Is There Something Fishy About Fish Oil?

Author(s): Miloš Šunderić* , Dragana Robajac , Nikola Gligorijević , Goran Miljuš , Olgica Nedić , Katarina Smilkov , Darinka Gjorgieva Ackova , Vesna Rudić-Grujić , Ana Penezić .

Journal Name: Current Pharmaceutical Design

Volume 25 , Issue 15 , 2019

Abstract:

Background: Fish is consumed as food worldwide and is considered as a rich source of essential nutrients required for a healthy life. Supplementation with fish oil has been adopted as a solution to prevent or cure many pathophysiological states and diseases by both the professionals and the civil population. The beneficial effects are, however, being questioned, as some controversial results were obtained in clinical and population studies.

Methods: Critical evaluation of studies regarding known effects of fish oil, both in favour of its consumption and related controversies.

Results: From the literature review, contradictory allegations about the positive action of the fish oil on human health emerged, so that a clear line about its beneficial effect cannot be withdrawn.

Conclusion: Scientific results on the application of fish oil should be taken with caution as there is still no standardised approach in testing its effects and there are significantly different baselines in respect to nutritional and other lifestyle habits of different populations.

Keywords: Fish oil, ω-3PUFA, CVD, diabetes, cancer, controversies.

[1]
Weichselbaum E, Coe S, Buttriss J, Stanner S. Fish in the diet: A review. Nutr Bull 2013; 38: 128-77. [http://dx.doi.org/10.1111/nbu.12021].
[2]
Lamberg-Allardt C. Vitamin D in foods and as supplements. Prog Biophys Mol Biol 2006; 92(1): 33-8. [http://dx.doi.org/10.1016/j.pbiomolbio.2006.02.017]. [PMID: 16618499].
[3]
SACN (Scientific Advisory Committee on Nutrition). 2004. Advice on fish consumption: Benefits & Risks. Office, T.S.: London.
[4]
Shahidi F. Functional seafood lipids and proteinsFunctional Foods: Biochemical and Processing Aspects. Lancaster, UK: Technomic Publ. 1998; pp. 381-401.
[5]
Shahidi F, Ambigaipalan P. Omega-3 polyunsaturated fatty acids and their health benefits. Annu Rev Food Sci Technol 2018; 9: 345-81. [http://dx.doi.org/10.1146/annurev-food-111317-095850]. [PMID: 29350557].
[6]
Strobel C, Jahreis G, Kuhnt K. Survey of n-3 and n-6 polyunsaturated fatty acids in fish and fish products. Lipids Health Dis 2012; 11: 144. [http://dx.doi.org/10.1186/1476-511X-11-144]. [PMID: 23110317].
[7]
WHO (World Health Organisation), Population nutrient intake goals for preventing diet-related chronic diseases. [updated 2018; cited 2018 Oct 28]. Available from: www.who.int/nutrition/ topics/5_population_nutrient/en/index13.html
[8]
Fats and fatty acids in human nutrition Report of an expert consultation. Rome: WHO 2010.
[9]
EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA); Scientific Opinion related to the Tolerable Upper Intake Level of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and docosapentaenoic acid (DPA). EFSA J 2012; 10(7): 2815-[48 pp.].
[http://dx.doi.org/10.2903/j.efsa.2012.2815.]
[10]
Fernandes A, Smith F, Petch R, et al. Investigation into the Levels of Environmental Contaminants in Scottish Marine and Freshwater Fin Fish and Shellfish York: Food and Environment Research Agency 2009.www.food.gov.uk/sites/default/files/media/document/572-1-1005_S14040-S14041__Environmental_Contaminants_in_Scottish_Marine_and__Freshwater_Fish.pdf [updated 2018; cited 2018 Dec 1] .
[11]
FAO/WHO. 2011. Report of the Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption. Rome and Geneva.
[12]
EUMOFA 2018. The EU Fish Market. HIGHLGHTS. THE EU IN THE WORLD. EU MARKET SUPPLY. CONSUMPTION.TRADE. EU LANDINGS. AQUACULTURE PRODUCTION. [updated 2019; cited 2019 Apr 26].Available from: http://www.eumofa.eu/.
[13]
FAOSTAT, FAO. Food Balance Sheets: Fish, Seafood - Food supply quantity (kg/capita/yr) [updated 2019; cited 2019 Apr 26]. Available from: www.fao.org/faostat/en/?#data/.
[14]
Burdge GC, Calder PC. Dietary alpha-linolenic acid and health-related outcomes: A metabolic perspective. Nutr Res Rev 2006; 19(1): 26-52. [http://dx.doi.org/10.1079/NRR2005113]. [PMID: 19079874].
[15]
Calder PC. Very long chain omega-3 (n-3) fatty acids and human health. Eur J Lipid Sci Technol 2014; 116(10): 1280-300. [http://dx.doi.org/10.1002/ejlt.201400025].
[16]
Welch AA, Shakya-Shrestha S, Lentjes MA, Wareham NJ, Khaw KT. 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 α-linolenic acid to long-chain n-3 polyunsaturated fatty acids: Results from the EPIC-Norfolk cohort. Am J Clin Nutr 2010; 92(5): 1040-51. [http://dx.doi.org/10.3945/ajcn.2010.29457]. [PMID: 20861171].
[17]
Nobili V, Alisi A, Musso G, Scorletti E, Calder PC, Byrne CD. Omega-3 fatty acids: Mechanisms of benefit and therapeutic effects in pediatric and adult NAFLD. Crit Rev Clin Lab Sci 2016; 53(2): 106-20. [http://dx.doi.org/10.3109/10408363.2015.1092106]. [PMID: 26463349].
