Chloroquine cardiomyopathy-a review of the literature

Immunopharmacology and Immunotoxicology

Volumn 35, Issue 3, 2013, Pages 434-442

  Tönnesmann, Ernst ^a   Kandolf, Reinhard ^b   Lewalter, Thorsten ^c  

^a Kaiser Karl Klinik   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c Isarklinikum Munich   (Germany)

Author keywords

Antimalarials; Cardiomyopathy; Cardiotoxicity; Chloroquine; Hydroxychloroquine; Rheumatoid arthritis; Systemic lupus erythematosus

Indexed keywords

CHLOROQUINE; HYDROXYCHLOROQUINE; HYDROXYCHLOROQUINE SULFATE;

ACUTE HEART FAILURE; AMYLOIDOSIS; ATRIOVENTRICULAR BLOCK; ATRIOVENTRICULAR CONDUCTION; CARDIAC IMAGING; CARDIOMYOPATHY; CARDIOTOXICITY; CARDIOVASCULAR RISK; COMPLETE HEART BLOCK; CONGESTIVE CARDIOMYOPATHY; CONGESTIVE HEART FAILURE; CORONARY ARTERY DISEASE; CORTICOSTEROID INDUCED MYOPATHY; DERMATOMYOSITIS; DIAGNOSTIC PROCEDURE; DIASTOLIC DYSFUNCTION; DIFFERENTIAL DIAGNOSIS; DRUG BIOAVAILABILITY; DRUG DISTRIBUTION; DRUG HALF LIFE; ECHOCARDIOGRAPHY; EYE INJURY; FABRY DISEASE; FAINTNESS; GASTROINTESTINAL DISEASE; HEART INJURY; HEART MUSCLE BIOPSY; HEART MUSCLE CONDUCTION DISTURBANCE; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; INCIDENCE; LIMB WEAKNESS; LYSOSOME STORAGE DISEASE; MALARIA; MIXED CONNECTIVE TISSUE DISEASE; MYOCARDITIS; MYOPATHY; NIEMANN PICK DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; POLYMYOSITIS; PRIORITY JOURNAL; PROGNOSIS; QT PROLONGATION; RESTRICTIVE CARDIOMYOPATHY; RETINOPATHY; REVIEW; RHEUMATOID ARTHRITIS; SICK SINUS SYNDROME; SKIN DISEASE; STEADY STATE; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTOLIC DYSFUNCTION; VASCULITIS; VIRUS MYOCARDITIS;

ANIMALS; ANTIMALARIALS; ANTIRHEUMATIC AGENTS; CARDIOMYOPATHIES; CHLOROQUINE; DIAGNOSIS, DIFFERENTIAL; HUMANS; INCIDENCE; MOLECULAR STRUCTURE; MYOCARDIUM;

EID: 84877862837     PISSN: 08923973     EISSN: 15322513     Source Type: Journal    
DOI: 10.3109/08923973.2013.780078     Document Type: Review

References (101)

