Statin-associated muscle symptoms: position paper from the Luso-Latin American Consortium

References

• Cholesterol Treatment Trialists C, Baigent C, Blackwell L, 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;376:1670-81
   PubMed Web of Science ®Google Scholar
• Nielsen SF, Nordestgaard BG. Statin use before diabetes diagnosis and risk of microvascular disease: a nationwide nested matched study. Lancet Diabetes Endocrinol 2014;2:894-900
   PubMed Web of Science ®Google Scholar
• Galper BZ, Moran A, Coxson PG, et al. Using stress testing to guide primary prevention of coronary heart disease among intermediate-risk patients: a cost-effectiveness analysis. Circulation 2012;125:260-70
   PubMed Web of Science ®Google Scholar
• Jackevicius CA, Mamdani M, Tu JV. Adherence with statin therapy in elderly patients with and without acute coronary syndromes. JAMA 2002;288:462-7
   PubMed Web of Science ®Google Scholar
• Chowdhury R, Khan H, Heydon E, et al. Adherence to cardiovascular therapy: a meta-analysis of prevalence and clinical consequences. Eur Heart J 2013;34:2940-8
   PubMed Web of Science ®Google Scholar
• Kent STSC, Muntner P, Colantonio L, et al. Statin intolerance is associated with increased risk for recurrent coronary heart disease hospitalizations. J Am Coll Cardiol 2016;67:1838-1838
   Web of Science ®Google Scholar
• Cohen JD, Brinton EA, Ito MK, Jacobson TA. Understanding Statin Use in America and Gaps in Patient Education (USAGE): an internet-based survey of 10,138 current and former statin users. J Clin Lipidol 2012;6:208-15
   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;19:403-14
   PubMed Web of Science ®Google Scholar
• Banach M, Serban MC. Discussion around statin discontinuation in older adults and patients with wasting diseases. J Cachexia Sarcopenia Muscle 2016;7:396?399
   PubMed Web of Science ®Google Scholar
• Banach M, Rizzo M, Toth PP, et al. Statin intolerance – an attempt at a unified definition. Position paper from an International Lipid Expert Panel. Expert Opin Drug Saf 2015;14:935-55
   PubMed Web of Science ®Google Scholar
• El-Salem K, Ababneh B, Rudnicki S, et al. Prevalence and risk factors of muscle complications secondary to statins. Muscle Nerve 2011;44:877-81
   PubMed Web of Science ®Google Scholar
• Hansen KE, Hildebrand JP, Ferguson EE, Stein JH. Outcomes in 45 patients with statin-associated myopathy. Arch Intern Med 2005;165:2671-6
   PubMed Web of Science ®Google Scholar
• Fung EC, Crook MA. Statin myopathy: a lipid clinic experience on the tolerability of statin rechallenge. Cardiovasc Therapeut 2012;30:e212-18
   PubMed Web of Science ®Google Scholar
• Zhang H, Plutzky J, Skentzos S, et al. Discontinuation of statins in routine care settings: a cohort study. Ann Intern Med 2013;158:526-34
   PubMed Web of Science ®Google Scholar
• Mampuya WM, Frid D, Rocco M, et al. Treatment strategies in patients with statin intolerance: the Cleveland Clinic experience. Am Heart J 2013;166:597-603
   PubMed Web of Science ®Google Scholar
• Parker BA, Capizzi JA, Grimaldi AS, et al. Effect of statins on skeletal muscle function. Circulation 2013;127:96-103
   PubMed Web of Science ®Google Scholar
• Patel J, Martin SS, Banach M. Expert opinion: the therapeutic challenges faced by statin intolerance. Expert Opin Pharmacother 2016;17:1497-507
   PubMed Web of Science ®Google Scholar
• Bingel U, Placebo Competence T. Avoiding nocebo effects to optimize treatment outcome. JAMA 2014;312:693-694