[18]
Scaioli E, Liverani E, Belluzzi A. The imbalance between n-6/n-3 polyunsaturated fatty acids and inflammatory bowel disease: A comprehensive review and future therapeutic perspectives. Int J Mol Sci 2017; 18(12)E2619 [http://dx.doi.org/10.3390/ijms18122619]. [PMID: 29206211].
[19]
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(4): 387-401. [http://dx.doi.org/10.1089/jmf.2004.7.387]. [PMID: 15671680].
[20]
Serhan CN. Pro-resolving lipid mediators are leads for resolution physiology. Nature 2014; 510: 92-101.
[21]
Schuchardt JP, Hahn A. Bioavailability of long-chain omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 2013; 89: 1-8.
[22]
Pike LJ. Lipid rafts: Bringing order to chaos. J Lipid Res 2003; 44(4): 655-67. [http://dx.doi.org/10.1194/jlr.R200021-JLR200]. [PMID: 12562849].
[23]
Yaqoob P. The nutritional significance of lipid rafts. Annu Rev Nutr 2009; 29: 257-82. [http://dx.doi.org/10.1146/annurev-nutr-080508-141205]. [PMID: 19400697].
[24]
Hou TY, McMurray DN, Chapkin RS. Omega-3 fatty acids, lipid rafts, and T cell signaling. Eur J Pharmacol 2016; 785: 2-9. [http://dx.doi.org/10.1016/j.ejphar.2015.03.091]. [PMID: 26001374].
[25]
Miles EA, Calder PC. Can early omega-3 fatty acid exposure reduce risk of childhood allergic disease? Nutrients 2017; 9(7): 784. [http://dx.doi.org/10.3390/nu9070784]. [PMID: 28754005].
[26]
Calder PC. Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. Biochim Biophys Acta 2015; 1851(4): 469-84. [http://dx.doi.org/10.1016/j.bbalip.2014.08.010]. [PMID: 25149823].
[27]
Vučić V. The Role of dietary polyunsaturated fatty acids in inflammation. Serb J Exp Clin Res 2013; 14: 93-9. [http://dx.doi.org/10.5937/sjecr14-4774].
[28]
U. S. Food and Drug Administration. Center for Food Safety and Applied Nutrition. Office of Nutritional Products, Labeling, and Dietary Supplements. 2000. Letter Regarding Dietary Supplement Health Claim for Omega-3 Fatty Acids and Coronary Heart Disease
[29]
Brunton S, Collins N. Differentiating prescription omega-3-acid ethyl esters (P-OM3) from dietary-supplement omega-3 fatty acids. Curr Med Res Opin 2007; 23(5): 1139-45. [http://dx.doi.org/10.1185/030079907X188017]. [PMID: 17519081].
[30]
Rosin S, Ojansivu I, Kopu A, Keto-Tokoi M, Gylling H. Optimal use of plant stanol ester in the management of hypercholesterolemia. Cholesterol 2015; 2015706970 [http://dx.doi.org/10.1155/2015/706970]. [PMID: 26543642].
[31]
Baigent C, Blackwell L, Emberson J, et al. Efficacy and safety of more intensive lowering of LDL cholesterol: A meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet 2010; 376(9753): 1670-81. [http://dx.doi.org/10.1016/S0140-6736(10)61350-5]. [PMID: 21067804].
[32]
Bang HO, Dyerberg J, Nielsen AB. Plasma lipid and lipoprotein pattern in Greenlandic West-coast Eskimos. Lancet 1971; 1(7710): 1143-5. [http://dx.doi.org/10.1016/S0140-6736(71)91658-8]. [PMID: 4102857].
[33]
Mori TA. Marine OMEGA-3 fatty acids in the prevention of cardiovascular disease. Fitoterapia 2017; 123: 51-8. [http://dx.doi.org/10.1016/j.fitote.2017.09.015]. [PMID: 28964873].
[34]
Bucher HC, Hengstler P, Schindler C, Meier G. N-3 polyunsaturated fatty acids in coronary heart disease: A meta-analysis of randomized controlled trials. Am J Med 2002; 112(4): 298-304. [http://dx.doi.org/10.1016/S0002-9343(01)01114-7]. [PMID: 11893369].
[35]
Whelton SP, He J, Whelton PK, Muntner P. Meta-analysis of observational studies on fish intake and coronary heart disease. Am J Cardiol 2004; 93(9): 1119-23. [http://dx.doi.org/10.1016/j.amjcard.2004.01.038]. [PMID: 15110203].
[36]
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(22): 2705-11. [http://dx.doi.org/10.1161/01.CIR.0000132503.19410.6B]. [PMID: 15184295].
[37]
Xun P, Qin B, Song Y, et al. Fish consumption and risk of stroke and its subtypes: Accumulative evidence from a meta-analysis of prospective cohort studies. Eur J Clin Nutr 2012; 66(11): 1199-207. [http://dx.doi.org/10.1038/ejcn.2012.133]. [PMID: 23031847].
[38]
Alexander DD, Miller PE, Van Elswyk ME, Kuratko CN, Bylsma LC. Eicosapentaenoic and docosahexaenoic long-chain omega-3 fatty acids and coronary heart disease risk. Mayo Clin Proc 2017; 92(1): 15-29. [http://dx.doi.org/10.1016/j.mayocp.2016.10.018]. [PMID: 28062061].
[39]
Maki KC, Palacios OM, Bell M, Toth PP. Use of supplemental long-chain omega-3 fatty acids and risk for cardiac death: An updated meta-analysis and review of research gaps. J Clin Lipidol 2017; 11(5): 1152-1160.e2. [http://dx.doi.org/10.1016/j.jacl.2017.07.010]. [PMID: 28818347].
