Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: A systematic review

Annals of the Rheumatic Diseases

Volumn 69, Issue 1, 2010, Pages 20-28

  Ruiz Irastorza, G ^a   Ramos Casals, M ^b   Brito Zeron, P ^b   Khamashta, M A ^c  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYCHLOROQUINE; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL; VITAMIN D;

ATHEROSCLEROSIS; ATRIOVENTRICULAR BLOCK; BLURRED VISION; BONE MASS; CARDIOMYOPATHY; CARDIOTOXICITY; CLINICAL TRIAL; DIARRHEA; DISEASE ACTIVITY; DISEASE EXACERBATION; DISEASE SEVERITY; DRUG EFFICACY; DRUG EXPOSURE; DRUG SAFETY; DRUG WITHDRAWAL; FETUS MALFORMATION; GASTROINTESTINAL TOXICITY; HEADACHE; HEART MUSCLE CONDUCTION DISTURBANCE; HUMAN; MYOPATHY; NAUSEA; OSTEOLYSIS; OTOTOXICITY; PREGNANT WOMAN; PRIORITY JOURNAL; QT INTERVAL; RASH; RETINA DISEASE; RETINOPATHY; REVIEW; RISK BENEFIT ANALYSIS; SIDE EFFECT; SKIN TOXICITY; SURVIVAL; SYSTEMATIC REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOSIS; URTICARIA;

ANTIMALARIALS; ATHEROSCLEROSIS; BONE DENSITY; EVIDENCE-BASED MEDICINE; HUMANS; LIPIDS; LUPUS ERYTHEMATOSUS, SYSTEMIC; OSTEOPOROSIS; RESEARCH DESIGN; SURVIVAL ANALYSIS; THROMBOSIS;

EID: 73449120372     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/ard.2008.101766     Document Type: Review

References (103)

1. Wallace D. The history of antimalarials. Lupus 1996;5(Suppl 1):S2-3.
2. Bertsias G, Ioannidis J, Boletis J, et al. EULAR recommendations for the management of systemic lupus erythematosus. Report of a Task Force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics. Ann Rheum Dis 2008;67:195-205.
3. Fernández M, McGwin GJ, Bertoli A, et al. Systemic lupus erythematosus in a multiethnic cohort (LUMINA XXXIX): relationship between hormone replacement therapy and disease activity over time. Lupus 2006;15:621-2.
4. Mok C, Tang S, To C, et al. Incidence and risk factors of thromboembolism in systemic lupus erythematosus: a comparison of three ethnic groups. Arthritis Rheum 2005;52:2774-82.
5. Cervera R, Khamashta M, Font J, et al. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003;82:299-308.
6. Toloza S, Uribe A, McGwin GJ, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum 2004;50:3947-57.
7. Atkins D, Best D, Briss P, et al. Grading quality of evidence and strength of recommendations. BMJ 2004;328:1490.
8. The Canadian Hydroxychloroquine Study Group. A randomized study of the effect of withdrawing hydroxychloroquine sulphate in systemic lupus erythematosus. N Engl J Med 1991;324:150-4.
9. Meinão I, Sato E, Andrade L, et al. Controlled trial with chloroquine diphosphate in systemic lupus erythematosus. Lupus 1996;5:237-41.
10. Williams H, Egger M, Singer J, et al. Comparison of hydroxychloroquine and placebo in the treatment of the arthropathy of mild systemic lupus erythematosus. J Rheumatol 1994;21:1457-62.
11. Levy R, Vilela V, Cataldo M, et al. Hydroxychloroquine (HCQ) in lupus pregnancy: a double-blind and placebo-controlled study. Lupus 2001;10:401-4.
12. Wozniacka A, Lesiak A, Narbutt J, et al. Chloroquine treatment influences proinflammatory cytokine levels in systemic lupus erythematosus patients. Lupus 2006;15:268-75.
13. Costedoat-Chalumeau N, Amoura Z, Hulot J, 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;54:3284-90.
14. Clowse M, Magder L, Witter F, et al. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum 2006;54:3640-7.
15. Cortés-Hernández J, Ordi-Ros J, Paredes F, et al. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: a prospective study of 103 pregnancies. Rheumatology (Oxford) 2002;41:643-50.