   PubMed Web of Science ®Google Scholar
• Colloca L, Finniss D. Nocebo effects, patient-clinician communication, and therapeutic outcomes. JAMA 2012;307:567-8
   PubMed Web of Science ®Google Scholar
• Mohaupt MG, Karas RH, Babiychuk EB, et al. Association between statin-associated myopathy and skeletal muscle damage. Can Med Assoc J 2009;181:E11-18
   PubMed Web of Science ®Google Scholar
• Vladutiu GD, Simmons Z, Isackson PJ, et al. Genetic risk factors associated with lipid-lowering drug-induced myopathies. Muscle Nerve 2006;34:153-62
   PubMed Web of Science ®Google Scholar
• Ahmad Z. Statin intolerance. Am J Cardiol 2014;113:1765-71
   PubMed Web of Science ®Google Scholar
• Mosshammer D, Schaeffeler E, Schwab M, Morike K. Mechanisms and assessment of statin-related muscular adverse effects. Br J Clin Pharmacol 2014;78:454-66
   PubMed Web of Science ®Google Scholar
• Taylor BA, Thompson PD. Muscle-related side-effects of statins: from mechanisms to evidence-based solutions. Curr Opin Lipidol 2015;26:221-7
   PubMed Web of Science ®Google Scholar
• Hodel C. Myopathy and rhabdomyolysis with lipid-lowering drugs. Toxicol Lett 2002;128:159-68
   PubMed Web of Science ®Google Scholar
• Baker SK. Molecular clues into the pathogenesis of statin-mediated muscle toxicity. Muscle Nerve 2005;31:572-80
   PubMed Web of Science ®Google Scholar
• Dirks AJ, Jones KM. Statin-induced apoptosis and skeletal myopathy. Am J Physiol Cell Physiol 2006;291:C1208-12
   PubMed Web of Science ®Google Scholar
• Guijarro C, Blanco-Colio LM, Ortego M, et al. 3-Hydroxy-3-methylglutaryl coenzyme a reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture. Circulation Res 1998;83:490-500
   PubMed Web of Science ®Google Scholar
• Baer AN, Wortmann RL. Myotoxicity associated with lipid-lowering drugs. Curr Opin Rheumatol 2007;19:67-73
   PubMed Web of Science ®Google Scholar
• 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;99:329-36
   PubMed Web of Science ®Google Scholar
• Laaksonen R, Jokelainen K, Sahi T, et al. Decreases in serum ubiquinone concentrations do not result in reduced levels in muscle tissue during short-term simvastatin treatment in humans. Clin Pharmacol Therapeut 1995;57:62-6
   PubMed Web of Science ®Google Scholar
• Schaefer WH, Lawrence JW, Loughlin AF, et al. Evaluation of ubiquinone concentration and mitochondrial function relative to cerivastatin-induced skeletal myopathy in rats. Toxicol Appl Pharmacol 2004;194:10-23
   PubMed Web of Science ®Google Scholar
• Banach M, Serban C, Sahebkar A, et al. Effects of coenzyme Q10 on statin-induced myopathy: a meta-analysis of randomized controlled trials. Mayo Clin Proc 2015;90:24-34
   PubMed Web of Science ®Google Scholar
• Shepherd J, Vidt DG, Miller E, et al. Safety of rosuvastatin: update on 16,876 rosuvastatin-treated patients in a multinational clinical trial program. Cardiol 2007;107:433-43
   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. Circulation Cardiovasc Genet 2013;6:400-8
   PubMed Web of Science ®Google Scholar
• Srinivas NR. Is pomegranate juice a potential perpetrator of clinical drug–drug interactions? Review of the in vitro, preclinical and clinical evidence. Eur J Drug Metabol Pharmacokinet 2013;38:223-9
   PubMed Web of Science ®Google Scholar
• Doad GJ, Kabange W. Cranberry juice, atorvastatin and back pain. J Med Assoc Georgia 2014;103:14
   PubMedGoogle Scholar