[40]
Djoussé L, Akinkuolie AO, Wu JH, Ding EL, Gaziano JM. Fish consumption, omega-3 fatty acids and risk of heart failure: A meta-analysis. Clin Nutr 2012; 31(6): 846-53. [http://dx.doi.org/10.1016/j.clnu.2012.05.010]. [PMID: 22682084].
[41]
Mozaffarian D, Bryson CL, Lemaitre RN, Burke GL, Siscovick DS. Fish intake and risk of incident heart failure. J Am Coll Cardiol 2005; 45(12): 2015-21. [http://dx.doi.org/10.1016/j.jacc.2005.03.038]. [PMID: 15963403].
[42]
Weisman D, Beinart R, Erez A, et al. Effect of supplemented intake of omega-3 fatty acids on arrhythmias in patients with ICD: Fish oil therapy may reduce ventricular arrhythmia. J Interv Card Electrophysiol 2017; 49(3): 255-61. [http://dx.doi.org/10.1007/s10840-017-0267-1]. [PMID: 28664342].
[43]
Nodari S, Metra M, Milesi G, et al. The role of n-3 PUFAs in preventing the arrhythmic risk in patients with idiopathic dilated cardiomyopathy. Cardiovasc Drugs Ther 2009; 23(1): 5-15. [http://dx.doi.org/10.1007/s10557-008-6142-7]. [PMID: 18982439].
[44]
Hidayat K, Yang J, Zhang Z, et al. Effect of omega-3 long-chain polyunsaturated fatty acid supplementation on heart rate: A meta-analysis of randomized controlled trials. Eur J Clin Nutr 2018; 72(6): 805-17. [http://dx.doi.org/10.1038/s41430-017-0052-3]. [PMID: 29284786].
[45]
Tribulova N, Szeiffova Bacova B, Egan Benova T, Knezl V, Barancik M, Slezak J. Omega-3 index and anti-arrhythmic potential of omega-3 PUFAs. Nutrients 2017; 9(11): 1191. [http://dx.doi.org/10.3390/nu9111191]. [PMID: 29084142].
[46]
Burke MF, Burke FM, Soffer DE. Review of cardiometabolic effects of prescription omega-3 fatty acids. Curr Atheroscler Rep 2017; 19(12): 60. [http://dx.doi.org/10.1007/s11883-017-0700-z]. [PMID: 29116404].
[47]
Zibaeenezhad MJ, Ghavipisheh M, Attar A, Aslani A. Comparison of the effect of omega-3 supplements and fresh fish on lipid profile: A randomized, open-labeled trial. Nutr Diabetes 2017; 7(12): 1. [http://dx.doi.org/10.1038/s41387-017-0007-8]. [PMID: 29259181].
[48]
Backes J, Anzalone D, Hilleman D, Catini J. The clinical relevance of omega-3 fatty acids in the management of hypertriglyceridemia. Lipids Health Dis 2016; 15(1): 118. [http://dx.doi.org/10.1186/s12944-016-0286-4]. [PMID: 27444154].
[49]
Jacobson TA, Glickstein SB, Rowe JD, Soni PN. Effects of eicosapentaenoic acid and docosahexaenoic acid on low-density lipoprotein cholesterol and other lipids: A review. J Clin Lipidol 2012; 6(1): 5-18. [http://dx.doi.org/10.1016/j.jacl.2011.10.018]. [PMID: 22264569].
[50]
Fialkow J. Omega-3 fatty acid formulations in cardiovascular disease: Dietary supplements are not substitutes for prescription products. Am J Cardiovasc Drugs 2016; 16(4): 229-39. [http://dx.doi.org/10.1007/s40256-016-0170-7]. [PMID: 27138439].
[51]
Nastel P, Shige H, Pomeroy S, Cehun M, Abbey M, Raederstorff D. The n-3 fatty acids eicosapentaenoic acid and docosahexaenoic acid increase systemic arterial compliance in humans. Am J Clin Nutr 2002; 76: 326-30.
[52]
Yamano T, Kubo T, Shiono Y, et al. Impact of eicosapentaenoic acid treatment on the fibrous cap thickness in patients with coronary atherosclerotic plaque: An optical coherence tomography study. J Atheroscler Thromb 2015; 22(1): 52-61. [http://dx.doi.org/10.5551/jat.25593]. [PMID: 25132379].
[53]
Vanschoonbeek K, Feijge MAH, Paquay M, et al. Variable hypocoagulant effect of fish oil intake in humans: Modulation of fibrinogen level and thrombin generation. Arterioscler Thromb Vasc Biol 2004; 24(9): 1734-40. [http://dx.doi.org/10.1161/01.ATV.0000137119.28893.0b]. [PMID: 15217806].
[54]
Miller PE, Van Elswyk M, Alexander DD. Long-chain omega-3 fatty acids eicosapentaenoic acid and docosahexaenoic acid and blood pressure: A meta-analysis of randomized controlled trials. Am J Hypertens 2014; 27(7): 885-96. [http://dx.doi.org/10.1093/ajh/hpu024]. [PMID: 24610882].
[55]
Chatterjee S, Khunti K, Davies MJ. Type 2 diabetes. Lancet 2017; 389(10085): 2239-51. [http://dx.doi.org/10.1016/S0140-6736(17)30058-2]. [PMID: 28190580].
[56]
De Fronzo RA, Ferrannini E, Groop L, et al. Type 2 diabetes mellitus. Nat Rev Dis Primers 2015; 1: 15019.
