Myasthenia gravis, an autoimmune manifestation of lymphoma and lymphoproliferative disorders: Case reports and review of literature

Leukemia and Lymphoma

Volumn 53, Issue 3, 2012, Pages 371-380

  Rezania, Kourosh ^a   Soliven, Betty ^a   Baron, Joseph ^a   Lin, Helen ^a   Penumalli, Vikram ^a   Van Besien, Koen ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Alopecia areata; CLL; Lymphoma; Myasthenia gravis; Rituximab; Waldenstr m

Indexed keywords

AZATHIOPRINE; CD103 ANTIGEN; CD20 ANTIGEN; CHLORAMBUCIL; CHOLINERGIC RECEPTOR ANTIBODY; CLADRIBINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN; DOXORUBICIN; FLUDARABINE; IMMUNOGLOBULIN; IMMUNOGLOBULIN M ANTIBODY; PREDNISONE; PYRIDOSTIGMINE; RITUXIMAB; STEROID;

ADULT; ALOPECIA AREATA; ANTIBODY TITER; BONE MARROW BIOPSY; CASE REPORT; CHRONIC INFLAMMATORY DEMYELINATING POLYNEUROPATHY; COMPUTER ASSISTED TOMOGRAPHY; DIPLOPIA; DISEASE ASSOCIATION; DRUG HYPERSENSITIVITY; DRUG SAFETY; DYSARTHRIA; DYSPHAGIA; FATIGUE; FEMALE; FLOW CYTOMETRY; FOLLICULAR LYMPHOMA; GAZE; HAIR LOSS; HEART FAILURE; HUMAN; HUMAN TISSUE; LIMB WEAKNESS; LYMPHADENOPATHY; LYMPHOID CELL; MALE; MONOCLONAL IMMUNOGLOBULINEMIA; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; MULTIPLE CYCLE TREATMENT; MYASTHENIA GRAVIS; OPHTHALMOPLEGIA; ORBICULARIS OCULI MUSCLE; PLASMAPHERESIS; PRIORITY JOURNAL; PTOSIS; REVIEW; SEPSIS; SPLENOMEGALY; TENDON REFLEX; TREATMENT OUTCOME; TUMOR BIOPSY; WALDENSTROEM MACROGLOBULINEMIA;

2-CHLOROADENOSINE; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CYCLOPHOSPHAMIDE; CYCLOSPORINE; DEOXYADENOSINES; FATAL OUTCOME; FEMALE; HUMANS; LYMPHOMA; LYMPHOMA, FOLLICULAR; LYMPHOPROLIFERATIVE DISORDERS; MALE; MIDDLE AGED; MYASTHENIA GRAVIS; PARANEOPLASTIC SYNDROMES, NERVOUS SYSTEM; PREDNISONE; PYRIDOSTIGMINE BROMIDE; RECURRENCE; REMISSION INDUCTION; WALDENSTROM MACROGLOBULINEMIA;

EID: 84863156589     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.3109/10428194.2011.615426     Document Type: Review

References (94)

