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January 2022; 9 (1) ArticleOpen Access

Interleukin-6 Receptor Blockade in Treatment-Refractory MOG-IgG–Associated Disease and Neuromyelitis Optica Spectrum Disorders

View ORCID ProfileMarius Ringelstein, Ilya Ayzenberg, Gero Lindenblatt, Katinka Fischer, Anna Gahlen, View ORCID ProfileGiovanni Novi, Helen Hayward-Könnecke, Sven Schippling, Paulus S. Rommer, Barbara Kornek, View ORCID ProfileTobias Zrzavy, Damien Biotti, View ORCID ProfileJonathan Ciron, View ORCID ProfileBertrand Audoin, View ORCID ProfileAchim Berthele, Katrin Giglhuber, Helene Zephir, Tania Kümpfel, Robert Berger, Joachim Röther, View ORCID ProfileVivien Häußler, View ORCID ProfileJan-Patrick Stellmann, Daniel Whittam, Anu Jacob, Markus Kraemer, Antoine Gueguen, Romain Deschamps, Antonios Bayas, Martin W. Hümmert, Corinna Trebst, Axel Haarmann, Sven Jarius, Brigitte Wildemann, View ORCID ProfileMatthias Grothe, Nadja Siebert, Klemens Ruprecht, Friedemann Paul, View ORCID ProfileNicolas Collongues, Romain Marignier, View ORCID ProfileMichael Levy, Michael Karenfort, Michael Deppe, View ORCID ProfilePhilipp Albrecht, View ORCID ProfileKerstin Hellwig, Ralf Gold, Hans-Peter Hartung, Sven G. Meuth, View ORCID ProfileIngo Kleiter, View ORCID ProfileOrhan Aktas, on behalf of the Neuromyelitis Optica Study Group (NEMOS)
First published November 16, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001100
Marius Ringelstein
Department of Neurology (M.R., K.F., M.K.,P.A., H.P.H., S.G.M., O.A.), Medical Faculty, Heinrich Heine University Düsseldorf; Department of Neurology (M.R.), Center for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich Heine University Düsseldorf; Department of Neurology (I.A., A.G., K.H., R.G., I.K.), St. Josef-Hospital, Ruhr University Bochum, Germany; Department of Neurology (I.A.), Sechenov First Moscow State Medical University, Russia; Department of Neurology (G.L.), Johanna Etienne Hospital, Neuss, Germany; Department of Neurology (G.N.), San Martino Hospital, Genova, Italy; Neuroimmunology and MS Research (H.H.K., S.S.), Department of Neurology, University Hospital Zürich, Switzerland; Department of Neurology (P.S.R., B.K., T.Z.), Medical University of Vienna, Austria; Department of Neurology (D.B., J.C.), B4 unit, CRC-SEP, Toulouse Purpan University Hospital, France; Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity) (D.B., J.C.) INSERM UMR1291-CNRS UMR5051 - Université Toulouse III, France; Aix Marseille University (B.A.), APHM, Hôpital de la Timone, Pôle de Neurosciences Cliniques, Service de Neurologie, Marseille, France; Technical University of Munich (A.B., K.G.), School of Medicine, Department of Neurology, Klinikum rechts der Isar, Germany; University of Lille (H.Z.), Inserm, CRC-SEP, CHU Lille, France; Institute of Clinical Neuroimmunology (T.K.), Faculty of Medicine, Ludwig Maximilian University, Munich; Department of Neurology (R.B., J.R.), Asklepios Klinik Altona, Hamburg; Department of Neurology and Institute of Neuroimmunology and MS (INIMS) (V.H.), University Medical Center Hamburg-Eppendorf, Germany; APHM, Hôpital de la Timone (J.P.S.), CEMEREM; Aix Marseille Univ, CNRS, CRMBM (J.P.S), UMR 7339, Marseille, France; Department of Neurology (D.W., A.J.), The Walton Centre, Liverpool, United Kingdom; the Cleveland Clinic Abu Dhabi, (A.J.) UAE; Department of Neurology (M.K.), Alfried Krupp Hospital, Essen, Germany; Department of Neurology (A.G.,R.D.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Department of Neurology (A.B.), Universitätsklinikum Augsburg; Department of Neurology (M.W.H., C.T.), Hannover Medical School; Department of Neurology (A.H.), University of Würzburg; Molecular Neuroimmunology Group (S.J., B.W.), Department of Neurology, University of Heidelberg; Department of Neurology (M.G.), University hospital Greifswald; NeuroCure Clinical Research Center and Experimental and Clinical Research Center (N.S., F.P), Max Delbrueck Center for Molecular Medicine and Charité Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health; Department of Neurology (K.R.), Charité Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin; Department of Neurology (N.C.), University Hospital Strasbourg; Service de neurologie (R.M.), sclérose en plaques, pathologies de la myéline et neuro-inflammation – Hôpital Neurologique Pierre Wertheimer Hospices Civils de Lyon, France; Department of Neurology (M.L.), Massachusetts General Hospital and Harvard Medical School, Boston; Department of General Pediatrics (M.K.), Neonatology and Pediatric Cardiology, University Children's Hospital, Medical Faculty, Heinrich Heine University Düsseldorf; Department of Neurology (M.D.), University Hospital, Münster; and Marianne-Strauß-Klinik (I.K.), Behandlungszentrum Kempfenhausen für Multiple Sklerose Kranke, Berg, Germany.
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Citation
Interleukin-6 Receptor Blockade in Treatment-Refractory MOG-IgG–Associated Disease and Neuromyelitis Optica Spectrum Disorders
Marius Ringelstein, Ilya Ayzenberg, Gero Lindenblatt, Katinka Fischer, Anna Gahlen, Giovanni Novi, Helen Hayward-Könnecke, Sven Schippling, Paulus S. Rommer, Barbara Kornek, Tobias Zrzavy, Damien Biotti, Jonathan Ciron, Bertrand Audoin, Achim Berthele, Katrin Giglhuber, Helene Zephir, Tania Kümpfel, Robert Berger, Joachim Röther, Vivien Häußler, Jan-Patrick Stellmann, Daniel Whittam, Anu Jacob, Markus Kraemer, Antoine Gueguen, Romain Deschamps, Antonios Bayas, Martin W. Hümmert, Corinna Trebst, Axel Haarmann, Sven Jarius, Brigitte Wildemann, Matthias Grothe, Nadja Siebert, Klemens Ruprecht, Friedemann Paul, Nicolas Collongues, Romain Marignier, Michael Levy, Michael Karenfort, Michael Deppe, Philipp Albrecht, Kerstin Hellwig, Ralf Gold, Hans-Peter Hartung, Sven G. Meuth, Ingo Kleiter, Orhan Aktas, on behalf of the Neuromyelitis Optica Study Group (NEMOS)
Neurol Neuroimmunol Neuroinflamm Jan 2022, 9 (1) e1100; DOI: 10.1212/NXI.0000000000001100

