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Review

Postprandial hyperlipidemia as a risk factor in patients with type 2 diabetes

ORCID Icon, & ORCID Icon
Pages 147-157 | Received 05 Dec 2019, Accepted 31 Mar 2020, Published online: 15 Apr 2020

References

  • Prospective Studies Collaboration and Asia Pacific Cohort Studies Collaboration. Sex-specific relevance of diabetes to occlusive vascular and other mortality: a collaborative meta-analysis of individual data from 980 793 adults from 68 prospective studies. Lancet Diabetes Endocrinol. 2018;6(7):538–546.
  • Sattar N. Revisiting the links between glycaemia, diabetes and cardiovascular disease. Diabetologia. 2013;56(4):686–695.
  • Biondi-Zoccai GG, Abbate A, Liuzzo G, et al. Atherothrombosis, inflammation, and diabetes. J Am Coll Cardiol. 2003;41(7):1071–1077.
  • Ray KK, Seshasai SR, Wijesuriya S, et al. Effect of intensive control of glucose on cardiovascular outcomes and death in patients with diabetes mellitus: a meta-analysis of randomised controlled trials. Lancet. 2009;373(9677):1765–1772.
  • Taskinen M-R, Borén J. New insights into the pathophysiology of dyslipidemia in type 2 diabetes. Atherosclerosis. 2015;239(2):483–495.
  • Fruchart JC, Sacks FM, Hermans MP, et al. The Residual Risk Reduction Initiative: a call to action to reduce residual vascular risk in dyslipidaemic patient. Diab Vasc Dis Res. 2008;5(4):319–335.
  • O’Keefe JH, Bell DS. Postprandial hyperglycemia/hyperlipidemia (postprandial dysmetabolism) is a cardiovascular risk factor. Am J Cardiol. 2007;100(5):899–904.
  • Mach F, Baigent C, Catapano AL, et al. 2019 ESC/EAS guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk. Eur Heart J. 2020;41(1):111–188.
  • Goldberg IJ, Eckel RH, McPherson R. Triglycerides and heart disease. Arterioscler Thromb Vasc Biol. 2011;31(8):1716–1725.
  • Emerging Risk Factors Collaboration, Di Angelantonio E, Sarwar N,  Perry P, et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA. 2009;302(18):1993–2000.
  • Yusuf S, Hawken S, Ounpuu S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364(9438):937–952.
  • Nordestgaard BG. Triglyceride-rich lipoproteins and atherosclerotic cardiovascular disease. Circ Res. 2016;118(4):547–563.
  • Nordestgaard BG. A test in context: lipid profile, fasting versus nonfasting. J Am Coll Cardiol. 2017;70(13):1637–1646. .
  • Watts GF, Ooi EM, Chan DC. Demystifying the management of hypertriglyceridaemia. Nat Rev Cardiol. 2013;10(11):648–661.
  • Ference BA, Kastelein JJP, Ray KK, et al. Association of triglyceride-lowering LPL variants and LDL-C-lowering LDLR variants with risk of coronary heart disease. JAMA. 2019;321(4):364–373. .
  • Sniderman AD, Thanassoulis G, Glavinovic T, et al. Apolipoprotein B particles and cardiovascular disease: a narrative review. JAMA Cardiol. 2019;4(12):1287–1295.
  • Katsiki N, Kolovou G. Postprandial lipid profile in patients with type 2 diabetes. Curr Med Res Opin. 2014;30(1):121.
  • Nakamura K, Miyoshi T, Yunoki K, et al. Postprandial hyperlipidemia as a potential residual risk factor. J Cardiol. 2016;67(4):335–339.
  • Varbo A, Benn M, Nordestgaard BG. Remnant cholesterol as a cause of ischemic heart disease: evidence, definition, measurement, atherogenicity, high risk patients, and present and future treatment. Pharmacol Ther. 2014;141(3):358–367.
  • Reiner Z. Hypertriglyceridaemia and risk of coronary artery disease. Nat Rev Cardiol. 2017;14(7):401–411.
  • Varbo A, Benn M, Tybjærg-Hansen A, et al. Elevated remnant cholesterol causes both low-grade inflammation and ischemic heart disease, whereas elevated low-density lipoprotein cholesterol causes ischemic heart disease without inflammation. Circulation. 2013;128(12):1298–1309.
