Personalised medicine in hypercholesterolaemia: the role of pharmacogenetics in statin therapy

References

• Alfonsi JE, Hegele RA, Gryn SE. Pharmacogenetics of lipid-lowering agents: precision or indecision medicine? Curr Atheroscler Rep. 2016;18(5):24.
   PubMed Web of Science ®Google Scholar
• Goldstein JL, Brown MS. Regulation of the mevalonate pathway. Nature. 1990;343(6257):425–430.
   PubMed Web of Science ®Google Scholar
• Grundy SM, Cleeman JI, Merz CNB, et al. Implications of recent clinical trials for the national cholesterol education program adult treatment panel III guidelines. J Am Coll Cardiol. 2004;44(3):720–732.
   PubMedGoogle Scholar
• Expert Panel on Detection E. Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA. 2001;285(19):2486.
   PubMed Web of Science ®Google Scholar
• Mach F, Baigent C, Catapano AL, et al.; ESC Scientific Document Group. 2019 ESC/EAS Guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk: The Task Force for the management of dyslipidaemias of the European Society of Cardiology (ESC) and European Atherosclerosis Society (EAS). Eur Heart J. 2020;41(1):111–188.
   PubMed Web of Science ®Google Scholar
• de Lemos JA, Blazing MA, Wiviott SD, et al.; Investigators. Early intensive vs a delayed conservative simvastatin strategy in patients with acute coronary syndromes: phase Z of the A to Z trial. JAMA. 2004;292(11):1307–1316.
   PubMed Web of Science ®Google Scholar
• Schwartz G. Myocardial Ischemia Reduction with Aggressive Cholesterol Lowering (MIRACL) Study Investigators. Effects of atorvastatin on early recurrent ischemic events in acute coronary syundromes; the MIRACL study; a randomized controlled trial. JAMA. 2001;285(13):1711–1718.
   PubMed Web of Science ®Google Scholar
• Pourhosseini H, Lashkari R, Aminorroaya A, et al. Effects of high dose atorvastatin before elective percutaneous coronary intervention on highly sensitive troponin T and one year major cardiovascular events; a randomized clinical trial. Int J Cardiol Heart Vasc. 2019;22:96–101.
   PubMed Web of Science ®Google Scholar
• Mangravite L, Thorn C, Krauss R. Clinical implications of pharmacogenomics of statin treatment. Pharmacogenomics J. 2006;6(6):360–374.
   PubMed Web of Science ®Google Scholar
• Simon JA, Lin F, Hulley SB, et al. Phenotypic predictors of response to simvastatin therapy among African-Americans and Caucasians: the Cholesterol and Pharmacogenetics (CAP) Study. The Am J Cardiol. 2006;97(6):843–850.
   PubMed Web of Science ®Google Scholar
• Sahebkar A, Serban M-C, Gluba-Brzozka A, et al. Lipid-modifying effects of nutraceuticals: an evidence-based approach. Nutrition. 2016;32(11-12):1179–1192.
   PubMed Web of Science ®Google Scholar
• Catapano AL, Graham I, De Backer G, et al.; Authors/Task Force Members. 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)). Atherosclerosis. 2016;253:281–344.
   PubMed Web of Science ®Google Scholar
• Bates T, Connaughton V, Watts G. Non-adherence to statin therapy: a major challenge for preventive cardiology. Expert Opin Pharmacother. 2009;10(18):2973–2985.
   PubMed Web of Science ®Google Scholar
• Schmitz G, Langmann T. Pharmacogenomics of cholesterol-lowering therapy. Vascul Pharmacol. 2006;44(2):75–89.
   PubMed Web of Science ®Google Scholar
• Mitchell D, Guertin JR, Iliza AC, et al. Economic evaluation of a pharmacogenomics test for statin-induced myopathy in cardiovascular high-risk patients initiating a statin. Mol Diagn Ther. 2017;21(1):95–105.
   PubMed Web of Science ®Google Scholar
• Abd TT, Jacobson TA. Statin-induced myopathy: a review and update. Expert Opin Drug Saf. 2011;10(3):373–387.