[57]
Itsiopoulos C, Marx W, Mayr HL, et al. The role of omega-3 polyunsaturated fatty acid supplementation in the management of type 2 diabetes mellitus: A narrative review. J Nutr Intermed Metab 2018; 14: 42-51. [http://dx.doi.org/10.1016/j.jnim.2018.02.002].
[58]
Coelho OGL, da Silva BP, Rocha DMUP, Lopes LL, Alfenas RCG. Polyunsaturated fatty acids and type 2 diabetes: Impact on the glycemic control mechanism. Crit Rev Food Sci Nutr 2017; 57(17): 3614-9. [http://dx.doi.org/10.1080/10408398.2015.1130016]. [PMID: 26853892].
[59]
Lalia AZ, Lanza IR. Insulin-Sensitizing Effects of Omega-3 Fatty Acids: Lost in Translation? Nutrients 2016; 8(6): 329-53. [http://dx.doi.org/10.3390/nu8060329]. [PMID: 27258299].
[60]
Ebbesson SO, Risica PM, Ebbesson LO, Kennish JM, Tejero ME. Omega-3 fatty acids improve glucose tolerance and components of the metabolic syndrome in Alaskan Eskimos: The Alaska Siberia project. Int J Circumpolar Health 2005; 64(4): 396-408. [http://dx.doi.org/10.3402/ijch.v64i4.18016]. [PMID: 16277123].
[61]
Rasic-Milutinovic Z, Perunicic G, Pljesa S, et al. Effects of N-3 PUFAs supplementation on insulin resistance and inflammatory biomarkers in hemodialysis patients. Ren Fail 2007; 29(3): 321-9. [http://dx.doi.org/10.1080/08860220601184092]. [PMID: 17497447].
[62]
Farsi PF, Djazayery A, Eshraghian MR, et al. Effects of supplementation with omega-3 on insulin sensitivity and non-esterified free fatty acid (NEFA) in type 2 diabetic patients. Arq Bras Endocrinol Metabol 2014; 58(4): 335-40. [http://dx.doi.org/10.1590/0004-2730000002861]. [PMID: 24936727].
[63]
Lepretti M, Martucciello S, Burgos Aceves MA, Putti R, Lionetti L. Omega-3 Fatty Acids and Insulin Resistance: Focus on the Regulation of Mitochondria and Endoplasmic Reticulum Stress. Nutrients 2018; 10(3): 349-59. [http://dx.doi.org/10.3390/nu10030350]. [PMID: 29538286].
[64]
Sala-Vila A, Díaz-López A, Valls-Pedret C, et al. Dietary Marine ω-3 Fatty Acids and Incident Sight-Threatening Retinopathy in Middle-Aged and Older Individuals With Type 2 Diabetes: Prospective Investigation From the PREDIMED Trial. JAMA Ophthalmol 2016; 134(10): 1142-9. [http://dx.doi.org/10.1001/jamaophthalmol.2016.2906]. [PMID: 27541690].
[65]
Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis andmanagement of the metabolic syndrome: An American Heart Association/NationalHeart, Lung, and Blood Institute scientific statement. Circulation 2005; 112(17): 2735-52. [http://dx.doi.org/10.1161/CIRCULATIONAHA.105.169404]. [PMID: 16157765].
[66]
Wilson PWF, D’Agostino RB, Parise H, Sullivan L, Meigs JB. Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation 2005; 112(20): 3066-72. [http://dx.doi.org/10.1161/CIRCULATIONAHA.105.539528]. [PMID: 16275870].
[67]
Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract 2014; 2014943162 [http://dx.doi.org/10.1155/2014/943162]. [PMID: 24711954].
[68]
Torres-Fuentes C, Schellekens H, Dinan TG, Cryan JF. A natural solution for obesity: Bioactives for the prevention and treatment of weight gain. A review. Nutr Neurosci 2015; 18(2): 49-65. [http://dx.doi.org/10.1179/1476830513Y.0000000099]. [PMID: 24621068].
[69]
Gao H, Geng T, Huang T, Zhao Q. Fish oil supplementation and insulin sensitivity: A systematic review and meta-analysis. Lipids Health Dis 2017; 16(1): 131. [http://dx.doi.org/10.1186/s12944-017-0528-0]. [PMID: 28673352].
[70]
Lorente-Cebrián S, Costa AGV, Navas-Carretero S, Zabala M, Martínez JA, Moreno-Aliaga MJ. Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: A review of the evidence. J Physiol Biochem 2013; 69(3): 633-51. [http://dx.doi.org/10.1007/s13105-013-0265-4]. [PMID: 23794360].
[71]
Torres DM, Williams CD, Harrison SA. Features, diagnosis, and treatment of nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2012; 10(8): 837-58. [http://dx.doi.org/10.1016/j.cgh.2012.03.011]. [PMID: 22446927].
[72]
Gupta V, Mah XJ, Garcia MC, Antonypillai C, van der Poorten D. Oily fish, coffee and walnuts: Dietary treatment for nonalcoholic fatty liver disease. World J Gastroenterol 2015; 21(37): 10621-35. [http://dx.doi.org/10.3748/wjg.v21.i37.10621]. [PMID: 26457022].
[73]
Yu L, Yuan M, Wang L. The effect of omega-3 unsaturated fatty acids on non-alcoholic fatty liver disease: A systematic review and meta-analysis of RCTs. Pak J Med Sci 2017; 33(4): 1022-8. [http://dx.doi.org/10.12669/pjms.334.12315]. [PMID: 29067086].
