Neuropathological Variability within a Spectrum of NMDAR-Encephalitis.


Journal

Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449

Informations de publication

Date de publication:
11 2021
Historique:
revised: 12 09 2021
received: 09 07 2021
accepted: 19 09 2021
pubmed: 26 9 2021
medline: 15 12 2021
entrez: 25 9 2021
Statut: ppublish

Résumé

To describe the neuropathological features of N-methyl-D-aspartate receptor (NMDAR)-encephalitis in an archival autopsy cohort. We examined four autopsies from patients with NMDAR-encephalitis; two patients were untreated, three had comorbidities: small cell lung cancer, brain post-transplant lymphoproliferative disease (PTLD), and overlapping demyelination. The two untreated patients had inflammatory infiltrates predominantly composed of perivascular and parenchymal CD3 The topographic distribution of inflammation in patients with NMDAR-encephalitis reflects the clinical symptoms of movement disorders, abnormal behavior, and memory dysfunction with inflammation dominantly observed in basal ganglia, amygdala, and hippocampus, and loss of NMDAR-immunoreactivity correlates with disease severity. Co-occurring pathologies influence the spatial distribution, composition, and intensity of inflammation, which may modify patients' clinical presentation and outcome. ANN NEUROL 2021;90:725-737.

Identifiants

pubmed: 34562035
doi: 10.1002/ana.26223
doi:

Substances chimiques

Receptors, N-Methyl-D-Aspartate 0
Complement System Proteins 9007-36-7

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

725-737

Subventions

Organisme : Austrian Science Fund FWF
ID : DOC 33
Pays : Austria
Organisme : Austrian Science Fund FWF
ID : I 4685
Pays : Austria

Informations de copyright

© 2021 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.