1. Costedoat-Chalumeau N, Leroux G, Amoura Z, Piette JC. Hydroxychloroquine dans le traitement du lupus: Le renouveau. Rev Med Interne 2008;29:735-737
2. Ruiz-Irastorza G, Ramos-Casals M, Brito-Zeron P, Khamashta M.A.. Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: a systematic review. Ann Rheum Dis 2010;69: 20-28
3. Ben-Zvi I, Kivity S, Langevitz P, Shoenfeld Y. Hydroxychloroquine: from malaria to autoimmunity. Clin Rev Allergy Immunol 2012;42:145-153
4. Lee SJ, Silverman E, Bargman M. The role of antimalarial agents in the treatment of SLE and lupus nephritis. Nat Rev Nephrol 2011; 7:718-729
5. Nelson AA, Fitzhugh OG. Chloroquine (SN-7618): pathologic changes observed in rats which for two years had been fed various proportions. Arch Pathol 1948;45:454-462
6. Alving AS, Eichelberger L, Craige Jr B, et al. Studies on the chronic toxicity of chloroquine. J Clin Invest 1948;27:60-65
7. Cambiaggi A. Unusual ocular lesions in a case of systemic lupus erythematosus. Arch Ophthalmol 1957;57:451-453
8. Loftus LR. Peripheral neuropathy following chloroquine therapy. Can Med Assoc J 1963;89:917-920
9. Whisnant JP, Espinosa RE, Kierland RR, Lambert EH. Chloroquine neuromyopathy. Proc Staff Meet Mayo Clin 1963;38:501-513
10. Hughes JT, Esiri M, Oxbury JM, Whitty CW. Chloroquine myopathy. Q J Med 1971;40:85-93
11. Edwards AC, Meredith TJ, Sowton E. Complete heart block due to chronic chloroquine toxicity managed with permanent pacemaker. Br Med J 1978;1:1109-1110
12. Tett SE. Clinical pharmacokinetics of slow-acting antirheumatic drugs. Clin Pharmacokinet 1993;25:392-407
13. Ducharme J, Farinotti R. Clinical pharmacokinetics and metabolism of chloroquine - focus on recent advancements. Clin Pharmacokinet 1996;31:257-274
14. Rubin M, Zvaifler N, Bernstein H, Mansour A. Chloroquine toxicity. Proc. 2nd Int. Pharm. Meeting, Prague, 1963. Vol. 4: Drugs and enzymes, pp. 467-487. Oxford/Prague, 1965
15. Halliwell WH. Cationic amphiphilic drug-induced phospholipidosis. Toxicol Pathol 1997;25:53-60
16. MacDonald RD, Engel AG. Experimental chloroquine myopathy. J Neuropathol Exp Neurol 1970;29:479-499
17. Klinghardt GW. Experimentelle Schadigungen von Nervensystem und Muskulatur durch Chlorochin: Modelle verschiedenartiger Speicherdystrophien. Acta Neuropathol 1974;28:117-141
18. Gerard JM, Stoupel N, Collier A, Flament-Durand J. Morphologic study of a neuromyopathy caused by prolonged chloroquine treatment. Eur Neurol 1973;9:363-379
19. Rewcastle NB, Humphrey JG. Vacuolar myopathy: clinical, histochemical, and microscopic study. Arch Neurol 1965;12: 570-582
20. Marmor MF, Carr RE, Easterbrook M, et al. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (A Report by the American Academy of Ophthalmology). Ophthalmology 2002;109:1377-1382
21. Tegner R, Tomé FMS, Godeau P, et al. Morphological study of peripheral nerve changes induced by chloroquine treatment. Acta Neuropathol 1988;75:253-260
22. Wang C, Fortin PR, Li Y, et al. Discontinuation of antimalarial drugs in systemic lupus erythematosus. J Rheumatol 1999;26: 808-815
23. Casado E, Gratacos J, Tolosa C, et al. Antimalarial myopathy: an underdiagnosed complication? Prospective longitudinal study of 119 patients. Ann Rheum Dis 2006;65:385-390
24. Estes ML, Ewing-Wilson D, Chou SM, et al. Chloroquine neuromyotoxicity - clinical and pathologic perspective. Am J Med 1987;82:447-455
25. Avina-Zubieta JA, Johnson ES, Suarez-Almazor ME, Russell AS. Incidence of myopathy in patients treated with antimalarials. A report of three cases and a review of the literature. Br J Rheumatol 1995;34:166-170
26. Stein M, Bell MJ, Ang LC. Hydroxychloroquine neuromyotoxicity. J Rheumatol 2000;27:2927-2931
27. Stevens MA, Yeaney GA, Lacomis D. 42-year-old man with discoid lupus and progressive weakness. Brain Pathol 2009;19: 153-156
28. Magnussen I, De Fine Olivarius B. Cardiomyopathy after chloroquine treatment. Acta Med Scand 1977;202:429-431
