The association of systemic lupus erythematosus and myasthenia gravis: A series of 17 cases, with a special focus on hydroxychloroquine use and a review of the literature

Journal of Neurology

Volumn 259, Issue 7, 2012, Pages 1290-1297

  Jallouli, M ^a   Saadoun, D ^a   Eymard, B ^b   Leroux, G ^a   Haroche, J ^a   Le Thi Huong, D ^a   De Gennes, C ^a   Chapelon, C ^a   Benveniste, O ^c   Wechsler, B ^a   Cacoub, P ^a   Amoura, Z ^a   Piette, J C ^a   Costedoat Chalumeau, N ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Antiphospholipid; Hydroxychloroquine; Myasthenia gravis; Systemic lupus erythematosus; Thymectomy

Indexed keywords

AUTOANTIBODY; AZATHIOPRINE; CARDIOLIPIN ANTIBODY; CHOLINERGIC RECEPTOR; CYCLOPHOSPHAMIDE; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; STEROID;

ARTHRITIS; ARTICLE; CLINICAL ARTICLE; CLINICAL FEATURE; CYTOPENIA; DIPLOPIA; DISEASE ASSOCIATION; DISEASE EXACERBATION; DYSARTHRIA; DYSPHAGIA; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; HUMAN; HYPERPLASIA; LABORATORY TEST; LIMB WEAKNESS; MEDICAL RECORD REVIEW; MYASTHENIA GRAVIS; OUTCOME ASSESSMENT; PLASMAPHERESIS; PRIORITY JOURNAL; RASH; RETROSPECTIVE STUDY; SYSTEMIC LUPUS ERYTHEMATOSUS; THYMOMA;

ADULT; ANTIRHEUMATIC AGENTS; FEMALE; HUMANS; HYDROXYCHLOROQUINE; LUPUS ERYTHEMATOSUS, SYSTEMIC; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MYASTHENIA GRAVIS; RETROSPECTIVE STUDIES; STATISTICS, NONPARAMETRIC; TOMOGRAPHY SCANNERS, X-RAY COMPUTED; YOUNG ADULT;

EID: 84864281931     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-011-6335-z     Document Type: Article

References (70)

