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ORIGINAL RESEARCH

Clinical Features and Prognostic Analysis of MuSK-Antibody-Positive Myasthenia Gravis versus Double-Seropositive Myasthenia Gravis: A Single-Center Study from Central South China

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Pages 725-735 | Received 02 Dec 2023, Accepted 13 Mar 2024, Published online: 29 Mar 2024

References

  • Gilhus NE, Tzartos S, Evoli A, Palace J, Burns TM, Verschuuren J. Myasthenia gravis. Nat Rev Dis Primers. 2019;5(1):30. doi:10.1038/s41572-019-0079-y
  • Vincent A, Leite MI. Neuromuscular junction autoimmune disease: muscle specific kinase antibodies and treatments for myasthenia gravis. Curr Opinion in Neurol. 2005;18(5):519–525. doi:10.1097/01.wco.0000180660.57801.3f
  • DeChiara TM, Bowen DC, Valenzuela DM, et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 1996;85(4):501–512. doi:10.1016/S0092-8674(00)81251-9
  • Kim N, Stiegler AL, Cameron TO, et al. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell. 2008;135(2):334–342. doi:10.1016/j.cell.2008.10.002
  • Kawakami Y, Ito M, Hirayama M, et al. Anti-MuSK autoantibodies block binding of collagen Q to MuSK. Neurology. 2011;77(20):1819–1826. doi:10.1212/WNL.0b013e318237f660
  • Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A. Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nature Med. 2001;7(3):365–368. doi:10.1038/85520
  • McConville J, Farrugia ME, Beeson D, et al. Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann Neurol. 2004;55(4):580–584. doi:10.1002/ana.20061
  • Klooster R, Plomp JJ, Huijbers MG, et al. Muscle-specific kinase myasthenia gravis IgG4 autoantibodies cause severe neuromuscular junction dysfunction in mice. Brain. 2012;135(Pt 4):1081–1101. doi:10.1093/brain/aws025
  • Fichtner ML, Jiang R, Bourke A, Nowak RJ, O’Connor KC. Autoimmune pathology in myasthenia gravis disease subtypes is governed by divergent mechanisms of immunopathology. Front Immunol. 2020;11:776. doi:10.3389/fimmu.2020.00776
  • Vergoossen DLE, Plomp JJ, Gstöttner C, et al. Functional monovalency amplifies the pathogenicity of anti-MuSK IgG4 in myasthenia gravis. Proc Natl Acad Sci USA. 2021;118(13). doi:10.1073/pnas.2020635118
  • Koneczny I, Stevens JAA, De Rosa A, et al. IgG4 autoantibodies against muscle-specific kinase undergo Fab-arm exchange in myasthenia gravis patients. J Autoimmun. 2017;77:104–115. doi:10.1016/j.jaut.2016.11.005
  • Evoli A, Tonali PA, Padua L, et al. Clinical correlates with anti-MuSK antibodies in generalized seronegative myasthenia gravis. Brain. 2003;126(Pt 10):2304–2311. doi:10.1093/brain/awg223
  • König N, Stetefeld HR, Dohmen C, et al. MuSK-antibodies are associated with worse outcome in myasthenic crisis requiring mechanical ventilation. J Neurol. 2021;268(12):4824–4833. doi:10.1007/s00415-021-10603-9
  • Farrugia ME, Robson MD, Clover L, et al. MRI and clinical studies of facial and bulbar muscle involvement in MuSK antibody-associated myasthenia gravis. Brain. 2006;129(Pt 6):1481–1492. doi:10.1093/brain/awl095
  • Modoni A, Mastrorosa A, Spagni G, Evoli A. Cholinergic hyperactivity in patients with myasthenia gravis with MuSK antibodies: a neurophysiological study. Clin Neurophysiol. 2021;132(8):1845–1849. doi:10.1016/j.clinph.2021.04.019
  • Leite MI, Ströbel P, Jones M, et al. Fewer thymic changes in MuSK antibody-positive than in MuSK antibody-negative MG. Ann Neurol. 2005;57(3):444–448. doi:10.1002/ana.20386
  • Clifford KM, Hobson-Webb LD, Benatar M, et al. Thymectomy may not be associated with clinical improvement in MuSK myasthenia gravis. Muscle and Nerve. 2019;59(4):404–410. doi:10.1002/mus.26404
  • Hehir MK, Hobson-Webb LD, Benatar M, et al. Rituximab as treatment for anti-MuSK myasthenia gravis: multicenter blinded prospective review. Neurology. 2017;89(10):1069–1077. doi:10.1212/WNL.0000000000004341
  • Zhou Y, Yan C, Gu X, et al. Short-term effect of low-dose rituximab on myasthenia gravis with muscle-specific tyrosine kinase antibody. Muscle and Nerve. 2021;63(6):824–830.
