Rituximab as a sole steroid-sparing agent in generalized myasthenia gravis: Long-term outcomes.

COVID-19 Long-term Myasthenia gravis Refractory Rituximab

Journal

Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175

Informations de publication

Date de publication:
13 Oct 2023
Historique:
received: 14 07 2023
accepted: 16 09 2023
medline: 13 10 2023
pubmed: 13 10 2023
entrez: 13 10 2023
Statut: aheadofprint

Résumé

Rituximab, a B-cell depleting monoclonal antibody, represents an option for the treatment of refractory myasthenia gravis (MG). Its use is more established in muscle-specific tyrosine kinase positive (MuSK +) patients, while its role in managing acetylcholine receptor positive (AChR +), or double seronegative (DSN) patients, remains less clear. This study evaluates the long-term effectiveness and safety of rituximab in MG of various serotypes. We conducted an open-label study of MG patients receiving rituximab. Adults with generalized refractory MG, either anti-AChR + or DSN, and anti-MuSK + , refractory or not, who had follow-up > 12 months were selected. Change in quantitative myasthenia gravis (QMG) score at last follow-up, compared with baseline was a primary outcome, as well as factors affecting response to treatment. Secondary outcomes included, long-term safety, the steroid-sparing effect and relapse rates post-rituximab. Thirty patients (16 anti-AChR + , 6 anti-MuSK + , 8 DSN) followed for a mean of 33.3 months were included. Mean scores pre-rituximab compared to last follow-up significantly decreased (p < 0.001), from 11 ± 4.1 to 4.3 ± 3.8, and from 1.9 to 0.3 regarding QMG and relapse rate per patient/year, respectively, while in 93.1% a daily steroid dose ≤ 10 mg was achieved. Antibody status was the only factor independently influencing several endpoints. Throughout the study period no crises or deaths occurred. The present study supports that rituximab is an effective and well tolerated treatment for refractory anti-AChR + and DSN MG patients, while anti-MuSK + remains the group experiencing the greater benefits.

Sections du résumé

BACKGROUND BACKGROUND
Rituximab, a B-cell depleting monoclonal antibody, represents an option for the treatment of refractory myasthenia gravis (MG). Its use is more established in muscle-specific tyrosine kinase positive (MuSK +) patients, while its role in managing acetylcholine receptor positive (AChR +), or double seronegative (DSN) patients, remains less clear. This study evaluates the long-term effectiveness and safety of rituximab in MG of various serotypes.
METHODS METHODS
We conducted an open-label study of MG patients receiving rituximab. Adults with generalized refractory MG, either anti-AChR + or DSN, and anti-MuSK + , refractory or not, who had follow-up > 12 months were selected. Change in quantitative myasthenia gravis (QMG) score at last follow-up, compared with baseline was a primary outcome, as well as factors affecting response to treatment. Secondary outcomes included, long-term safety, the steroid-sparing effect and relapse rates post-rituximab.
RESULTS RESULTS
Thirty patients (16 anti-AChR + , 6 anti-MuSK + , 8 DSN) followed for a mean of 33.3 months were included. Mean scores pre-rituximab compared to last follow-up significantly decreased (p < 0.001), from 11 ± 4.1 to 4.3 ± 3.8, and from 1.9 to 0.3 regarding QMG and relapse rate per patient/year, respectively, while in 93.1% a daily steroid dose ≤ 10 mg was achieved. Antibody status was the only factor independently influencing several endpoints. Throughout the study period no crises or deaths occurred.
CONCLUSION CONCLUSIONS
The present study supports that rituximab is an effective and well tolerated treatment for refractory anti-AChR + and DSN MG patients, while anti-MuSK + remains the group experiencing the greater benefits.

Identifiants

pubmed: 37831214
doi: 10.1007/s10072-023-07082-3
pii: 10.1007/s10072-023-07082-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. Fondazione Società Italiana di Neurologia.