1. Conti-Fine BM, Milani M, Kaminski HJ (2006) Myasthenia gravis: past, present, and future. J Clin Invest 116(11):2843-2854 (Pubitemid 44684466)
2. Park MJ, Kim YA, Lee SS, Kim BC, Kim MK, Cho KH (2004) Appearance of systemic lupus erythematosus in patients with myasthenia gravis following thymectomy: two case reports. J Korean Med Sci 19(1):134-136
3. Costedoat-Chalumeau N, Amoura Z, Hulot JS, Lechat P, Piette JC (2007) Hydroxychloroquine in systemic lupus erythematosus. Lancet 369(9569):1257-1258 (Pubitemid 46552044)
4. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725
5. LM Miyakis S, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, de Groot PG, Koike T, Meroni PL, Reber G, Shoenfeld Y, Tincani A, Vlachoyiannapoulos PG, Kritis SA (2006) International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemostasis 4(2):295-306
6. Bouchez B, Arnott G, Delandsheer E, Courteville-Delamarre V (1983) Association of myasthenia and disseminated lupus erythematosus. Review of the literature apropos of a case. LARC Med 3(8):541-549
7. Isaacs P (1971) Myasthenia with systemic lupus and palmoplantar keratosis. Br Med J 4(5783):339-340
8. MacKechnie HL, Squires AH, Platts M, Pruzanski W (1973) Thymoma, myasthenia gravis, erythroblastopenic anemia and systemic lupus erythematosus in one patient. Can Med Assoc J 109(8):733-738
9. Saint-Faust M, Perelman S, Dupont D, Velin P, Chatel M (2010) Transient neonatal myasthenia gravis revealing a myasthenia gravis and a systemic lupus erythematosus in the mother: case report and review of the literature. Am J Perinatol 27(2):107-110
10. Gerli R, Paganelli R, Cossarizza A, Muscat C, Piccolo G, Barbieri D, Mariotti S, Monti D, Bistoni O, Raiola E, Venanzi FM, Bertotto A, Franceschi C (1999) Long-term immunologic effects of thymectomy in patients with myasthenia gravis. J Allergy Clin Immunol 103(5 Pt 1):865-872 (Pubitemid 29297590)
11. Aarli JA, Milde EJ, Thunold S (1975) Arthritis in myasthenia gravis. J Neurol Neurosurg Psychiatry 38(11):1048-1055
12. Alarcon Segovia D, Galbraith RF, Maldonado JE, Howard FM Jr (1963) Systemic lupus erythematosus following thymectomy for myasthenia gravis. Report of two cases. Lancet 2(7309):662-665
13. Denney D, Rose RL (1961) Myasthenia gravis followed by systemic lupus erythematosus. A case report. Neurology 11:710-713
14. Kennes B, Delespesse G, Vandenbossche JL, Sternon J (1978) Systemic lupus erythematosus triggered by adult thymectomy in myasthenia gravis patient: report of a case. Acta Clin Belg 33(2):110-116 (Pubitemid 9017243)
15. Laukaitis JP, Borenstein DG (1989) Multiple autoimmune diseases in a predisposed patient. Arthritis Rheum 32(1):119-120
16. Mevorach D, Perrot S, Buchanan NM, Khamashta M, Laoussadi S, Hughes GR, Menkes CJ (1995) Appearance of systemic lupus erythematosus after thymectomy: four case reports and review of the literature. Lupus 4(1):33-37
17. Schoenen J, Delwaide PJ (1976) The association of myasthenia and disseminated lupus erythematosus. 2 cases. Nouv Presse Med 5(18):1185-1188
18. Vaiopoulos G, Sfikakis PP, Kapsimali V, Boki K, Panayiotidis P, Aessopos A, Tsokos GC, Kaklamanis P (1994) The association of systemic lupus erythematosus and myasthenia gravis. Postgrad Med J 70(828):741-745 (Pubitemid 24314037)
19. Mizon JP, Morcamp D, Lefebvre P, Froissart M, Guidicelli CP, Goasguen J (1979) Associated myasthenia and disseminated lupus erythematosus. A report on two cases and complete review of the published literature (author's transl). Ann Med Interne (Paris) 130(11):489-500 (Pubitemid 10165241)
20. Abbruzzese G, Abbruzzese M, Bacigalupo A, Ratto S (1979) Systemic lupus erythematosus after thymectomy in a patient with myasthenia gravis. Neurology 29(10):1436-1437
21. Calabrese LH, Bach JF, Currie T, Vidt D, Clough J, Krakauer RS (1981) Development of systemic lupus erythematosus after thymectomy for myasthenia gravis. Studies of suppressor cell function. Arch Intern Med 141(2):253-255 (Pubitemid 11130268)
22. Ciaccio M, Parodi A, Rebora A (1989) Myasthenia gravis and lupus erythematosus. Int J Dermatol 28(5):317-320 (Pubitemid 19179637)
23. Le Loet X, Pouyol F, Lees O, Ducastelle T, Godin M, Deshayes P (1986) Acute systemic lupus erythematosus after thymectomy for myasthenia. Sequential study of lymphocyte subpopulations. Rev Med Interne 7(4):425-432 (Pubitemid 16002521)
24. Sant SM (1997) Systemic lupus erythematosus after thymectomy in a patient with myasthenia gravis. Ir Med J 90(3):116-118
