Diagnostic and prognostic biomarkers in immune checkpoint inhibitor-related encephalitis: a retrospective cohort study.

Adverse events Autoimmune encephalitis Biomarkers Cancer Cancer immunotherapy Encephalitis Immune checkpoint inhibitors Neural antibodies Neurological immune-related adverse events Paraneoplastic neurological syndromes Prognostic factors

Journal

The Lancet regional health. Europe
ISSN: 2666-7762
Titre abrégé: Lancet Reg Health Eur
Pays: England
ID NLM: 101777707

Informations de publication

Date de publication:
Sep 2024
Historique:
received: 07 04 2024
revised: 06 07 2024
accepted: 11 07 2024
medline: 22 8 2024
pubmed: 22 8 2024
entrez: 22 8 2024
Statut: epublish

Résumé

Immune checkpoint inhibitor-related encephalitis (ICI-encephalitis) is not well characterised and diagnostic and prognostic biomarkers are lacking. We aimed to comprehensively characterise ICI-encephalitis and identify diagnostic biomarkers and outcome predictors. This retrospective observational study included all patients with ICI-encephalitis studied in the French Reference Centre on Paraneoplastic Neurological Syndromes (PNS) and Autoimmune Encephalitis (2015-2023). ICI encephalitis was considered definite in case of inflammatory findings at paraclinical tests and/or well-characterised neural antibodies. Predictors of immune-related adverse event (irAE) treatment response, defined as a Common Terminology Criteria for Adverse Events v5.0 grade < 3 at any time after therapeutic intervention, were assessed by logistic regression analysis, and predictors of mortality by Cox regression analysis. Neurofilament light chain (NfL) was measured by enzyme-linked immunosorbent assay. Sixty-seven patients with definite encephalitis were identified (median age, 69 years; 66% male). A focal syndrome was observed in 43/67 patients (64%; limbic encephalitis, cerebellar ataxia, and/or brainstem encephalitis), while 24/67 (36%) had meningoencephalitis, a non-focal syndrome with altered mental status (22/24 patients, 92%) and pleocytosis (24/24 patients, 100%). Patients with focal encephalitis more frequently had abnormal brain MRI (26/42, 62% ICI-encephalitis corresponds to a set of clinically-recognisable syndromes. Patients with focal encephalitis, PNS-related antibodies, and/or higher serum NfL have low irAE treatment response rates. Research is needed on the underlying immunopathogenesis to foster therapeutic innovations. Agence Nationale de la Recherche.

Sections du résumé

Background UNASSIGNED
Immune checkpoint inhibitor-related encephalitis (ICI-encephalitis) is not well characterised and diagnostic and prognostic biomarkers are lacking. We aimed to comprehensively characterise ICI-encephalitis and identify diagnostic biomarkers and outcome predictors.
Methods UNASSIGNED
This retrospective observational study included all patients with ICI-encephalitis studied in the French Reference Centre on Paraneoplastic Neurological Syndromes (PNS) and Autoimmune Encephalitis (2015-2023). ICI encephalitis was considered definite in case of inflammatory findings at paraclinical tests and/or well-characterised neural antibodies. Predictors of immune-related adverse event (irAE) treatment response, defined as a Common Terminology Criteria for Adverse Events v5.0 grade < 3 at any time after therapeutic intervention, were assessed by logistic regression analysis, and predictors of mortality by Cox regression analysis. Neurofilament light chain (NfL) was measured by enzyme-linked immunosorbent assay.
Findings UNASSIGNED
Sixty-seven patients with definite encephalitis were identified (median age, 69 years; 66% male). A focal syndrome was observed in 43/67 patients (64%; limbic encephalitis, cerebellar ataxia, and/or brainstem encephalitis), while 24/67 (36%) had meningoencephalitis, a non-focal syndrome with altered mental status (22/24 patients, 92%) and pleocytosis (24/24 patients, 100%). Patients with focal encephalitis more frequently had abnormal brain MRI (26/42, 62%
Interpretation UNASSIGNED
ICI-encephalitis corresponds to a set of clinically-recognisable syndromes. Patients with focal encephalitis, PNS-related antibodies, and/or higher serum NfL have low irAE treatment response rates. Research is needed on the underlying immunopathogenesis to foster therapeutic innovations.
Funding UNASSIGNED
Agence Nationale de la Recherche.

Identifiants

pubmed: 39170102
doi: 10.1016/j.lanepe.2024.101011
pii: S2666-7762(24)00178-9
pmc: PMC11338149
doi:

Types de publication

Journal Article

Langues

eng

Pagination

101011

Informations de copyright

© 2024 The Author(s).