   PubMed Web of Science ®Google Scholar
• Bruckert E, Hayem G, Dejager S, et al. Mild to moderate muscular symptoms with high-dosage statin therapy in hyperlipidemic patients—the PRIMO study. Cardiovasc Drugs Ther. 2005;19(6):403–414.
   PubMed Web of Science ®Google Scholar
• Joy TR, Hegele RA. Narrative review: statin-related myopathy. Ann Intern Med. 2009;150(12):858–868.
   PubMed Web of Science ®Google Scholar
• Nichols GA, Koro CE. Does statin therapy initiation increase the risk for myopathy? An observational study of 32,225 diabetic and nondiabetic patients. Clin Ther. 2007;29(8):1761–1770.
   PubMed Web of Science ®Google Scholar
• Yan AT, Yan RT, Tan M, et al. Contemporary management of dyslipidemia in high-risk patients: targets still not met. Am J Med. 2006;119(8):676–683.
   PubMed Web of Science ®Google Scholar
• Martineau P, Gaw A, De Teresa E, et al. Effect of individualizing starting doses of a statin according to baseline LDL-cholesterol levels on achieving cholesterol targets: the achieve cholesterol targets fast with atorvastatin stratified titration (ACTFAST) study. Atherosclerosis. 2007;191(1):135–146.
   PubMed Web of Science ®Google Scholar
• Iakoubova OA, Sabatine MS, Rowland CM, et al. Polymorphism in KIF6 gene and benefit from statins after acute coronary syndromes: results from the PROVE IT-TIMI 22 study. J Am Coll Cardiol. 2008;51(4):449–455.
   PubMed Web of Science ®Google Scholar
• Assimes TL, Hólm H, Kathiresan S, et al. Lack of association between the trp719Arg polymorphism in kinesin-like protein-6 and coronary artery disease in 19 case-control studies. J Am Coll Cardiol. 2011;56(4):155–263.
   Google Scholar
• Kitzmiller JP, Mikulik EB, Dauki AM, et al. Pharmacogenomics of statins: understanding susceptibility to adverse effects. Pharmgenomics Pers Med. 2016;9:97–106.
   PubMed Web of Science ®Google Scholar
• de Denus S, Spinler SA, Miller K, Peterson AM. Statins and liver toxicity: a meta-analysis. Pharmacotherapy J Hum Pharmacol Drug Therapy. 2004;24(5):584–591.
   Google Scholar
• Gradhand U, Kim RB. Pharmacogenomics of MRP transporters (ABCC1-5) and BCRP (ABCG2). Drug Metab Rev. 2008;40(2):317–354.
   PubMed Web of Science ®Google Scholar
• Sparreboom A, Loos WJ, Burger H, et al. Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol Ther. 2005;4(6):650–653.
   PubMed Web of Science ®Google Scholar
• Keskitalo J, Zolk O, Fromm M, et al. ABCG2 polymorphism markedly affects the pharmacokinetics of atorvastatin and rosuvastatin. Clin Pharmacol Ther. 2009;86(2):197–203.
   PubMed Web of Science ®Google Scholar
• DeGorter MK, Tirona RG, Schwarz UI, et al. Clinical and pharmacogenetic predictors of circulating atorvastatin and rosuvastatin concentrations in routine clinical care. Circ Cardiovasc Genet. 2013;6(4):400–408.
   PubMed Web of Science ®Google Scholar
• Morisaki K, Robey RW, Özvegy-Laczka C, et al. Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother Pharmacol. 2005;56(2):161–172.
   PubMed Web of Science ®Google Scholar
• Kondo C, Suzuki H, Itoda M, et al. Functional analysis of SNPs variants of BCRP/ABCG2. Pharm Res. 2004;21(10):1895–1903.
   PubMed Web of Science ®Google Scholar
• Imai Y, Nakane M, Kage K, et al. C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance 1 supported in part by grants from the ministry of education, culture, sports, science and technology, the ministry of health, labour and welfare, Japan, and the virtual research institute of aging of Nippon Boehringer Ingelheim. Mol Cancer Therapeutics. 2002;1(8):611–616.