Références

Gilhus NE (2016) Myasthenia Gravis. N Engl J Med 375:2570–2581. https://doi.org/10.1056/NEJMra1602678
doi: 10.1056/NEJMra1602678 pubmed: 28029925
Rodolico C, Nicocia G, Damato V, Antonini G, Liguori R, Evoli A (2021) Benefit and danger from immunotherapy in myasthenia gravis. Neurol Sci 42(4):1367–1375. https://doi.org/10.1007/s10072-021-05077-6
doi: 10.1007/s10072-021-05077-6 pubmed: 33543421 pmcid: 7861968
Narayanaswami P, Sanders DB, Wolfe G et al (2021) International Consensus Guidance for Management of Myasthenia Gravis: 2020 Update. Neurology 96:114–122. https://doi.org/10.1212/WNL.0000000000011124
doi: 10.1212/WNL.0000000000011124 pubmed: 33144515 pmcid: 7884987
Mantegazza R, Antozzi C (2018) When myasthenia gravis is deemed refractory: clinical signposts and treatment strategies. Ther Adv Neurol Disord 11:1756285617749134. https://doi.org/10.1177/1756285617749134
doi: 10.1177/1756285617749134 pubmed: 29403543 pmcid: 5791553
Cortes-Vicente E, Alvarez-Velasco R, Pla-Junca F et al (2022) Drug-refractory myasthenia gravis: Clinical characteristics, treatments, and outcome. Ann Clin Transl Neurol 9:122–131. https://doi.org/10.1002/acn3.51492
doi: 10.1002/acn3.51492 pubmed: 35080153 pmcid: 8862423
Gilhus NE, Verschuuren JJ (2015) Myasthenia Gravis: Subgroup Classification and Therapeutic Strategies. Lancet Neurol 14:1023–1036. https://doi.org/10.1016/S1474-4422(15)00145-3
doi: 10.1016/S1474-4422(15)00145-3 pubmed: 26376969
Hehir MK, Hobson-Webb LD, Benatar M et al (2017) Rituximab as treatment for anti-MuSK myasthenia gravis: Multicenter blinded prospective review. Neurology 89:1069–1077. https://doi.org/10.1212/WNL.0000000000004341
doi: 10.1212/WNL.0000000000004341 pubmed: 28801338
Morren J, Li Y (2018) Myasthenia gravis with muscle-specific tyrosine kinase antibodies: A narrative review. Muscle Nerve 58:344–358. https://doi.org/10.1002/mus.26107
doi: 10.1002/mus.26107 pubmed: 29461627
Dos Santos A, Noury JB, Genestet S et al (2020) Efficacy and safety of rituximab in myasthenia gravis: a French multicentre real-life study. Eur J Neurol 27:2277–2285. https://doi.org/10.1111/ene.14391
doi: 10.1111/ene.14391 pubmed: 32526053
Di Stefano V, Lupica A, Rispoli MG, Di Muzio A, Brighina F, Rodolico C (2020) Rituximab in AChR subtype of myasthenia gravis: systematic review. J Neurol Neurosurg Psychiatry 91:392–395. https://doi.org/10.1136/jnnp-2019-322606
doi: 10.1136/jnnp-2019-322606 pubmed: 32098874
Zhao C, Pu M, Chen D et al (2021) Effectiveness and Safety of Rituximab for Refractory Myasthenia Gravis: A Systematic Review and Single-Arm Meta-Analysis. Front Neurol 12:736190. https://doi.org/10.3389/fneur.2021.736190
doi: 10.3389/fneur.2021.736190 pubmed: 34721267 pmcid: 8548630
Nowak RJ, Coffey CS, Goldstein JM et al (2021) Phase 2 Trial of Rituximab in Acetylcholine Receptor Antibody-Positive Generalized Myasthenia Gravis: The BeatMG Study. Neurology 98(4):e376–e389. https://doi.org/10.1212/WNL.0000000000013121
doi: 10.1212/WNL.0000000000013121 pubmed: 34857535
Siddiqi ZA, Khan W, Hussain FS (2021) Rituximab in Myasthenia Gravis - Where do we stand? Expert Opin Biol Ther 21:1013–1023. https://doi.org/10.1080/14712598.2021.1889509
doi: 10.1080/14712598.2021.1889509 pubmed: 33566716
Wang L, Zhang Y, He M (2017) Clinical predictors for the prognosis of myasthenia gravis. BMC Neurol 17:77. https://doi.org/10.1186/s12883-017-0857-7
doi: 10.1186/s12883-017-0857-7 pubmed: 28420327 pmcid: 5395963
Memon AB, Javed A, Caon C, Srivastawa S, Bao F, Bernitsas E et al (2018) Long-term safety of rituximab induced peripheral B-cell depletion in autoimmune neurological diseases. PLoS ONE 13(1):e0190425. https://doi.org/10.1371/journal.pone.0190425
doi: 10.1371/journal.pone.0190425 pubmed: 29309416 pmcid: 5757948