25. Tellez-Zenteno JF, Remes-Troche JM, Mimenza-Alvarado A, Garcia-Ramos G, Estanol B, Vega-Boada F (2003) The association of myasthenia gravis and connective tissue diseases. Effects of thymectomy in six cases with rheumatoid arthritis and one case with systemic lupus erythematosus. Neurologia 18(2):54-58 (Pubitemid 36358889)
26. Omar HA, Alzahrani MA, Al Bshabshe AA, Assiri A, Shalaby M, Dwedar A, Abdulwahed SR, Hussein MR (2010) Systemic lupus erythematosus after thymectomy for myasthenia gravis: a case report and review of the literature. Clin Exp Nephrol 14(3):272-276
27. Lee H, Chen W, Su K, Chou C, Tsai C (2008) Myasthenia gravis associated with lupus nephritis. Lupus 17(9):860-861
28. Iwadate H, Kobayashi H, Shio K, Noguchi E, Watanabe K, Sasajima T, Sekine H, Watanabe H, Ohira H, Obara K, Sato Y (2006) A case of systemic lupus erythematosus complicated by pure red cell aplasia and idiopathic portal hypertension after thymectomy. Mod Rheumatol 16(2):109-112
29. Grinlinton FM, Lynch NM, Hart HH (1991) A pair of monozygotic twins who are concordant for myasthenia gravis but became discordant for systemic lupus erythematosus post-thymectomy. Arthritis Rheum 34(7):916-919
30. Sthoeger Z, Neiman A, Elbirt D, Zinger H, Magen E, Burstein R, Eitan S, Abarbanel J, Mozes E (2006) High prevalence of systemic lupus erythematosus in 78 myasthenia gravis patients: a clinical and serologic study. Am J Med Sci 331(1):4-9 (Pubitemid 43177508)
31. Hrycek A (2009) A sequence of pathologic events in a patient after thymectomy for myasthenia gravis. Rheumatol Int [Epub ahead of print]
32. Meloni F, Gueli N, Villatico Campbell S, Di Maio F, Di Bernardo MG, Di Nuzzo M, Carmenini G (1996) A case of systemic lupus erythematosus (SLE) and myasthenia gravis (MG). Allergy 51(5):362-363
33. Branch CE Jr, Swift TR (1978) Systemic lupus erythematosus, myasthenia gravis, and Ehlers-Danlos syndrome. Ann Neurol 4(4):374-375 (Pubitemid 9009867)
34. Chan MK, Britton M (1980) Comparative clinical features in patients with myasthenia gravis with systemic lupus erythematosus. J Rheumatol 7(6):838-842 (Pubitemid 11181500)
35. Killian PJ, Hoffman GS (1980) Coexistence of systemic lupus erythematosus and myasthenia gravis. South Med J 73(2):244-246 (Pubitemid 10154662)
36. Valesini G, Pastore R, de Berardinis PG, Serafini U, Vincent A, Bottazzo GN (1983) Appearance of anti-acetylcholine receptor antibodies coincident with onset of myasthenic weakness in patient with systemic lupus erythematosus. Lancet 1(8328):831
37. Thorlacius S, Aarli JA, Riise T, Matre R, Johnsen HJ (1989) Associated disorders in myasthenia gravis: autoimmune diseases and their relation to thymectomy. Acta Neurol Scand 80(4):290-295 (Pubitemid 19264758)
38. Ben-Chetrit E, Pollack A, Flusser D, Rubinow A (1990) Coexistence of systemic lupus erythematosus and myasthenia gravis: two distinct populations of anti-DNA and anti-acetylcholine receptor antibodies. Clin Exp Rheumatol 8(1):71-74 (Pubitemid 20158232)
39. Barbosa RE, Cordova S, Cajigas JC (2000) Coexistence of systemic lupus erythematosus and myasthenia gravis. Lupus 9(2):156-157 (Pubitemid 30171117)
40. Chaturvedi V, Handa R, Aggarwal P, Wali JP (2001) Systemic lupus erythematosus and myasthenia gravis. J Assoc Physicians India 49:670 (Pubitemid 33702133)
41. Bhinder S, Majithia V, Harisdangkul V (2006) Myasthenia gravis and systemic lupus erythematosus: truly associated or coincidental-two case reports and review of the literature. Clin Rheumatol 25(4):555-556 (Pubitemid 44137637)
42. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Domenech I, Aydintug AO, Jedryka-Goral A, de Ramon E et al (1993) Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1, 000 patients. The European working party on systemic lupus erythematosus. Medicine (Baltimore) 72(2):113-124 (Pubitemid 23097765)
43. Meriggioli MN, Sanders DB (2009) Autoimmune myasthenia gravis: emerging clinical and biological heterogeneity. Lancet Neurol 8(5):475-490. pii:S1474-4422(09)70063-8
44. Grob D, Brunner N, Namba T, Pagala M (2008) Lifetime course of myasthenia gravis. Muscle Nerve 37(2):141-149 (Pubitemid 351214160)
45. Mantegazza R, Baggi F, Antozzi C, Confalonieri P, Morandi L, Bernasconi P, Andreetta F, Simoncini O, Campanella A, Beghi E, Cornelio F (2003) Myasthenia gravis (MG): epidemiological data and prognostic factors. Ann NY Acad Sci 998:413-423 (Pubitemid 37194193)
46. Tsinzerling N, Lefvert AK, Matell G, Pirskanen-Matell R (2007) Myasthenia gravis: a long term follow-up study of Swedish patients with specific reference to thymic histology. J Neurol Neurosurg Psychiatry 78(10):1109-1112
