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March 14, 2023; 100 (11) Research Article

Significance of Myelin Oligodendrocyte Glycoprotein Antibodies in CSF

A Retrospective Multicenter Study

Sara Carta, Álvaro Cobo Calvo, Thaís Armangué, Albert Saiz, Christian Lechner, Kevin Rostásy, Markus Breu, Matthias Baumann, Romana Höftberger, Ilya Ayzenberg, Carolin Schwake, Maria Sepulveda, Eugenia Martínez-Hernández, Gemma Olivé-Cirera, Georgina Arrambide, Mar Tintoré, Raphael Bernard-Valnet, Renaud Du Pasquier, Fabienne Brilot, Sudarshini Ramanathan, Kathrin Schanda, Alberto Gajofatto, Sergio Ferrari, Elia Sechi, Eoin P. Flanagan, Sean J. Pittock, Vyanka Redenbaugh, Markus Reindl, Romain Marignier, Sara Mariotto
First published December 16, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201662
Sara Carta
From the Neurology Unit (S.C., A.G., S.F., S.M.), Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Italy; Servei de Neurologia-Neuroimmunologia (A.C.C., G.A., M.T.), Centre d'Esclerosi Múltiple de Catalunya, (CEMCAT), Vall d'Hebron Institut de Recerca, Vall d'Hebron Hospital Universitari, Universitat Autònoma de Barcelona, Spain; Pediatric Neuroimmunology Unit (T.A.), Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neuroimmunology and Multiple Sclerosis Unit (T.A., A.S., M.S., E.M-H., G.O-C.), Service of Neurology, Hospital Clinic de Barcelona, Neuroimmunology Program, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) and, University of Barcelona, Spain; Division of Pediatric Neurology (C.L., M.B.), Department of Pediatric and Adolescent Medicine, Medical University of Innsbruck, Austria; Division of Pediatric Neurology (K.R.), University of Witten/Herdecke Childrens' Hospital, Datteln, Germany; Division of Pediatric Pulmonology (M.B.), Allergology and Endocrinology, Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Austria; Division of Neuropathology and Neurochemistry (R.H.), Department of Neurology, Medical University of Vienna, Austria; Department of Neurology (I.A., C.S.), St. Josef-Hospital, Ruhr-University Bochum, Germany; Department of Clinical Neurosciences (R.B-V., R.d.P.), Service of Neurology, Lausanne University Hospital and University of Lausanne, Switzerland; Faculty of Medicine and Health and Brain and Mind Centre (F.B.), Brain Autoimmunity Group, Kids Neuroscience Centre, Kids Research at the Children's Hospital at Westmead, School of Medical Sciences, The University of Sydney, Australia; Translational Neuroimmunology Group (S.R.), Kids Neuroscience Centre, Children's Hospital at Westmead; Sydney Medical School and Brain and Mind Centre, Faculty of Medicine and Health, University of Sydney; Department of Neurology (S.R.), Concord Hospital, Sydney, Australia; Clinical Department of Neurology (K.S., M.R.), Medical University of Innsbruck, Austria; Department of Medical, Surgical and Experimental Sciences (E.S.), University of Sassari, Italy; Department of Neurology, Department of Laboratory Medicine and Pathology (E.P.F., S.J.P., V.R.), Mayo Clinic College of Medicine and Science, Rochester; Service de Neurologie (R.M.), Sclérose en Plaques, Pathologies de la Myéline et Neuro-inflammation, Centre de Référence des Maladies Inflammatoires Rares du Cerveau et de la Moelle, Hôpital Neurologique Pierre Wertheimer, Hospices Civils de Lyon, France.
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Álvaro Cobo Calvo
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Thaís Armangué
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Albert Saiz
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Christian Lechner
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Kevin Rostásy
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Markus Breu
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Matthias Baumann
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Romana Höftberger
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Ilya Ayzenberg
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Carolin Schwake
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Maria Sepulveda
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Eugenia Martínez-Hernández
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Gemma Olivé-Cirera
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Georgina Arrambide
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Mar Tintoré
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Raphael Bernard-Valnet
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Renaud Du Pasquier
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Fabienne Brilot
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Sudarshini Ramanathan
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Kathrin Schanda
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Alberto Gajofatto
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Sergio Ferrari
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Elia Sechi
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Eoin P. Flanagan
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Sean J. Pittock
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Vyanka Redenbaugh
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Markus Reindl
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Romain Marignier
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Sara Mariotto
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Citation
Significance of Myelin Oligodendrocyte Glycoprotein Antibodies in CSF
A Retrospective Multicenter Study
Sara Carta, Álvaro Cobo Calvo, Thaís Armangué, Albert Saiz, Christian Lechner, Kevin Rostásy, Markus Breu, Matthias Baumann, Romana Höftberger, Ilya Ayzenberg, Carolin Schwake, Maria Sepulveda, Eugenia Martínez-Hernández, Gemma Olivé-Cirera, Georgina Arrambide, Mar Tintoré, Raphael Bernard-Valnet, Renaud Du Pasquier, Fabienne Brilot, Sudarshini Ramanathan, Kathrin Schanda, Alberto Gajofatto, Sergio Ferrari, Elia Sechi, Eoin P. Flanagan, Sean J. Pittock, Vyanka Redenbaugh, Markus Reindl, Romain Marignier, Sara Mariotto
Neurology Mar 2023, 100 (11) e1095-e1108; DOI: 10.1212/WNL.0000000000201662