Chroni E, Veltsista D, Malefaki S, Dimitriou E (2021) Optimum treatment strategy for myasthenia gravis: a single-center experience. Arch Clin Neurol 30:18–26
Jaretzki A 3rd, Barohn RJ, Ernstoff RM et al (2000) Myasthenia gravis: recommendations for clinical research standards. Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America. Neurol 55:16–23. https://doi.org/10.1212/wnl.55.1.16
doi: 10.1212/wnl.55.1.16
World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194. https://doi.org/10.1001/jama.2013.281053
doi: 10.1001/jama.2013.281053
National Cancer Institute (U.S.) (2009) Common terminology criteria for adverse events (CTCAE). Rev. edn. Bethesda, Md.: U.S. Dept. of Health and Human Services, National Institutes of Health, National Cancer Institute
Barlow-Pay F, Htut TW, Khezrian M, Myint PK (2021) Systematic review of immunosuppressant guidelines in the COVID-19 pandemic. Ther Adv Drug Saf 12:2042098620985687. https://doi.org/10.1177/2042098620985687
doi: 10.1177/2042098620985687 pubmed: 33628418 pmcid: 7882764
Guidon AC, Amato AA (2020) COVID-19 and neuromuscular disorders. Neurology 94:959–969. https://doi.org/10.1212/WNL.0000000000009566
doi: 10.1212/WNL.0000000000009566 pubmed: 32284362
Spiliopoulos KC, Kasdaglis N, Veltsista D, Lykouras D, Lagadinou M, Chroni E (2022) Teleneurology in a center for neuromuscular diseases during the COVID-19 pandemic. Acta Neurol Belg 122:721–724. https://doi.org/10.1007/s13760-021-01808-w
doi: 10.1007/s13760-021-01808-w pubmed: 34585321
Morren J, Li Y (2020) Maintenance immunosuppression in myasthenia gravis, an update. J Neurol Sci 410:116648. https://doi.org/10.1016/j.jns.2019.116648
doi: 10.1016/j.jns.2019.116648 pubmed: 31901719
Brauner S, Eriksson-Dufva A, Hietala MA, Frisell T, Press R, Piehl F (2020) Comparison Between Rituximab Treatment for New-Onset Generalized Myasthenia Gravis and Refractory Generalized Myasthenia Gravis. JAMA Neurol 77:974–981. https://doi.org/10.1001/jamaneurol.2020.0851
doi: 10.1001/jamaneurol.2020.0851 pubmed: 32364568
Piehl F, Eriksson-Dufva A, Budzianowska A et al (2022) Efficacy and Safety of Rituximab for New-Onset Generalized Myasthenia Gravis: The RINOMAX Randomized Clinical Trial. JAMA Neurol 79(11):1105–1112. https://doi.org/10.1001/jamaneurol.2022.2887
doi: 10.1001/jamaneurol.2022.2887 pubmed: 36121672 pmcid: 9486640
Vitturi BK, Kim AIH, Mitre LP, Pellegrinelli A, Valerio BCO (2021) Social, professional and neuropsychiatric outcomes in patients with myasthenia gravis. Neurol Sci 42(1):167–173. https://doi.org/10.1007/s10072-020-04528-w
doi: 10.1007/s10072-020-04528-w pubmed: 32592102
Cortes-Vicente E, Rojas-Garcia R, Diaz-Manera J et al (2018) The impact of rituximab infusion protocol on the long-term outcome in anti-MuSK myasthenia gravis. Ann Clin Transl Neurol 5:710–716. https://doi.org/10.1002/acn3.564
doi: 10.1002/acn3.564 pubmed: 29928654 pmcid: 5989782
Litchman T, Roy B, Kumar A, Sharma A, Njike V, Nowak RJ (2020) Differential response to rituximab in anti-AChR and anti-MuSK positive myasthenia gravis patients: a single-center retrospective study. J Neurol Sci 411:116690. https://doi.org/10.1016/j.jns.2020.116690
Afanasiev V, Demeret S, Bolgert F, Eymard B, Laforet P, Benveniste O (2017) Resistant myasthenia gravis and rituximab: A monocentric retrospective study of 28 patients. Neuromuscul Disord 27:251–258. https://doi.org/10.1016/j.nmd.2016.12.004
doi: 10.1016/j.nmd.2016.12.004 pubmed: 28082209
Veltsista D, Kefalopoulou Z, Tzartos J, Chroni E (2022) Autoantibody profile in myasthenia gravis patients with a refractory phase. Muscle Nerve 65:607–611. https://doi.org/10.1002/mus.27521
doi: 10.1002/mus.27521 pubmed: 35195920