• Maggo SD, Kennedy MA, Clark DW. Clinical implications of pharmacogenetic variation on the effects of statins. Drug Saf 2011;34:1-19
   PubMed Web of Science ®Google Scholar
• Lee P, Greenfield JR, Campbell LV. Vitamin D insufficiency – a novel mechanism of statin-induced myalgia? Clin Endocrinol 2009;71:154-5
   PubMed Web of Science ®Google Scholar
• Thummel KE, Brimer C, Yasuda K, et al. Transcriptional control of intestinal cytochrome P-4503A by 1alpha,25-dihydroxy vitamin D3. Mol Pharmacol 2001;60:1399-406
   PubMed Web of Science ®Google Scholar
• Perez-Castrillon JL, Abad Manteca L, Vega G, et al. Vitamin D levels and lipid response to atorvastatin. Int J Endocrinol 2010;2010:320721
   PubMed Web of Science ®Google Scholar
• Michalska-Kasiczak M, Sahebkar A, Mikhailidis DP, et al. Analysis of vitamin D levels in patients with and without statin-associated myalgia – a systematic review and meta-analysis of 7 studies with 2420 patients. Int J Cardiol 2015;178:111-16
   PubMed Web of Science ®Google Scholar
• Neuvonen PJ, Niemi M, Backman JT. Drug interactions with lipid-lowering drugs: mechanisms and clinical relevance. Clin Pharmacol Therapeut 2006;80:565-81
   PubMed Web of Science ®Google Scholar
• Link E, Parish S, Armitage J, et al. SLCO1B1 variants and statin-induced myopathy – a genomewide study. N Engl J Med 2008;359:789-99
   PubMed Web of Science ®Google Scholar
• Niemi M. Transporter pharmacogenetics and statin toxicity. Clin Pharmacol Therapeut 2010;87:130-3
   PubMed Web of Science ®Google Scholar
• Danik JS, Chasman DI, MacFadyen JG, et al. Lack of association between SLCO1B1 polymorphisms and clinical myalgia following rosuvastatin therapy. Am Heart J 2013;165:1008-14
   PubMed Web of Science ®Google Scholar
• Nies AT, Schwab M, Keppler D. Interplay of conjugating enzymes with OATP uptake transporters and ABCC/MRP efflux pumps in the elimination of drugs. Expert Opin Drug Metabol Toxicol 2008;4:545-68
   PubMed Web of Science ®Google Scholar
• Stulc T, Ceska R, Gotto AM Jr. Statin intolerance: the clinician’s perspective. Curr Atherosclerosis Rep 2015;17:69
   PubMed Web of Science ®Google Scholar
• Rosenson RS, Baker SK, Jacobson TA, et al. An assessment by the Statin Muscle Safety Task Force: 2014 update. J Clin Lipidol 2014;8:S58-S71
   PubMed Web of Science ®Google Scholar
• Stroes ES, Thompson PD, Corsini A, et al. Statin-associated muscle symptoms: impact on statin therapy – European Atherosclerosis Society Consensus Panel Statement on Assessment, Aetiology and Management. Eur Heart J 2015;36:1012-22
   PubMed Web of Science ®Google Scholar
• Thomas JE, Lee N, Thompson PD. Statins provoking MELAS syndrome. A case report. Eur Neurol 2007;57:232-5
   PubMed Web of Science ®Google Scholar
• Patel J, Superko HR, Martin SS, et al. Genetic and immunologic susceptibility to statin-related myopathy. Atherosclerosis 2015;240:260-71
   PubMed Web of Science ®Google Scholar
• Harper CR, Jacobson TA. Evidence-based management of statin myopathy. Curr Atherosclerosis Rep 2010;12:322-30
   PubMed Web of Science ®Google Scholar
• Sociedade Brasileira de Cardiologia, Xavier HT, Izar MC, et al. [V Brazilian Guidelines on Dyslipidemias and Prevention of Atherosclerosis]. Arq Bras Cardiol 2013;101:1-20
   Web of Science ®Google Scholar
• Ward MM. Factors predictive of acute renal failure in rhabdomyolysis. Arch Intern Med 1988;148:1553-7
   PubMed Web of Science ®Google Scholar