Références

Dalmau J, Gleichman AJ, Hughes EG, et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol 2008;7:1091-1098.
Hughes EG, Peng X, Gleichman AJ, et al. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J Neurosci 2010;30:5866-5875.
Mikasova L, de Rossi P, Bouchet D, et al. Disrupted surface cross-talk between NMDA and Ephrin-B2 receptors in anti-NMDA encephalitis. Brain 2012;135:1606-1621.
Planagumà J, Leypoldt F, Mannara F, et al. Human N-methyl D-aspartate receptor antibodies alter memory and behaviour in mice. Brain 2015;138:94-109.
Titulaer MJ, McCracken L, Gabilondo I, et al. Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol 2013;12:157-165.
Tüzün E, Zhou L, Baehring JM, et al. Evidence for antibody-mediated pathogenesis in anti-NMDAR encephalitis associated with ovarian teratoma. Acta Neuropathol 2009;118:737.
Bien CG, Vincent A, Barnett MH, et al. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 2012;135:1622-1638.
Martinez-Hernandez E, Horvath J, Shiloh-Malawsky Y, et al. Analysis of complement and plasma cells in the brain of patients with anti-NMDAR encephalitis. Neurology 2011;77:589-593.
Dalmau J, Tüzün E, Wu HY, et al. Paraneoplastic anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma. Ann Neurol 2007;61:25-36.
Mariotto S, Zamó A, Franchini E, et al. Lymphomatosis cerebri and anti-NMDAR antibodies: a unique constellation. J Neurol Sci 2019;398:19-21.
Maat P, de Beukelaar JW, Jansen C, et al. Pathologically confirmed autoimmune encephalitis in suspected Creutzfeldt-Jakob disease. Neurol Neuroimmunol Neuroinflamm 2015;2:1-8.
Nauen DW. Extra-central nervous system target for assessment and treatment in refractory anti-N-methyl-d-aspartate receptor encephalitis. J Crit Care 2017;37:234-236.
Kobayashi M, Nishioka K, Takanashi M, et al. Anti-NMDA receptor encephalitis due to large-cell neuroendocrine carcinoma of the uterus. J Neurol Sci 2017;383:72-74.
Hirano M, Itoh T, Fujimura H, et al. Pathological findings in male patients with anti-N-methyl-d-aspartate receptor encephalitis. J Neuropathol Exp Neurol 2019;78:735-741.
Graus F, Saiz A, Lai M, et al. Neuronal surface antigen antibodies in limbic encephalitis: clinical-immunologic associations. Neurology 2008;71:930-936.
Roetzer T, Leskovar K, Peter N, et al. Evaluating cellularity and structural connectivity on whole brain slides using a custom-made digital pathology pipeline. J Neurosci Methods 2019;311:215-221.
Bauer J, Lassmann H. Neuropathological techniques to investigate central nervous system sections in multiple sclerosis. Multiple Sclerosis. Methods in Molecular Biology vol. 1304. New York, NY: Humana Press; 2016;211-229.
Zrzavy T, Schwaiger C, Wimmer I, et al. Acute and non-resolving inflammation associate with oxidative injury after human spinal cord injury. Brain 2021;144:144-161.
Bankhead P, Loughrey MB, Fernández JA, et al. QuPath: open source software for digital pathology image analysis. Sci Rep 2017;7:1-7.
Kuhlmann T, Ludwin S, Prat A, et al. An updated histological classification system for multiple sclerosis lesions. Acta Neuropathol 2017;133:13-24.
Lucchinetti C, Bruck W, Parisi J, et al. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 2000;47:707-717.
Bernal F, Graus F, Pifarré À, et al. Immunohistochemical analysis of anti-Hu-associated paraneoplastic encephalomyelitis. Acta Neuropathol 2002;103:509-515.
Dalmau J, Rosenfeld MR. Paraneoplastic syndromes of the CNS. Lancet Neurol 2008;7:327-340.
Konen FF, Schwenkenbecher P, Jendretzky KF, et al. Severe anti-N-methyl-d-aspartate receptor encephalitis under immunosuppression after liver transplantation. Front Neurol 2019;10:987.
Randall A, Huda S, Jacob A, Larner AJ. Autoimmune encephalitis (NMDAR antibody) in a patient receiving chronic post-transplant immunosuppression. Pract Neurol 2018;18:320-322.
Zhao CZ, Erickson J, Dalmau J. Clinical reasoning: agitation and psychosis in a patient after renal transplantation. Neurology 2012;79:e41-e44.
Garré J, Sprengers M, van Melkebeke D, Laureys G. EBV-NMDA double positive encephalitis in an immunocompromised patient. J Neurol Sci 2019;396:76-77.
Derksen S, Goraj B, Molenaar J, van der Hoeven J. Severe anti NMDA encephalitis and EBV infection. Neth J Crit Care 2013;17:19-21.
Cohen DA, Lopez-Chiriboga AS, Pittock SJ, et al. Posttransplant autoimmune encephalitis. Neurol Neuroimmunol Neuroinflamm 2018;5:1-3.
Toda J, Maeda T, Akuta K, et al. Limbic encephalitis with antibodies to N-methyl-d-aspartate (NMDA)-type glutamate receptor after allogeneic transplantation. Int J Hematol 2020;254-277.
Armangue T, Spatola M, Vlagea A, et al. Frequency, symptoms, risk factors, and outcomes of autoimmune encephalitis after herpes simplex encephalitis: a prospective observational study and retrospective analysis. Lancet Neurol 2018;17:760-772.
Titulaer MJ, Höftberger R, Iizuka T, et al. Overlapping demyelinating syndromes and anti-N-methyl-D-aspartate receptor encephalitis. Ann Neurol 2014;75:411-428.
Hacohen Y, Absoud M, Hemingway C, et al. NMDA receptor antibodies associated with distinct white matter syndromes. Neurol Neuroimmunol Neuroinflamm 2014;1:1-11.
Ramberger M, Bsteh G, Schanda K, et al. NMDA receptor antibodies: a rare association in inflammatory demyelinating diseases. Neurol Neuroimmunol Neuroinflamm 2015;2:1-4.
Fleischmann R, Prüss H, Rosche B, et al. Severe cognitive impairment associated with intrathecal antibodies to the NR1 subunit of the N-methyl-D-aspartate receptor in a patient with multiple sclerosis. JAMA Neurol 2015;72:96-99.
Waschbisch A, Kallmünzer B, Schwab S, et al. Demyelinating disease and anti-N-methyl-D-aspartate receptor immunoglobulin G antibodies: a case report. BMC Res Notes 2014;7:1-4.
Takeda A, Shimada H, Tamura A, et al. A case of anti-N-methyl-D-aspartate receptor encephalitis with multiple sclerosis-like demyelinated lesions. Mult Scler Relat Disord 2014;3:391-397.
Gahr M, Lauda F, Wigand ME, et al. Periventricular white matter lesion and incomplete MRZ reaction in a male patient with anti-N-methyl-D-aspartate receptor encephalitis presenting with dysphoric mania. Case Rep 2015;2015:bcr2014209075.
Baheerathan A, Brownlee W, Chard D, et al. Antecedent anti-NMDA receptor encephalitis in two patients with multiple sclerosis. Mult Scler Relat Disord 2017;12:20-22.
Suleman S, Javed Q. NMDAR (N-methyl-D-aspartate receptor) encephalitis in a patient with MS (multiple sclerosis): a rare and challenging case. Case Rep 2018;2018:bcr-2017-222086.
Gulec B, Kurucu H, Bozbay S, et al. Co-existence of multiple sclerosis and anti-NMDA receptor encephalitis: a case report and review of literature. Mult Scler Relat Disord 2020;42:102075.
Tappatà M, Riguzzi P, Volpi L, et al. Long-term persistence of NMDAR antibodies after encephalitis with de novo occurrence of demyelinating disorder. Neurol Sci 2021;42:301-303.
Huang Y, Wang Q, Zeng S, et al. Case report: overlapping multiple sclerosis with anti-N-methyl-D-aspartate receptor encephalitis: a case report and review of literature. Front Immunol 2020;11:1-6.
Tietz AK, Angstwurm K, Baumgartner T, et al. Genome-wide association study identifies two new loci associated with anti-NMDAR encephalitis. medRxiv 2021.
Wang Z, Sadovnick AD, Traboulsee AL, et al. Nuclear receptor NR1H3 in familial multiple sclerosis. Neuron 2016;90:948-954.
Zrzavy T, Hametner S, Wimmer I, et al. Loss of ‘homeostatic’ microglia and patterns of their activation in active multiple sclerosis. Brain 2017;140:1900-1913.
Matute C, Palma A, Serrano-Regal MP, et al. N-methyl-D-aspartate receptor antibodies in autoimmune encephalopathy Alter Oligodendrocyte function. Ann Neurol 2020;87:670-676.
Phillips OR, Joshi SH, Narr KL, et al. Superficial white matter damage in anti-NMDA receptor encephalitis. J Neurol Neurosurg Psychiatry 2018;89:518-525.
Camdessanché JP, Streichenberger N, Cavillon G, et al. Brain immunohistopathological study in a patient with anti-NMDAR encephalitis. Eur J Neurol 2011;18:929-931.
Filatenkov A, Richardson TE, Daoud E, et al. Persistence of parenchymal and perivascular T-cells in treatment-refractory anti-NMDA receptor encephalitis. Neuroreport 2017;28:890.