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Abstract

Background and Objectives To evaluate the long-term safety and efficacy of tocilizumab (TCZ), a humanized anti–interleukin-6 receptor antibody in myelin oligodendrocyte glycoprotein–IgG–associated disease (MOGAD) and neuromyelitis optica spectrum disorders (NMOSD).

Methods Annualized relapse rate (ARR), Expanded Disability Status Scale score, MRI, autoantibody titers, pain, and adverse events were retrospectively evaluated in 57 patients with MOGAD (n = 14), aquaporin-4 (AQP4)-IgG seropositive (n = 36), and seronegative NMOSD (n = 7; 12%), switched to TCZ from previous immunotherapies, particularly rituximab.

Results Patients received TCZ for 23.8 months (median; interquartile range 13.0–51.1 months), with an IV dose of 8.0 mg/kg (median; range 6–12 mg/kg) every 31.6 days (mean; range 26–44 days). For MOGAD, the median ARR decreased from 1.75 (range 0.5–5) to 0 (range 0–0.9; p = 0.0011) under TCZ. A similar effect was seen for AQP4-IgG+ (ARR reduction from 1.5 [range 0–5] to 0 [range 0–4.2]; p < 0.001) and for seronegative NMOSD (from 3.0 [range 1.0–3.0] to 0.2 [range 0–2.0]; p = 0.031). During TCZ, 60% of all patients were relapse free (79% for MOGAD, 56% for AQP4-IgG+, and 43% for seronegative NMOSD). Disability follow-up indicated stabilization. MRI inflammatory activity decreased in MOGAD (p = 0.04; for the brain) and in AQP4-IgG+ NMOSD (p < 0.001; for the spinal cord). Chronic pain was unchanged. Regarding only patients treated with TCZ for at least 12 months (n = 44), ARR reductions were confirmed, including the subgroups of MOGAD (n = 11) and AQP4-IgG+ patients (n = 28). Similarly, in the group of patients treated with TCZ for at least 12 months, 59% of them were relapse free, with 73% for MOGAD, 57% for AQP4-IgG+, and 40% for patients with seronegative NMOSD. No severe or unexpected safety signals were observed. Add-on therapy showed no advantage compared with TCZ monotherapy.

Discussion This study provides Class III evidence that long-term TCZ therapy is safe and reduces relapse probability in MOGAD and AQP4-IgG+ NMOSD.

Glossary

ADEM=
acute disseminated encephalomyelitis;
AQP4=
aquaporin-4;
ARR=
annualized relapse rate;
AZA=
azathioprine;
EDSS=
Expanded Disability Status Scale;
HDS=
high-dose steroid;
IL-6=
interleukin-6;
IQR=
interquartile range;
IVIG=
IV immunoglobulin;
LDS=
low-dose steroid;
MMF=
mycophenolate mofetil;
MOG=
myelin oligodendrocyte glycoprotein;
MOGAD=
myelin oligodendrocyte glycoprotein–IgG–associated disease;
MTX=
methotrexate;
NMOSD=
neuromyelitis optica spectrum disorder;
ON=
optic neuritis;
RTX=
rituximab;
SLE=
systemic lupus erythematosus;
TCZ=
tocilizumab;
UTI=
urinary tract infection

Footnotes

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • The Article Processing Charge was funded by Heinrich Heine University Düsseldorf, Germany.

  • Neuromyelitis Optica Study Group (NEMOS) coinvestigators are listed in the appendix at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Received February 8, 2021.
  • Accepted in final form August 25, 2021.
  • Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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