Neuromyelitis optica spectrum disorders in patients with myasthenia gravis: Ten new aquaporin-4 antibody positive cases and a review of the literature

Multiple Sclerosis Journal

Volumn 18, Issue 8, 2012, Pages 1135-1143

  Jarius, S ^a   Paul, F ^b   Franciotta, D ^c   De Seze, J ^d   Munch C ^b   Salvetti, M ^e   Ruprecht, K ^b   Liebetrau, M ^f   Wandinger, K P ^g,h   Akman Demir, G ⁱ   Melms, A ^j   Kristoferitsch, W ^k   Wildemann, B ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f DR HORST SCHMIDT KLINIKEN   (Germany)

^g UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^h Institute for Experimental Immunology   (Germany)

ⁱ ISTANBUL UNIVERSITY   (Turkey)

^j UNIVERSITY OF TÜBINGEN   (Germany)

^k DANUBE HOSPITAL   (Austria)

more..

Author keywords

Acetylcholine receptor antibody (AchR Ab); aquaporin 4 antibody (AQP4 Ab); longitudinally extensive transverse myelitis; myasthenia gravis; neuromyelitis optica (Devic disease); NMO IgG; optic neuritis; thymectomy

Indexed keywords

AQUAPORIN 4 ANTIBODY; PYRIDOSTIGMINE;

ADULT; ARTICLE; CAUCASIAN; CLINICAL ARTICLE; DISEASE ASSOCIATION; DISEASE CONTROL; FEMALE; FOLLOW UP; HUMAN; MALE; MYASTHENIA GRAVIS; MYELOOPTIC NEUROPATHY; REMISSION; RETROSPECTIVE STUDY; THYMECTOMY;

EID: 84864124795     PISSN: 13524585     EISSN: 14770970     Source Type: Journal    
DOI: 10.1177/1352458511431728     Document Type: Article

References (60)