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Abstract

Background and Objectives Although the diagnosis of myelin oligodendrocyte glycoprotein antibody-associated disease (MOGAD) is based on serum MOG antibodies (MOG-Abs) positivity, patients with coexisting or restricted MOG-Abs in the CSF have been reported. The aim of this study is to characterize the relevance of CSF MOG-Abs positivity in clinical practice.

Methods Eleven medical centers retrospectively collected clinical and laboratory data of adult and pediatric patients with suspected inflammatory CNS disease and MOG-Abs positivity in serum and/or CSF using live cell-based assays. Comparisons were performed using parametric or nonparametric tests, as appropriate. Potential factors of unfavorable outcomes were explored by Cox proportional hazard models and logistic regression.

Results The cohort included 255 patients: 139 (55%) women and 132 (52%) children (i.e., <18-year-old). Among them, 145 patients (56.8%) had MOG-Abs in both serum and CSF (MOG-Abs seropositive and CSF positive), 79 (31%) only in serum (MOG-Abs seropositive and CSF negative), and 31 (12%) only in CSF (MOG-Abs seronegative and CSF positive). MOG-Abs seronegative and CSF positive predominated in adults (22% vs 3% of children), presented more commonly with motor (n = 14, 45%) and sensory symptoms (n = 13, 42%), and all but 4 (2 multiple sclerosis, 1 polyradiculoneuritis, and 1 Susac syndrome) had a final diagnosis compatible with MOGAD. When comparing seropositive patients according to MOG-Abs CSF status, MOG-Abs seropositive and CSF positive patients had a higher Expanded Disability Status Scale (EDSS) at nadir during the index event (median 4.5, interquartile range [IQR] 3.0–7.5 vs 3.0, IQR 2.0–6.8, p = 0.007) and presented more commonly with sensory (45.5% vs 24%, p = 0.002), motor (33.6% vs 19%, p = 0.021), and sphincter symptoms (26.9% vs 7.8%, p = 0.001) than MOG-Abs seropositive and CSF negative. At the last follow-up, MOG-Abs seropositive and CSF positive cases had more often persistent sphincter dysfunction (17.3% vs 4.3%, p = 0.008). Compared with seropositive patients, those MOG-Abs seronegative and CSF positive had higher disability at the last follow-up (p ≤ 0.001), and MOG-Abs seronegative and CSF positive status were independently associated with an EDSS ≥3.0.

Discussion Paired serum and CSF MOG-Abs positivity are common in MOGAD and are associated with a more severe clinical presentation. CSF-only MOG-Abs positivity can occur in patients with a phenotype suggestive of MOGAD and is associated with a worse outcome. Taken together, these data suggest a clinical interest in assessing CSF MOG-Abs in patients with a phenotype suggestive of MOGAD, regardless of the MOG-Abs serostatus.

Glossary

Abs=
antibodies;
ADEM=
acute disseminated encephalomyelitis;
ARR=
annualized relapse rate;
CBA=
cell-based assays;
CNS=
central nervous system;
CI=
confidence interval;
DMD=
disease-modifying drug;
EDSS=
Expanded Disability Status Scale;
IF=
immunofluorescence;
IQR=
interquartile range;
MOG=
myelin oligodendrocyte glycoprotein;
MOG-Abs=
MOG antibodies;
MOGAD=
myelin oligodendrocyte glycoprotein antibody associated disease;
MS=
multiple sclerosis;
NMOSD=
neuromyelitis optica spectrum disorder;
OR=
odds ratio

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Deputy Editor Olga Ciccarelli, MD, PhD, FRCP.

  • ↵* S. Carta and A. Cobo Calvo equally contributed to the study as first authors.

  • ↵† S. Mariotto and R. Marignier equally contributed to the study as senior authors.

  • Editorial, page 497

  • CME Course: NPub.org/cmelist

  • Received March 27, 2022.
  • Accepted in final form October 24, 2022.
  • © 2022 American Academy of Neurology
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