  • Varbo A, Benn M, Tybjaerg-Hansen A, et al. Remnant cholesterol as a causal risk factor for ischemic heart disease. J Am Coll Cardiol. 2013;61(4):427–436.
  • Nordestgaard BG, Benn M, Schnohr P, et al. Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. JAMA. 2007;298(3):299–308.
  • Masuda D, Yamashita S. Postprandial hyperlipidemia and remnant lipoproteins. J Atheroscler Thromb. 2017;24(2):95–109.
  • Chan DC, Pang J, Romic G, et al. Postprandial hypertriglyceridemia and cardiovascular disease: current and future therapies. Curr Atheroscler Rep. 2013;15(3):309.
  • Cosentino F, Grant PJ, Aboyans V, et al. 2019 ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD. Eur Heart J. 2019;41(2):255–323.
  • Hegele RA, Ginsberg HN, Chapman MJ, et al. The polygenic nature of hypertriglyceridaemia: implications for definition, diagnosis, and management. Lancet Diabetes Endocrinol. 2014;2(8):655–666.
  • Grundy SM, Stone NJ, Bailey AL, et al. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA guideline on the management of blood cholesterol: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on clinical practice guidelines. Circulation. 2019;139(25):e1046–e1081.
  • 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(11):1345–1361.
  • Cartier L-J, Collins C, Lagace M, et al. Comparison of fasting and non-fasting lipid profiles in a large cohort of patients presenting at a community hospital. Clin Biochem. 2018;52:61–66.
  • Joint British Societies’ Board. Joint British Societies’ consensus recommendations for the prevention of cardiovascular disease (JBS3). Heart. 2014;100(Suppl 2):ii1–ii67.
  • Eriksson M, Zethelius B, Eeg-Olofsson K, et al. Blood lipids in 75,048 type 2 diabetic patients: a population-based survey from the Swedish National diabetes register. Eur J Prev Cardiol. 2011;18(1):97–105.
  • Taskinen M-R. Diabetic dyslipidaemia: from basic research to clinical practice. Diabetologia. 2003;46(6):733–749.
  • Hiukka A, Fruchart-Najib J, Leinonen E, et al. Alterations of lipids and apolipoprotein CIII in very low density lipoprotein subspecies in type 2 diabetes. Diabetologia. 2005;48(6):1207–1215.
  • Xiao C, Dash S, Morgantini C, et al. New and emerging regulators of intestinal lipoprotein secretion. Atherosclerosis. 2014;233(2):608–615.
  • Brunzell JD, Hazzard WR, Porte D Jr., et al. Evidence for a common, saturable, triglyceride removal mechanism for chylomicrons and very low density lipoproteins in man. J Clin Invest. 1973;52(7):1578–1585.
  • Cohn JS, Johnson EJ, Millar JS, et al. Contribution of apoB-48 and apoB-100 triglyceride-rich lipoproteins (TRL) to postprandial increases in the plasma concentration of TRL triglycerides and retinyl esters. J Lipid Res. 1993;34(12):2033–2040.
  • Karpe F, Bell M, Björkegren J, et al. Quantification of postprandial triglyceride-rich lipoproteins in healthy men by retinyl ester labeling and simultaneous measurement of apolipoproteins B-48 and B-100. Arterioscler Thromb Vasc Biol. 1995;15(2):199–207.
  • 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(9):999–1008.
  • Su JW, Nzekwu MM, Cabezas MC, et al. Methods to assess impaired post-prandial metabolism and the impact for early detection of cardiovascular disease risk. Eur J Clin Invest. 2009;39(9):741–754.
  • Smith D, Watts GF, Dane-Stewart C, et al. Post-prandial chylomicron response may be predicted by a single measurement of plasma apolipoprotein B48 in the fasting state. Eur J Clin Invest. 1999;29(3):204–209.
  • Welty FK, Lichtenstein AH, Barrett PH, et al. Human apolipoprotein (Apo) B-48 and ApoB-100 kinetics with stable isotopes. Arterioscler Thromb Vasc Biol. 1999;19(12):2966–2974.
  • Nakajima K, Saito T, Tamura A, et al. Cholesterol in remnant-like lipoproteins in human serum using monoclonal anti apo B-100 and anti apo A-I immunoaffinity mixed gels. Clin Chim Acta. 1993;223(1–2):53–71.