16. Barber C, Geldenhuys L, Hanly J. Sustained remission of lupus nephritis. Lupus 2006;15:94-101.
17. Kasitanon N, Fine D, Haas M, et al. Hydroxychloroquine use predicts complete renal remission within 12 months among patients treated with mycophenolate mofetil therapy for membranous lupus nephritis. Lupus 2006;15:366-70.
18. Tsakonas E, Joseph L, Esdaile J, et al. A long-term study of hydroxychloroquine withdrawal on exacerbations in systemic lupus erythematosus. The Canadian Hydroxychloroquine Study Group. Lupus 1998;7:80-5.
19. Sachet J, Borba E, Bonfá E, et al. Chloroquine increases low-density lipoprotein removal from plasma in systemic lupus patients. Lupus 2007;16:273-8.
20. Muñoz-Valle J, Vázquez-Del Mercado M, Ruiz-Quezada S, et al. Polymorphism of the beta3-adrenergic receptor and lipid profile in patients with rheumatoid arthritis and systemic lupus erythematosus treated with chloroquine. Rheumatol Int 2003;23:99-103.
21. Borba E, Bonfá E. Longterm beneficial effect of chloroquine diphosphate on lipoprotein profile in lupus patients with and without steroid therapy. J Rheumatol 2001;28:780-5.
22. Tam L, Gladman D, Hallett D, et al. Effect of antimalarial agents on the fasting lipid profile in systemic lupus erythematosus. J Rheumatol 2000;27:2142-5.
23. Tam L, Li E, Lam C, et al. Hydroxychloroquine has no significant effect on lipids and apolipoproteins in Chinese systemic lupus erythematosus patients with mild or inactive disease. Lupus 2000;9:413-16.
24. Hodis H, Quismorio FJ, Wickham E, et al. The lipid, lipoprotein, and apolipoprotein effects of hydroxychloroquine in patients with systemic lupus erythematosus. J Rheumatol 1993;20:661-5.
25. Rahman P, Gladman D, Urowitz M, et al. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. J Rheumatol 1999;26:325-30.
26. Petri M, Lakatta C, Magder L, et al. Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med 1994;96:254-9.
27. Karimifar M, Gharibdoost F, Akbarian M, et al. Triglyceride and high-density lipoprotein levels as the markers of disease activity and their association with TNFa and TNF receptor system in systemic lupus erythematosus. APLAR J Rheumatol 2007;10:221-6.
28. Chung C, Avalos I, Oeser A, et al. High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis 2007;66:208-14.
29. Mok C, Mak A, Ma K. Bone mineral density in postmenopausal Chinese patients with systemic lupus erythematosus. Lupus 2005;14:106-12.
30. Lakshminarayanan S, Walsh S, Mohanraj M, et al. Factors associated with low bone mineral density in female patients with systemic lupus erythematosus. J Rheumatol 2001;28:102-8.
31. Calvo-Alén J, McGwin G, Toloza S, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXIV. Cytotoxic treatment is an additional risk factor for the development of symptomatic osteonecrosis in lupus patients: results of a nested matched case-control study. Ann Rheum Dis 2006;65:785-90.
32. Prasad R, Ibanez D, Gladman D, et al. The role of non-corticosteroid related factors in osteonecrosis (ON) in systemic lupus erythematosus: a nested case-control study of inception patients. Lupus 2007;16:157-62.
33. Huisman A, White K, Algra A, et al. Vitamin D levels in women with systemic lupus erythematosus and fibromyalgia. J Rheumatol 2001;28:2535-9.
34. Manzi S, Selzer F, Sutton-Tyrrell K, et al. Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 1999;42:51-60.
35. Selzer F, Sutton-Tyrrell K, Fitzgerald S, et al. Vascular stiffness in women with systemic lupus erythematosus. Hypertension 2001;37:1075-82.