Déclaration de conflit d'intérêts

AF, MVG, BJ, and JH are supported by BETPSY, project as part of the second Investissements d'Avenir programme (ANR-18-RHUS-0012) supported by a public grant overseen by the Agence Nationale de la Recherche (ANR). AF received a grant to perform research abroad by the European Academy of Neurology. MVG is supported by Fundación Martín Escudero (non-profit Spanish foundation) to perform research abroad. JH receives royalties from licensing fees to Athena Diagnostics, Euroimmun, and ravo Diagnostika for a patent for the use of anti-CV2/CRMP5 as diagnostic tests. All other authors declare no competing interests.

Auteurs

Antonio Farina (A)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Macarena Villagrán-García (M)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Anthony Fourier (A)

Lyon Neuroscience Research Center (CRNL), Université de Lyon, CNRS, INSERM, Lyon, France.

Anne-Laurie Pinto (AL)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Fatima Chorfa (F)

Service de Biostatistique et Bioinformatique, Pôle Santé Publique, Hospices Civils de Lyon, Lyon, France.

Noémie Timestit (N)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Tifanie Alberto (T)

Department of Neurology, CRC SEP, Centre Hospitalier of Lille, Lille, France.

Jérôme Aupy (J)

Department of Clinical Neurosciences, Centre Hospitalier of Bordeaux, Bordeaux, France.
CNRS, IMN, UMR 5293, University of Bordeaux, Bordeaux, France.

Marie Benaiteau (M)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Cristina Birzu (C)

AP-HP, Hospital Group Pitié-Salpêtrière, Neuro-oncology Department Paris, France.
Inserm U1127, CNRS, Paris Brain Institute, Institut du Cerveau (ICM), Paris, France.

Lucia Campetella (L)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

François Cotton (F)

Radiology Department, Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, Pierre-Bénite, France.

Stéphane Dalle (S)

Deparment of Dermatology, Hospices Civils de Lyon, Centre Hospitalier Lyon Sud, Pierre Bénite, France.
ImmuCare, Institute of Cancerology, Hospices Civils de Lyon, Lyon 69002, France.

Clara Fontaine Delaruelle (CF)

ImmuCare, Institute of Cancerology, Hospices Civils de Lyon, Lyon 69002, France.
Department of Pneumology, Hospices Civils de Lyon, Centre Hospitalier Lyon Sud, Pierre Bénite, France.

Pauline Dumez (P)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Rafaele Germi (R)

Virology, Grenoble-Alpes University Hospital, Grenoble, France.

Marion Le Maréchal (M)

Infectious Disease Unit, Grenoble-Alpes University Hospital, Grenoble, France.

Denis Maillet (D)

ImmuCare, Institute of Cancerology, Hospices Civils de Lyon, Lyon 69002, France.
Department of Medical Oncology, Hospices Civils de Lyon, Centre Hospitalier Lyon Sud, Pierre Bénite, France.

Romain Marignier (R)

Service de Neurologie, Sclérose en Plaques, Pathologies de la Myéline et Neuro-inflammation, Hospices Civils de Lyon, Lyon, France.

Antoine Pegat (A)

Service ENMG et Pathologies Neuromusculaires, Hôpital Neurologique Pierre Wertheimer, Hospices Civils de Lyon, Lyon, France.
Pathophysiology and Genetics of Neuron and Muscle, CNRS UMR 5261, INSERM U1315, INMG, Université Claude Bernard Lyon 1, Faculté de Médecine Lyon Est, Lyon, France.

Dimitri Psimaras (D)

AP-HP, Hospital Group Pitié-Salpêtrière, Neuro-oncology Department Paris, France.
Inserm U1127, CNRS, Paris Brain Institute, Institut du Cerveau (ICM), Paris, France.

Marie Rafiq (M)

Department of Cognitive Neurology, Epilepsy and Movement Disorders, Toulouse Purpan University Hospital Center, Toulouse, France.

Géraldine Picard (G)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Virginie Desestret (V)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Isabelle Quadrio (I)

Lyon Neuroscience Research Center (CRNL), Université de Lyon, CNRS, INSERM, Lyon, France.

Jérôme Honnorat (J)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.

Bastien Joubert (B)

French Reference Centre on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique, Bron, France.
MeLiS-UCBL-CNRS UMR 5284, INSERM U1314, Université Claude Bernard Lyon 1, Lyon, France.
ImmuCare, Institute of Cancerology, Hospices Civils de Lyon, Lyon 69002, France.

Classifications MeSH