The early protective effect of hydroxychloroquine on the risk of cumulative damage in patients with systemic lupus erythematosus

Journal of Rheumatology

Volumn 40, Issue 6, 2013, Pages 831-841

  Akhavan, Pooneh S ^a   Su, Jiandong ^b   Lou, Wendy ^b   Gladman, Dafna D ^a,b,c   Urowitz, Murray B ^a,b,c   Fortin, Paul R ^a,b,c,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d LAVAL UNIVERSITY   (Canada)

Author keywords

Damage; Disease activity; Hydroxychloroquine; Outcomes research; Systemic lupus erythematosus

Indexed keywords

AZATHIOPRINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; HYDROXYCHLOROQUINE; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; STEROID;

ADULT; AGE; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DRUG USE; FEMALE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LONG TERM CARE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RISK FACTOR; RISK REDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC LUPUS INTERNATIONAL COLLABORATING CLINICS DAMAGE INDEX;

DAMAGE; DISEASE ACTIVITY; HYDROXYCHLOROQUINE; OUTCOMES RESEARCH; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADULT; ANTIRHEUMATIC AGENTS; CASE-CONTROL STUDIES; FEMALE; HUMANS; HYDROXYCHLOROQUINE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; TREATMENT OUTCOME;

EID: 84878655408     PISSN: 0315162X     EISSN: 14992752     Source Type: Journal    
DOI: 10.3899/jrheum.120572     Document Type: Article

References (82)

