npj Parkinson's Disease (Nov 2024)
A worldwide study of subcortical shape as a marker for clinical staging in Parkinson’s disease
- Max A. Laansma,
- Yuji Zhao,
- Eva M. van Heese,
- Joanna K. Bright,
- Conor Owens-Walton,
- Sarah Al-Bachari,
- Tim J. Anderson,
- Francesca Assogna,
- Tim D. van Balkom,
- Henk W. Berendse,
- Fernando Cendes,
- John C. Dalrymple-Alford,
- Ines Debove,
- Michiel F. Dirkx,
- Jason Druzgal,
- Hedley C. A. Emsley,
- Jean-Paul Fouche,
- Gaëtan Garraux,
- Rachel P. Guimarães,
- Rick C. Helmich,
- Michele Hu,
- Odile A. van den Heuvel,
- Dmitry Isaev,
- Ho-Bin Kim,
- Johannes C. Klein,
- Christine Lochner,
- Corey T. McMillan,
- Tracy R. Melzer,
- Benjamin Newman,
- Laura M. Parkes,
- Clelia Pellicano,
- Fabrizio Piras,
- Toni L. Pitcher,
- Kathleen L. Poston,
- Mario Rango,
- Leticia F. Ribeiro,
- Cristiane S. Rocha,
- Christian Rummel,
- Lucas S. R. Santos,
- Reinhold Schmidt,
- Petra Schwingenschuh,
- Letizia Squarcina,
- Dan J. Stein,
- Daniela Vecchio,
- Chris Vriend,
- Jiunjie Wang,
- Daniel Weintraub,
- Roland Wiest,
- Clarissa L. Yasuda,
- Neda Jahanshad,
- Paul M. Thompson,
- Ysbrand D. van der Werf,
- Boris A. Gutman
Affiliations
- Max A. Laansma
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Yuji Zhao
- Department of Biomedical Engineering, Illinois Institute of Technology
- Eva M. van Heese
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Joanna K. Bright
- Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London
- Conor Owens-Walton
- Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California
- Sarah Al-Bachari
- Faculty of Health and Medicine, The University of Lancaster
- Tim J. Anderson
- Department of Medicine, University of Otago, Christchurch
- Francesca Assogna
- Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation
- Tim D. van Balkom
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Henk W. Berendse
- Amsterdam UMC, Department Neurology, Vrije Universiteit Amsterdam
- Fernando Cendes
- Department of Neurology, University of Campinas—UNICAMP
- John C. Dalrymple-Alford
- New Zealand Brain Research Institute
- Ines Debove
- Department of Neurology, Inselspital, University of Bern
- Michiel F. Dirkx
- Department of Neurology and Center of Expertise for Parkinson & Movement Disorders, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre
- Jason Druzgal
- Department of Radiology and Medical Imaging, University of Virginia
- Hedley C. A. Emsley
- Lancaster Medical School, Lancaster University
- Jean-Paul Fouche
- Department of Psychiatry and Mental Health, University of Cape Town
- Gaëtan Garraux
- GIGA-CRC in vivo imaging, University of Liège
- Rachel P. Guimarães
- Department of Neurology, University of Campinas—UNICAMP
- Rick C. Helmich
- Department of Neurology and Center of Expertise for Parkinson & Movement Disorders, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre
- Michele Hu
- Division of Clinical Neurology, Department of Clinical Neurosciences, Oxford Parkinson’s Disease Centre, Nuffield, University of Oxford
- Odile A. van den Heuvel
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Dmitry Isaev
- Department of Biomedical Engineering, Duke University
- Ho-Bin Kim
- Department of Neurology & Neurological Sciences, Stanford University
- Johannes C. Klein
- Division of Clinical Neurology, Department of Clinical Neurosciences, Oxford Parkinson’s Disease Centre, Nuffield, University of Oxford
- Christine Lochner
- SA MRC Unit on Risk and Resilience in Mental Disorders, Department of Psychiatry, Stellenbosch University
- Corey T. McMillan
- University of Pennsylvania Perelman School of Medicine
- Tracy R. Melzer
- Department of Medicine, University of Otago, Christchurch
- Benjamin Newman
- Department of Radiology and Medical Imaging, University of Virginia
- Laura M. Parkes
- Division of Psychology, Communication and Human Neuroscience, School of Health Sciences, Faculty of Biology, Medicine and Health, The University of Manchester
- Clelia Pellicano
- Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation
- Fabrizio Piras
- Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation
- Toni L. Pitcher
- Department of Medicine, University of Otago, Christchurch
- Kathleen L. Poston
- Department of Neurology & Neurological Sciences, Stanford University
- Mario Rango
- Excellence Center for Advanced MR Techniques and Parkinson’s Disease Center, Neurology unit, Fondazione IRCCS Cà Granda Maggiore Policlinico Hospital, University of Milan
- Leticia F. Ribeiro
- Department of Neurology, University of Campinas—UNICAMP
- Cristiane S. Rocha
- Department of Neurology, University of Campinas—UNICAMP
- Christian Rummel
- Support Center for Advanced Neuroimaging, (SCAN) University Institute of Diagnostic and Interventional Neuroradiology, Inselspital, Bern University Hospital, University of Bern
- Lucas S. R. Santos
- Department of Neurology, University of Campinas—UNICAMP
- Reinhold Schmidt
- Department of Neurology, Medical University of Graz
- Petra Schwingenschuh
- Department of Neurology, Medical University of Graz
- Letizia Squarcina
- Department of Pathophysiology and Transplantation, University of Milan
- Dan J. Stein
- SA MRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry and Neuroscience Institute, University of Cape Town
- Daniela Vecchio
- Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation
- Chris Vriend
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Jiunjie Wang
- Department of Medical Imaging and Radiological Sciences, Chang Gung University
- Daniel Weintraub
- University of Pennsylvania Perelman School of Medicine
- Roland Wiest
- Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern
- Clarissa L. Yasuda
- Department of Neurology, University of Campinas—UNICAMP
- Neda Jahanshad
- Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California
- Paul M. Thompson
- Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California
- Ysbrand D. van der Werf
- Amsterdam UMC, Department of Anatomy and Neurosciences, Vrije Universiteit Amsterdam
- Boris A. Gutman
- Department of Biomedical Engineering, Illinois Institute of Technology
- DOI
- https://doi.org/10.1038/s41531-024-00825-9
- Journal volume & issue
-
Vol. 10,
no. 1
pp. 1 – 13
Abstract
Abstract Alterations in subcortical brain regions are linked to motor and non-motor symptoms in Parkinson’s disease (PD). However, associations between clinical expression and regional morphological abnormalities of the basal ganglia, thalamus, amygdala and hippocampus are not well established. We analyzed 3D T1-weighted brain MRI and clinical data from 2525 individuals with PD and 1326 controls from 22 global sources in the ENIGMA-PD consortium. We investigated disease effects using mass univariate and multivariate models on the medial thickness of 27,120 vertices of seven bilateral subcortical structures. Shape differences were observed across all Hoehn and Yahr (HY) stages, as well as correlations with motor and cognitive symptoms. Notably, we observed incrementally thinner putamen from HY1, caudate nucleus and amygdala from HY2, hippocampus, nucleus accumbens, and thalamus from HY3, and globus pallidus from HY4–5. Subregions of the thalami were thicker in HY1 and HY2. Largely congruent patterns were associated with a longer time since diagnosis and worse motor symptoms and cognitive performance. Multivariate regression revealed patterns predictive of disease stage. These cross-sectional findings provide new insights into PD subcortical degeneration by demonstrating patterns of disease stage-specific morphology, largely consistent with ongoing degeneration.