1. Wingerchuk DM, Hogancamp WF, O'Brien PC, Weinshenker BG. The clinical course of neuromyelitis optica (Devic's syndrome). Neurology. 1999 ; 53: 1107-1114
2. Cree BA, Goodin DS, Hauser SL. Neuromyelitis optica. Semin Neurol. 2002 ; 22: 105-122
3. Jarius S, Paul F, Franciotta D, Waters P, Zipp F, Hohlfeld R, et al. Mechanisms of Disease: aquaporin-4 antibodies in neuromyelitis optica. Nat Clin Pract Neurol. 2008 ; 4: 202-214
4. Jarius S, Wildemann B. AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat Rev Neurol. 2010 ; 6: 383-392
5. de Seze J, Stojkovic T, Ferriby D, Gauvrit JY, Montagne C, Mounier-Vehier F, et al. Devic's neuromyelitis optica: clinical, laboratory, MRI and outcome profile. J Neurol Sci. 2002 ; 197: 57-61
6. Jarius S, Franciotta D, Bergamaschi R, Wright H, Littleton E, Palace J, et al. NMO-IgG in the diagnosis of neuromyelitis optica. Neurology. 2007 ; 68: 1076-1077
7. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet. 2004 ; 364: 2106-2112
8. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med. 2005 ; 202: 473-477
9. Paul F, Jarius S, Aktas O, Bluthner M, Bauer O, Appelhans H, et al. Antibody to aquaporin 4 in the diagnosis of neuromyelitis optica. PLoS Med. 2007 ; 4: e133
10. Bradl M, Misu T, Takahashi T, Watanabe M, Mader S, Reindl M, et al. Neuromyelitis optica: Pathogenicity of patient immunoglobulin in vivo. Ann Neurol. 2009 ; 66: 630-643
11. Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009 ; 66: 617-629
12. Saadoun S, Waters P, Bell BA, Vincent A, Verkman AS, Papadopoulos MC. Intra-cerebral injection of neuromyelitis optica immunoglobulin G and human complement produces neuromyelitis optica lesions in mice. Brain. 2010 ; 133: 349-361
13. Jarius S, Aboul-Enein F, Waters P, Kuenz B, Hauser A, Berger T, et al. Antibody to aquaporin-4 in the long-term course of neuromyelitis optica. Brain. 2008 ; 131: 3072-3080
14. Wandinger KP, Stangel M, Witte T, Venables P, Charles P, Jarius S, et al. Autoantibodies against aquaporin-4 in patients with neuropsychiatric systemic lupus erythematosus and primary Sjogren's syndrome. Arthritis Rheum. 2010 ; 62: 1198-1200
15. Pittock SJ, Lennon VA, de Seze J, Vermersch P, Homburger HA, Wingerchuk DM, et al. Neuromyelitis optica and non organ-specific autoimmunity. Arch Neurol. 2008 ; 65: 78-83
16. Jarius S, Jacobi C, de Seze J, Zephir H, Paul F, Franciotta D, et al. Frequency and syndrome specificity of antibodies to aquaporin-4 in neurological patients with rheumatic disorders. Mult Scler. 2011 ; 17: 1067-1073
17. Weinshenker BG, Wingerchuk DM, Vukusic S, Linbo L, Pittock SJ, Lucchinetti CF, et al. Neuromyelitis optica IgG predicts relapse after longitudinally extensive transverse myelitis. Ann Neurol. 2006 ; 59: 566-569
18. Jarius S, Frederikson J, Waters P, Paul F, Akman-Demir G, Marignier R, et al. Frequency and prognostic impact of antibodies to aquaporin-4 in patients with optic neuritis. J Neurol Sci. 2010 ; 298: 158-162
19. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology. 2006 ; 66: 1485-1489
20. Antoine JC, Camdessanche JP, Absi L, Lassabliere F, Feasson L. Devic disease and thymoma with anti-central nervous system and antithymus antibodies. Neurology. 2004 ; 62: 978-980
21. Bichuetti DB, Barros TM, Oliveira EM, Annes M, Gabbai AA. Demyelinating disease in patients with myasthenia gravis. Arq Neuropsiquiatr. 2008 ; 66: 5-7
22. Furukawa Y, Yoshikawa H, Yachie A, Yamada M. Neuromyelitis optica associated with myasthenia gravis: characteristic phenotype in Japanese population. Eur J Neurol. 2006 ; 13: 655-658
23. Ikeda K, Araki Y, Iwasaki Y. Occurrence of CNS demyelinating disease in patients with myasthenia gravis. Neurology. 2007 ; 68: 1326
24. Isbister CM, Mackenzie PJ, Anderson D, Wade NK, Oger J. Co-occurrence of multiple sclerosis and myasthenia gravis in British Columbia. Mult Scler. 2003 ; 9: 550-553
25. Nakamura M, Nakashima I, Sato S, Miyazawa I, Fujihara K, Itoyama Y. Clinical and laboratory features of neuromyelitis optica with oligoclonal IgG bands. Mult Scler. 2007 ; 13: 332-335
26. Kay CS, Scola RH, Lorenzoni PJ, Jarius S, Arruda WO, Werneck LC. NMO-IgG positive neuromyelitis optica in a patient with myasthenia gravis but no thymectomy. J Neurol Sci. 2008 ; 275: 148-150
27. Uzawa A, Mori M, Iwai Y, Kobayashi M, Hayakawa S, Kawaguchi N, et al. Association of anti-aquaporin-4 antibody-positive neuromyelitis optica with myasthenia gravis. J Neurol Sci. 2009 ; 287: 105-107
28. Kister I, Gulati S, Boz C, Bergamaschi R, Piccolo G, Oger J, et al. Neuromyelitis optica in patients with myasthenia gravis who underwent thymectomy. Arch Neurol. 2006 ; 63: 851-856
29. Gotkine M, Fellig Y, Abramsky O. Occurrence of CNS demyelinating disease in patients with myasthenia gravis. Neurology. 2006 ; 67: 881-883.30
30. O'Riordan JI, Gallagher HL, Thompson AJ, Howard RS, Kingsley DP, Thompson EJ, et al. Clinical, CSF, and MRI findings in Devic's neuromyelitis optica. J Neurol Neurosurg Psychiatry. 1996 ; 60: 382-387
31. Waters P, Jarius S, Littleton E, Leite MI, Jacob S, Gray B, et al. Aquaporin-4 antibodies in neuromyelitis optica and longitudinally extensive transverse myelitis. Arch Neurol. 2008 ; 65: 913-919