1. Ruiz-Irastorza G, Ramos-Casals M, Brito-Zeron P, Khamashta MA. Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: A systematic review. Ann Rheum Dis 2010;69:20-8.
2. Wallace DJ, Gudsoorkar VS, Weisman MH, Venuturupalli SR. New insights into mechanisms of therapeutic effects of antimalarial agents in SLE. Nat Rev Rheumatol 2012;8:522-33.
3. Fox R. Anti-malarial drugs: Possible mechanisms of action in autoimmune disease and prospects for drug development. Lupus 1996;5 Suppl 1:S4-10.
4. A randomized study of the effect of withdrawing hydroxychloroquine sulfate in systemic lupus erythematosus. The Canadian Hydroxychloroquine Study Group. N Engl J Med 1991;324:150-4.
5. Barber CE, Geldenhuys L, Hanly JG. Sustained remission of lupus nephritis. Lupus 2006;15:94-101.
6. Clowse ME, Magder L, Witter F, Petri M. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum 2006;54:3640-7.
7. Cortes-Hernandez J, Ordi-Ros J, Paredes F, Casellas M, Castillo F, Vilardell-Tarres M. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: A prospective study of 103 pregnancies. Rheumatology 2002;41:643-50.
8. Kasitanon N, Fine DM, Haas M, Magder LS, Petri M. 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.
9. Meinao IM, Sato EI, Andrade LE, Ferraz MB, Atra E. Controlled trial with chloroquine diphosphate in systemic lupus erythematosus. Lupus 1996;5:237-41.
10. Tsakonas E, Joseph L, Esdaile JM, Choquette D, Senecal JL, Cividino A, 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.
11. Williams HJ, Egger MJ, Singer JZ, Willkens RF, Kalunian KC, Clegg DO, et al. Comparison of hydroxychloroquine and placebo in the treatment of the arthropathy of mild systemic lupus erythematosus. J Rheumatol 1994;21:1457-62.
12. Wozniacka A, Lesiak A, Narbutt J, McCauliffe DP, Sysa-Jedrzejowska A. Chloroquine treatment influences proinflammatory cytokine levels in systemic lupus erythematosus patients. Lupus 2006;15:268-75.
13. Levy R, Vilela V, Cataldo M, Ramos RC, Duarte JL, Tura BR, et al. Hydroxychloroquine (HCQ) in lupus pregnancy: A double-blind and placebo-controlled study. Lupus 2001;10:401-4.
14. Costedoat-Chalumeau N, Amoura Z, Hulot J, Hammoud HA, Aymard G, Cacoub P, 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.
15. Erkan D, Yazici Y, Peterson MG, Sammaritano L, Lockshin MD. A cross-sectional study of clinical thrombotic risk factors and preventive treatments in antiphospholipid syndrome. Rheumatology 2002;41:924-9.
16. Mok CC, Tang SS, To CH, Petri M. Incidence and risk factors of thromboembolism in systemic lupus erythematosus: A comparison of three ethnic groups. Arthritis Rheum 2005;52:2774-82.
17. Mok CC, Tong KH, To CH, Siu YP, Ho LY, Au TC. Risk and predictors of arterial thrombosis in lupus and non-lupus primary glomerulonephritis: A comparative study. Medicine 2007;86:203-9.
18. Ruiz-Irastorza G, Egurbide MV, Pijoan JI, Garmendia M, Villar I, Martinez-Berriotxoa A, et al. Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus 2006;15:577-83.
19. Sabio JM, Zamora-Pasadas M, Jimenez-Jaimez J, Albadalejo F, Vargas-Hitos J, Rodriguez del Aguila MD, et al. Metabolic syndrome in patients with systemic lupus erythematosus from Southern Spain. Lupus 2008;17:849-59.
20. Wallace DJ. Does hydroxychloroquine sulfate prevent clot formation in systemic lupus erythematosus? Arthritis Rheum 1987;30:1435-6.
21. Fessler BJ, Alarcon GS, McGwin G Jr, Roseman J, Bastian HM, Friedman AW, 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.
22. Molad Y, Gorshtein A, Wysenbeek AJ, Guedj D, Majadla R, Weinberger A, et al. Protective effect of hydroxychloroquine in systemic lupus erythematosus. Prospective long-term study of an Israeli cohort. Lupus 2002;11:356-61.
23. Alarcon GS, McGwin G, Bertoli AM, Fessler BJ, Calvo-Alen J, Bastian HM, 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.
24. Borba EF, Bonfa E. Longterm beneficial effect of chloroquine diphosphate on lipoprotein profile in lupus patients with and without steroid therapy. J Rheumatol 2001;28:780-5.
25. Chung CP, Avalos I, Oeser A, Gebretsadik T, Shintani A, Raggi P, 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.
26. Hodis HN, Quismorio FP Jr, Wickham E, Blankenhorn DH. The lipid, lipoprotein, and apolipoprotein effects of hydroxychloroquine in patients with systemic lupus erythematosus. J Rheumatol 1993;20:661-5.
27. Munoz-Valle JF, Vazquez-Del Mercado M, Ruiz-Quezada S, Oregon-Romero E, Navarro-Hernandez RE, Ramirez-Barragan J, 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.
28. Petri M, Lakatta C, Magder L, Goldman D. 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.
29. Rahman P, Gladman DD, Urowitz MB, Yuen K, Hallett D, Bruce IN. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. J Rheumatol 1999;26:325-30.