   PubMed Web of Science ®Google Scholar
• Kobayashi D, Ieiri I, Hirota T, et al. Functional assessment of ABCG2 (BCRP) gene polymorphisms to protein expression in human placenta. Drug Metab Dispos. 2005;33(1):94–101.
   PubMed Web of Science ®Google Scholar
• Mizuarai S, Aozasa N, Kotani H. Single nucleotide polymorphisms result in impaired membrane localization and reduced atpase activity in multidrug transporter ABCG2. Int J Cancer. 2004;109(2):238–246.
   PubMed Web of Science ®Google Scholar
• Sparreboom A, Gelderblom H, Marsh S, et al. Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype. Clin Pharmacol Ther. 2004;76(1):38–44.
   PubMed Web of Science ®Google Scholar
• Yamasaki Y, Ieiri I, Kusuhara H, et al. Pharmacogenetic characterization of sulfasalazine disposition based on NAT2 and ABCG2 (BCRP) gene polymorphisms in humans. Clin Pharmacol Ther. 2008;84(1):95–103.
   PubMed Web of Science ®Google Scholar
• Baxter K, Preston C. Stockley’s drug interactions. London: Pharmaceutical Press
   Google Scholar
• Voora D, Shah SH, Reed CR, et al. Pharmacogenetic predictors of statin-mediated low-density lipoprotein cholesterol reduction and dose response. Circ Cardiovasc Genet. 2008;1(2):100–106.
   PubMedGoogle Scholar
• Kajinami K, Takekoshi N, Brousseau ME, et al. Pharmacogenetics of HMG-CoA reductase inhibitors: exploring the potential for genotype-based individualization of coronary heart disease management. Atherosclerosis. 2004;177(2):219–234.
   PubMed Web of Science ®Google Scholar
• Kajinami K, Brousseau ME, Ordovas JM, et al. CYP3A4 genotypes and plasma lipoprotein levels before and after treatment with atorvastatin in primary hypercholesterolemia. Am J Cardiol. 2004;93(1):104–107.
   PubMed Web of Science ®Google Scholar
• Kadam P, Ashavaid TF, Ponde CK, et al. Genetic determinants of lipid-lowering response to atorvastatin therapy in an Indian population. J Clin Pharm Ther. 2016;41(3):329–333.
   PubMed Web of Science ®Google Scholar
• Poduri A, Khullar M, Bahl A, et al. Common variants of HMGCR, CETP, APOAI, ABCB1, CYP3A4, and CYP7A1 genes as predictors of lipid-lowering response to atorvastatin therapy. DNA and Cell Biology. 2010;29(10):629–637.
   PubMed Web of Science ®Google Scholar
• Tirkkonen T, Ryynänen A, Vahlberg T, et al. Frequency and clinical relevance of drug interactions with lovastatin and simvastatin: an observational database study. Drug Saf. 2008;31(3):231–240.
   PubMed Web of Science ®Google Scholar
• Jermendy G, Horváth T, Littvay L, et al. Effect of genetic and environmental influences on cardiometabolic risk factors: a twin study. Cardiovasc Diabetol. 2011;10(1):96.
   PubMedGoogle Scholar
• Elder SJ, Lichtenstein AH, Pittas AG, et al. Genetic and environmental influences on factors associated with cardiovascular disease and the metabolic syndrome. J Lipid Res. 2009;50(9):1917–1926.
   PubMed Web of Science ®Google Scholar
• Li S, Duan H, Pang Z, et al. Heritability of eleven metabolic phenotypes in Danish and Chinese twins: A cross-population comparison. Obesity (Silver Spring)). 2013;21(9):1908–1914.
   PubMed Web of Science ®Google Scholar
• Medina MW, Krauss RM. Alternative splicing in the regulation of cholesterol homeostasis. Curr Opin Lipidol. 2013;24(2):147–152.
   PubMed Web of Science ®Google Scholar
• Medina MW, Krauss RM. The role of HMGCR alternative splicing in statin efficacy. Trends Cardiovasc Med. 2009;19(5):173–177.
