Signature of altered retinal microstructures and electrophysiology in schizophrenia spectrum disorders is associated with disease severity and polygenic risk.

electroretinography (ERG) genetics magnetic resonance imaging (MRI) optical coherence tomography (OCT) retina schizophrenia

Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
26 Apr 2024
Historique:
received: 03 08 2023
revised: 30 03 2024
accepted: 14 04 2024
medline: 29 4 2024
pubmed: 29 4 2024
entrez: 28 4 2024
Statut: aheadofprint

Résumé

Optical coherence tomography (OCT) and electroretinography (ERG) studies have revealed structural and functional retinal alterations in individuals with schizophrenia spectrum disorders (SSD). However, it remains unclear which specific retinal layers are affected, how the retina, brain, and clinical symptomatology are connected, and how alterations of the visual system are related to genetic disease risk. OCT, ERG, and brain magnetic resonance imaging (MRI) were applied to comprehensively investigate the visual system in a cohort of 103 patients with SSD and 130 healthy control individuals. The sparse partial least squares (SPLS) algorithm was used to identify multivariate associations between clinical disease phenotype and biological alterations of the visual system. The association of the revealed patterns with the individual polygenetic disease risk for schizophrenia was explored in a post hoc analysis. In addition, covariate-adjusted case-control comparisons were performed for each individual OCT and ERG parameter. The SPLS analysis yielded a phenotype-eye-brain signature of SSD in which greater disease severity, longer duration of illness, and impaired cognition were associated with electrophysiological alterations and microstructural thinning of most retinal layers. Higher individual loading onto this disease-relevant signature of the visual system was significantly associated with elevated polygenic risk for schizophrenia. In case-control comparisons, patients with SSD had lower macular thickness, thinner retinal nerve fiber and inner plexiform layers, less negative a-wave amplitude, and lower b-wave amplitude. This study demonstrates multimodal microstructural and electrophysiological retinal alterations in individuals with SSD that are associated with disease severity and individual polygenetic burden.

Sections du résumé

BACKGROUND BACKGROUND
Optical coherence tomography (OCT) and electroretinography (ERG) studies have revealed structural and functional retinal alterations in individuals with schizophrenia spectrum disorders (SSD). However, it remains unclear which specific retinal layers are affected, how the retina, brain, and clinical symptomatology are connected, and how alterations of the visual system are related to genetic disease risk.
METHODS METHODS
OCT, ERG, and brain magnetic resonance imaging (MRI) were applied to comprehensively investigate the visual system in a cohort of 103 patients with SSD and 130 healthy control individuals. The sparse partial least squares (SPLS) algorithm was used to identify multivariate associations between clinical disease phenotype and biological alterations of the visual system. The association of the revealed patterns with the individual polygenetic disease risk for schizophrenia was explored in a post hoc analysis. In addition, covariate-adjusted case-control comparisons were performed for each individual OCT and ERG parameter.
RESULTS RESULTS
The SPLS analysis yielded a phenotype-eye-brain signature of SSD in which greater disease severity, longer duration of illness, and impaired cognition were associated with electrophysiological alterations and microstructural thinning of most retinal layers. Higher individual loading onto this disease-relevant signature of the visual system was significantly associated with elevated polygenic risk for schizophrenia. In case-control comparisons, patients with SSD had lower macular thickness, thinner retinal nerve fiber and inner plexiform layers, less negative a-wave amplitude, and lower b-wave amplitude.
CONCLUSIONS CONCLUSIONS
This study demonstrates multimodal microstructural and electrophysiological retinal alterations in individuals with SSD that are associated with disease severity and individual polygenetic burden.