1. M acDonald BK, Cockerell OC, Sander JW., et al. Th e incidence and lifetime prevalence of neurological disorders in a prospective community-based study in the UK. Brain 2000;123:665-676. (Pubitemid 30162716)
2. H och W, McConville J, Helms S., et al. Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med 2001;7:365-368. (Pubitemid 32224355)
3. v an der Geld HW, Strauss AJ. Myasthenia gravis. Immunological relationship between striated muscle and thymus. Lancet 1966;1: 57-60.
4. G ilhus NE, Aarli JA, Matre R. Myasthenia gravis: The specifi cities of skeletal muscle and thymus antibodies. Acta Neurol Scand 1983;68: 328-336. (Pubitemid 14201750)
5. A tassi N, Amato AA. Muscle-specifi c kinase (MuSK) antibodyassociated myasthenia gravis after bone marrow transplantation. Muscle Nerve 2008;38:1074-1075.
6. Simon Z, Ress Z, Toldi J., et al. Rare association of Hodgkin lymphoma, Graves ' disease and myasthenia gravis complicated by postradiation neurofi brosarcoma: Coincidence or genetic susceptibility? Int J Hematol 2009;89:523-528.
7. Gilhus NE, Aarli JA, Matre R. Myasthenia gravis: diff erence between thymoma-associated antibodies and cross-striational skeletal muscle antibodies. Neurology 1984;34:246-249. (Pubitemid 14185380)
8. C ikes N, Momoi MY, Williams CL., et al. Striational autoantibodies: quantitative detection by enzyme immunoassay in myasthenia gravis, thymoma, and recipients of D-penicillamine or allogeneic bone marrow. Mayo Clin Proc 1988;63:474-481.
9. Williams CL, Hay JE, Huiatt TW., et al. Paraneoplastic IgG striational autoantibodies produced by clonal thymic B cells and in serum of patients with myasthenia gravis and thymoma react with titin. Lab Invest 1992;66:331-336.
10. Romi F, Skeie GO, Gilhus NE., et al. Striational antibodies in myasthenia gravis: Reactivity and possible clinical signifi cance. Arch Neurol 2005;62:442-446. (Pubitemid 40349480)
11. Castleman B. Th e pathology of the thymus gland in myasthenia gravis. Ann NY Acad Sci 1966;135:496-505.
12. Genkins G, Papatestas AE, Horowitz SH., et al. Studies in myasthenia gravis: Early thymectomy. Electrophysiologic and pathologic correlations. Am J Med 1975;58:517-524.
13. Conti-Fine BM, Milani M, Kaminski HJ. Myasthenia gravis: Past, present, and future. J. Clin. Invest. 2006;116:2843-2854. (Pubitemid 44684466)
14. Skeie GO, Romi F. Paraneoplastic myasthenia gravis: Immunological and clinical aspects. Eur. J. Neurol 2008;15:1029-1033.
15. Mackey JR, Desai S, Larratt L., et al. Myasthenia gravis in association with allogeneic bone marrow transplantation: Clinical observations, therapeutic implications and review of literature. BoneMarrow Transplant 1997;19:939-942. (Pubitemid 27217663)
16. Dowell JE, Moots PL, Stein RS. Myasthenia gravis after allogeneic bone marrow transplantation for lymphoblastic lymphoma. Bone Marrow Transplant 1999;24:1359-1361. (Pubitemid 30052795)
17. Vogel JM, Kornfeld P, Forte FA., et al. Myasthenia gravis: Association with chronic lymphocytic leukemia. NY State J Med 1977;77:2252-2256. (Pubitemid 8251735)
18. Fujimaki K, Takasaki H, Koharazawa H., et al. Idiopathic thrombocytopenic purpura and myasthenia gravis after fl udarabine treatment for chronic lymphocytic leukemia. Leuk Lymphoma 2005; 46:1101-1102. (Pubitemid 40975035)
19. Cohen SM, Waxman S. Myasthenia gravis, chronic lymphocytic leukemia, and autoimmune hemolytic anemia. A spectrum of thymic abnormalities? Arch Intern Med 1967;120:717-720.
20. Null JA, Livolsi VA, Glenn WW. Hodgkins disease of the thymus (granulomatous thymoma) and myasthenia gravis: A unique association. Am. J. Clin. Pathol. 1977;67:521-525. (Pubitemid 8131937)
21. Tranchant C, Racamier E, Warter JM. Seronegative myasthenia gravis and familial Hodgkins disease. Eur. Neurol. 1993;33:17-19. (Pubitemid 23081414)
22. Quilichini R, Fuentes P, Metge G., et al. [Myasthenic syndromedisclosing Hodgkin disease]. Rev Neurol (Paris) 1994;150:81-82.