[74]
Yan J-H, Guan B-J, Gao H-Y, Peng XE. Omega-3 polyunsaturated fatty acid supplementation and non-alcoholic fatty liver disease: A meta-analysis of randomized controlled trials. Medicine (Baltimore) 2018; 97(37)E12271 [http://dx.doi.org/10.1097/MD.0000000000012271]. [PMID: 30212963].
[75]
Musa-Veloso K, Venditti C, Lee HY, et al. Systematic review and meta-analysis of controlled intervention studies on the effectiveness of long-chain omega-3 fatty acids in patients with nonalcoholic fatty liver disease. Nutr Rev 2018; 76(8): 581-602. [http://dx.doi.org/10.1093/nutrit/nuy022]. [PMID: 29917092].
[76]
World Health Organization. [updated 2018; cited 2018 Dec 6]. Availbale from: www.who.int/cancer/en/.
[77]
Bartsch H, Nair J, Owen RW. Dietary polyunsaturated fatty acids and cancers of the breast and colorectum: Emerging evidence for their role as risk modifiers. Carcinogenesis 1999; 20(12): 2209-18. [http://dx.doi.org/10.1093/carcin/20.12.2209]. [PMID: 10590211].
[78]
Abel S, Riedel S, Gelderblom WCA. Dietary PUFA and cancer. Proc Nutr Soc 2014; 73(3): 361-7. [http://dx.doi.org/10.1017/S0029665114000585]. [PMID: 24850051].
[79]
Zhang Y, Zhuang P, He W, et al. Association of fish and long-chain omega-3 fatty acids intakes with total and cause-specific mortality: Prospective analysis of 421 309 individuals. J Intern Med 2018; 284(4): 399-417. [http://dx.doi.org/10.1111/joim.12786]. [PMID: 30019399].
[80]
Li J, Li K, Gao J, et al. Maternal exposure to an n-3 polyunsaturated fatty acid diet decreases mammary cancer risk of female offspring in adulthood. Food Funct 2018; 9(11): 5768-77. [http://dx.doi.org/10.1039/C8FO01006D]. [PMID: 30327803].
[81]
Mikirova N, Riordan HD, Jackson JA, Wong K, Miranda-Massari JR, Gonzalez MJ. Erythrocyte membrane fatty acid composition in cancer patients. P R Health Sci J 2004; 23(2): 107-13. [PMID: 15377058].
[82]
Coviello G, Tutino V, Notarnicola M, Caruso MG. Erythrocyte membrane fatty acids profile in colorectal cancer patients: A preliminary study. Anticancer Res 2014; 34(9): 4775-9. [PMID: 25202057].
[83]
Camargo CQ, Mocellin MC, Brunetta HS, et al. Fish oil decreases the severity of treatment-related adverse events in gastrointestinal cancer patients undergoing chemotherapy: A randomized, placebo-controlled, triple-blind clinical trial. Clin Nutr ESPEN 2019; 31: 61-70. [http://dx.doi.org/10.1016/j.clnesp.2019.02.015]. [PMID: 31060836].
[84]
Lovegrove C, Ahmed K, Challacombe B, Khan MS, Popert R, Dasgupta P. Systematic review of prostate cancer risk and association with consumption of fish and fish-oils: Analysis of 495,321 participants. Int J Clin Pract 2015; 69(1): 87-105. [http://dx.doi.org/10.1111/ijcp.12514]. [PMID: 25495842].
[85]
Luu HN, Cai H, Murff HJ, et al. A prospective study of dietary polyunsaturated fatty acids intake and lung cancer risk. Int J Cancer 2018; 143(9): 2225-37. [http://dx.doi.org/10.1002/ijc.31608]. [PMID: 29905376].
[86]
Volpato M, Hull MA. Omega-3 polyunsaturated fatty acids as adjuvant therapy of colorectal cancer. Cancer Metastasis Rev 2018; 37(2-3): 545-55. [http://dx.doi.org/10.1007/s10555-018-9744-y]. [PMID: 29971573].
[87]
Song M, Zhang X, Meyerhardt JA, et al. Marine ω-3 polyunsaturated fatty acid intake and survival after colorectal cancer diagnosis. Gut 2017; 66(10): 1790-6. [http://dx.doi.org/10.1136/gutjnl-2016-311990]. [PMID: 27436272].
[88]
Cockbain AJ, Toogood GJ, Hull MA. ω-3 polyunsaturated fatty acids for the treatment and prevention of colorectal cancer. Gut 2012; 61(1): 135-49. [http://dx.doi.org/10.1136/gut.2010.233718]. [PMID: 21490374].
[89]
Bougnoux P, Hajjaji N, Ferrasson MN, Giraudeau B, Couet C, Le Floch O. Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: A phase II trial. Br J Cancer 2009; 101(12): 1978-85. [http://dx.doi.org/10.1038/sj.bjc.6605441]. [PMID: 19920822].
[90]
Murphy RA, Mourtzakis M, Chu QS, Baracos VE, Reiman T, Mazurak VC. Supplementation with fish oil increases first-line chemotherapy efficacy in patients with advanced nonsmall cell lung cancer. Cancer 2011; 117(16): 3774-80. [http://dx.doi.org/10.1002/cncr.25933]. [PMID: 21328326].
[91]
Ma YJ, Yu J, Xiao J, Cao BW. The consumption of ω-3 polyunsaturated fatty acids improves clinical outcomes and prognosis in pancreatic cancer patients: A systematic evaluation. Nutr Cancer 2015; 67(1): 112-8. [http://dx.doi.org/10.1080/01635581.2015.976315]. [PMID: 25425246].
