM (2006) Dietary polyunsaturated fatty acids in gestation alter fetal cortical phospholipids, fatty acids and phosphatidylserine synthesis. Dev Neurosci 28:222–229PubMedGoogle Scholar
  184. Tanveer A (2009) Effects of Tamoxifen in women with benign breast disease not having any risks of developing breast cancer.
  185. Tapiero H, Ba GN, Couvreur P et al (2002) Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies. Biomed Pharmacother 56:215–222PubMedGoogle Scholar
  186. Taylor LAL, Pletschen J, Arends C, et al. (2010) Marine phospholipids-a promising new dietary approach to tumor-associated weight oss. Support Cancer Care 18:159–170Google Scholar
  187. Topkan E, Yavuz AA, Ozyilkan O (2007) Cancer cachexia: pathophysiologic aspects and treatment options. Asian Pac J Cancer Prev 8:445–451PubMedGoogle Scholar
  188. Toufektsian MC, Salen P, Laporte F et al (2011) Dietary flavonoids increase plasma very long-chain (n-3) fatty acids in rats. J Nutr 141:37–41PubMedGoogle Scholar
  189. Tramm R, Mccarthy AL, Yates P (2011) Dietary modification for women after breast cancer treatment: a narrative review. Eur J Cancer Care (Engl) 20:294–304Google Scholar
  190. Tur JA, Bibiloni MM, Sureda A et al (2012) Dietary sources of omega 3 fatty acids: public health risks and benefits. Br J Nutr 107(Suppl 2):S23–S52PubMedGoogle Scholar
  191. Tvrzicka E, Kremmyda LS, Stankova B et al (2011) Fatty acids as biocompounds: their role in human metabolism, health and disease–a review. Part 1: classification, dietary sources and biological functions. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 155:117–130PubMedGoogle Scholar
  192. Ulven SM, Kirkhus B, Lamglait A et al (2010) Metabolic effects of krill oil are essentially similar to those of fish oil but at lower dose of EPA and DHA, in healthy volunteers. Lipids 46:37–46PubMedCentralPubMedGoogle Scholar
  193. Van Der Meij BS, Langius JA, Spreeuwenberg MD et al (2012) Oral nutritional supplements containing n-3 polyunsaturated fatty acids affect quality of life and functional status in lung cancer patients during multimodality treatment: an RCT. Eur J Clin Nutr 66:399–404PubMedCentralPubMedGoogle Scholar
  194. Van’t Spijker A, Trijsburg RW, Duivenvoorden HJ (1997) Psychological sequelae of cancer diagnosis: a meta-analytical review of 58 studies after 1980. Psychosom Med 59:280–293PubMedGoogle Scholar
  195. Venegas-Caleron M, Sayanova O, Napier JA (2009) An alternative to fish oils: metabolic engineering of oil-seed crops to produce omega-3 long chain polyunsaturated fatty acids. Prog Lipid Res 49:108–119PubMedGoogle Scholar
  196. Von Hazura K (1887) Untersuchungen über die Hanfölsäure. Monatsh 8:147–155Google Scholar
  197. Wang PY, Chen JJ, Su HM (2009) Docosahexaenoic acid supplementation of primary rat hippocampal neurons attenuates the neurotoxicity induced by aggregated amyloid beta protein(42) and up-regulates cytoskeletal protein expression. J Nutr Biochem 21:345–350PubMedGoogle Scholar
  198. Watkins BA, Hutchins H, Li Y et al (2010) The endocannabinoid signaling system: a marriage of PUFA and musculoskeletal health. J Nutr Biochem 21:1141–1152PubMedGoogle Scholar
  199. Weed HG, Ferguson ML, Gaff RL et al (2011) Lean body mass gain in patients with head and neck squamous cell cancer treated perioperatively with a protein- and energy-dense nutritional supplement containing eicosapentaenoic acid. Head Neck 33:1027–1033PubMedGoogle Scholar
  200. Welch AA, Shakya-Shrestha S, Lentjes MA et al (2010) Dietary intake and status of n-3 polyunsaturated fatty acids in a population of fish-eating and non-fish-eating meat-eaters, vegetarians, and vegans and the product-precursor ratio [corrected] of alpha-linolenic acid to long-chain n-3 polyunsaturated fatty acids: results from the EPIC-Norfolk cohort. Am J Clin Nutr 92:1040–1051PubMedGoogle Scholar
  201. Whitehouse AS, Smith HJ, Drake JL et al (2001) Mechanism of attenuation of skeletal muscle protein catabolism in cancer cachexia by eicosapentaenoic acid. Cancer Res 61:3604–3609PubMedGoogle Scholar
  202. Wigmore SJ, Ross JA, Falconer JS et al (1996) The effect of polyunsaturated fatty acids on the progress of cachexia in patients with pancreatic cancer. Nutrition 12:S27–S30PubMedGoogle Scholar
  203. Wijesundera C, Kitessa S, Abeywardena M, et al. (2011) Long-chain omega-3 oils: current and future supplies, food and feed applications, and stability. Lipid Technol 23:55–8Google Scholar
  204. Willatts P, Forsyth JS, Dimodugno MK et al (1998) Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet 352:688–691PubMedGoogle Scholar
  205. Williams CM, Burdge G (2006) Long-chain n-3 PUFA: plant v. marine sources. Proceed Nutr Soc 65:42–50Google Scholar
  206. Wolyniak CJ, Brenna JT, Murphy KJ, Sinclair AJ (2005) Gas chromatography-chemical ionization-mass spectrometric fatty acid analysis of a commercial supercritical carbon dioxide lipid extract from New Zealand green-lipped mussel (Perna canaliculus). Lipids 40(4):355–360Google Scholar
  207. Wu G, Truksa M, Datla N et al (2005) Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants. Nat Biotechnol 23:1013–1017PubMedGoogle Scholar
  208. Yee LD (2011) Dietary fish and omega 3 fatty acids for breast cancer prevention.
  209. Youdim KA, Martin A, Joseph JA (2000) Essential fatty acids and the brain: possible health implications. Int J Dev Neurosci 18:383–399PubMedGoogle Scholar
  210. Yurko-Mauro K, Mccarthy D, Rom D et al (2010) Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimers Dement 6:456–464PubMedGoogle Scholar
  211. Zuijdgeest-Van Leeuwen SD, Dagnelie PC, Wattimena JL et al. (2000) Eicosapentaenoic acid ethyl ester supplementation in cachectic cancer patients and healthy subjects: effects on lipolysis and lipid oxidation. Clin Nutr 19:417–423 ( NCT01218841)Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • L. Pottel
    • 1
    • 2
  • M. Lycke
    • 1
    • 2
  • T. Boterberg
    • 2
  • I. Foubert
    • 3
  • H. Pottel
    • 4
  • F. Duprez
    • 2
  • L. Goethals
    • 1
  • P. R. Debruyne
    • 1
    Email author
  1. 1.Cancer CenterGeneral Hospital GroeningeKortrijkBelgium
  2. 2.Department of Radiation OncologyGhent University HospitalGhentBelgium
  3. 3.Subfaculty of SciencesCatholic University of Leuven KulakKortrijkBelgium
  4. 4.Subfaculty of MedicineCatholic University of Leuven KulakKortrijkBelgium

Personalised recommendations