47. Vincent A, Newsom-Davis J (1985) Acetylcholine receptor antibody as a diagnostic test for myasthenia gravis: results in 153 validated cases and 2967 diagnostic assays. J Neurol Neurosurg Psychiatry 48(12):1246-1252 (Pubitemid 16229407)
48. Oh SJ (2009) Muscle-specific receptor tyrosine kinase antibody positive myasthenia gravis current status. J Clin Neurol 5(2):53-64
49. (1999) The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42(4):599-608
50. Manoussakis MN, Georgopoulou C, Zintzaras E, Spyropoulou M, Stavropoulou A, Skopouli FN, Moutsopoulos HM (2004) Sjogren's syndrome associated with systemic lupus erythematosus: clinical and laboratory profiles and comparison with primary Sjogren's syndrome. Arthritis Rheum 50(3):882-891 (Pubitemid 38326189)
51. Xu D, Tian X, Zhang W, Zhang X, Liu B, Zhang F (2010) Sjogren's syndrome-onset lupus patients have distinctive clinical manifestations and benign prognosis: a case-control study. Lupus 19(2):197-200
52. Bagavant H, Thompson C, Ohno K, Setiady Y, Tung KS (2002) Differential effect of neonatal thymectomy on systemic and organ-specific autoimmune disease. Int Immunol 14(12):1397-1406 (Pubitemid 36024605)
53. Bagavant H, Tung KS (2005) Failure of CD25+ T cells from lupus-prone mice to suppress lupus glomerulonephritis and sialoadenitis. J Immunol 175(2):944-950 (Pubitemid 41094978)
54. Hang L, Theofilopoulos AN, Balderas RS, Francis SJ, Dixon FJ (1984) The effect of thymectomy on lupus-prone mice. J Immunol 132(4):1809-1813 (Pubitemid 14168141)
55. Steinberg AD, Law LD, Talal N (1970) The role of NZB-NZW F1 thymus in experimental tolerance and auto-immunity. Arthritis Rheum 13(4):369-377
56. Boonen A, Rennenberg R, van der Linden S (2000) Thymomaassociated systemic lupus erythematosus, exacerbating after thymectomy. A case report and review of the literature. Rheumatology (Oxford) 39(9):1044-1046
57. Bozzolo E, Bellone M, Quaroni N, Voci C, Sabbadini MG (2000) Thymoma associated with systemic lupus erythematosus and immunologic abnormalities. Lupus 9(2):151-154 (Pubitemid 30171115)
58. Balandina A, Lecart S, Dartevelle P, Saoudi A, Berrih-Aknin S (2005) Functional defect of regulatory CD4(?)CD25+ T cells in the thymus of patients with autoimmune myasthenia gravis. Blood 105(2):735-741 (Pubitemid 40070760)
59. Bonelli M, Smolen JS, Scheinecker C (2010) Treg and lupus. Ann Rheum Dis 69(Suppl 1):i65-i66
60. Meraouna A, Cizeron-Clairac G, Panse RL, Bismuth J, Truffault F, Tallaksen C, Berrih-Aknin S (2006) The chemokine CXCL13 is a key molecule in autoimmune myasthenia gravis. Blood 108(2):432-440 (Pubitemid 44061339)
61. Schiffer L, Kumpers P, Davalos-Misslitz AM, Haubitz M, Haller H, Anders HJ, Witte T, Schiffer M (2009) B-cell-attracting chemokine CXCL13 as a marker of disease activity and renal involvement in systemic lupus erythematosus (SLE). Nephrol Dial Transplant 24(12):3708-3712
62. Li LH, Li WX, Wu O, Zhang GQ, Pan HF, Li XP, Xu JH, Dai H, Ye DQ (2009) Fas expression on peripheral blood lymphocytes in systemic lupus erythematosus: relation to the organ damage and lymphocytes apoptosis. Mol Biol Rep 36(8):2047-2052
63. Moulian N, Bidault J, Truffault F, Yamamoto AM, Levasseur P, Berrih-Aknin S (1997) Thymocyte Fas expression is dysregulated in myasthenia gravis patients with anti-acetylcholine receptor antibody. Blood 89(9):3287-3295 (Pubitemid 27229814)
64. Stein M, Bell MJ, Ang LC (2000) Hydroxychloroquine neuromyotoxicity. J Rheumatol 27(12):2927-2931
65. Robberecht W, Bednarik J, Bourgeois P, van Hees J, Carton H (1989) Myasthenic syndrome caused by direct effect of chloroquine on neuromuscular junction. Arch Neurol 46(4):464-468 (Pubitemid 19099345)
66. Sghirlanzoni A, Mantegazza R, Mora M, Pareyson D, Cornelio F (1988) Chloroquine myopathy and myasthenia-like syndrome. Muscle Nerve 11(2):114-119 (Pubitemid 18039609)
67. Ritenour RJ, Cruess AF, Mishra AV (2008) Chloroquine-related myasthenic syndrome with severe retinopathy. Can J Ophthalmol 43(2):241-243 (Pubitemid 351518184)
68. De Bleecker J, De Reuck J, Quatacker J, Meire F (1991) Persisting chloroquine-induced myasthenia? Acta Clin Belg 46(6):401-406
69. Pichon P, Soichot P, Loche D, Chapelon M (1984) Myasthenic syndrome induced by chloroquine poisoning: an unusual clinical form confirmed by ocular involvement. Bull Soc Ophtalmol Fr 84 (2):219-222, 225
70. Schumm F, Wietholter H, Fateh-Moghadam A (1981) Myasthenia syndrome during chloroquine treatment (author's transl). Dtsch Med Wochenschr 106(51-52):1745-1747 (Pubitemid 12244411)