1,874
Views
34
CrossRef citations to date
0
Altmetric
Original Article

Effect of omega-3 supplements on plasma apolipoprotein C-III concentrations: a systematic review and meta-analysis of randomized controlled trials

ORCID Icon, , , ORCID Icon, , & ORCID Icon show all
Pages 565-575 | Received 27 Jun 2018, Accepted 03 Aug 2018, Published online: 29 Sep 2018

References

  • Fidalgo Rodríguez JL, Dynarowicz-Latka P, Miñones Conde J. Structure of unsaturated fatty acids in 2D system. Colloids Surf B Biointerf. 2017;158:634–642.
  • Colussi G, Catena C, Novello M, et al. Impact of omega-3 polyunsaturated fatty acids on vascular function and blood pressure: relevance for cardiovascular outcomes. Nutr Metab Cardiovasc Dis. 2017;27:191–200.
  • Dasilva G, Pazos M, García-Egido E, et al. A lipidomic study on the regulation of inflammation and oxidative stress targeted by marine ω-3 PUFA and polyphenols in high-fat high-sucrose diets. J Nutr Biochem. 2017;43:53–67.
  • Catapano AL, Graham I, De Backer G, et al. 2016 ESC/EAS Guidelines for the management of dyslipidaemias: the task force for the management of dyslipidaemias of the European Society of Cardiology (ESC) and European Atherosclerosis Society (EAS) developed with the special contribution of the European Assocciation for Cardiovascular Prevention & Rehabilitation (EACPR). Eur Heart J. 2016;37:2999–3058.
  • Davidson MH. Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol. 2006;98:27i–33i.
  • Marchioli R, Barzi F, Bomba E, et al. Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation. 2002;105:1897–1903.
  • Mozaffarian D, Psaty BM, Rimm EB, et al. Fish intake and risk of incident atrial fibrillation. Circulation. 2004;110:368–373.
  • Cunha DNQ, Hamlin RL, Billman GE, et al. N-3 (omega-3) polyunsaturated fatty acids prevent acute atrial electrophysiological remodeling. Brit J Pharmacol. 2007;150:281–285.
  • Leaf A. Omega-3 fatty acids and prevention of arrhythmias. Curr Opin Lipidol. 2007;18:31–34.
  • Wong S, Nestel PJ. Eicosapentaenoic acid inhibits the secretion of triacylglycerol and of apoprotein B and the binding of LDL in Hep G2 cells. Atherosclerosis. 1987;64:139–146.
  • Wang H, Chen X, Fisher EA. N-3 fatty acids stimulate intracellular degradation of apoprotein B in rat hepatocytes. J Clin Invest. 1993;91:1380–1389.
  • Park Y, Harris WS. Omega-3 fatty acid supplementation accelerates chylomicron triglyceride clearance. J Lipid Res. 2003;44:455–463.
  • Chan DC, Watts GF, Nguyen MN, et al. Factorial study of the effect of n-3 fatty acid supplementation and atorvastatin on the kinetics of HDL apolipoproteins A-I and A-II in men with abdominal obesity. Am J Clin Nutr. 2006;84:37–43.
  • Reiner Ž. Are elevated serum triglycerides really a risk factor for coronary artery disease? Cardiology. 2015;131:225–227.
  • Reiner Ž. Hypertriglyceridaemia and risk of coronary artery disease. Nat Rev Cardiol. 2017;14:401–411.
  • Sacks FM, Alaupovic P, Moye LA, et al. VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation. 2000;102:1886–1892.
  • Chivot L, Mainard F, Bigot E, et al. Logistic discriminant analysis of lipids and apolipoproteins in a population of coronary bypass patients and the significance of apolipoproteins C-III and E. Atherosclerosis. 1990;82:205–211.
  • Luc G, Fievet C, Arveiler D, et al. Apolipoproteins C-III and E in apoB- and non-apoB-containing lipoproteins in two populations at contrasting risk for myocardial infarction: the ECTIM study. Etude Cas Témoins sur 'Infarctus du Myocarde. J Lipid Res. 1996;37:508–517.