32. Chan KH, Kwan JS, Ho PW, Ho JW, Chu AC, Ramsden DB. Aquaporin-4 autoantibodies in neuromyelitis optica spectrum disorders: comparison between tissue-based and cell-based indirect immunofluorescence assays. J Neuroinflamm. 2010 ; 7: 50
33. Takahashi T, Fujihara K, Nakashima I, Misu T, Miyazawa I, Nakamura M, et al. Anti-aquaporin-4 antibody is involved in the pathogenesis of NMO: a study on antibody titre. Brain. 2007 ; 130: 1235-1243
34. Jarius S, Probst C, Borowski K, Franciotta D, Wildemann B, Stoecker W, et al. Standardized method for the detection of antibodies to aquaporin-4 based on a highly sensitive immunofluorescence assay employing recombinant target antigen. J Neurol Sci. 2010 ; 291: 52-56
35. Jarius S, Franciotta D, Paul F, Ruprecht K, Bergamaschi R, Rommer PS, et al. Cerebrospinal fluid antibodies to aquaporin-4 in neuromyelitis optica and related disorders: frequency, origin, and diagnostic relevance. J Neuroinflamm. 2010 ; 7: 52
36. Jarius S, Paul F, Franciotta D, Ruprecht K, Ringelstein M, Bergamaschi R, et al. Cerebrospinal fluid findings in aquaporin-4 antibody positive neuromyelitis optica: Results from 211 lumbar punctures. J Neurol Sci. 2011 ; 306: 82-90
37. Asgari N, Lillevang ST, Skejoe HP, Falah M, Stenager E, Kyvik KO. A population-based study of neuromyelitis optica in Caucasians. Neurology. 2011 ; 76: 1589-1595
38. Carr AS, Cardwell CR, McCarron PO, McConville J. A systematic review of population based epidemiological studies in myasthenia gravis. BMC Neurol. 2010 ; 10: 46
39. Mantegazza R, Baggi F, Antozzi C, Confalonieri P, Morandi L, Bernasconi P, et al. Myasthenia gravis (MG): epidemiological data and prognostic factors. Ann N Y Acad Sci. 2003 ; 998: 413-423
40. Aarli JA, Romi F, Skeie GO, Gilhus NE. Myasthenia gravis in individuals over 40. Ann N Y Acad Sci. 2003 ; 998: 424-431
41. Christensen PB, Jensen TS, Tsiropoulos I, Sorensen T, Kjaer M, Hojer-Pedersen E, et al. Incidence and prevalence of myasthenia gravis in western Denmark: 1975 to 1989. Neurology. 1993 ; 43: 1779-1783
42. Wingerchuk DM. Neuromyelitis optica: Effect of gender. J Neurol Sci. 2009 ; 286: 18-23
43. McGrogan A, Sneddon S, de Vries CS. The incidence of myasthenia gravis: a systematic literature review. Neuroepidemiology. 2010 ; 34: 171-183
44. Mevorach D, Perrot S, Buchanan N, Khamashta M, Laoussadi S, Hughes G, et al. Appearance of systemic lupus erythematosus after thymectomy: four case reports and review of the literature. Lupus. 1995 ; 4: 33-37
45. Sant S. Systemic lupus erythematosus after thymectomy in a patient with myasthenia gravis. Ir Med J. 1997 ; 90: 116-118
46. Zonana M, Reyes E, Weisman A. Coexistence of four autoimmune diseases in one patient: the kaleidoscope of autoimmunity. J Clin Rheumatol. 2002 ; 8: 322-325
47. Rosman A, Atsumi T, Khamashta M, Ames P, Hughes G. Development of systemic lupus erythematosus after chemotherapy and radiotherapy for malignant thymoma. Br J Rheumatol. 1995 ; 34: 1175-1176
48. Gerli R, Paganelli R, Cossarizza A, Muscat C, Piccolo G, Barbieri D, et al. Long-term immunologic effects of thymectomy in patients with myasthenia gravis. J Allergy Clin Immunol. 1999 ; 103: 865-872
49. Parambil J, Keogh K, Fervenza F, Ryu J. Microscopic polyangiitis associated with thymoma, exacerbating after thymectomy. Am J Kidney Dis. 2006 ; 48: 827-831
50. Suzuki S, Shimoda M, Kawamura M, Sato H, Nogawa S, Tanaka K, et al. Myasthenia gravis accompanied by alopecia areata: clinical and immunogenetic aspects. Eur J Neurol. 2005 ; 12: 566-570
51. Wakata N, Kiyozuka T, Konno S, Nakazora H, Nomoto N, Sugimoto H, et al. Autoimmune thrombocytopenic purpura, autoimmune hemolytic anemia and gastric cancer appeared in a patient with myasthenia gravis. Intern Med. 2006 ; 45: 479-481
52. Gonlugur U, Sahin E, Yildiz E, Gonlugur TE. Early autoimmune complications after thymomectomy in a patient with interstitial lung disease. Case report. Acta Microbiol Immunol Hung. 2006 ; 53: 105-111
53. Kojima A, Prehn R. Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics. 1981 ; 14: 15-27
54. Itoh M, Takahashi T, Sakaguchi N, Kuniyasu Y, Shimizu J, Otsuka F, et al. Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol. 1999 ; 162: 5317-5326
55. Asano M, Toda M, Sakaguchi N, Sakaguchi S. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med. 1996 ; 184: 387-396
56. Chi Y, Fan Y, He L, Liu W, Wen X, Zhou S, et al. Novel role of aquaporin-4 in CD4(+) CD25(+) T regulatory cell development and severity of Parkinson's disease. Aging Cell. 2011 ; 10: 368-382
57. Barrett S, Toh B, Alderuccio F, van Driel I, Gleeson P. Organ-specific autoimmunity induced by adult thymectomy and cyclophosphamide-induced lymphopenia. Eur J Immunol. 1995 ; 25: 238-244
58. Schulze-Koops H. Lymphopenia and autoimmune diseases. Arthritis Res Ther. 2004 ; 6: 178-180
59. Chan KH, Kwan JS, Ho PW, Ho SL, Chui WH, Chu AC, et al. Aquaporin-4 water channel expression by thymoma of patients with and without myasthenia gravis. J Neuroimmunol. 2010 ; 227: 178-184
60. Pittock SJ, Lennon VA. Aquaporin-4 autoantibodies in a paraneoplastic context. Arch Neurol. 2008 ; 65: 629-632