The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

the PRONIA consortium

doi:10.1038/s41386-022-01385-3

The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

the PRONIA consortium

Clinic of Psychiatry and Psychotherapy

12 Citations (Scopus)

Abstract

Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

Original language	English
Journal	Neuropsychopharmacology
Volume	47
Issue number	12
Pages (from-to)	2051-2060
Number of pages	10
ISSN	0893-133X
DOIs	https://doi.org/10.1038/s41386-022-01385-3
Publication status	Published - 11.2022

Funding

The presented work was supported by the grant for the Personalized Prognostic Indicators for early Psychosis management (PRONIA Study): EU-FP7-HEALTH; agreement number: 602152. LK-I is a recipient of an NARSAD Young Investigator Award of the Brain & Behavior Research Foundation No. 28474. TL was additionally supported by the Koeln Fortune Program/Faculty of Medicine, University of Cologne. RL received additional funding from the European Unions Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 734227. Open Access funding enabled and organized by Projekt DEAL. The PRONIA consortium : Principal investigator and primary contact is Prof. Nikolaos Koutsouleris ([email protected]). PRONIA consortium members listed here performed the screening, recruitment, rating, examination, and follow-up of the study participants and were involved in implementing the examination protocols of the study, setting up its information technological infrastructure, and organizing the flow and quality control of the data analyzed in this article between the local study sites and the central study database. Department of Psychiatry and Psychotherapy, Ludwig-Maximilian-University, Munich, Germany: Alkomiet Hasan, Claudius Hoff, Ifrah Khanyaree, Aylin Melo, Susanna Muckenhuber-Sternbauer, Yanis Köhler, Ömer Öztürk, Nora Penzel, David Popovic, Adrian Rangnick, Sebastian von Saldern, Rachele Sanfelici, Moritz Spangemacher, Ana Tupac, Maria Fernanda Urquijo, Johanna Weiske, Antonia Wosgien, Camilla Krämer. Department of Psychiatry and Psychotherapy, University of Cologne, Cologne, Germany: Karsten Blume, Dominika Julkowski, Nathalie Kaden, Ruth Milz, Alexandra Nikolaides, Mauro, Silke Vent, Martina Wassen. Department of Psychiatry (Psychiatric University Hospital, UPK), University of Basel, Switzerland: Christina Andreou, Laura Egloff, Fabienne Harrisberger, Ulrike Heitz, Claudia Lenz, Letizia Leanza, Amatya Mackintosh, Renata Smieskova, Erich Studerus, Anna Walter, Sonja Widmayer. Institute for Mental Health & School of Psychology, University of Birmingham, United Kingdom: Chris Day, Sian Lowri Griffiths, Mariam Iqbal, Mirabel Pelton, Pavan Mallikarjun, Alexandra Stainton, Ashleigh Lin, Paris Lalousis. Department of Psychiatry, University of Turku, Finland : Alexander Denissoff, Anu Ellilä, Tiina From, Markus Heinimaa, Tuula Ilonen, Päivi Jalo, Heikki Laurikainen, Antti Luutonen, Akseli Mäkela, Janina Paju, Henri Pesonen, Reetta-Liina Säilä, Anna Toivonen, Otto Turtonen. Department of Psychiatry (Psychiatric University Hospital LVR/HHU Düsseldorf), University of Düsseldorf, Germany: Sonja Botterweck, Norman Kluthausen, Gerald Antoch, Julian Caspers, Hans-Jörg Wittsack. General Electric Global Research Inc., USA. Ana Beatriz Solana, Manuela Abraham, Timo Schirmer. Workgroup of Paolo Brambilla, University of Milan, Italy: Department of Neuroscience and Mental Health, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, University of Milan, Milan, Italy: Carlo Altamura, Marika Belleri, Francesca Bottinelli, Adele Ferro, Marta Re. Programma2000, Niguarda Hospital, Milan: Emiliano Monzani, Maurizio Sberna. San Paolo Hospital, Milan: Armando D’Agostino, Lorenzo Del Fabro. Villa San Benedetto Menni, Albese con Cassano (CO): Giampaolo Perna, Maria Nobile, Alessandra Alciati. Workgroup of Paolo Brambilla at the University of Udine, Italy. Department of Medical Area, University of Udine, Udine, Italy: Matteo Balestrieri, Carolina Bonivento, Giuseppe Cabras, Franco Fabbro. IRCCS Scientific Institute “E. Medea”, Polo FVG, Udine: Marco Garzitto, Sara Piccin RU reports grants from the Medical Research Council, National Institute for Health Research: Health Technology Assessment, the National Institute of Mental Health, and personal fees from Sunovion, Springer Heathcare and Vitaris outside the submitted work. TL reports funding from Koeln Fortune Program/Faculty of Medicine, University of Cologne (No 370/2020) outside the submitted work. RL participated in advisory boards and received honoraria for talks presented at educational meetings organized by Janssen-Cilag, Otsuka/Lundbeck and ROVI outside the submitted work. No other conflicts of interest were reported.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 10 Reduced Inequalities