23. Ferro MT, Riccardi T, Montanelli A., et al. Myasthenia gravis remission and anti-AChR ab reduction after immunosuppressive and anti-neoplastic therapy in a patient with thymic Hodgkins disease. J Neurol 2006;253:1241-1242. (Pubitemid 44511489)
24. A brey LE. Association of myasthenia gravis with extrathymic Hodgkins lymphoma: Complete resolution of myasthenic symptoms following antineoplastic therapy. Neurology 1995;45:1019.
25. Mohri H, Harano H, Okubo T. Concomitant association of myasthenia gravis and pure red cell aplasia after chemotherapy for Hodgkins disease. Am J Hematol 1997;54:343. (Pubitemid 27160879)
26. L iu KL, Herbrecht R, Tranchant C., et al. Malignant thymic lymphoblastic lymphoma and myasthenia gravis: An exceptional association. Nouv Rev Fr Hematol 1992;34:221-223.
27. B owen JD, Kidd P. Myasthenia gravis associated with T helper cell lymphoma. Neurology 1987;37:1405-1408.
28. M ortimer JE, Kidd P. Myasthenia gravis and lymphoblastic lymphoma antiacetylcholine receptor antibody as a tumor marker-a case report. Cancer Invest 1989;7:327-331. (Pubitemid 20063528)
29. S trauchen JA. Indolent T-lymphoblastic proliferation: Report of a case with an 11-year history and association with myasthenia gravis. Am. J. Surg. Pathol. 2001;25:411-415. (Pubitemid 32174212)
30. Uner AH, Abali H, Engin H., et al. Myasthenia gravis and lymphoblastic lymphoma involving the thymus: A rare association. Leuk Lymphoma 2001;42:527-531. (Pubitemid 32725611)
31. B artoloni C, Scoppetta C, Flamini G., et al. Waldenstrom ' s macroglobulinemia and myasthenia gravis. J Clin Lab Immunol 1981;6:275-278.
32. L in YT, Kuo HC, Chang YT., et al. Myasthenia gravis and Waldenstrom ' s macroglobulinemia: A case report and review of the literature. Acta Neurol Scand 2001;104:246-248.
33. D avis S, Schumacher MJ. Myasthenia gravis and lymphoma. A clinical and immunological association. JAMA 1979;242:2096-2097. (Pubitemid 10204055)
34. G ajra A, Vajpayee N, Grethlein SJ. Response of myasthenia gravis to rituximab in a patient with non-Hodgkin lymphoma. Am. J. Hematol. 2004;77:196-197. (Pubitemid 39281869)
35. T akagi K, Yoshida A, Iwasaki H., et al. Anti-CD20 antibody (rituximab) therapy in a myasthenia gravis patient with follicular lymphoma. Ann. Hematol. 2005;84:548-550. (Pubitemid 41001467)
36. Manckoundia P, Martin-Pfi tzenmeyer I, Pfi tzenmeyer P. Myasthenia gravis associated with a B-cell, non-Hodgkins lymphoma. Eur. J. Intern Med 2006;17:146. (Pubitemid 43265871)
37. M ontes M, Tomasi TB Jr, Noehren TH., et al. Lymphoid interstitial pneumonia with monoclonal gammopathy. Am Rev Respir Dis 1968;98:277-280.
38. G abrielli GB, Codella O, Capra F., et al. Pulmonary mucosaassociated lymphoid tissue lymphoma and myasthenia gravis. A case report. Haematologica 1998;83:381-382. (Pubitemid 28217864)
39. S ilberstein EB. Myasthenia gravis, haemolytic anaemia, and lymphoreticular malignancy. Br Med J 1970;3:445-446.
40. L evo Y, Kott E, Atsmon A. Association between myasthenia gravis and malignant lymphoma. Eur. Neurol. 1975;13:245-250.
41. R owland LP, Osserman EF, Scharfman WB., et al. Myasthenia gravis with a myeloma-type, gamma-G (IgG) immunoglobulin abnormality. Am J Med 1969;46:599-605.
42. F aure A, Gattegno L, Modigliani E., et al. Antibodies against myoid thymic cells and striated muscle, and monoclonal gammapathy in myasthenia gravis. Biomedicine 1975;23:241-245.
43. S omer H, Pirskanen R, Lefvert AK., et al. Myasthenia gravis and monoclonal IgG gammopathy. Neurology 1979;29:842-847. (Pubitemid 9160986)
44. G alli M, Landi G, Restelli DL., et al. Myasthenia gravis with a monoclonal gammopathy-report of a case. J Neurol Sci 1980;45: 103-108. (Pubitemid 10182133)
45. M ottier D, Fine JM, Youinou P., et al. [Myasthenia gravis and asymptomatic monoclonal gammapathy. Detection of autoantibody activity of the monoclonal immunoglobulin]. Rev Fr Transfus Immunohematol 1981;24:571-577.
46. P oloni M, Rocchelli B, Pinelli P., et al. Neuromuscular diseases associated with benign monoclonal gammopathy. Study of CSF and serum proteins by isoelectric focusing. Acta Neurol Scand 1982;65: 154-159. (Pubitemid 12183216)