30. Sachet JC, Borba EF, Bonfa E, Vinagre CG, Silva VM, Maranhao RC. Chloroquine increases low-density lipoprotein removal from plasma in systemic lupus patients. Lupus 2007;16:273-8.
31. Tam LS, Gladman DD, Hallett DC, Rahman P, Urowitz MB. Effect of antimalarial agents on the fasting lipid profile in systemic lupus erythematosus. J Rheumatol 2000;27:2142-5.
32. Tam LS, Li EK, Lam CW, Tomlinson B. Hydroxychloroquine has no significant effect on lipids and apolipoproteins in Chinese systemic lupus erythematosus patients with mild or inactive disease. Lupus 2000;9:413-6.
33. Jung H, Bobba R, Su J, Shariati-Sarabi Z, Gladman D, Urowitz MB, et al. The protective effect of antimalarial drug on thrombovascular events in systemic lupus erythematosus. Arthritis Rheum 2010;62:863-8.
34. Mak A, Isenberg DA, Lau CS. Global trends, potential mechanisms and early detection of organ damage in SLE. Nat Rev Rheumatol 2012 [E-pub ahead of print].
35. Urowitz MB, Gladman DD, Tom BD, Ibanez D, Farewell VT. Changing patterns in mortality and disease outcomes for patients with systemic lupus erythematosus. J Rheumatol 2008;35:2152-8.
36. Rivest C, Lew RA, Welsing PM, Sangha O, Wright EA, Roberts WN, et al. Association between clinical factors, socioeconomic status, and organ damage in recent onset systemic lupus erythematosus. J Rheumatol 2000;27:680-4.
37. Lopez R, Davidson JE, Beeby MD, Egger PJ, Isenberg DA. Lupus disease activity and the risk of subsequent organ damage and mortality in a large lupus cohort. Rheumatology 2012;51:491-8.
38. Pons-Estel GJ, Alarcon GS, Gonzalez LA, Zhang J, Vila LM, Reveille JD, et al. Possible protective effect of hydroxychloroquine on delaying the occurrence of integument damage in lupus: LXXI, data from a multiethnic cohort. Arthritis Care Res 2010;62:393-400.
39. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7.
40. Gladman DD, Ibanez D, Urowitz MB. Systemic Lupus Erythematosus Disease Activity Index 2000. J Rheumatol 2002;29:288-91.
41. Gladman DD, Urowitz M, Goldsmith C, Fortin PR, Ginzler E, Gordon C, et al. The reliability of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index in patients with systemic lupus erythematosus. Arthritis Rheum 1997;40:809-13.
42. Gladman DD, Goldsmith CH, Urowitz MB, Bacon P, Fortin P, Ginzler E, 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.
43. Gladman DD, Ginzler E, Goldsmith C, Fortin PR, Liang MH, Urowitz M, et al. The development and initial validation of the SLICC/ACR Damage Index for SLE. Arthritis Rheum 1996;39:363-9.
44. Ibanez D, Urowitz MB, Gladman DD. Summarizing disease features over time: I. Adjusted mean SLEDAI derivation and application to an index of disease activity in lupus. J Rheumatol 2003;30:1977-82.
45. Collins GB, McAllister MS. Chloroquine psychosis masquerading as PCP: A case report. J Psychoactive Drugs 2008;40:211-4.
46. Costedoat-Chalumeau N, Hulot JS, Amoura Z, Leroux G, Lechat P, Funck-Brentano C, 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;46:808-10.
47. Ferreras A, Pinilla I, Abecia E, Pajarin AB, Honrubia FM. [Retinal toxicity following chloroquine therapy - in Spanish]. Arch Soc Esp Oftalmol 2007;82:103-8.
48. Fleury O, Droitcourt C, Polard E, Chevrant-Breton J. Reversible ageusia as an adverse effect of hydroxychloroquine treatment. J Eur Acad Dermatol Venereol 2009;23:604-5.
49. Hsu WY, Chiu NY, Huang SS. Hydroxychloroquine-induced acute psychosis in a systemic lupus erythematosus female. Acta Neuropsychiatr 2011;23:318-9.
50. Lateef A, Tan KB, Lau TC. Acute generalized exanthematous pustulosis and toxic epidermal necrolysis induced by hydroxychloroquine. Clin Rheumatol 2009;28:1449-52.
51. Lee WJ, Ko MK, Lee BR. Hydroxychloroquine retinopathy combined with retinal pigment epithelium detachment. Cutan Ocul Toxicol 2012;31:144-7.
52. Manohar VA, Moder KG, Edwards WD, Klarich K. Restrictive cardiomyopathy secondary to hydroxychloroquine therapy. J Rheumatol 2009;36:440-1.
53. Muslimani AA, Spiro TP, Chaudhry AA, Daw HA. Secondary myelodysplastic syndrome after hydroxychloroquine therapy. Ann Hematol 2007;86:531-4.
54. Muthukrishnan P, Roukoz H, Grafton G, Jessurun J, Colvin-Adams M. Hydroxychloroquine-induced cardiomyopathy: A case report. Circ Heart Fail 2011;4:e7-8.
55. Puri PK, Lountzis NI, Tyler W, Ferringer T. Hydroxychloroquine-induced hyperpigmentation: the staining pattern. J Cutan Pathol 2008;35:1134-7.
56. Skare T, Ribeiro CF, Souza FH, Haendchen L, Jordao JM. Antimalarial cutaneous side effects: A study in 209 users. Cutan Ocul Toxicol 2011;30:45-9.
57. Stas P, Faes D, Noyens P. Conduction disorder and QT prolongation secondary to long-term treatment with chloroquine. Int J Cardiol 2008;127:e80-2.
58. Wolfe F, Marmor MF. Rates and predictors of hydroxychloroquine retinal toxicity in patients with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res 2010;62:775-84.