Research Areas and Centers

Academic Focus: Center for Brain, Behavior and Metabolism (CBBM)

DFG Research Classification Scheme

2.23-08 Human Cognitive and Systems Neuroscience
2.23-09 Biological Psychiatry

Access to Document

10.1038/s41386-022-01385-3

Cite this

@article{b67440d70ab6494b99bdf6e81ef6db63,

title = "The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis",

abstract = "Subtle subjective visual dysfunctions (VisDys) are reported by about 50\% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34\%), and CHR (55.94\%) than in ROD (16.56\%), and HC (4.28\%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17\%, p = 0.0001) and CHR (67.38\%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11\%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.",

author = "Schwarzer, \{Johanna M.\} and Inga Meyhoefer and Antonucci, \{Linda A.\} and Lana Kambeitz-Ilankovic and Marian Surmann and Olga Bienek and Georg Romer and Udo Dannlowski and Tim Hahn and Alexandra Korda and Dwyer, \{Dominic B.\} and Anne Ruef and Haas, \{Shalaila S.\} and Marlene Rosen and Theresa Lichtenstein and Stephan Ruhrmann and Joseph Kambeitz and Salokangas, \{Raimo K.R.\} and Christos Pantelis and Frauke Schultze-Lutter and Eva Meisenzahl and Paolo Brambilla and Alessandro Bertolino and Stefan Borgwardt and Rachel Upthegrove and Nikolaos Koutsouleris and Rebekka Lencer and Alkomiet Hasan and Claudius Hoff and Ifrah Khanyaree and Aylin Melo and Susanna Muckenhuber-Sternbauer and Yanis K{\"o}hler and {\"O}mer {\"O}zt{\"u}rk and Nora Penzel and David Popovic and Adrian Rangnick and \{von Saldern\}, Sebastian and Rachele Sanfelici and Moritz Spangemacher and Ana Tupac and Urquijo, \{Maria Fernanda\} and Johanna Weiske and Antonia Wosgien and Camilla Kr{\"a}mer and Karsten Blume and Dominika Julkowski and Nathalie Kaden and Ruth Milz and \{the PRONIA consortium\} and Christina Andreou",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = nov,

doi = "10.1038/s41386-022-01385-3",

language = "English",

volume = "47",

pages = "2051--2060",

journal = "Neuropsychopharmacology",

issn = "0893-133X",

publisher = "Springer Nature",

number = "12",

}

TY - JOUR

T1 - The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

AU - Schwarzer, Johanna M.

AU - Meyhoefer, Inga

AU - Antonucci, Linda A.

AU - Kambeitz-Ilankovic, Lana

AU - Surmann, Marian

AU - Bienek, Olga

AU - Romer, Georg

AU - Dannlowski, Udo

AU - Hahn, Tim

AU - Korda, Alexandra

AU - Dwyer, Dominic B.

AU - Ruef, Anne

AU - Haas, Shalaila S.

AU - Rosen, Marlene

AU - Lichtenstein, Theresa

AU - Ruhrmann, Stephan

AU - Kambeitz, Joseph

AU - Salokangas, Raimo K.R.

AU - Pantelis, Christos

AU - Schultze-Lutter, Frauke

AU - Meisenzahl, Eva

AU - Brambilla, Paolo

AU - Bertolino, Alessandro

AU - Borgwardt, Stefan

AU - Upthegrove, Rachel

AU - Koutsouleris, Nikolaos

AU - Lencer, Rebekka

AU - Hasan, Alkomiet

AU - Hoff, Claudius

AU - Khanyaree, Ifrah

AU - Melo, Aylin

AU - Muckenhuber-Sternbauer, Susanna

AU - Köhler, Yanis

AU - Öztürk, Ömer

AU - Penzel, Nora

AU - Popovic, David

AU - Rangnick, Adrian

AU - von Saldern, Sebastian

AU - Sanfelici, Rachele

AU - Spangemacher, Moritz

AU - Tupac, Ana

AU - Urquijo, Maria Fernanda

AU - Weiske, Johanna

AU - Wosgien, Antonia

AU - Krämer, Camilla

AU - Blume, Karsten

AU - Julkowski, Dominika

AU - Kaden, Nathalie

AU - Milz, Ruth

AU - the PRONIA consortium

AU - Andreou, Christina

PY - 2022/11

Y1 - 2022/11

N2 - Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

AB - Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

UR - https://www.scopus.com/pages/publications/85136273843

U2 - 10.1038/s41386-022-01385-3

DO - 10.1038/s41386-022-01385-3

M3 - Journal articles

C2 - 35982238

AN - SCOPUS:85136273843

SN - 0893-133X

VL - 47

SP - 2051

EP - 2060

JO - Neuropsychopharmacology

JF - Neuropsychopharmacology

IS - 12

ER -

The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

Abstract

Funding

UN SDGs

Research Areas and Centers

DFG Research Classification Scheme

Access to Document

Other files and links

Fingerprint

Cite this