29. Cervera A, Espinosa G, Cervera R, et al. Cardiac toxicity secondary to long term treatment with chloroquine (letter to the editor). Ann Rheum Dis 2001;60:301
30. Motan J, Topinka I, Dura J, Kvapilova H. Chlorochinova kardiodystrofie. Vnitr Lek 1978;24:1122-1128
31. Godeau P, Guillevin L, Fechner J, et al. Les troubles de conduction au cours du lupus erythemateux: frequence et incidence dans une population de 112 patients. Ann Med Interne 1981;132: 234-240
32. Ratliff NB, Estes ML, Myles JL, et al. Diagnosis of chloroquine cardiomyopathy by endomyocardial biopsy. N Engl J Med 1987; 316:191-193
33. McAllister Jr HA, Ferrans VJ, Hall RJ, et al. Chloroquine-induced cardiomyopathy. Arch Pathol Lab Med 1987;111:953-956
34. Verny C, de Gennes C, Sebastien P, et al. Troubles de la conduction cardiaque au cours dun traitement prolongé par chloroquine - deux nouvelles observations. Presse Med 1992; 21:800-804
35. Iglesias Cubero G, Rodriguez Reguero JJ, Rojo Ortega JM. Restrictive cardiomyopathy caused by chloroquine. Br Heart J 1993;69:451-452
36. August C, Holzhausen HJ, Schmoldt A, et al. Histological and ultrastructural findings in chloroquine-induced cardiomyopathy. J Mol Med 1995;73:73-77
37. Veinot JP, Mai KT, Zarychanski R. Chloroquine related cardiac toxicity. J Rheumatol 1998;25:1221-1225
38. Baguet JP, Tremel F, Fabre M. Chloroquine cardiomyopathy with conduction disorders. Heart 1999;81:221-223
39. Teixeira RA, Martinelli Filho M, Benvenuti LA, et al. Cardiac damage from chronic use of chloroquine: a case report and review of the literature. Arq Bras Cardiol 2002;79:85-88
40. Roos JM, Aubry M.C., Edwards WD. Chloroquine cardiotoxicity: clinicopathologic features in three patients and comparison with three patients with Fabry disease. Cardiovasc Pathol 2002;11: 277-283
41. Charlier P, Cochand-Priollet B, Polivka M, et al. Cardiomyopathie a' la chloroquine revelee par un bloc auriculo-ventriculaire complet. Arch Mal Coeur Vaiss 2002;95:833-837
42. Freihage JH, Patel NC, Jacobs WR, et al. Heart transplantation in a patient with chloroquine-induced cardiomyopathy. J Heart Lung Transplant 2004;23:252-255
43. Nord JE, Shah PK, Rinaldi RZ, Weisman MH. Hydroxychloroquine cardiotoxicity in systemic lupus erythematosus: a report of 2 cases and review of the literature. Semin Arthritis Rheum 2004;33: 336-351
44. Naqvi TZ, Luthringer D, Marchevsky A, et al. Chloroquine-induced cardiomyopathy - echocardiographic features. J Am Soc Echocardiogr 2005;18:384-388
45. Keating RJ, Bhatia S, Amin S, et al. Hydroxychloroquine-induced cardiotoxicity in a 39-year-old woman with systemic lupus erythematosus and systolic dysfunction. J Am Soc Echocardiogr 2005;18:981.e1-5
46. Reffelmann T, Naami A, Spuentrup E, Ku?hl HP. Contrast-enhanced magnetic resonance imaging of a patient with chloroquine-induced cardiomyopathy confirmed by endomyocardial biopsy. Circulation 2006;114:357-358
47. Costedoat-Chalumeau N, Hulot JS, Amoura Z, et al. Cardiomyopathy related to antimalarial therapy with illustrative case report. Cardiology 2007;107:73-80
48. Cotroneo J, Sleik KM, Rene Rodriguez E, Klein AL. Hydroxychloroquine- induced restrictive cardiomyopathy. Eur J Echocardiogr 2007;8:247-251
49. Hernandez Jimenez V, Saavedra Falero J, Navas R. Miocardiopatia restrictiva reversible secundaria a cloroquina (Cartas al editor). Med Clin (Barc) 2007;129:157
50. Soong TR, Barouch LA, Champion HC, et al. New clinical and ultrastructural findings in hydroxychloroquine-induced cardiomyopathy - a report of 2 cases. Hum Pathol 2007;38:1858-1863
51. Manohar VA, Moder KG, Edwards WD, Klarich KW. Restrictive cardiomyopathy secondary to hydroxychloroquine therapy. J Rheumatol 2009;36:440-441
52. Saussine A, Loriot M-A, Picard C, et al. Cardiotoxicité après un traitement au long cours par chloroquine chez deux patientes lupiques. Ann Dermatol Venereol 2009;136:530-535