36. Roman M, Shanker B, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003;349:2399-406.
37. Souza A, Hatta F, Miranda FJ, et al. Atherosclerotic plaque in carotid arteries in systemic lupus erythematosus: frequency and associated risk factors. Sao Paulo Med J 2005;123:137-42.
38. Von Feldt J, Scalzi L, Cucchiara A, et al. Homocysteine levels and disease duration independently correlate with coronary artery calcification in patients with systemic lupus erythematosus. Arthritis Rheum 2006;54:2220-7.
39. Maksimowicz-McKinnon K, Magder L, Petri M. Predictors of carotid atherosclerosis in systemic lupus erythematosus. J Rheumatol 2006;33:2458-63.
40. Ahmad Y, Shelmerdine J, Bodill H, et al. Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype. Rheumatology (Oxford) 2007;46:983-8.
41. Tanay A, Leibovitz E, Frayman A, et al. Vascular elasticity of systemic lupus erythematosus patients is associated with steroids and hydroxychloroquine treatment. Ann N Y Acad Sci 2007;1108:24-34.
42. Wallace D. Does hydroxychloroquine sulfate prevent clot formation in systemic lupus erythematosus? Arthritis Rheum 1987;30:1435-6.
43. Ho K, Ahn C, Alarcón G, et al. Systemic lupus erythematosus in a multiethnic cohort (LUMINA): XXVIII. Factors predictive of thrombotic events. Rheumatology (Oxford) 2005;44:1303-7.
44. Ruiz-Irastorza G, Egurbide M, Pijoan J, et al. Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus 2006;15:577-83.
45. Erkan D, Yazici Y, Peterson M, et al. A cross-sectional study of clinical thrombotic risk factors and preventive treatments in antiphospholipid syndrome. Rheumatology (Oxford) 2002;41:924-9.
46. de Leeuw K, Freire B, Smit A, et al. Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus. Lupus 2006;15:675-82.
47. Mok C, Tong K, To C, et al. Risk and predictors of arterial thrombosis in lupus and non-lupus primary glomerulonephritis: a comparative study. Medicine (Baltimore) 2007;86:203-9.
48. Gladman D, Goldsmith C, Urowitz M, et al. The Systemic Lupus International Collaborating Clinics/American College of Rheumatology (SLICC/ACR) damage index for systemic lupus erythematosus international comparison. J Rheumatol 2000;27:373-6.
49. Molad Y, Gorshtein A, Wysenbeek A, et al. Protective effect of hydroxychloroquine in systemic lupus erythematosus. Prospective long-term study of an Israeli cohort. Lupus 2002;11:356-61.
50. Fessler B, Alarcón G, McGwin GJ, et al. Systemic lupus erythematosus in three ethnic groups: XVI. Association of hydroxychloroquine use with reduced risk of damage accrual. Arthritis Rheum 2005;52:1473-80.
51. Rosembaum PR, Rubin DB. The central role of propensity scores in estimating dose-response functions. Biometrika 1983;70:41-55.
52. Alarcón G, McGwin G, Bertoli A, et al. Effect of hydroxychloroquine on the survival of patients with systemic lupus erythematosus: data from LUMINA, a multiethnic US cohort (LUMINA L). Ann Rheum Dis 2007;66:1168-72.
53. Hernández-Cruz B, Tapia N, Villa-Romero A, et al. Risk factors associated with mortality in systemic lupus erythematosus. A case-control study in a tertiary care center in Mexico City. Clin Exp Rheumatol 2001;19:395-401.
54. Bezerra E, Vilar M, da Trindade Neto P, et al. Double-blind, randomized, controlled clinical trial of clofazimine compared with chloroquine in patients with systemic lupus erythematosus. Arthritis Rheum 2005;52:3073-8.
55. Wang C, Fortin P, Li Y, et al. Discontinuation of antimalarial drugs in systemic lupus erythematosus. J Rheumatol 1999;26:808-15.
56. Morand E, McCloud P, Littlejohn G. Continuation of long term treatment with hydroxychloroquine in systemic lupus erythematosus and rheumatoid arthritis. Ann Rheum Dis 1992;51:1318-21.