47. S oppi E, Eskola J, Roytta M., et al. Th ymoma with immunodefi ciency (Good ' s syndrome) associated with myasthenia gravis and benign IgG gammopathy. Arch Intern Med 1985;145:1704-1707. (Pubitemid 16258214)
48. A hmed AR, Marchbank AJ, Nicholson AG., et al. Extramedullary plasmacytoma presenting with myasthenia gravis and mediastinal mass. Ann Th orac Surg 2000;70:1390-1392.
49. U rbanska-Rys H, Robak E, Kordek R., et al. Multiple myeloma in a patient with systemic lupus erythematosus, myasthenia gravis and non-familial diff use palmoplantar keratoderma. Leuk Lymphoma 2004;45:1913-1918. (Pubitemid 38997161)
50. M odigliani E, Charbord P, Landman C., et al. [Myasthenia with monoclonal kappa IgM gammapathy and presence of anti-striated muscle antibodies]. Ann Med Interne (Paris) 1973;124:193-200.
51. G oodnow CC. Multistep pathogenesis of autoimmune disease. Cell 2007;130:25-35. (Pubitemid 47031326)
52. Z intzaras E, Voulgarelis M, Moutsopoulos HM. Th e risk of lymphoma development in autoimmune diseases: A meta-analysis. Arch. Intern. Med. 2005;165:2337-2344. (Pubitemid 41640845)
53. M ackay IR, Rose NR. Autoimmunity and lymphoma: Tribulations of B cells. Nat Immunol 2001;2:793-795.
54. H ansen BA, Sorensen PS, Lauritzen MJ., et al. A case of malignant lymphoma and myasthenia gravis. Scand J Haematol 1983;31:155-160. (Pubitemid 13038238)
55. E hrenfeld M, Abu-Shakra M, Buskila D., et al. Th e dual association between lymphoma and autoimmunity. Blood Cells Mol Dis 2001; 27:750-756.
56. J ardin F, Levesque H, Tilly H. [Auto-immune manifestations in non-Hodgkins lymphoma]. Rev Med Interne 2005;26:557-571.
57. V aroczy L, Gergely L, Zeher M., et al. Malignant lymphomaassociated autoimmune diseases-a descriptive epidemiological study. Rheumatol Int 2002;22:233-237. (Pubitemid 35341019)
58. J onsson V, Wiik A, Hou-Jensen K., et al. Autoimmunity and extranodal lymphocytic infi ltrates in lymphoproliferative disorders. J Intern Med 1999;245:277-286. (Pubitemid 29132971)
59. J onsson V, Kierkegaard A, Salling S., et al. Autoimmunity in Waldenstrom ' s macroglobulinaemia. Leuk Lymphoma 1999;34:373-379.
60. Mihovilovic M, Denning S, Mai Y., et al. Th ymocytes and cultured thymic epithelial cells express transcripts encoding alpha-3, alpha-5, and beta-4 subunits of neuronal nicotinic acetylcholine receptors. Preferential transcription of the alpha-3 and beta-4 genes by immature CD4- 8- thymocytes and evidence for response to nicotine in thymocytes. Ann NY Acad Sci 1998;841:388-392.
61. N elson S, Conti-Tronconi BM. Adult thymus expresses an embryonic nicotinic acetylcholine receptor-like protein. J Neuroimmunol 1990;29:81-92. (Pubitemid 20283785)
62. H ohlfeld R, Wekerle H. Th e thymus in myasthenia gravis. Neurol Clin 1994;12:331-342. (Pubitemid 24160952)
63. Meriggioli MN, Sanders DB. Autoimmune myasthenia gravis: Emerging clinical and biological heterogeneity. Lancet Neurol 2009;8:475-490.
64. Lefvert AK, Bergstrom K, Matell G., et al. Determination of acetylcholine receptor antibody in myasthenia gravis: Clinical usefulness and pathogenetic implications. J Neurol Neurosurg Psychiatry 1978;41:394-403. (Pubitemid 8323892)
65. Eng H, Lefvert AK, Mellstedt H., et al. Human monoclonal immunoglobulins that bind the human acetylcholine receptor. Eur J. Immunol. 1987;17:1867-1869. (Pubitemid 18052060)
66. Avrameas S, Ternynck T. Th e natural autoantibodies system: between hypotheses and facts. Mol Immunol 1993;30:1133-1142.
67. S akaguchi S, Sakaguchi N, Shimizu J., et al. Immunologic tolerance maintained by CD25- CD4- regulatory T cells: Their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 2001;182:18-32. (Pubitemid 33070205)
68. L uther C, Adamopoulou E, Stoeckle C., et al. Prednisolone treatment induces tolerogenic dendritic cells and a regulatory milieu in myasthenia gravis patients. J. Immunol. 2009;183:841-848.