   PubMed Web of Science ®Google Scholar
• Johnson JM, Castle J, Garrett-Engele P, et al. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science. 2003;302(5653):2141–2144.
   PubMed Web of Science ®Google Scholar
• Istvan ES, Palnitkar M, Buchanan SK, et al. Crystal structure of the catalytic portion of human HMG-CoA reductase: insights into regulation of activity and catalysis. Embo J. 2000;19(5):819–830.
   PubMed Web of Science ®Google Scholar
• Istvan ES, Deisenhofer J. Structural mechanism for statin inhibition of HMG-CoA reductase. Science. 2001;292(5519):1160–1164.
   PubMed Web of Science ®Google Scholar
• Yu C-Y, Theusch E, Lo K, et al. HNRNPA1 regulates HMGCR alternative splicing and modulates cellular cholesterol metabolism. Hum Mol Genet. 2014;23(2):319–332.
   PubMed Web of Science ®Google Scholar
• Burkhardt R, Kenny EE, Lowe JK, et al. Common SNPs in HMGCR in micronesians and whites associated with LDL-cholesterol levels affect alternative splicing of exon13. Arterioscler Thromb Vasc Biol. 2008;28(11):2078–2084.
   PubMed Web of Science ®Google Scholar
• Chung JY, Cho SK, Oh ES, et al. Effect of HMGCR variant alleles on low-density lipoprotein cholesterol—lowering response to atorvastatin in healthy Korean subjects. J Clin Pharmacol. 2012;52(3):339–346.
   PubMed Web of Science ®Google Scholar
• Leduc V, Bourque L, Poirier J, et al. Role of rs3846662 and HMGCR alternative splicing in statin efficacy and baseline lipid levels in familial hypercholesterolemia. Pharmacogenet Genomics. 2016;26(1):1.
   PubMed Web of Science ®Google Scholar
• Catapano AL, Graham I, De Backer G, et al.; ESC Scientific Document Group. 2016 ESC/EAS guidelines for the management of dyslipidaemias. Eur Heart J. 2016;37(39):2999–3058.
   PubMed Web of Science ®Google Scholar
• Silverman MG, Ference BA, Im K, et al. Association between lowering LDL-C and cardiovascular risk reduction among different therapeutic interventions: a systematic review and meta-analysis. Jama. 2016;316(12):1289–1297.
   PubMed Web of Science ®Google Scholar
• Muallem H, North KE, Kakoki M, et al. Quantitative effects of common genetic variations in the 3′ UTR of the human LDL-receptor gene and their associations with plasma lipid levels in the Atherosclerosis Risk in Communities study. Hum Genet. 2007;121(3-4):421–431.
   PubMed Web of Science ®Google Scholar
• Polisecki E, Muallem H, Maeda N, et al.; Prospective Study of Pravastatin in the Elderly at Risk (PROSPER) Investigators. Genetic variation at the LDL receptor and HMG-CoA reductase gene loci, lipid levels, statin response, and cardiovascular disease incidence in PROSPER. Atherosclerosis. 2008;200(1):109–114.
   PubMed Web of Science ®Google Scholar
• Mangravite LM, Medina MW, Cui J, et al. Combined influence of LDLR and HMGCR sequence variation on lipid-lowering response to simvastatin. Arterioscler Thromb Vasc Biol. 2010;30(7):1485–1492.
   PubMed Web of Science ®Google Scholar
• Ference BA, Kastelein JJ, 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.
   PubMed Web of Science ®Google Scholar
• Kniffin CL. Solute carrier organic anion transporter family, Member 1B1: OMIM; 2015.
   Google Scholar
• Voora D, Shah SH, Spasojevic I, et al. The SLCO1B1* 5genetic variant is associated with statin-induced side effects. J Am Coll Cardiol. 2009;54(17):1609–1616.
   PubMed Web of Science ®Google Scholar
• Group SC. SLCO1B1 variants and statin-induced myopathy—a genomewide study. New Eng J Med. 2008;359(8):789–799.