57. Aviña-Zubieta J, Galindo-Rodriguez G, Newman S, et al. Long-term effectiveness of antimalarial drugs in rheumatic diseases. Ann Rheum Dis 1998;57:582-7.
58. Leecharoen S, Wangkaew S, Louthrenoo W. Ocular side effects of chloroquine in patients with rheumatoid arthritis, systemic lupus erythematosus and scleroderma. J Med Assoc Thai 2007;90:52-8.
59. Mavrikakis I, Sfikakis P, Mavrikakis E, et al. The incidence of irreversible retinal toxicity in patients treated with hydroxychloroquine: a reappraisal. Ophthalmology 2003;110:1321-6.
60. Levy G, Munz S, Paschal J, et al. Incidence of hydroxychloroquine retinopathy in 1,207 patients in a large multicenter outpatient practice. Arthritis Rheum 1997;40:1482-6.
61. Johnson M, Vine A. Hydroxychloroquine therapy in massive total doses without retinal toxicity. Am J Ophthalmol 1987;104:139-44.
62. Finbloom D, Silver K, Newsome D, et al. Comparison of hydroxychloroquine and chloroquine use and the development of retinal toxicity. J Rheumatol 1985;12:692-4.
63. Frenkel M. Safety of hydroxychloroquine. Arch Ophthalmol 1982;100:841.
64. Bonanomi M, Dantas N, Medeiros F. Retinal nerve fibre layer thickness measurements in patients using chloroquine. Clin Exp Ophthalmol 2006;34:130-6.
65. Spalton D, Verdon Roe G, Hughes G. Hydroxychloroquine, dosage parameters and retinopathy. Lupus 1993;2:355-8.
66. Costedoat-Chalumeau N, Hulot J, 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 (Oxford) 2007;46:808-10.
67. 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;15:521-5.
68. Araiza-Casillas R, Cárdenas F, Morales Y, et al. Factors associated with chloroquine-induced retinopathy in rheumatic diseases. Lupus 2004;13:119-24.
69. Cervera A, Espinosa G, Font J, et al. Cardiac toxicity secondary to long term treatment with chloroquine. Ann Rheum Dis 2001;60:301.
70. Alarcón G. How frequently and how soon should we screen our patients for the presence of antimalarial retinopathy? Arthritis Rheum 2002;46:561.
71. Warner A. Early hydroxychloroquine macular toxicity. Arthritis Rheum 2001;44:1959-61.
72. Weiner A, Sandberg M, Gaudio A, et al. Hydroxychloroquine retinopathy. Am J Ophthalmol 1991;112:528-34.
73. Bienfang D, Coblyn J, Liang M, et al. Hydroxychloroquine retinopathy despite regular ophthalmologic evaluation: a consecutive series. J Rheumatol 2000;27:2703-6.
74. Marmor M, Carr R, Easterbrook M, et al. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy: a report by the American Academy of Ophthalmology. Ophthalmology 2002;109:1377-82.
75. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 38-1988. A 58-year-old woman with fever, sweats, congestive heart failure, and lymphadenopathy after treatment for a diagnosis of systemic lupus erythematosus. N Engl J Med 1988;319:768-81.
76. Chen C, Wang F, Lin C. Chronic hydroxychloroquine use associated with QT prolongation and refractory ventricular arrhythmia. Clin Toxicol 2006;44:173-5.
77. Comín-Colet J, Sánchez-Corral M, Alegre-Sancho J, et al. Complete heart block in an adult with systemic lupus erythematosus and recent onset of hydroxychloroquine therapy. Lupus 2001;10:59-62.
78. Keating R, 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.
79. Nord J, Shah P, Rinaldi R, et al. Hydroxychloroquine cardiotoxicity in systemic lupus erythematosus: a report of 2 cases and review of the literature. Semin Arthritis Rheum 2004;33:336-51.
80. Ratliff N, Estes M, Myles J, et al. Diagnosis of chloroquine cardiomyopathy by endomyocardial biopsy. N Engl J Med 1987;316:191-3.