  • Di Stefano V, Lupica A, Rispoli MG, Di Muzio A, Brighina F, Rodolico C. Rituximab in AChR subtype of myasthenia gravis: systematic review. J Neurol Neurosurg. 2020;91(4):392–395. doi:10.1136/jnnp-2019-322606
  • Sanders DB, Wolfe GI, Benatar M, et al. International consensus guidance for management of myasthenia gravis: executive summary. Neurology. 2016;87(4):419–425. doi:10.1212/WNL.0000000000002790
  • Dalakas MC. IgG4-mediated neurologic autoimmunities: understanding the pathogenicity of IgG4, ineffectiveness of IVIg, and long-lasting benefits of anti-B cell therapies. Neurol Neuroimmunol Neuroinflam. 2022;9(1):e1116.
  • Yeh JH, Chen WH, Chiu HC, Vincent A. Low frequency of MuSK antibody in generalized seronegative myasthenia gravis among Chinese. Neurology. 2004;62(11):2131–2132. doi:10.1212/01.WNL.0000128042.28877.C3
  • Li Z, Zhang C, Chang T, et al. A multicentre, prospective, double-blind study comparing the accuracy of autoantibody diagnostic assays in myasthenia gravis: the SCREAM study. Lancet Reg Health West Pac. 2023;38:100846. doi:10.1016/j.lanwpc.2023.100846
  • Zhou Y, Chen J, Li Z, et al. Clinical features of myasthenia gravis with antibodies to MuSK based on age at onset: a multicenter retrospective study in China. Front Neurol. 2022;13:879261. doi:10.3389/fneur.2022.879261
  • Zhang Z, Guan Y, Han J, Li M, Shi M, Deng H. Regional features of MuSK antibody-positive myasthenia gravis in Northeast China. Front Neurol. 2020;11:516211. doi:10.3389/fneur.2020.516211
  • Zhao S, Zhang K, Ren K, et al. Clinical features, treatment and prognosis of MuSK antibody-associated myasthenia gravis in Northwest China: a single-centre retrospective cohort study. BMC Neurol. 2021;21(1):428. doi:10.1186/s12883-021-02439-7
  • Huang Q, Li F, Zhao S. Spotlight on MuSK positive myasthenia gravis: clinical characteristics, treatment and outcomes. BMC Neurol. 2022;22(1):73. doi:10.1186/s12883-022-02593-6
  • Seth V, Kushwaha S, Bapat P, Rajashekar K, Grover D. Is double-seropositive myasthenia gravis a distinct subtype? Acta Neurologica Belgica. 2023;123(1):251–252. doi:10.1007/s13760-021-01759-2
  • Zhang J, Chen Y, Chen J, et al. AChRAb and MuSKAb double-seropositive myasthenia gravis: a distinct subtype? Neurol Sci. 2021;42(3):863–869. doi:10.1007/s10072-021-05042-3
  • Li M, Ren L, Zhang Y, et al. Clinical characteristics of AChRAb and MuSKAb double seropositive myasthenia gravis patients. Clin Neurol Neurosurg. 2018;172:69–73. doi:10.1016/j.clineuro.2018.06.041
  • Zouvelou V, Zisimopoulou P, Psimenou E, Matsigkou E, Stamboulis E, Tzartos SJ. AChR-myasthenia gravis switching to double-seropositive several years after the onset. J Neuroimmunol. 2014;267(1–2):111–112. doi:10.1016/j.jneuroim.2013.12.012
  • Jordan B, Schilling S, Zierz S. Switch to double positive late onset MuSK myasthenia gravis following thymomectomy in paraneoplastic AChR antibody positive myasthenia gravis. J Neurol. 2016;263(1):174–176. doi:10.1007/s00415-015-7982-2
  • Lu Y, Ran H, Yang W, et al. AChR myasthenia gravis switching to MuSK or double antibody positive myasthenia gravis in two children and literature review. Neuromusc disord. 2020;30(7):534–538. doi:10.1016/j.nmd.2020.03.012
  • Muppidi S, Silvestri NJ, Tan R, Riggs K, Leighton T, Phillips GA. Utilization of MG-ADL in myasthenia gravis clinical research and care. Muscle and Nerve. 2022;65(6):630–639. doi:10.1002/mus.27476
  • Jaretzki A, Barohn RJ, Ernstoff RM, et al. Myasthenia gravis: recommendations for clinical research standards. Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America. Neurology. 2000;55(1):16–23. doi:10.1212/WNL.55.1.16
  • Hothorn T, Lausen B. Maximally selected rank statistics in R. R News. 2002;2(1):3–5.