  • Watanabe N, Taniguchi T, Taketoh H, et al. Elevated remnant-like lipoprotein particles in impaired glucose tolerance and type 2 diabetic patients. Diabetes Care. 1999;22(1):152–156.
  • Miyauchi K, Kayahara N, Ishigami M, et al. Development of a homogeneous assay to measure remnant lipoprotein cholesterol. Clin Chem. 2007;53(12):2128–2135.
  • Teng K-T, Chang C-Y, Kanthimathi MS, et al. Effects of amount and type of dietary fats on postprandial lipemia and thrombogenic markers in individuals with metabolic syndrome. Atherosclerosis. 2015;242(1):281–287.
  • Monfort-Pires M, Delgado-Lista J, Gomez-Delgado F, et al. Impact of the content of fatty acids of oral fat tolerance tests on postprandial triglyceridemia: systematic review and meta-analysis. Nutrients. 2016;8(9):580.
  • Kolovou GD, Mikhailidis DP, Kovar J, et al. Assessment and clinical relevance of non-fasting and postprandial triglycerides: an expert panel statement. Curr Vasc Pharmacol. 2011;9(3):258–270.
  • Kolovou GD, Watts GF, Mikhailidis DP, et al. Postprandial hypertriglyceridaemia revisited in the era of non-fasting lipid profiles: executive summary of a 2019 expert panel statement. Curr Vasc Pharmacol. 2019;17(5):538–540.
  • Kolovou GD, Watts GF, Mikhailidis DP, et al. Postprandial hypertriglyceridaemia revisited in the era of non-fasting lipid profile testing: a 2019 expert panel statement, main text. Curr Vasc Pharmacol. 2019;17(5):498–514.
  • Kolovou GD, Watts GF, Mikhailidis DP, et al. Postprandial hypertriglyceridaemia revisited in the era of non-fasting lipid profile testing: a 2019 expert panel statement, narrative review. Curr Vasc Pharmacol. 2019;17(5):515–537.
  • Maraki M, Aggelopoulou N, Christodoulou N, et al. Validity of abbreviated oral fat tolerance tests for assessing postprandial lipemia. Clin Nutr. 2011;30(6):852–857.
  • Tentolouris N, Kanellos PT, Siami E, et al. Assessment of the validity and reproducibility of a novel standardized test meal for the study of postprandial triacylglycerol concentrations. Lipids. 2017;52(8):675–686.
  • Gavra P, Melidonis A, Iraklianou S, et al. Alterations in plasma triglyceride concentrations following two oral meals with different fat content in patients with type 2 diabetes mellitus. Curr Vasc Pharmacol. 2018;16(4):385–392.
  • Orem A, Yaman SO, Altinkaynak B, et al. Relationship between postprandial lipemia and atherogenic factors in healthy subjects by considering gender differences. Clin Chim Acta. 2018;480:34–40.
  • Maraki MI, Sidossis LS. Physiology in Medicine: update on lifestyle determinants of postprandial triacylglycerolemia with emphasis on the Mediterranean lifestyle. Am J Physiol Endocrinol Metab. 2015;309(5):E440–E449.
  • Thomsen C, Storm H, Holst JJ, et al. Differential effects of saturated and monounsaturated fats on postprandial lipemia and glucagon-like peptide 1 responses in patients with type 2 diabetes. Am J Clin Nutr. 2003;77(3):605–611.
  • Leon-Acuna A, Torres-Pena JD, Alcala-Diaz JF, et al. Lifestyle factors modulate postprandial hypertriglyceridemia: from the CORDIOPREV study. Atherosclerosis. 2019;290:118–124.
  • Kolovou GD, Salpea KD, Anagnostopoulou KK, et al. Alcohol use, vascular disease, and lipid-lowering drugs. J Pharmacol Exp Ther. 2006;318(1):1–7.
  • Ginsberg H, Olefsky J, Farquhar JW, et al. Moderate ethanol ingestion and plasma triglyceride levels. A study in normal and hypertriglyceridemic persons. Ann Inter Med. 1974;80(2):143–149.