   PubMed Web of Science ®Google Scholar
• Olsson AG, Istad H, Luurila O, et al. Effects of rosuvastatin and atorvastatin compared over 52 weeks of treatment in patients with hypercholesterolemia. American Heart Journal. 2002;144(6):1044–1051.
   PubMed Web of Science ®Google Scholar
• Prueksaritanont T, Chu X, Evers R, et al. Pitavastatin is a more sensitive and selective organic anion-transporting polypeptide 1B clinical probe than rosuvastatin. Br J Clin Pharmacol. 2014;78(3):587–598.
   PubMed Web of Science ®Google Scholar
• Tornio A, Vakkilainen J, Neuvonen M, et al. SLCO1B1 polymorphism markedly affects the pharmacokinetics of lovastatin acid. Pharmacogenet Genomics. 2015;25(8):382–387.
   PubMed Web of Science ®Google Scholar
• Pasanen MK, Fredrikson H, Neuvonen PJ, et al. Different effects of SLCO1B1 polymorphism on the pharmacokinetics of atorvastatin and rosuvastatin. Clin Pharmacol Ther. 2007;82(6):726–733.
   PubMed Web of Science ®Google Scholar
• Link E, Parish S, Armitage J, Bowman L, et al.; The Study of the Effectiveness of Additional Reductions in Cholesterol and Homocysteine (SEARCH) Collaborative Group. SLCO1B1 variants and statin‐induced myopathy‐a genomewide study. N Engl J Med. 2008;359(8):789–799.
   PubMed Web of Science ®Google Scholar
• Kozyra M, Ingelman-Sundberg M, Lauschke VM. Rare genetic variants in cellular transporters, metabolic enzymes, and nuclear receptors can be important determinants of interindividual differences in drug response. Genet Med. 2017;19(1):20–29.
   PubMed Web of Science ®Google Scholar
• Bush WS, Crosslin DR, Owusu-Obeng A, et al. Genetic variation among 82 pharmacogenes: the PGRNseq data from the eMERGE network. Clin Pharmacol Ther. 2016;100(2):160–169.
   PubMed Web of Science ®Google Scholar
• Ingelman-Sundberg M, Mkrtchian S, Zhou Y, et al. Integrating rare genetic variants into pharmacogenetic drug response predictions. Hum Genomics. 2018;12(1):26.
   PubMedGoogle Scholar
• Fujikura K, Ingelman-Sundberg M, Lauschke VM. Genetic variation in the human cytochrome P450 supergene family. Pharmacogenet Genomics. 2015;25(12):584–594.
   PubMed Web of Science ®Google Scholar
• Tirona RG, Leake BF, Merino G, et al. Polymorphisms in OATP-C: identification of multiple allelic variants associated with altered transport activity among European- and African-Americans. J Biol Chem. 2001;276(38):35669–35675.
   PubMed Web of Science ®Google Scholar
• Schachter M. Chemical, pharmacokinetic and pharmacodynamic properties of statins: an update. Fundam Clin Pharmacol. 2005;19(1):117–125.
   PubMed Web of Science ®Google Scholar
• Davidson MH. Rosuvastatin: a highly efficacious statin for the treatment of dyslipidaemia. Expert Opin Investig Drugs. 2002;11(1):125–141.
   Web of Science ®Google Scholar
• Gazzerro P, Proto MC, Gangemi G, et al. Pharmacological actions of statins: a critical appraisal in the management of cancer. Pharmacol Rev. 2012;64(1):102–146.
   PubMed Web of Science ®Google Scholar
• Garcia M, Reinoso R, Sanchez Navarro A, et al. Clinical pharmacokinetics of statins. Methods Find Exp Clin Pharmacol. 2003;25(6):457–481.
   PubMed Web of Science ®Google Scholar
• Marciante KD, Durda JP, Heckbert SR, et al. Cerivastatin, genetic variants, and the risk of rhabdomyolysis. Pharmacogenet Genomics. 2011;21(5):280.
   PubMed Web of Science ®Google Scholar
• Carr D, O'meara H, Jorgensen A, et al. SLCO1B1 genetic variant associated with statin-induced myopathy: a proof-of-concept study using the clinical practice research datalink. Clin Pharmacol Ther. 2013;94(6):695–701.