  • Onat A, Hergenç G, Sansoy V, et al. Apolipoprotein C-III, a strong discriminant of coronary risk in men and a determinant of the metabolic syndrome in both genders. Atherosclerosis. 2003;168:81–89.
  • Pollin T, Damcott CM, Shen H, et al. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science. 2008;322:1702–1705.
  • Jorgensen AB, Frikke-Schmidt R, Nordestgaard BG, et al. Loss-of-function mutations in APOC3 and risk of ischemic vascular disease. N Engl J Med. 2014;371:32–41.
  • TG and HDL Working Group of the Exome Sequencing Project, National Heart, Lung, and Blood Institute, Crosby J, Peloso GM, et al. Loss-of-function mutations in APOC3, triglycerides, and coronary disease. N Engl J Med. 2014;371:22–31.
  • Davidson MH, Maki KC, Bays H, et al. Effects of prescription omega-3-acid ethyl esters on lipoprotein particle concentrations, apolipoproteins AI and CIII, and lipoprotein-associated phospholipase A2 mass in statin-treated subjects with hypertriglyceridemia. J Clin Lipidol. 2009;3:332–340.
  • Maki KC, Bays HE, Dicklin MR, et al. Effects of prescription omega-3-acid ethyl esters, coadministered with atorvastatin, on circulating levels of lipoprotein particles, apolipoprotein CIII, and lipoprotein-associated phospholipase A2 mass in men and women with mixed dyslipidemia. J Clin Lipidol. 2011;5:483–492.
  • Dunbar RL, Nicholls SJ, Maki KC, et al. Effects of omega-3 carboxylic acids on lipoprotein particles and other cardiovascular risk markers in high-risk statin-treated patients with residual hypertriglyceridemia: a randomized, controlled, double-blind trial. Lipids Health Dis. 2015;14:98.
  • Balk EM, Lichtenstein AH, Chung M, et al. Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review. Atherosclerosis. 2006;189:19–30.
  • Ballantyne CM, Bays HE, Kastelein JJ, et al. Efficacy and safety of eicosapentaenoic acid ethyl ester (AMR101) therapy in statin-treated patients with persistent high triglycerides (from the ANCHOR study). Am J Cardiol. 2012;110:984–992.
  • Bays HE, Ballantyne CM, Kastelein JJ, et al. Eicosapentaenoic acid ethyl ester (AMR101) therapy in patients with very high triglyceride levels (from the Multi-center, plAcebo-controlled, Randomized, double-blINd, 12-week study with an open-label Extension [MARINE] trial). Am J Cardiol. 2011;108:682–690.
  • Casula M, Soranna D, Catapano AL, et al. Long-term effect of high dose omega-3 fatty acid supplementation for secondary prevention of cardiovascular outcomes: a meta-analysis of randomized, placebo controlled trials [corrected]. Atheroscler Suppl. 2013;14:243–251.
  • Hooper L, Thompson RL, Harrison RA, et al. Risks and benefits of omega 3 fats for mortality, cardiovascular disease, and cancer: systematic review. BMJ. 2006;332:752–760.
  • Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.
  • Higgins JPT, Green S, eds. Cochrane handbook for systematic reviews of interventions. Version 5.0.2. London: The Cochrane Collaboration; 2009.
  • Borenstein M, Hedges L, Higgins J, et al. Comprehensive meta-analysis version 2. Englewood NJ: Biostat; 2005.
  • Sutton AJ, Abrams KR, Jones DR, et al. Methods for meta-analysis in medical research. NJ, USA: Wiley; 2000.
  • Wan X, Wang W, Liu J, et al. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:135.
  • Banach M, Serban C, Sahebkar A, et al. Impact of statin therapy on coronary plaque composition: a systematic review and meta-analysis of virtual histology intravascular ultrasound studies. BMC Med. 2015;13:229.
  • Banach M, Serban C, Ursoniu S, et al. Statin therapy and plasma coenzyme Q10 concentrations – a systematic review and meta-analysis of placebo-controlled trials. Pharmacol Res. 2015;99:329–336.
  • Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56:455–463.
  • Swahn E, von Schenck H, Olsson AG. Omega-3 ethyl ester concentrate decreases total apolipoprotein CIII and increases antithrombin III in postmyocardial infarction patients. Clin Drug Investig. 1998;15:473–482.
  • Ballantyne CM, Bays HE, Braeckman RA, et al. Icosapent ethyl (eicosapentaenoic acid ethyl ester): effects on plasma apolipoprotein C-III levels in patients from the MARINE and ANCHOR studies. J Clin Lipidol. 2016;10:635–645.
  • Bays HE, Hallén J, Vige R, et al. Icosabutate for the treatment of very high triglycerides: a placebo-controlled, randomized, double-blind, 12-week clinical trial. J Clin Lipidol. 2016;10:181–191.
  • Morton AM, Furtado JD, Lee J, et al. The effect of omega-3 carboxylic acids on apolipoprotein CIII-containing lipoproteins in severe hypertriglyceridemia. J Clin Lipidol. 2016;10:1442–1451.
  • Buckley R, Shewring B, Turner R, et al. Circulating triacylglycerol and apoE levels in response to EPA and docosahexaenoic acid supplementation in adult human subjects. Br J Nutr. 2004;92:477–483.
  • Savinova OV, Fillaus K, Harris WS, et al. Effects of niacin and omega-3 fatty acids on the apolipoproteins in overweight patients with elevated triglycerides and reduced HDL cholesterol. Atherosclerosis. 2015;240:520–525.
  • Skulas-Ray AC, Alaupovic P, Kris-Etherton PM, et al. Dose-response effects of marine omega-3 fatty acids on apolipoproteins, apolipoprotein-defined lipoprotein subclasses, and Lp-PLA2 in individuals with moderate hypertriglyceridemia. J Clin Lipidol. 2015;9:360–367.
  • Chan DC, Watts GF, Mori TA, et al. Factorial study of the effects of atorvastatin and fish oil on dyslipidaemia in visceral obesity. Eur J Clin Invest. 2002;32:429–436.
  • Chan DC, Nguyen MN, Watts GF, et al. Effects of atorvastatin and n-3 fatty acid supplementation on VLDL apolipoprotein C-III kinetics in men with abdominal obesity. Am J Clin Nutr. 2010;91:900–906.
  • Fruchart JC, Sacks F, Hermans MP, et al. The residual risk reduction initiative: a call to action to reduce residual vascular risk in dyslipidemic patients. A position paper by the Residual Risk Reduction Initiative (R3I). Diabetes Vasc Dis Res. 2008;5:319–335.
  • Chapman MJ, Ginsberg HN, Amarenco P, et al. Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol in patients at high risk of cardiovascular disease: evidence and guidance for management. Eur Heart J. 2011;32:1345–1361.
  • Sacks FM, Hermans MP, Fioretto P, et al. Association between plasma triglycerides and high-density lipoprotein cholesterol and microvascular kidney disease and retinopathy in type 2 diabetes mellitus: a global case-control study in 13 countries. Circulation. 2014;129:999–1008.
  • Reiner Ž. Combined therapy in the treatment of dyslipidemia. Fundam Clin Pharmacol. 2010;24:19–28.
  • Kastelein JJ, Maki KC, Susekov A, et al. Omega-3 free fatty acids for the treatment of severe hypertriglyceridemia: the EpanoVa for Lowering Very high triglyceridEs (EVOLVE) trial. J Clin Lipidol. 2014;8:94–106.
  • Cicero AFG, Colletti A, Bajraktari G, et al. Lipid-lowering nutraceuticals in clinical practice: position paper from an International Lipid Expert Panel. Nutr Rev. 2017;75:731–767.
  • Kawakami A, Osaka M, Tani M, et al. Apolipoprotein CIII links hyperlipidemia with vascular endothelial cell dysfunction. Circulation. 2008;118:731–742.
  • Norata GD, Tsimikas S, Pirillo A, et al. Apolipoprotein C-III: from pathophysiology to pharmacology. Trends Pharmacol Sci. 2015;36:675–687.