  • American Diabetes Association. 9. Pharmacologic approaches to glycemic treatment: standards of medical care in diabetes—2020. Diabetes Care. 2020;43(Supplement 1):S98–S110.
  • Weintraub MS, Charach G, Grosskopf I. Effects of fibric acid derivatives and metformin on postprandial lipemia. Atherosclerosis. 1998;141(Suppl 1):S71–S75.
  • Eleftheriadou I, Grigoropoulou P, Katsilambros N, et al. The effects of medications used for the management of diabetes and obesity on postprandial lipid metabolism. Curr Diabetes Rev. 2008;4(4):340–356.
  • Hein GJ, Baker C, Hsieh J, et al. GLP-1 and GLP-2 as Yin and Yang of intestinal lipoprotein production: evidence for predominance of GLP-2-stimulated postprandial lipemia in normal and insulin-resistant states. Diabetes. 2013;62(2):373–381.
  • Xiao C, Dash S, Morgantini C, et al. Gut peptides are novel regulators of intestinal lipoprotein secretion: experimental and pharmacological manipulation of lipoprotein metabolism. Diabetes. 2015;64(7):2310–2318.
  • Verges B, Duvillard L, Pais de Barros JP, et al. Liraglutide reduces postprandial hyperlipidemia by increasing ApoB48 (apolipoprotein B48) catabolism and by reducing ApoB48 production in patients with type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol. 2018;38(9):2198–2206.
  • Xiao C, Dash S, Morgantini C, et al. Sitagliptin, a DPP-4 inhibitor, acutely inhibits intestinal lipoprotein particle secretion in healthy humans. Diabetes. 2014;63(7):2394–2401.
  • Noda Y, Miyoshi T, Oe H, et al. Alogliptin ameliorates postprandial lipemia and postprandial endothelial dysfunction in non-diabetic subjects: a preliminary report. Cardiovasc Diabetol. 2013;12(1):8.
  • Gerstein HC, Colhoun HM, Dagenais GR, et al. Dulaglutide and cardiovascular outcomes in type 2 diabetes (REWIND): a double-blind, randomised placebo-controlled trial. Lancet. 2019;394(10193):121–130.
  • Marso SP, Daniels GH, Brown-Frandsen K, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375(4):311–322.
  • Marso SP, Bain SC, Consoli A, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med. 2016;375(19):1834–1844.
  • Tomlinson B, Hu M, Zhang Y, et al. An overview of new GLP-1 receptor agonists for type 2 diabetes. Expert Opin Investig Drugs. 2016;25(2):145–158.
  • Tomlinson B, Hu M, Zhang Y, et al. Effects of glucose-lowering drugs on cardiovascular outcomes in patients with type 2 diabetes. Expert Opin Drug Metab Toxicol. 2016;12(11):1267–1271.
  • Zinman B, Wanner C, Lachin JM, et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373(22):2117–2128.
  • Wiviott SD, Raz I, Bonaca MP, et al. Dapagliflozin and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2019;380(4):347–357.
  • Neal B, Perkovic V, Mahaffey KW, et al. Canagliflozin and cardiovascular and renal events in type 2 diabetes. N Engl J Med. 2017;377(7):644–657.
  • Lam KS, Chow CC, Tan KC, et al. Practical considerations for the use of sodium-glucose co-transporter type 2 inhibitors in treating hyperglycemia in type 2 diabetes. Curr Med Res Opin. 2016;32(6):1097–1108.
  • Chan DC, Watts GF. Postprandial lipoprotein metabolism in familial hypercholesterolemia: thinking outside the box. Metabolism. 2012;61(1):3–11.
  • American Diabetes Association. 10. Cardiovascular disease and risk management: standards of medical care in diabetes—2020. Diabetes Care. 2020;43(Supplement 1):S111–S134.
  • Pang J, Chan DC, Barrett PH, et al. Postprandial dyslipidaemia and diabetes: mechanistic and therapeutic aspects. Curr Opin Lipidol. 2012;23(4):303–309.
  • Ridker PM. Clinician’s guide to reducing inflammation to reduce atherothrombotic risk: JACC review topic of the week. J Am Coll Cardiol. 2018;72(25):3320–3331.
  • Ginsberg HN, Elam MB, Lovato LC, et al. Effects of combination lipid therapy in type 2 diabetes mellitus. N Engl J Med. 2010;362(17):1563–1574.
