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November 2021; 8 (6) ArticleOpen Access

Intrathecal Antibody Production Against Epstein-Barr, Herpes Simplex, and Other Neurotropic Viruses in Autoimmune Encephalitis

Philipp Schwenkenbecher, Thomas Skripuletz, Peter Lange, Marc Dürr, Felix F. Konen, Nora Möhn, Marius Ringelstein, Til Menge, View ORCID ProfileManuel A. Friese, View ORCID ProfileNico Melzer, Michael P. Malter, Martin Häusler, Franziska S. Thaler, Martin Stangel, Jan Lewerenz, Kurt-Wolfram Sühs
First published August 24, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001062
Philipp Schwenkenbecher
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Thomas Skripuletz
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Peter Lange
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Marc Dürr
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Felix F. Konen
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Nora Möhn
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Marius Ringelstein
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Til Menge
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Manuel A. Friese
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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  • For correspondence: manuel.friese@zmnh.uni-hamburg.de
Nico Melzer
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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  • For correspondence: nico.melzer@ukmuenster.de
Michael P. Malter
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Martin Häusler
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Franziska S. Thaler
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Martin Stangel
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Jan Lewerenz
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Kurt-Wolfram Sühs
From the Department of Neurology (P.S., T.S., F.F.K., Nora Möhn, M.S., K.-W.S.), Hannover Medical School; Department of Neurology (P.L.), Georg August University Göttingen; Department of Neurology (M.D., J.L.), Ulm University; Department of Neurology (M.R.), Medical Faculty, Heinrich-Heine-University Düsseldorf; Department of Neurology (M.R., T.M.), Centre for Neurology and Neuropsychiatry, LVR-Klinikum, Heinrich-Heine-University Düsseldorf; Institute of Neuroimmunology and Multiple Sclerosis (M.A.F.), University Medical Center Hamburg-Eppendorf; Department of Neurology with Institute of Translational Neurology (Nico Melzer), University Hospital Muenster; Department of Neurology (M.P.M.), University Hospital Cologne; Division of Neuropediatrics and Social Pediatrics (M.H.), Department of Pediatrics, Medical Faculty, RWTH Aachen University; and Institute of Clinical Neuroimmunology (F.S.T.), University Hospital and Biomedical Center, Ludwig-Maximilians University Munich, Germany.
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Citation
Intrathecal Antibody Production Against Epstein-Barr, Herpes Simplex, and Other Neurotropic Viruses in Autoimmune Encephalitis
Philipp Schwenkenbecher, Thomas Skripuletz, Peter Lange, Marc Dürr, Felix F. Konen, Nora Möhn, Marius Ringelstein, Til Menge, Manuel A. Friese, Nico Melzer, Michael P. Malter, Martin Häusler, Franziska S. Thaler, Martin Stangel, Jan Lewerenz, Kurt-Wolfram Sühs
Neurol Neuroimmunol Neuroinflamm Nov 2021, 8 (6) e1062; DOI: 10.1212/NXI.0000000000001062

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Abstract

Background and Objectives Neurotropic viruses are suspected to play a role in the pathogenesis of autoimmune diseases of the CNS such as the association between the Epstein-Barr virus (EBV) and multiple sclerosis (MS). A group of autoimmune encephalitis (AE) is linked to antibodies against neuronal cell surface proteins. Because CNS infection with the herpes simplex virus can trigger anti–NMDA receptor (NMDAR) encephalitis, a similar mechanism for EBV and other neurotropic viruses could be postulated. To investigate for previous viral infections of the CNS, intrathecally produced virus-specific antibody synthesis was determined in patients with AE.

Methods Antibody-specific indices (AIs) against EBV and measles, rubella, varicella zoster, herpes simplex virus, and cytomegalovirus were determined in 27 patients having AE (anti-NMDAR encephalitis, n = 21, and LGI1 encephalitis, n = 6) and in 2 control groups comprising of 30 patients with MS and 21 patients with noninflammatory CNS diseases (NIND), which were sex and age matched.

Results An intrathecal synthesis of antibodies against EBV was found in 5/27 (19%) patients with AE and 2/30 (7%) of the patients with MS. All these patients had also at least 1 additional elevated virus-specific AI. In contrast, in none of the patients with NIND, an elevated virus-specific AI was detected.

Discussion Intrathecally produced antibodies against EBV can be found in patients with AE and MS but only together with antibodies against different neurotropic viruses. Evidence of these antibodies is the result of a polyspecific immune response similar yet distinct from MS response rather than an elapsed infection of the CNS.

Glossary

AE=
autoimmune encephalitis;
AI=
antibody-specific index;
CMV=
cytomegalovirus;
EBNA-1=
EBV-encoded nuclear antigen-I;
EBV=
Epstein-Barr virus;
EBV-VCA=
EBV-virus capsid antigen;
HSV=
herpes simplex virus;
LGI1=
leucine-rich, glioma-inactivated 1;
mRS=
modified Rankin Scale;
MRZ=
measles, rubella, varicella zoster;
MS=
multiple sclerosis;
NIND=
noninflammatory neurologic disease;
NMDAR=
NMDA receptor;
NPH=
normal pressure hydrocephalus;
IIH=
idiopathic intracranial hypertension;
OCB=
oligoclonal band;
QAlb=
CSF/serum albumin ratio;
VZV=
varicella zoster virus

Footnotes

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

  • German Network for Research on Autoimmune Encephalitis (GENERATE) coinvestigators are listed in Appendix 2 at links.lww.com/NXI/A541.

  • The Article Processing Charge was funded by Hannover Medical School.

  • Received March 24, 2021.
  • Accepted in final form June 21, 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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Neurology: Neuroimmunology & Neuroinflammation
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