• Mubarak S, Owen CA. Compartmental syndrome and its relation to the crush syndrome: a spectrum of disease. A review of 11 cases of prolonged limb compression. Clin Orthop Relat Res 1975;113:81-9
   PubMed Web of Science ®Google Scholar
• Molokhia M, McKeigue P, Curcin V, Majeed A. Statin induced myopathy and myalgia: time trend analysis and comparison of risk associated with statin class from 1991–2006. PLoS One 2008;3:e2522
   PubMed Web of Science ®Google Scholar
• Mohassel P, Mammen AL. Statin-associated autoimmune myopathy and anti-HMGCR autoantibodies. Muscle Nerve 2013;48:477-83
   PubMed Web of Science ®Google Scholar
• Grable-Esposito P, Katzberg HD, Greenberg SA, et al. Immune-mediated necrotizing myopathy associated with statins. Muscle Nerve 2010;41:185-90
   PubMed Web of Science ®Google Scholar
• Alfirevic A, Neely D, Armitage J, et al. Phenotype standardization for statin-induced myotoxicity. Clin Pharmacol Therapeut 2014;96:470-6
   PubMed Web of Science ®Google Scholar
• Pasternak RC, Smith SC Jr, Bairey-Merz CN, et al. ACC/AHA/NHLBI clinical advisory on the use and safety of statins. Circulation 2002;106:1024-8
   PubMed Web of Science ®Google Scholar
• Stone NJ, Robinson JG, Lichtenstein AH, et al. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2014;63(25 Pt B):2889-934
   PubMed Web of Science ®Google Scholar
• Dabby R, Sadeh M, Herman O, et al. Asymptomatic or minimally symptomatic hyperCKemia: histopathologic correlates. Israel Med Assoc J 2006;8:110-13
   PubMed Web of Science ®Google Scholar
• Graham DJ, Staffa JA, Shatin D, et al. Incidence of hospitalized rhabdomyolysis in patients treated with lipid-lowering drugs. JAMA 2004;292:2585-90
   PubMed Web of Science ®Google Scholar
• Law M, Rudnicka AR. Statin safety: a systematic review. Am J Cardiol 2006;97:52-60C
   PubMed Web of Science ®Google Scholar
• Christopher-Stine L, Casciola-Rosen LA, Hong G, et al. A novel autoantibody recognizing 200-kd and 100-kd proteins is associated with an immune-mediated necrotizing myopathy. Arthritis Rheum 2010;62:2757-66
   PubMed Web of Science ®Google Scholar
• Needham M, Fabian V, Knezevic W, et al. Progressive myopathy with up-regulation of MHC-I associated with statin therapy. Neuromuscul Disord 2007;17:194-200
   PubMed Web of Science ®Google Scholar
• Sullivan D, Olsson AG, Scott R, et al. Effect of a monoclonal antibody to PCSK9 on low-density lipoprotein cholesterol levels in statin-intolerant patients: the GAUSS randomized trial. JAMA 2012;308:2497-506
   PubMed Web of Science ®Google Scholar
• Group SC, Link E, Parish S, et al. SLCO1B1 variants and statin-induced myopathy – a genomewide study. N Engl J Med 2008;359:789-99
   PubMed Web of Science ®Google Scholar
• Mancini GB, Baker S, Bergeron J, et al. Diagnosis, prevention, and management of statin adverse effects and intolerance: proceedings of a Canadian Working Group Consensus Conference. Can J Cardiol 2011;27:635-62
   Web of Science ®Google Scholar
• Bartley H, Faasse K, Horne R, Petrie KJ. You can’t always get what you want: the influence of choice on nocebo and placebo responding. Ann Behavioral Med 2016;50:445-51
   PubMed Web of Science ®Google Scholar
• Carvalho LS, Sposito AC. Vitamin D for the prevention of cardiovascular disease: are we ready for that? Atherosclerosis 2015;241:729-40
   PubMed Web of Science ®Google Scholar
• HPS2-THRIVE. HPS2-THRIVE randomized placebo-controlled trial in 25 673 high-risk patients of ER niacin/laropiprant: trial design, pre-specified muscle and liver outcomes, and reasons for stopping study treatment. Eur Heart J 2013;34:1279-91