Identifiants

pubmed: 38679358
pii: S0006-3223(24)01262-9
doi: 10.1016/j.biopsych.2024.04.014
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Investigateurs

Valéria de Almeida (V)
Stephanie Behrens (S)
Emanuel Boudriot (E)
Mattia Campana (M)
Fanny Dengl (F)
Peter Falkai (P)
Laura E Fischer (LE)
Nadja Gabellini (N)
Vanessa Gabriel (V)
Thomas Geyer (T)
Katharina Hanken (K)
Alkomiet Hasan (A)
Genc Hasanaj (G)
Georgios Ioannou (G)
Iris Jäger (I)
Sylvia de Jonge (S)
Temmuz Karali (T)
Susanne Karch (S)
Berkhan Karslı (B)
Daniel Keeser (D)
Christoph Kern (C)
Nicole Klimas (N)
Lenka Krčmář (L)
Julian Melcher (J)
Matin Mortazavi (M)
Joanna Moussiopoulou (J)
Karin Neumeier (K)
Frank Padberg (F)
Boris Papazov (B)
Sergi Papiol (S)
Pauline Pingen (P)
Oliver Pogarell (O)
Siegfried Priglinger (S)
Florian J Raabe (FJ)
Lukas Roell (L)
Moritz J Rossner (MJ)
Andrea Schmitt (A)
Susanne Schmölz (S)
Enrico Schulz (E)
Benedikt Schworm (B)
Elias Wagner (E)
Sven Wichert (S)
Vladislav Yakimov (V)
Peter Zill (P)
Florian J Raabe (FJ)

Informations de copyright

Copyright © 2024. Published by Elsevier Inc.

Auteurs

Emanuel Boudriot (E)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany.

Vanessa Gabriel (V)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

David Popovic (D)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany.

Pauline Pingen (P)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Vladislav Yakimov (V)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; International Max Planck Research School for Translational Psychiatry (IMPRS-TP), 80804 Munich, Germany.

Sergi Papiol (S)

Max Planck Institute of Psychiatry, 80804 Munich, Germany; Institute of Psychiatric Phenomics and Genomics, LMU Munich, 80336 Munich, Germany.

Lukas Roell (L)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; NeuroImaging Core Unit Munich (NICUM), LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Genc Hasanaj (G)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Evidence-based psychiatry and psychotherapy, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany.

Simiao Xu (S)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Joanna Moussiopoulou (J)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Siegfried Priglinger (S)

Department of Ophthalmology, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Christoph Kern (C)

Department of Ophthalmology, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Eva C Schulte (EC)

Institute of Psychiatric Phenomics and Genomics, LMU Munich, 80336 Munich, Germany; Institute of Human Genetics, University Hospital, Faculty of Medicine, University of Bonn, 53127 Bonn, Germany; Department of Psychiatry and Psychotherapy, University Hospital, Faculty of Medicine, University of Bonn, 53127 Bonn, Germany.

Alkomiet Hasan (A)

Department of Psychiatry, Psychotherapy, and Psychosomatics, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany; German Center for Mental Health (DZPG), partner site Munich-Augsburg.

Oliver Pogarell (O)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany.

Peter Falkai (P)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany; German Center for Mental Health (DZPG), partner site Munich-Augsburg.

Andrea Schmitt (A)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany; German Center for Mental Health (DZPG), partner site Munich-Augsburg.

Benedikt Schworm (B)

Department of Ophthalmology, LMU University Hospital, LMU Munich, 80336 Munich, Germany.
Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany; Evidence-based psychiatry and psychotherapy, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany; Department of Psychiatry, Psychotherapy, and Psychosomatics, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany.

Elias Wagner (E)

Evidence-based psychiatry and psychotherapy, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany; Department of Psychiatry, Psychotherapy, and Psychosomatics, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany.

Daniel Keeser (D)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; NeuroImaging Core Unit Munich (NICUM), LMU University Hospital, LMU Munich, 80336 Munich, Germany; Munich Center for Neurosciences (MCN), LMU Munich, 82152 Planegg-Martinsried, Germany.

Florian J Raabe (FJ)

Department of Psychiatry and Psychotherapy, LMU University Hospital, LMU Munich, 80336 Munich, Germany; Max Planck Institute of Psychiatry, 80804 Munich, Germany. Electronic address: florian.raabe@med.uni-muenchen.de.

Classifications MeSH