Auteurs

Tobias Zrzavy (T)

Department of Neurology, Medical University of Vienna, Vienna, Austria.

Verena Endmayr (V)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

Jan Bauer (J)

Department of Neuroimmunology, Center for Brain Research, Medical University of Vienna, Vienna, Austria.

Stefan Macher (S)

Department of Neurology, Medical University of Vienna, Vienna, Austria.

Nilufar Mossaheb (N)

Department of Psychiatry and Psychotherapy, Clinical Division of Social Psychiatry, Medical University of Vienna, Vienna, Austria.

Carmen Schwaiger (C)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

Gerda Ricken (G)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

Michael Winklehner (M)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

Sarah Glatter (S)

Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Vienna, Austria.

Markus Breu (M)

Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Vienna, Austria.

Isabella Wimmer (I)

Department of Neurology, Medical University of Vienna, Vienna, Austria.

Gabor G Kovacs (GG)

Department of Laboratory Medicine and Pathobiology and Tanz Centre for Research in Neurodegenerative Disease, University of Toronto, Toronto, ON, Canada.

Daniele U Risser (DU)

Center for Forensic Medicine, Medical University of Vienna, Vienna, Austria.

Nikolaus Klupp (N)

Center for Forensic Medicine, Medical University of Vienna, Vienna, Austria.

Ingrid Simonitsch-Klupp (I)

Department of Pathology, Medical University of Vienna, Vienna, Austria.

Thomas Roetzer (T)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

Paulus Rommer (P)

Department of Neurology, Medical University of Vienna, Vienna, Austria.

Thomas Berger (T)

Department of Neurology, Medical University of Vienna, Vienna, Austria.

Ellen Gelpi (E)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.
Neurological Tissue Bank of the Biobank-Hospital Clinic-IDIBAPS, Barcelona, Spain.

Hans Lassmann (H)

Department of Neuroimmunology, Center for Brain Research, Medical University of Vienna, Vienna, Austria.

Francesc Graus (F)

Neuroimmunology Programme, Institut d'Investigacions Biomèdiques August Pi i Sunyer Hospital Clínic, University of Barcelona, Barcelona, Spain.

Josep Dalmau (J)

Neuroimmunology Programme, Institut d'Investigacions Biomèdiques August Pi i Sunyer Hospital Clínic, University of Barcelona, Barcelona, Spain.
Department of Neurology, University of Pennsylvania, Philadelphia, PA.
Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.

Romana Höftberger (R)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.

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