  • Mazaherioun M, Saedisomeolia A, Javanbakht MH, et al. Beneficial effects of n-3 polyunsaturated fatty acids on adiponectin levels and AdipoR gene expression in patients with type 2 diabetes mellitus: a randomized, placebo-controlled, double-blind clinical trial. Arch Med Sci. 2017;13:716–724.
  • Tai ES, Corella D, Demissie S, et al. Polyunsaturated fatty acids interact with the PPARA-L162V polymorphism to affect plasma triglyceride and apolipoprotein C-III concentrations in the Framingham Heart Study. J Nutr. 2005;135:397–403.
  • Olivieri O, Martinelli N, Sandri M, et al. Apolipoprotein C-III, n-3 polyunsaturated fatty acids, and “insulin-resistant” T − 455C APOC3 gene polymorphism in heart disease patients: example of gene-diet interaction. Clin Chem. 2005;51:360–367.
  • Fallaize R, Carvalho-Wells AL, Tierney AC, Marin C, et al. APOE genotype influences insulin resistance, apolipoprotein CII and CIII according to plasma fatty acid profile in the metabolic syndrome. Sci Rep. 2017;7:6274.
  • Skulas-Ray AC, Kris-Etherton PM, Harris WS, et al. Dose-response effects of omega-3 fatty acids on triglycerides, inflammation, and endothelial function in healthy persons with moderate hypertriglyceridemia. Am J Clin Nutr. 2011;93:243–252.
  • Wei MY, Jacobson TA. Effects of eicosapentaenoic acid versus docosahexaenoic acid on serum lipids: a systematic review and meta-analysis. Curr Atheroscler Rep. 2011;13:474–483.
  • Mori TA, Burke V, Puddey IB, et al. Purified eicosapentaenoic and docosahexaenoic acids have differential effects on serum lipids and lipoproteins, LDL particle size, glucose, and insulin in mildly hyperlipidemic men. Am J Clin Nutr. 2000;71:1085–1094.
  • Lee SJ, Campos H, Moye LA, et al. LDL containing apolipoprotein CIII is an independent risk factor for coronary events in diabetic patients. Arterioscler Thromb Vasc Biol. 2003;23:853–858.
  • Mendivil CO, Rimm EB, Furtado J, et al. Low-density lipoproteins containing apolipoprotein C-III and the risk of coronary heart disease. Circulation. 2011;124:2065–2072.
  • Maki KC, McKenney JM, Reeves MS, et al. Effects of adding prescription omega-3 acid ethyl esters to simvastatin (20 mg/day) on lipids and lipoprotein particles in men and women with mixed dyslipidemia. Am J Cardiol. 2008;102:429–433.
  • Mikhailidis DP, Elisaf M, Rizzo M, et al. “European panel on low density lipoprotein (LDL) subclasses”: a statement on the pathophysiology, atherogenicity and clinical significance of LDL subclasses: executive summary. Curr Vasc Pharmacol. 2011;9:531–532.
  • Mikhailidis DP, Elisaf M, Rizzo M, et al. "European panel on low density lipoprotein (LDL) subclasses": a statement on the pathophysiology, atherogenicity and clinical significance of LDL subclasses. Curr Vasc Pharmacol. 2011;9:533–571.
  • Pećin I, Nedic M, Reiner Ž. Volanesorsen (ISIS-APOCIII-LRx). Drugs Fut. 2016;41:417–421.
  • Gaudet D, Alexander VJ, Baker BF, et al. Antisense inhibition of apolipoprotein C-III in patients with hypertriglyceridemia. N Engl J Med. 2015; 373:438–447.
  • Yang X, Lee SR, Choi YS, et al. Reduction in lipoprotein-associated apoC-III levels following volanesorsen therapy: phase 2 randomized trial results. J Lipid Res. 2016;57:706–713.
  • Pechlaner R, Tsimikas S, Yin X, et al. Very-low-density lipoprotein-associated apolipoproteins predict cardiovascular events and are lowered by inhibition of APOC-III. J Am Coll Cardiol. 2017;69:789–800.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.