69. Z hang Y, Wang HB, Chi LJ., et al. Th e role of FoxP3 + CD4 + CD25hi Tregs in the pathogenesis of myasthenia gravis. Immunol Lett 2009;122:52-57.
70. Robak T, Blasinska-Morawiec M, Krykowski E., et al. Autoimmune haemolytic anaemia in patients with chronic lymphocytic leukaemia treated with 2-chlorodeoxyadenosine (cladribine). Eur. J. Haematol. 1997;58:109-113. (Pubitemid 27140396)
71. G ooptu C, Littlewood TJ, Frith P., et al. Paraneoplastic pemphigus: An association with fl udarabine? Br J Dermatol 2001;144:1255-1261.
72. Stern M, Buser AS, Lohri A., et al. Autoimmunity and malignancy in hematology-more than an association. Crit Rev Oncol Hematol 2007;63:100-110. (Pubitemid 46994748)
73. Suzuki S, Shimoda M, Kawamura M., et al. Myasthenia gravis accompanied by alopecia areata: Clinical and immunogenetic aspects. Eur. J. Neurol 2005;12:566-570. (Pubitemid 40956816)
74. Vincent A, Leite MI. Neuromuscular junction autoimmune disease: muscle specifi c kinase antibodies and treatments for myasthenia gravis. Curr Opin Neurol 2005;18:519-525. (Pubitemid 41476137)
75. Lennon VA, Kryzer TJ, Griesmann GE., et al. Calcium-channel antibodies in the Lambert-Eaton syndrome and other paraneoplastic syndromes. N. Engl. J. Med. 1995;332:1467-1474.
76. L iesveld JL, Stern A, Rosenthal SN. Myasthenic (Eaton-Lambert) syndrome in association with an indolent non-Hodgkins lymphoma. NY State J Med 1991;91:29-30.
77. Tyagi A, Connolly S, Hutchinson M. Lambert-Eaton myaesthenic syndrome: A possible association with Hodgkins lymphoma. Ir Med J 2001;94:18-19. (Pubitemid 32279581)
78. O ' Neill JH, Murray NM, Newsom-Davis J. Th e Lambert-Eaton myasthenic syndrome. A review of 50 cases. Brain 1988;111:577-596.
79. Vallat JM, De Mascarel HA, Bordessoule D., et al. Non-Hodgkin malignant lymphomas and peripheral neuropathies-13 cases. Brain 1995;118:1233-1245.
80. Terenghi F, Ardolino G, Nobile-Orazio E. Guillain-Barre syndrome after combined CHOP and rituximab therapy in non-Hodgkin lymphoma. J Peripher Nerv Syst 2007;12:142-143. (Pubitemid 46906337)
81. Kelly JJ, Karcher DS. Lymphoma and peripheral neuropathy: A clinical review. Muscle Nerve 2005;31:301-313. (Pubitemid 40261403)
82. Baehring JM, Damek D, Martin EC., et al. Neurolymphomatosis. Neuro Oncol 2003;5:104-115. (Pubitemid 36416839)
83. Bennett M, Berrebi A, Katz A. Myasthenia gravis and chronic lymphocytic leukaemia. Eur. J. Haematol. 1989;42:104.
84. R ichman DP, Agius MA. Treatment of autoimmune myasthenia gravis. Neurology 2003;61:1652-1661.
85. W ylam ME, Anderson PM, Kuntz NL., et al. Successful treatment of refractory myasthenia gravis using rituximab: A pediatric case report. J Pediatr 2003;143:674-677. (Pubitemid 37452801)
86. Z aja F, Russo D, Fuga G., et al. Rituximab for myasthenia gravis developing after bone marrow transplant. Neurology 2000;55:1062-1063.
87. Th akre M, Inshasi J, Marashi M. Rituximab in refractory MuSK antibody myasthenia gravis. J Neurol 2007;254:968-969. (Pubitemid 47222302)
88. H ain B, Jordan K, Deschauer M., et al. Successful treatment of MuSK antibody-positive myasthenia gravis with rituximab. Muscle Nerve 2006;33:575-580.
89. B aek WS, Bashey A, Sheean GL. Complete remission induced by rituximab in refractory, seronegative, muscle-specifi c, kinase-positive myasthenia gravis. J Neurol Neurosurg Psychiatry 2007;78:771. (Pubitemid 46998860)
90. Z ebardast N, Patwa HS, Novella SP., et al. Rituximab in the management of refractory myasthenia gravis. Muscle Nerve 2010; 41:375-378.
91. Nelson RP Jr, Pascuzzi RM, Kessler K., et al. Rituximab for the treatment of thymoma-associated and de novo myasthenia gravis: 3 cases and review. J Clin Neuromuscul Dis 2009;10: 170-177.
92. Rey J, Attarian S, Disdier P., et al. [Myasthenia gravis and chronic lymphocytic leukemia: A lucky association?]. Rev Med Interne 2001;22:1129-1130. (Pubitemid 33081272)
93. T alvalkar GV, Meher-Homji DR. Chronic lymphatic leukaemia associated with myasthenia gravis. Indian J Cancer 1968;5:114-119.
94. Simpson JA. Myasthenia gravis: A new hypothesis. Scott Med J 1960;5:419-436.