53. Fragasso G, Sanvito F, Baratto F, et al. Cardiotoxicity after low-dose chloroquine antimalarial therapy. Heart Vessels 2009;24: 385-387
54. Lee JH, Chung WB, Kang JH, et al. A case of chloroquine-induced cardiomyopathy that presented as sick sinus syndrome. Korean Circ J 2010;40:604-608
55. Pieroni M, Smaldone C, Camporeale A, et al. Chloroquine-induced transition from dilated to restrictive cardiomyopathy (Images in Cardiology). J Am Coll Cardiol 2011;57:515
56. Muthukrishnan P, Roukoz H, Grafton G, et al. Hydroxychloroquine-induced cardiomyopathy: a case report. Circ Heart Fail 2011;4:e7-e8
57. Newton-Cheh C, Lin AE, Baggish AL, Wang H. A 47-year-old man with systemic lupus erythematosus and heart failure (Case 11-2011). N Engl J Med 2011;364:1450-1460
58. Hartmann M, Meek IL, van Houwelingen GK, et al. Acute left ventricular failure in a patient with hydroxychloroquine-induced cardiomyopathy. Neth Heart J 2011;19:482-485
59. Tonnesmann E, Stroehmann I, Kandolf R, et al. Cardiomyopathy caused by longterm treatment with Chloroquine: a rare disease, or a rare diagnosis? (letter to the editor). J Rheumatol 2012;39: 1099-1104
60. Frustaci A, Morgante E, Antuzzi D, et al. Inhibition of cardiomyocyte lysosomal activity in hydroxychloroquine cardiomyopathy. Int J Cardiol 2012;157:117-119
61. Abbasi S, Tarter L, Farzaneh-Far R, Farzaneh-Far A. Hydroxychloroquine: a treatable cause of cardiomyopthy (Images in Cardiology). J Am Coll Cardiol 2012;60:786
62. Azimian M, Gultekin S.H., Hata JL, et al. Fatal antimalarial-induced cardiomyopathy - report of 2 cases. J Clin Rheumatol 2012;18: 363-366
63. Oli JM, Ihenacho HN, Talwar RS. Chronic chloroquine toxicity and heart block: a report of two cases. East Afr Med J 1980;57: 505-507
64. Ladipo GO, Essien EE, Andy JJ. Complete heart block in chronic chloroquine poisoning. Int J Cardiol 1983;4:198-200
65. Ihenacho HN, Magulike E. Chloroquine abuse and heart block in Africans. Aust NZ J Med 1989;19:17-21
66. Ogola ES, Muita AK, Adala H. Chloroquine related complete heart block with blindness: case report. East Afr Med J 1992;69:50-52
67. Fellahi JL, Dumazer P, Delayance S, et al. Cardiomyopathie sous traitement par hydroxychloroquine revelee par un bloc auriculoventriculaire complet. Rev Med Interne 1993;14:275-276
68. Guedira N, Hajjaj-Hassouni N, Srairi JE, et al. Third-degree atrioventricular block in a patient under chloroquine therapy. Rev Rhum (Engl. Ed.) 1998;65:58-62
69. Reuss-Borst M, Berner B, Wulf G, Mu?ller GA. Complete heart block as a rare complication of treatment with chloroquine. J Rheumatol 1999;26:1394-1395
70. Duvic C, Pats B, Rouvier B. Bloc auriculoventriculaire complet après prise chronique de chloroquine (Lettres a' la redaction). Rev Med Interne 2000;21:462-463
71. El aichaoui S, Amine B, Saoud B, et al. Bloc auriculoventriculaire complet au cours dun traitement par chloroquine. Rev Méd Interne 2007;28:134-136
72. Puymirat E, Douard H, Roudaut R. Bloc auriculo-ventriculaire complet après prise de chloroquine au long cours. Rev Med Interne 2008;29:741-743
73. Queyriaux B, Carlioz R, Perrier E, et al. Les effets cardiovasculaires lies a' lutilisation de la chloroquine. Ann Cardiol Angeiol 2001;50:285-292
74. Chen CY, Wang FL, Lin CC. Chronic hydroxychloroquine use associated with QT prolongation and refractory ventricular arrhythmia (case report). Clin Toxicol (Phila.) 2006;44:173-175
75. Stas P, Faes D, Noyens P. Conduction disorder and QT prolongation secondary to long-term treatment with chloroquine (letter to the editor). Int J Cardiol 2008;127:e80-e82
76. Sanghvi LM, Mathur BB. Electrocardiogram after chloroquine and emetine. Circulation 1965;32:281-289
77. Seferovic PM, Ristic AD, Maksimovic R, et al. Cardiac arrhythmias and conduction disturbances in autoimmune rheumatic diseases. Rheumatology 2006;45:iv, 39-42
78. Smith B, OGrady F. Experimental chloroquine myopathy. J Neurol Neurosurg Psychiatry 1966;29:255-258