81. McAllister HJ, Ferrans V, Hall R, et al. Chloroquine-induced cardiomyopathy. Arch Pathol Lab Med 1987;111:953-6.
82. Naqvi T, Luthringer D, Marchevsky A, et al. Chloroquine-induced cardiomyopathyechocardiographic features. J Am Soc Echocardiogr 2005;18:383-7.
83. Richards A. Hydroxychloroquine myopathy. J Rheumatol 1998;25:1642-3.
84. Malcangi G, Fraticelli P, Palmieri C, et al. Hydroxychloroquine-induced seizure in a patient with systemic lupus erythematosus. Rheumatol Int 2000;20:31-3.
85. Sabbagh M. Diplopia in a patient under hydroxychloroquine for systemic lupus erythematosus. Rev Rhum Engl Ed 1997;64:65.
86. Sghirlanzoni A, Mantegazza R, Mora M, et al. Chloroquine myopathy and myasthenia-like syndrome. Muscle Nerve 1988;11:114- 19.
87. Tristano A, Falcón L, Willson M, et al. Seizure associated with chloroquine therapy in a patient with systemic lupus erythematosus. Rheumatol Int 2004;24:315-16.
88. Reynaert S, Setterfield J, Black M. Hydroxychloroquine-induced pigmentation in two patients with systemic lupus erythematosus. J Eur Acad Dermatol Venereol 2006;20:487-8.
89. Jiménez-Alonso J, Tercedor J, Jáimez L, et al. Antimalarial drug-induced aquagenic-type pruritus in patients with lupus. Arthritis Rheum 1998;41:744-5.
90. Holme S, Holmes S. Hydroxychloroquine-induced pruritus. Acta Derm Venereol 1999;79:333.
91. Johansen P, Gran J. Ototoxicity due to hydroxychloroquine: report of two cases. Clin Exp Rheumatol 1998;16:472-4.
92. Muslimani A, Spiro T, Chaudhry A, et al. Secondary myelodysplastic syndrome after hydroxychloroquine therapy. Ann Hematol 2007;86:531-4.
93. Makin A, Wendon J, Fitt S, et al. Fulminant hepatic failure secondary to hydroxychloroquine. Gut 1994;35:569-70.
94. Levy M, Buskila D, Gladman D, et al. Pregnancy outcome following first trimester exposure to chloroquine. Am J Perinatol 1991;8:174-8.
95. Parke A, West B. Hydroxychloroquine in pregnant patients with systemic lupus erythematosus. J Rheumatol 1996;23:1715-18.
96. Buchanan N, Toubi E, Khamashta M, et al. Hydroxychloroquine and lupus pregnancy: review of a series of 36 cases. Ann Rheum Dis 1996;55:486-8.
97. Klinger G, Morad Y, Westall C, et al. Ocular toxicity and antenatal exposure to chloroquine or hydroxychloroquine for rheumatic diseases. Lancet 2001;358:813-14.
98. Costedoat-Chalumeau N, Amoura Z, Duhaut P, et al. Safety of hydroxychloroquine in pregnant patients with connective tissue diseases: a study of one hundred thirty-three cases compared with a control group. Arthritis Rheum 2003;48:3207-11.
99. Borba E, Turrini-Filho J, Kuruma K, et al. Chloroquine gestational use in systemic lupus erythematosus: assessing the risk of child ototoxicity by pure tone audiometry. Lupus 2004;13:223-7.
100. Motta M, Tincani A, Faden D, et al. Follow-up of infants exposed to hydroxychloroquine given to mothers during pregnancy and lactation. J Perinatol 2005;25:86-9.
101. Cimaz R, Brucato A, Meregalli E, et al. Electroretinograms of children born to mothers treated with hydroxychloroquine during pregnancy and breast-feeding: comment on the article by Costedoat-Chalumeau et al. Arthritis Rheum 2004;50:3056-7.
102. James J, Kim-Howard X, Bruner B, et al. Hydroxychloroquine sulfate treatment is associated with later onset of systemic lupus erythematosus. Lupus 2007;16:401-9.
103. Ruiz-Irastorza G, Ugarte A, Egurbide M, et al. Antimalarials may influence the risk of malignancy in systemic lupus erythematosus. Ann Rheum Dis 2007;66:815-17.