59. Becker-Merok A, Nossent J. Prevalence, predictors and outcome of vascular damage in systemic lupus erythematosus. Lupus 2009;18:508-15.
60. Broder A, Putterman C. Hydroxychloroquine use is associated with lower odds of persistently positive antiphospholipid antibodies and/or lupus anticoagulant in systemic lupus erythematosus. J Rheumatol 2013;40:30-3.
61. Choojitarom K, Verasertniyom O, Totemchokchyakarn K, Nantiruj K, Sumethkul V, Janwityanujit S. Lupus nephritis and Raynaud's phenomenon are significant risk factors for vascular thrombosis in SLE patients with positive antiphospholipid antibodies. Clin Rheumatol 2008;27:345-51.
62. Kaiser R, Cleveland CM, Criswell LA. Risk and protective factors for thrombosis in systemic lupus erythematosus: Results from a large, multi-ethnic cohort. Ann Rheum Dis 2009;68:238-41.
63. Tektonidou MG, Laskari K, Panagiotakos DB, Moutsopoulos HM. Risk factors for thrombosis and primary thrombosis prevention in patients with systemic lupus erythematosus with or without antiphospholipid antibodies. Arthritis Rheum 2009;61:29-36.
64. Feng X, Zou Y, Pan W, Wang X, Wu M, Zhang M, et al. Prognostic indicators of hospitalized patients with systemic lupus erythematosus: A large retrospective multicenter study in China. J Rheumatol 2011;38:1289-95.
65. Shinjo SK, Bonfa E, Wojdyla D, Borba EF, Ramirez LA, Scherbarth HR, et al. Antimalarial treatment may have a time-dependent effect on lupus survival: Data from a multinational Latin American inception cohort. Arthritis Rheum 2010;62:855-62.
66. Shinjo SK. Systemic lupus erythematosus in the elderly: Antimalarials in disease remission. Rheumatol Int 2009;29:1087-90.
67. Willis R, Seif AM, McGwin G Jr, Martinez-Martinez LA, Gonzalez EB, Dang N, et al. Effect of hydroxychloroquine treatment on pro-inflammatory cytokines and disease activity in SLE patients: Data from LUMINA (LXXV), a multiethnic US cohort. Lupus 2012;21:830-5.
68. Cardoso CR, Signorelli FV, Papi JA, Salles GF. Prevalence and factors associated with dyslipoproteinemias in Brazilian systemic lupus erythematosus patients. Rheumatol Int 2008;28:323-7.
69. Chong YB, Yap DY, Tang CS, Chan TM. Dyslipidaemia in patients with lupus nephritis. Nephrology 2011;16:511-7.
70. Nikpour M, Gladman DD, Ibanez D, Harvey PJ, Urowitz MB. Variability over time and correlates of cholesterol and blood pressure in systemic lupus erythematosus: A longitudinal cohort study. Arthritis Res Ther 2010;12:R125.
71. Penn SK, Kao AH, Schott LL, Elliott JR, Toledo FG, Kuller L, et al. Hydroxychloroquine and glycemia in women with rheumatoid arthritis and systemic lupus erythematosus. J Rheumatol 2010;37:1136-42.
72. Rossoni C, Bisi MC, Keiserman MW, Staub HL. Antimalarials and cholesterol profile of patients with systemic lupus erythematosus. Rev Bras Reumatol 2011;51:383-4, 386-7.
73. Gonzalez LA, Pons-Estel GJ, Zhang J, Vila LM, Reveille JD, Alarcon GS. Time to neuropsychiatric damage occurrence in LUMINA (LXVI): A multi-ethnic lupus cohort. Lupus 2009;18:822-30.
74. Okpechi IG, Ayodele OE, Jones ES, Duffield M, Swanepoel CR. Outcome of patients with membranous lupus nephritis in Cape Town South Africa. Nephrol Dial Transplant 2012;27:3509-15.
75. Petri M, Purvey S, Fang H, Magder LS. Predictors of organ damage in systemic lupus erythematosus: The Hopkins Lupus Cohort. Arthritis Rheum 2012;64:4021-8.
76. Pons-Estel GJ, Alarcon GS, Hachuel L, Boggio G, Wojdyla D, Pascual-Ramos V, et al. Anti-malarials exert a protective effect while Mestizo patients are at increased risk of developing SLE renal disease: Data from a Latin-American cohort. Rheumatology 2012;51:1293-8.
77. Pons-Estel GJ, Alarcon GS, McGwin G Jr, Danila MI, Zhang J, Bastian HM, et al. Protective effect of hydroxychloroquine on renal damage in patients with lupus nephritis: LXV, data from a multiethnic US cohort. Arthritis Rheum 2009;61:830-9.
78. Siso A, Ramos-Casals M, Bove A, Brito-Zeron P, Soria N, Munoz S, et al. Previous antimalarial therapy in patients diagnosed with lupus nephritis: Influence on outcomes and survival. Lupus 2008;17:281-8.
79. James JA, Kim-Howard XR, Bruner BF, Jonsson MK, McClain MT, Arbuckle MR, et al. Hydroxychloroquine sulfate treatment is associated with later onset of systemic lupus erythematosus. Lupus 2007;16:401-9.
80. Ruiz-Irastorza G, Olivares N, Ruiz-Arruza I, Martinez-Berriotxoa A, Egurbide MV, Aguirre C. Predictors of major infections in systemic lupus erythematosus. Arthritis Res Ther 2009;11:R109.
81. Ruiz-Irastorza G, Ugarte A, Egurbide MV, Garmendia M, Pijoan JI, Martinez-Berriotxoa A, et al. Antimalarials may influence the risk of malignancy in systemic lupus erythematosus. Ann Rheum Dis 2007;66:815-7.
82. Winkelmayer WC, Kurth T. Propensity scores: Help or hype? Nephrol Dial Transplant 2004;19:1671-3.