  • Keech A, Simes RJ, Barter P, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366(9500):1849–1861.
  • Aguiar C, Alegria E, Bonadonna RC, et al. A review of the evidence on reducing macrovascular risk in patients with atherogenic dyslipidaemia: A report from an expert consensus meeting on the role of fenofibrate-statin combination therapy. Atheroscler Suppl. 2015;19:1–12.
  • Iovine C, Lilli S, Gentile A, et al. Atorvastatin or fenofibrate on post-prandial lipaemia in type 2 diabetic patients with hyperlipidaemia. Eur J Clin Invest. 2006;36(8):560–565.
  • Fruchart JC, Santos RD, Aguilar-Salinas C, et al. The selective peroxisome proliferator-activated receptor alpha modulator (SPPARMalpha) paradigm: conceptual framework and therapeutic potential: a consensus statement from the International Atherosclerosis Society (IAS) and the Residual Risk Reduction Initiative (R3i) Foundation. Cardiovasc Diabetol. 2019;18(1):71.
  • Pradhan AD, Paynter NP, Everett BM, et al. Rationale and design of the Pemafibrate to Reduce Cardiovascular Outcomes by Reducing Triglycerides in Patients with Diabetes (PROMINENT) study. Am Heart J. 2018;206:80–93.
  • Ooi EM, Watts GF, Ng TW, et al. Effect of dietary fatty acids on human lipoprotein metabolism: a comprehensive update. Nutrients. 2015;7(6):4416–4425.
  • Bhatt DL, Steg PG, Miller M, et al. Cardiovascular risk reduction with icosapent ethyl for hypertriglyceridemia. N Engl J Med. 2019;380(1):11–22. .
  • FDA approves use of Vascepa (icosapent ethyl) to reduce risk of cardiovascular events in certain adult patient groups. 2019 Dec 13. cited 2020 Mar 1. Available from: https://www.fda.gov/news-events/press-announcements/fda-approves-use-drug-reduce-risk-cardiovascular- events -certain-adult-patient-groups
  • Sahebkar A, Simental-Mendia LE, Mikhailidis DP, et al. Effect of omega-3 supplements on plasma apolipoprotein C-III concentrations: a systematic review and meta-analysis of randomized controlled trials. Ann Med. 2018;50(7):565–575.
  • Jamilian M, Tabassi Z, Reiner Z, et al. The effects of n-3 fatty acids from flaxseed oil on genetic and metabolic profiles in patients with gestational diabetes mellitus: a randomised, double-blind, placebo-controlled trial. Br J Nutr. 2020;123(7):792–799.
  • Yunoki K, Nakamura K, Miyoshi T, et al. Ezetimibe improves postprandial hyperlipemia and its induced endothelial dysfunction. Atherosclerosis. 2011;217(2):486–491.
  • Hiramitsu S, Miyagishima K, Ishii J, et al. The effect of ezetimibe on lipid and glucose metabolism after a fat and glucose load. J Cardiol. 2012;60(5):395–400.
  • Kikuchi K, Nezu U, Inazumi K, et al. Double-blind randomized clinical trial of the effects of ezetimibe on postprandial hyperlipidaemia and hyperglycaemia. J Atheroscler Thromb. 2012;19(12):1093–1101.
  • Sharifi F, Hojeghani N, Mazloomzadeh S, et al. The efficacy of ezetimibe added to ongoing fibrate-statin therapy on postprandial lipid profile in the patients with type 2 diabetes mellitus. J Diabetes Metab Disord. 2013;12(1):24.
  • Westerink J, Deanfield JE, Imholz BP, et al. High-dose statin monotherapy versus low-dose statin/ezetimibe combination on fasting and postprandial lipids and endothelial function in obese patients with the metabolic syndrome: the PANACEA study. Atherosclerosis. 2013;227(1):118–124.
  • Cannon CP, Blazing MA, Giugliano RP, et al. Ezetimibe added to statin therapy after acute coronary syndromes. N Engl J Med. 2016; 2105;372(25):2387–2397.
  • Giugliano RP, Cannon CP, Blazing MA, et al. Benefit of adding ezetimibe to statin therapy on cardiovascular outcomes and safety in patients with versus without diabetes mellitus: results from IMPROVE-IT (Improved Reduction of Outcomes: Vytorin Efficacy International Trial). Circulation. 2018;137(15):1571–1582.