[92]
Fuentes NR, Kim E, Fan YY, Chapkin RS. Omega-3 fatty acids, membrane remodeling and cancer prevention. Mol Aspects Med 2018; 64: 79-91. [http://dx.doi.org/10.1016/j.mam.2018.04.001]. [PMID: 29627343].
[93]
Miccadei S, Masella R, Mileo AM, Gessani S. ω3 Polyunsaturated Fatty Acids as Immunomodulators in Colorectal Cancer: New Potential Role in Adjuvant Therapies. Front Immunol 2016; 7: 486. [http://dx.doi.org/10.3389/fimmu.2016.00486]. [PMID: 27895640].
[94]
Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J 2017; 474(11): 1823-36. [http://dx.doi.org/10.1042/BCJ20160510]. [PMID: 28512250].
[95]
Gilbert JA, Blaser MJ, Caporaso JG, Jansson JK, Lynch SV, Knight R. Current understanding of the human microbiome. Nat Med 2018; 24(4): 392-400. [http://dx.doi.org/10.1038/nm.4517]. [PMID: 29634682].
[96]
Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis 2015; 26: 26191. [PMID: 25651997].
[97]
Flint HJ, Duncan SH, Louis P. The impact of nutrition on intestinal bacterial communities. Curr Opin Microbiol 2017; 38: 59-65. [http://dx.doi.org/10.1016/j.mib.2017.04.005]. [PMID: 28486162].
[98]
Costantini L, Molinari R, Farinon B, Merendino N. Impact of Omega-3 Fatty Acids on the Gut Microbiota. Int J Mol Sci 2017; 18(12): 2645-63. [http://dx.doi.org/10.3390/ijms18122645]. [PMID: 29215589].
[99]
Menni C, Zierer J, Pallister T, et al. Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women. Sci Rep 2017; 7(1): 11079. [http://dx.doi.org/10.1038/s41598-017-10382-2]. [PMID: 28894110].
[100]
Cândido FG, Valente FX, Grześkowiak LM, Moreira APB, Rocha DMUP, Alfenas RCG. Impact of dietary fat on gut microbiota and low-grade systemic inflammation: Mechanisms and clinical implications on obesity. Int J Food Sci Nutr 2018; 69(2): 125-43. [http://dx.doi.org/10.1080/09637486.2017.1343286]. [PMID: 28675945].
[101]
Watson H, Mitra S, Croden FC, et al. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut 2018; 67(11): 1974-83. [http://dx.doi.org/10.1136/gutjnl-2017-314968]. [PMID: 28951525].
[102]
Global Iniative For Asthma (GINA). Pocket Guide for Astma Management and Prevention (for adults and Children Older than 5 Years). A Pocket Guide for Health Professionals. [updated 2018; cited 2018 Dec 1]. Available from: Https://ginasthma.org/2018-pocket-guide-for-asthma-management-and-prevention/.
[103]
Hall S, Agrawal DK. Key mediators in the immunopathogenesis of allergic asthma. Int Immunopharmacol 2014; 23(1): 316-29. [http://dx.doi.org/10.1016/j.intimp.2014.05.034]. [PMID: 24933589].
[104]
Miyata J, Arita M. Role of omega-3 fatty acids and their metabolites in asthma and allergic diseases. Allergol Int 2015; 64(1): 27-34. [http://dx.doi.org/10.1016/j.alit.2014.08.003]. [PMID: 25572556].
[105]
Olsen SF, Østerdal ML, Salvig JD, et al. Fish oil intake compared with olive oil intake in late pregnancy and asthma in the offspring: 16 y of registry-based follow-up from a randomized controlled trial. Am J Clin Nutr 2008; 88(1): 167-75. [http://dx.doi.org/10.1093/ajcn/88.1.167]. [PMID: 18614738].
[106]
Bisgaard H, Stokholm J, Chawes BL, et al. Fish oil-derived fatty acids in pregnancy and wheeze and asthma in offspring. N Engl J Med 2016; 375(26): 2530-9. [http://dx.doi.org/10.1056/NEJMoa1503734]. [PMID: 28029926].
[107]
Damsgaard CT, Lauritzen L, Kjaer TM, et al. Fish oil supplementation modulates immune function in healthy infants. J Nutr 2007; 137(4): 1031-6. [http://dx.doi.org/10.1093/jn/137.4.1031]. [PMID: 17374672].
[108]
Best KP, Gold M, Kennedy D, Martin J, Makrides M. Omega-3 long-chain PUFA intake during pregnancy and allergic disease outcomes in the offspring: A systematic review and meta-analysis of observational studies and randomized controlled trials. Am J Clin Nutr 2016; 103(1): 128-43. [http://dx.doi.org/10.3945/ajcn.115.111104]. [PMID: 26675770].
[109]
Abdulrazaq M, Innes JK, Calder PC. Effect of ω-3 polyunsaturated fatty acids on arthritic pain: A systematic review. Nutrition 2017; 39-40: 57-66. [http://dx.doi.org/10.1016/j.nut.2016.12.003]. [PMID: 28606571].
[110]
Musumeci G. The effect of mechanical loading on articular cartilage. J Funct Morphol Kinesiol 2016; 1: 154-61. [http://dx.doi.org/10.3390/jfmk1020154].
[111]
Kaneko Y, Takeuchi T. A paradigm shift in rheumatoid arthritis over the past decade. Intern Med 2014; 53(17): 1895-903. [http://dx.doi.org/10.2169/internalmedicine.53.2834]. [PMID: 25175120].
[112]
Reynard LN, Loughlin J. Genetics and epigenetics of osteoarthritis. Maturitas 2012; 71(3): 200-4. [http://dx.doi.org/10.1016/j.maturitas.2011.12.001]. [PMID: 22209350].