Doughty CT, Suh J, David WS, Amato AA, Guidon AC (2021) Retrospective analysis of safety and outcomes of rituximab for myasthenia gravis in patients >/=65 years old. Muscle Nerve 64:651–656. https://doi.org/10.1002/mus.27393
doi: 10.1002/mus.27393 pubmed: 34378210
Li T, Zhang GQ, Li Y et al (2021) Efficacy and safety of different dosages of rituximab for refractory generalized AChR myasthenia gravis: A meta-analysis. J Clin Neurosci 85:6–12. https://doi.org/10.1016/j.jocn.2020.11.043
doi: 10.1016/j.jocn.2020.11.043 pubmed: 33581791
Jiang R, Fichtner ML, Hoehn KB et al (2020) Single-cell repertoire tracing identifies rituximab-resistant B cells during myasthenia gravis relapses. JCI Insight 5:e136471. https://doi.org/10.1172/jci.insight.136471
doi: 10.1172/jci.insight.136471 pubmed: 32573488 pmcid: 7453893
Ruetsch-Chelli C, Bresch S, Seitz-Polski B, Rosenthal A, Desnuelle C, Cohen M et al (2021) Memory B Cells Predict Relapse in Rituximab-Treated Myasthenia Gravis. Neurotherapeutics 18:938–948. https://doi.org/10.1007/s13311-021-01006-9
doi: 10.1007/s13311-021-01006-9 pubmed: 33768513 pmcid: 8423951
Min YG, Park C, Kwon YN, Shin JY, Sung JJ, Hong YH (2019) B Cell Immunophenotyping and Transcriptional Profiles of Memory B Cells in Patients with Myasthenia Gravis. Exp Neurobiol 28:720–726. https://doi.org/10.5607/en.2019.28.6.720
doi: 10.5607/en.2019.28.6.720 pubmed: 31902159 pmcid: 6946110
Kim Y, Li X, Huang Y et al (2022) COVID-19 Outcomes in Myasthenia Gravis Patients: Analysis From Electronic Health Records in the United States. Front Neurol 13:802559. https://doi.org/10.3389/fneur.2022.802559
doi: 10.3389/fneur.2022.802559 pubmed: 35418937 pmcid: 8996116
Abbas AS, Hardy N, Ghozy S et al (2022) Characteristics, treatment, and outcomes of Myasthenia Gravis in COVID-19 patients: A systematic review. Clin Neurol Neurosurg 213:107140. https://doi.org/10.1016/j.clineuro.2022.107140
doi: 10.1016/j.clineuro.2022.107140 pubmed: 35091255 pmcid: 8782728
Rodrigues CL, de Freitas HC, Lima PRO, de Oliveira Junior PH, Fernandes JMA, D’Almeida JAC et al (2022) Myasthenia gravis exacerbation and myasthenic crisis associated with COVID-19: case series and literature review. Neurol Sci 43(4):2271–2276. https://doi.org/10.1007/s10072-021-05823-w
doi: 10.1007/s10072-021-05823-w pubmed: 35039987 pmcid: 8763445
Menon D, Bril V (2022) Pharmacotherapy of Generalized Myasthenia Gravis with Special Emphasis on Newer Biologicals. Drugs 82:865–887. https://doi.org/10.1007/s40265-022-01726-y
doi: 10.1007/s40265-022-01726-y pubmed: 35639288 pmcid: 9152838
Schneider-Gold C, Gilhus NE (2021) Advances and challenges in the treatment of myasthenia gravis. Ther Adv Neurol Disord 14:17562864211065406. https://doi.org/10.1177/17562864211065406
doi: 10.1177/17562864211065406 pubmed: 34987614 pmcid: 8721395

Auteurs

Zinovia-Maria Kefalopoulou (ZM)

Department of Neurology, University Hospital of Patras, 26504, Patras, Rio, Greece. zkefalopoulou@gmail.com.
Neuromuscular Centre, University Hospital of Patras, 26504, Patras, Rio, Greece. zkefalopoulou@gmail.com.

Dimitra Veltsista (D)

Department of Neurology, University Hospital of Patras, 26504, Patras, Rio, Greece.
Neuromuscular Centre, University Hospital of Patras, 26504, Patras, Rio, Greece.

Alexandra Germeni (A)

Department of Neurology, University Hospital of Patras, 26504, Patras, Rio, Greece.

Dimosthenis Lykouras (D)

Department of Respiratory Medicine, University Hospital of Patras, 26504, Patras, Rio, Greece.

Eirini Tsiamaki (E)

Department of Neurology, University Hospital of Patras, 26504, Patras, Rio, Greece.

Elisabeth Chroni (E)

Department of Neurology, University Hospital of Patras, 26504, Patras, Rio, Greece.
Neuromuscular Centre, University Hospital of Patras, 26504, Patras, Rio, Greece.

Classifications MeSH