   PubMed Web of Science ®Google Scholar
• The AIM-HIGH Investigators, Boden WE, Probstfield JL, et al. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N Engl J Med 2011;365:2255-67
   PubMed Web of Science ®Google Scholar
• Backes JM, Gibson CA, Ruisinger JF, Moriarty PM. The high-dose rosuvastatin once weekly study (the HD-ROWS). J Clin Lipidol 2012;6:362-7
   PubMed Web of Science ®Google Scholar
• Bangalore S, Breazna A, DeMicco DA, et al. Visit-to-visit low-density lipoprotein cholesterol variability and risk of cardiovascular outcomes: insights from the TNT trial. J Am Coll Cardiol 2015;65:1539-48
   PubMed Web of Science ®Google Scholar
• Mannarino MR, Ministrini S, Pirro M. Nutraceuticals for the treatment of hypercholesterolemia. Eur J Intern Med 2014;25:592-9
   PubMed Web of Science ®Google Scholar
• Lu Z, Kou W, Du B, et al. Effect of xuezhikang, an extract from red yeast Chinese rice, on coronary events in a Chinese population with previous myocardial infarction. Am J Cardiol 2008;101:1689-93
   PubMed Web of Science ®Google Scholar
• Shang Q, Liu Z, Chen K, et al. A systematic review of xuezhikang, an extract from red yeast rice, for coronary heart disease complicated by dyslipidemia. Evid base Compl Alternative Med 2012;2012:636547
   PubMed Web of Science ®Google Scholar
• Becker DJ, Gordon RY, Halbert SC, et al. Red yeast rice for dyslipidemia in statin-intolerant patients: a randomized trial. Ann Intern Med 2009;150:830-9, W147-9
   PubMed Web of Science ®Google Scholar
• Venero CV, Venero JV, Wortham DC, Thompson PD. Lipid-lowering efficacy of red yeast rice in a population intolerant to statins. Am J Cardiol 2010;105:664-6
   PubMed Web of Science ®Google Scholar
• Bennett JW, Klich M. Mycotoxins. Clin Microbiol Rev 2003;16:497-516
   PubMed Web of Science ®Google Scholar
• Sahebkar A, Serban MC, Gluba-Brzozka A, et al. Lipid-modifying effects of nutraceuticals: an evidence-based approach. Nutrition 2016;32:1179-92
   PubMed Web of Science ®Google Scholar
• Serban MC, Sahebkar A, Dragan S, et al. A systematic review and meta-analysis of the impact of spirulina supplementation on plasma lipid concentrations. Clin Nutrition 2016;35:842-51
   PubMed Web of Science ®Google Scholar
• Stein EA, Raal F. Reduction of low-density lipoprotein cholesterol by monoclonal antibody inhibition of PCSK9. Annu Rev Med 2014;65:417-31
   PubMed Web of Science ®Google Scholar
• Moriarty PMTPD, Cannon CP, Guyton JR, et al. ODYSSEY ALTERNATIVE: efficacy and safety of the proprotein convertase subtilisin/kexin type 9 monoclonal antibody, alirocumab, versus ezetimibe, in patients with statin intolerance as defined by a placebo run-in and statin rechallenge arm. Circulation 2014;130:2108-2109
   Web of Science ®Google Scholar
• Stroes E, Colquhoun D, Sullivan D, et al. Anti-PCSK9 antibody effectively lowers cholesterol in patients with statin intolerance: the GAUSS-2 randomized, placebo-controlled phase 3 clinical trial of evolocumab. J Am Coll Cardiol 2014;63:2541-8
   PubMed Web of Science ®Google Scholar
• Nissen SE, Stroes E, Dent-Acosta RE, et al. Efficacy and tolerability of evolocumab vs ezetimibe in patients with muscle-related statin intolerance: the GAUSS-3 randomized clinical trial. JAMA 2016;315:1580-90
   PubMed Web of Science ®Google Scholar
• 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;35:2249-59
   PubMed Web of Science ®Google Scholar