  • Qiu P, Sheng J. A two-stage procedure for comparing hazard rate functions. J Royal Stat Soci Ser B. 2008;70(1):191–208. doi:10.1111/j.1467-9868.2007.00622.x
  • Evoli A, Alboini PE, Iorio R, Damato V, Bartoccioni E. Pattern of ocular involvement in myasthenia gravis with MuSK antibodies. J Neurol Neurosurg. 2017;88(9):761–763. doi:10.1136/jnnp-2017-315782
  • Frampton JE. Inebilizumab: first Approval. Drugs. 2020;80(12):1259–1264. doi:10.1007/s40265-020-01370-4
  • Howard JF, Bril V, Vu T, et al. Safety, efficacy, and tolerability of efgartigimod in patients with generalised myasthenia gravis (ADAPT): a multicentre, randomised, placebo-controlled, Phase 3 trial. Lancet Neurol. 2021;20(7):526–536. doi:10.1016/S1474-4422(21)00159-9
  • Zhang Z, Wang Z, Du X, Huang X, Zhang Y. Refractory generalized myasthenia gravis treated successfully with telitacicept: two cases report. J Neurol. 2024;271(1):584–588. doi:10.1007/s00415-023-12036-y
  • Di Stefano V, Alonge P, Rini N, et al. Efgartigimod beyond myasthenia gravis: the role of FcRn-targeting therapies in stiff-person syndrome. J Neurol. 2024;271(1):254–262. doi:10.1007/s00415-023-11970-1
  • Poulas K, Koutsouraki E, Kordas G, Kokla A, Tzartos SJ. Anti-MuSK- and anti-AChR-positive myasthenia gravis induced by d-penicillamine. J Neuroimmunol. 2012;250(1–2):94–98. doi:10.1016/j.jneuroim.2012.05.011
  • Zouvelou V, Psimenou E. AChR-and MuSK-positive myasthenia gravis: double trouble. J Neuroimmunol. 2020;348:577364. doi:10.1016/j.jneuroim.2020.577364
  • Rajakulendran S, Viegas S, Spillane J, Howard RS. Clinically biphasic myasthenia gravis with both AChR and MuSK antibodies. J Neurol. 2012;259(12):2736–2739. doi:10.1007/s00415-012-6661-9
  • Zouvelou V, Michail M, Belimezi M, Zisimopoulou P. Subunit specificity of the acetylcholine receptor antibodies in double seropositive myasthenia gravis. Muscle and Nerve. 2021;63(4):E36–E37. doi:10.1002/mus.27177
  • Tan Y, Shi J, Huang Y, et al. Long-term efficacy of non-steroid immunosuppressive agents in anti-muscle-specific kinase positive myasthenia gravis patients: a prospective study. Front Neurol. 2022;13:877895. doi:10.3389/fneur.2022.877895
  • Tomschik M, Hilger E, Rath J, et al. Subgroup stratification and outcome in recently diagnosed generalized myasthenia gravis. Neurology. 2020;95(10):e1426–e1436. doi:10.1212/WNL.0000000000010209