  • Schwartz GG, Steg PG, Szarek M, et al. Alirocumab and cardiovascular outcomes after acute coronary syndrome. N Engl J Med. 2018;379(22):2097–2107.
  • Sabatine MS, Giugliano RP, Keech AC, et al. Evolocumab and clinical outcomes in patients with cardiovascular disease. N Engl J Med. 2017;376(18):1713–1722.
  • Tomlinson B, Hu M, Zhang Y, et al. Alirocumab for the treatment of hypercholesterolemia. Expert Opin Biol Ther. 2017;17(5):633–643.
  • Tomlinson B, Hu M, Zhang Y, et al. Evoocumab for the treatment of hypercholesterolemia. Expert Opin Biol Ther. 2017;17(11):1447–1461.
  • Stein EA, Giugliano RP, Koren MJ, et al. Efficacy and safety of evolocumab (AMG 145), a fully human monoclonal antibody to PCSK9, in hyperlipidaemic patients on various background lipid therapies: pooled analysis of 1359 patients in four phase 2 trials. Eur Heart J. 2014;35(33):2249–2259.
  • Chan DC, Wong AT, Pang J, et al. Inter-relationships between proprotein convertase subtilisin/kexin type 9, apolipoprotein C-III and plasma apolipoprotein B-48 transport in obese subjects: a stable isotope study in the postprandial state. Clin Sci (Lond). 2015;128(6):379–385.
  • Ray KK, Landmesser U, Leiter LA, et al. Inclisiran in patients at high cardiovascular risk with elevated LDL cholesterol. N Engl J Med. 2017;376(15):1430–1440.
  • Rader DJ, Kastelein JJ. Lomitapide and mipomersen: two first-in-class drugs for reducing low-density lipoprotein cholesterol in patients with homozygous familial hypercholesterolemia. Circulation. 2014;129(9):1022–1032.
  • Hegele RA, Tsimikas S. Lipid-lowering agents. Circ Res. 2019;124(3):386–404. .
  • Bempedoic Acid FDA approval. Drugs@FDA: FDA-approved drugs. 2020 Feb 21 cited 2020 Mar 1. Available from: https://www.accessdata.fda.gov/scripts/cder/daf/index.cfm?event=overview.process&ApplNo=211616
  • Crosby J, Peloso GM, Auer PL, et al. TG and HDL Working Group of the Exome Sequencing Project, National Heart, Lung, and Blood Institute. Loss-of-function mutations in APOC3, triglycerides, and coronary disease. N Engl J Med. 2014;371(1):22–31.
  • 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(1):32–41.
  • Stitziel NO, Stirrups KE, Masca NG, et al. Coding variation in ANGPTL4, LPL, and SVEP1 and the risk of coronary disease. N Engl J Med. 2016;374(12):1134–1144.
  • Dewey FE, Gusarova V, O’Dushlaine C, et al. Inactivating variants in ANGPTL4 and risk of coronary artery disease. N Engl J Med. 2016;374(12):1123–1133.
  • Musunuru K, Pirruccello JP, Do R, et al. Exome sequencing, ANGPTL3 mutations, and familial combined hypolipidemia. N Engl J Med. 2010;363(23):2220–2227.
  • Dewey FE, Gusarova V, Dunbar RL, et al. Genetic and pharmacologic inactivation of ANGPTL3 and cardiovascular disease. N Engl J Med. 2017;377(3):211–221.
  • Paik J, Duggan S. Volanesorsen: first global approval. Drugs. 2019;79(12):1349–1354.
  • Zhang J, Rocha NA, McCullough PA. Contribution of ApoCIII to diabetic dyslipidemia and treatment with volanesorsen. Rev Cardiovasc Med. 2018;19(1):13–19.
  • Gaudet D, Gipe DA, Pordy R, et al. ANGPTL3 inhibition in homozygous familial hypercholesterolemia. N Engl J Med. 2017;377(3):296–297.
  • Ahmad Z, Banerjee P, Hamon S, et al. inhibition of angiopoietin-like protein 3 with a monoclonal antibody reduces triglycerides in hypertriglyceridemia. Circulation. 2019;140(6):470–486.

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