[113]
Brandt KD, Dieppe P, Radin EL. Etiopathogenesis of osteoarthritis. Rheum Dis Clin North Am 2008; 34(3): 531-59. [http://dx.doi.org/10.1016/j.rdc.2008.05.011]. [PMID: 18687271].
[114]
Woo SJ, Lim K, Park SY, et al. Endogenous conversion of n-6 to n-3 polyunsaturated fatty acids attenuates K/BxN serum-transfer arthritis in fat-1 mice. J Nutr Biochem 2015; 26(7): 713-20. [http://dx.doi.org/10.1016/j.jnutbio.2015.01.011]. [PMID: 25910895].
[115]
Bannenberg G, Arita M, Serhan CN. Endogenous receptor agonists: Resolving inflammation. ScientificWorldJournal 2007; 7: 1440-62. [http://dx.doi.org/10.1100/tsw.2007.188]. [PMID: 17767360].
[116]
Landewé R, van der Heijde D, van der Linden S, Boers M. Twenty-eight-joint counts invalidate the DAS28 remission definition owing to the omission of the lower extremity joints: A comparison with the original DAS remission. Ann Rheum Dis 2006; 65(5): 637-41. [http://dx.doi.org/10.1136/ard.2005.039859]. [PMID: 16219709].
[117]
Rajaei E, Mowla K, Ghorbani A, Bahadoram S, Bahadoram M, Dargahi-Malamir M. The Effect of Omega-3 Fatty Acids in Patients With Active Rheumatoid Arthritis Receiving DMARDs Therapy: Double-Blind Randomized Controlled Trial. Glob J Health Sci 2015; 8(7): 18-25. [http://dx.doi.org/10.5539/gjhs.v8n7p18]. [PMID: 26925896].
[118]
Veselinovic M, Vasiljevic D, Vucic V, et al. Clinical Benefits of n-3 PUFA and ɤ-Linolenic Acid in Patients with Rheumatoid Arthritis Nutrients 2017; 25. 9(4 )
[119]
Woodman RJ, Baghdadi LR, Shanahan EM, de Silva I, Hodgson JM, Mangoni AA. Diets high in n-3 fatty acids are associated with lower arterial stiffness in patients with rheumatoid arthritis: A latent profile analysis. Br J Nutr 2019; 121(2): 182-94. [http://dx.doi.org/10.1017/S0007114518003100]. [PMID: 30430957].
[120]
Gioxari A, Kaliora AC, Marantidou F, Panagiotakos DP. Intake of ω-3 polyunsaturated fatty acids in patients with rheumatoid arthritis: A systematic review and meta-analysis. Nutrition 2018; 45: 114-124.e4. [http://dx.doi.org/10.1016/j.nut.2017.06.023]. [PMID: 28965775].
[121]
Di Giuseppe D, Wallin A, Bottai M, Askling J, Wolk A. Long-term intake of dietary long-chain n-3 polyunsaturated fatty acids and risk of rheumatoid arthritis: A prospective cohort study of women. Ann Rheum Dis 2014; 73(11): 1949-53. [http://dx.doi.org/10.1136/annrheumdis-2013-203338]. [PMID: 23940215].
[122]
Philippou E, Nikiphorou E. Are we really what we eat? Nutrition and its role in the onset of rheumatoid arthritis. Autoimmun Rev 2018; 17(11): 1074-7. [http://dx.doi.org/10.1016/j.autrev.2018.05.009]. [PMID: 30213695].
[123]
Parr CL, Magnus MC, Karlstad Ø, et al. Vitamin A and D intake in pregnancy, infant supplementation, and asthma development: The Norwegian Mother and Child Cohort Am J Clin Nutrn 107(5): 789-98.
[124]
Bastie JN, Balitrand N, Guidez F, et al. 1 alpha,25-dihydroxyvitamin D3 transrepresses retinoic acid transcriptional activity via vitamin D receptor in myeloid cells. Mol Endocrinol 2004; 18(11): 2685-99. [http://dx.doi.org/10.1210/me.2003-0412]. [PMID: 15284334].
[125]
Roy J, Oger C, Thireau J, et al. Nonenzymatic lipid mediators, neuroprostanes, exert the antiarrhythmic properties of docosahexaenoic acid. Free Radic Biol Med 2015; 86: 269-78. [http://dx.doi.org/10.1016/j.freeradbiomed.2015.04.014]. [PMID: 25911196].
[126]
He K, Rimm EB, Merchant A, et al. Fish consumption and risk of stroke in men. JAMA 2002; 288(24): 3130-6. [http://dx.doi.org/10.1001/jama.288.24.3130]. [PMID: 12495393].
[127]
Driss F, Vericel E, Lagarde M, Dechavanne M, Darcet P. Inhibition of platelet aggregation and thromboxane synthesis after intake of small amount of icosapentaenoic acid. Thromb Res 1984; 36(5): 389-96. [http://dx.doi.org/10.1016/0049-3848(84)90295-0]. [PMID: 6098051].
[128]
Folsom AR, Demissie Z. Fish intake, marine omega-3 fatty acids, and mortality in a cohort of postmenopausal women. Am J Epidemiol 2004; 160(10): 1005-10. [http://dx.doi.org/10.1093/aje/kwh307]. [PMID: 15522857].
[129]
Järvinen R, Knekt P, Rissanen H, Reunanen A. Intake of fish and long-chain n-3 fatty acids and the risk of coronary heart mortality in men and women. Br J Nutr 2006; 95(4): 824-9. [http://dx.doi.org/10.1079/BJN20051687]. [PMID: 16571163].