   PubMed Web of Science ®Google Scholar
• Mangravite LM, Engelhardt BE, Medina MW, et al. A statin-dependent QTL for GATM expression is associated with statin-induced myopathy. Nature. 2013;502(7471):377–380.
   PubMed Web of Science ®Google Scholar
• Carr D, Alfirevic A, Johnson R, et al. GATM gene variants and statin myopathy risk. Nature. 2014;513(7518):E1.
   PubMed Web of Science ®Google Scholar
• Neřoldová M, Stránecký V, Hodaňová K, et al. Rare variants in known and novel candidate genes predisposing to statin-associated myopathy. Pharmacogenomics. 2016;17(13):1405–1414.
   PubMed Web of Science ®Google Scholar
• Karaźniewicz-Łada M, Bąba K, Dolatowski F, et al. The polymorphism of statins and its effect on their physicochemical properties. Polim Med. 2018;48(2):77–82.
   PubMedGoogle Scholar
• O'Donnell CJ, Nabel EG. Genomics of cardiovascular disease. N Engl J Med. 2011;365(22):2098–2109.
   PubMed Web of Science ®Google Scholar
• Wang L, McLeod HL, Weinshilboum RM. Genomics and drug response. N Engl J Med. 2011;364(12):1144–1153.
   PubMed Web of Science ®Google Scholar
• Niemi M, Schaeffeler E, Lang T, et al. High plasma pravastatin concentrations are associated with single nucleotide polymorphisms and haplotypes of organic anion transporting polypeptide-C (OATP-C, SLCO1B1). Pharmacogenet Genomics. 2004;14(7):429–440.
   Google Scholar
• Niemi M, Neuvonen PJ, Hofmann U, et al. Acute effects of pravastatin on cholesterol synthesis are associated with SLCO1B1 (encoding OATP1B1) haplotype *17. Pharmacogenet Genomics. 2005;15(5):303–309.
   PubMed Web of Science ®Google Scholar
• Oh ES, Kim CO, Cho SK, Park MS, et al. Impact of ABCC2, ABCG2 and SLCO1B1 polymorphisms on the pharmacokinetics of pitavastatin in humans. Drug Metab Pharmacokinet. 2013;28(3):196–202.
   PubMed Web of Science ®Google Scholar
• Tomlinson B, Hu M, Lee V, et al. ABCG2 polymorphism is associated with the low-density lipoprotein cholesterol response to rosuvastatin . Clin Pharmacol Ther. 2010;87(5):558–562.
   PubMed Web of Science ®Google Scholar
• Hu M, Lui SS, Mak VW, et al. Pharmacogenetic analysis of lipid responses to rosuvastatin in Chinese patients. Pharmacogenet Genomics. 2010;20(10):634–637.
   PubMed Web of Science ®Google Scholar
• Medina MW, Sangkuhl K, Klein TE, et al. PharmGKB: very important pharmacogene-HMGCR. Pharmacogenet Genomics. 2011;21(2):98–101.
   PubMed Web of Science ®Google Scholar
• Kathiresan S, Melander O, Anevski D, et al. Polymorphisms associated with cholesterol and risk of cardiovascular events. N Engl J Med. 2008;358(12):1240–1249.
   PubMed Web of Science ®Google Scholar
• Hu M, To KK, Mak VW, et al. The ABCG2 transporter and its relations with the pharmacokinetics, drug interaction and lipid-lowering effects of statins. Expert Opin Drug Metab Toxicol. 2011;7(1):49–62.
   PubMed Web of Science ®Google Scholar
• Catalan VS, LeLorier J. Predictors of long-term persistence on statins in a subsidized clinical population. Value Health. 2000;3(6):417–426.
   PubMedGoogle Scholar
• Dorais M, Chirovsky D, Ambegaonkar B, et al. Utilization patterns of extended-release niacin in Canada: analysis of an administrative claims database. Can J Cardiol. 2010;26(7):e229–e35.
   PubMed Web of Science ®Google Scholar