79. Jain D, Halushka MK. Cardiac pathology of systemic lupus erythematosus. J Clin Pathol 2009;62:584-592
80. Voskuyl AE. The heart and cardiovascular manifestations in rheumatoid arthritis. Rheumatology 2006;45:iv, 4-7
81. Costedoat-Chalumeau N, Amoura Z, Hulot JS, et al. Low blood concentration of hydroxychloroquine is a marker for and predictor of disease exacerbations in patients with systemic lupus erythematosus. Arthritis Rheum 2006;54:3284-3290
82. Baccouche H, Mahrholdt H, Meinhardt G, et al. Diagnostic synergy of non-invasive cardiovascular magnetic resonance and invasive endomyocardial biopsy in troponin-positive patients without coronary artery disease. Eur Heart J 2009;30:2869-2879
83. Yilmaz A, Kindermann I, Kindermann M, et al. Comparative evaluation of left and right ventricular endomyocardial biopsy - differences in complication rate and diagnostic performance. Circulation 2010;122:900-909
84. Boldrini R, Biselli R, Santorelli FM, Bosmann C. Neuronal ceroid lipofuscinosis: an ultrastructural, genetic, and clinical study report. Ultrastruct Pathol 2001;25:51-58
85. Dolman CL, Chang E. Visceral lesions in amaurotic familial idiocy with curvilinear bodies. Arch Pathol Lab Med 1972;94:425-430
86. Neville HE, Maunder-Sewry CA, McDougall J, et al. Chloroquineinduced cytosomes with curvilinear profiles in muscle. Muscle Nerve 1979;2:376-381
87. Ramsey MS, Fine BS. Chloroquine toxicity in the human eye: histopathologic observations by electron microscopy. Am J Ophthalmol 1972;73:229-235
88. Lee HS, Daniels BH, Salas E, et al. Clinical utility of LC3 and p62 immunohistochemistry in diagnosis of drug-induced autophagic vacuolar myopathies: a case-control study. PLoS One 2012;7: e36221
89. Marmor MF, Kellner U, Lai TYY, et al. Revised recommendations on screening for chloroquine and hydroxychloroquine retinopathy. Ophthalmology 2011;118:415-422
90. Wolfe F, Marmor MF. Rates and predictors of hydroxychloroquine retinal toxicity in patients with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res 2010;62:775-784
91. Wozniacka A, Cygankiewicz I, Chudzik M, et al. The cardiac safety of chloroquine phosphate treatment in patients with systemic lupus erythematosus: the influence on arrhythmia, heart rate variability and repolarization parameters. Lupus 2006;15:521-525
92. Costedoat-Chalumeau N, Hulot JS, Amoura Z, et al. Heart conduction disorders related to antimalarials toxicity: an analysis of electrocardiograms in 85 patients treated with hydroxychloroquine for connective tissue diseases. Rheumatology 2007;46: 808-810
93. Morand EF, McCloud PI, Littlejohn GO. Continuation of long term treatment with hydroxychloroquine in systemic lupus erythematosus and rheumatoid arthritis. Ann Rheum Dis 1992; 51:1318-1321
94. Avina-Zubieta JA, Galindo-Rodriguez G, Newman S, et al. Long term effectiveness of antimalarial drugs in rheumatic diseases. Ann Rheum Dis 1998;57:582-587
95. Jover JA, Leon L, Pato E, et al. Long-term use of antimalarial drugs in rheumatic diseases. Clin Exp Immunol 2012;30: 380-387
96. Mastaglia FL, Papadimitriou JM, Dawkins RL, Beveridge B. Vacuolar myopathy associated with chloroquine, lupus erythematosus and thymoma. J Neurol Sci 1977;34:315-328
97. Abdel-Hamid H, Oddis CV, Lacomis D. Severe hydroxychloroquine myopathy. Muscle Nerve 2008;38:1206-1210
98. Shinjo SK, Maia Junior OO, Tizziani VAP, et al. Chloroquineinduced bulls eye maculopathy in rheumatoid arthritis: related to disease duration? Clin Rheumatol 2007;26:1248-1253
99. Michaelides M, Stover NB, Francis PJ, Weleber RG. Retinal toxicity associated with hydroxychloroquine and chloroquine. Arch Ophthalmol 2011;129:30-39
100. Tang C, Godfrey T, Stawell R, Nikpour M. Hydroxychloroquine in lupus: emerging evidence supportive multiple beneficial effects. Intern Med J 2012;42:968-978
101. Mackenzie AH. Dose refinements in long-term therapy of rheumatoid arthritis with antimalarials. Am J Med 1983;75:40-45