[130]
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(16): 2024-30. [http://dx.doi.org/10.1093/eurheartj/ehn294]. [PMID: 18641046].
[131]
de Goede J, Geleijnse JM, Boer JM, Kromhout D, Verschuren WM. Marine (n-3) fatty acids, fish consumption, and the 10-year risk of fatal and nonfatal coronary heart disease in a large population of Dutch adults with low fish intake. J Nutr 2010; 140(5): 1023-8. [http://dx.doi.org/10.3945/jn.109.119271]. [PMID: 20335635].
[132]
Rhee JJ, Kim E, Buring JE, Kurth T. Fish consumption, omega-3 fatty acids, and risk of cardiovascular disease. Am J Prev Med 2017; 52(1): 10-9. [http://dx.doi.org/10.1016/j.amepre.2016.07.020]. [PMID: 27646568].
[133]
Harris WS. Are n-3 fatty acids still cardioprotective? Curr Opin Clin Nutr Metab Care 2013; 16(2): 141-9. [http://dx.doi.org/10.1097/MCO.0b013e32835bf380]. [PMID: 23196817].
[134]
Rauch B, Schiele R, Schneider S, et al. OMEGA, a randomized, placebo-controlled trial to test the effect of highly purified omega-3 fatty acids on top of modern guideline-adjusted therapy after myocardial infarction. Circulation 2010; 122(21): 2152-9. [http://dx.doi.org/10.1161/CIRCULATIONAHA.110.948562]. [PMID: 21060071].
[135]
Bosch J, Gerstein HC, Dagenais GR, et al. n-3 fatty acids and cardiovascular outcomes in patients with dysglycemia. N Engl J Med 2012; 367(4): 309-18. [http://dx.doi.org/10.1056/NEJMoa1203859]. [PMID: 22686415].
[136]
Aung T, Halsey J, Kromhout D, et al. Associations of Omega-3 Fatty Acid Supplement Use With Cardiovascular Disease Risks: Meta-analysis of 10 Trials Involving 77 917 Individuals. JAMA Cardiol 2018; 3(3): 225-34. [http://dx.doi.org/10.1001/jamacardio.2017.5205]. [PMID: 29387889].
[137]
Chen C, Yang Y, Yu X, Hu S, Shao S. Association between omega-3 fatty acids consumption and the risk of type 2 diabetes: A meta-analysis of cohort studies. J Diabetes Investig 2017; 8(4): 480-8. [http://dx.doi.org/10.1111/jdi.12614]. [PMID: 28032469].
[138]
Daenen LG, Cirkel GA, Houthuijzen JM, et al. Increased plasma levels of chemoresistance-inducing fatty acid 16:4(n-3) after consumption of fish and fish oil. JAMA Oncol 2015; 1(3): 350-8. [http://dx.doi.org/10.1001/jamaoncol.2015.0388]. [PMID: 26181186].
[139]
Weylandt KH, Serini S, Chen YQ, et al. Omega-3 Polyunsaturated Fatty Acids: The Way Forward in Times of Mixed Evidence. BioMed Res Int 2015; 2015143109 [http://dx.doi.org/10.1155/2015/143109]. [PMID: 26301240].
[140]
Chua ME, Sio MC, Sorongon MC, Dy JS. Relationship of dietary intake of omega-3 and omega-6 Fatty acids with risk of prostate cancer development: A meta-analysis of prospective studies and review of literature. Prostate Cancer 2012; 2012826254 [http://dx.doi.org/10.1155/2012/826254]. [PMID: 23193480].
[141]
Haas-Haseman M. Weighing the Benefits of Fish Oil for Patients With Prostate Cancer: A Subcohort Review From the SELECT Trial. J Adv Pract Oncol 2015; 6(4): 376-8. [PMID: 26705498].
[142]
Stark KD, Van Elswyk ME, Higgins MR, Weatherford CA, Salem N Jr. Global survey of the omega-3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the blood stream of healthy adults. Prog Lipid Res 2016; 63: 132-52. [http://dx.doi.org/10.1016/j.plipres.2016.05.001]. [PMID: 27216485].
[143]
Nakamura Y, Ueshima H, Okamura T, et al. Association between fish consumption and all-cause and cause-specific mortality in Japan: NIPPON DATA80, 1980-99. Am J Med 2005; 118(3): 239-45. [http://dx.doi.org/10.1016/j.amjmed.2004.12.016]. [PMID: 15745721].
[144]
von Schacky C. Omega-3 Index and sudden cardiac death. Nutrients 2010; 2(3): 375-88. [http://dx.doi.org/10.3390/nu2030375]. [PMID: 22254028].
[145]
Elvevoll EO, Osterud B. Impact of processing on nutritional quality of marine food items. Forum Nutr 2003; 56: 337-40. [PMID: 15806925].
[146]
Clayton PR, Ladi S. From alga to omega; have we reached peak (fish) oil? J R Soc Med 2015; 108(9): 351-7. [http://dx.doi.org/10.1177/0141076815599673]. [PMID: 26359136].
[147]
Harris WS, Pottala JV, Sands SA, Jones PG. Comparison of the effects of fish and fish-oil capsules on the n 3 fatty acid content of blood cells and plasma phospholipids. Am J Clin Nutr 2007; 86(6): 1621-5. [http://dx.doi.org/10.1093/ajcn/86.6.1621]. [PMID: 18065578].


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 25
ISSUE: 15
Year: 2019
Page: [1747 - 1759]
Pages: 13
DOI: 10.2174/1381612825666190705185800
Price: $58

Article Metrics

PDF: 12
HTML: 3
EPUB: 2
PRC: 2