Brain age and Alzheimer's-like atrophy are domain-specific predictors of cognitive impairment in Parkinson's disease

Daniel Charissé; Guray Erus; Raymond Pomponio; Martin Gorges; Nele Schmidt; Christine Schneider; Inga Liepelt-Scarfone; Oliver Riedel; Kathrin Reetz; Jörg B Schulz; Daniela Berg; Alexander Storch; Karsten Witt; Richard Dodel; Elke Kalbe; Jan Kassubek; Rüdiger Hilker-Roggendorf; Simon Baudrexel

doi:10.1016/j.neurobiolaging.2021.08.020

Brain age and Alzheimer's-like atrophy are domain-specific predictors of cognitive impairment in Parkinson's disease

Neurobiol Aging. 2022 Jan:109:31-42. doi: 10.1016/j.neurobiolaging.2021.08.020. Epub 2021 Sep 6.

Authors

Daniel Charissé¹, Guray Erus², Raymond Pomponio², Martin Gorges³, Nele Schmidt⁴, Christine Schneider⁵, Inga Liepelt-Scarfone⁶, Oliver Riedel⁷, Kathrin Reetz⁸, Jörg B Schulz⁸, Daniela Berg⁹, Alexander Storch¹⁰, Karsten Witt¹¹, Richard Dodel¹², Elke Kalbe¹³, Jan Kassubek¹⁴, Rüdiger Hilker-Roggendorf¹⁵, Simon Baudrexel¹⁶

Affiliations

¹ Department of Neurology, Goethe University, Frankfurt am Main, Germany; Brain Imaging Center, Goethe University, Frankfurt am Main, Germany.
² Department of Radiology, Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, PA, USA.
³ Germany Institute of Medical Technology, Brandenburg University of Technology Cottbus - Senftenberg, Cottbus, Germany.
⁴ Department of Neurology, Christian Albrecht University, Kiel, Germany; Department of Neurology, Carl von Ossietzky University Oldenburg, Oldenburg, Germany.
⁵ Department of Neurology and Clinical Neurophysiology, University Hospital Augsburg, Augsburg, Germany; Division of Neurodegenerative Diseases, Department of Neurology, Technische Universität Dresden, Dresden, Germany.
⁶ Department of Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, Tübingen, Germany; Studienzentrum Stuttgart, IB Hochschule Stuttgart, Stuttgart, Germany.
⁷ Leibniz Institute for Prevention Research and Epidemiology, Bremen, Germany.
⁸ Department of Neurology, University Hospital, RWTH Aachen University, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Forschungszentrum Jülich GmbH and RWTH Aachen University, Aachen, Germany.
⁹ Department of Neurology, Christian Albrecht University, Kiel, Germany; Department of Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, Tübingen, Germany.
¹⁰ Division of Neurodegenerative Diseases, Department of Neurology, Technische Universität Dresden, Dresden, Germany; Department of Neurology, University of Rostock, Rostock, Germany; German Center for Neurodegenerative Diseases (DZNE) Rostock/Greifswald, Rostock, Germany.
¹¹ Department of Neurology, Christian Albrecht University, Kiel, Germany; Department of Neurology, Carl von Ossietzky University Oldenburg, Oldenburg, Germany; Research Center Neurosensory Science, Carl von Ossietzky University Oldenburg, Oldenburg, Germany.
¹² Department of Neuro-Geriatrics, University Hospital Essen, Essen, Germany; Department of Neurology, Philipps University Marburg, Marburg, Germany.
¹³ Medical Psychology - Neuropsychology and Gender Studies & Center for Neuropsychological Diagnostics and Intervention (CeNDI), Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
¹⁴ Department of Neurology, University of Ulm, Ulm, Germany.
¹⁵ Department of Neurology, Goethe University, Frankfurt am Main, Germany; Department of Neurology, Klinikum Vest, Knappschaftskrankenhaus Recklinghausen, Recklinghausen, Germany.
¹⁶ Department of Neurology, Goethe University, Frankfurt am Main, Germany; Brain Imaging Center, Goethe University, Frankfurt am Main, Germany. Electronic address: simon.baudrexel@kgu.de.

PMID: 34649002
DOI: 10.1016/j.neurobiolaging.2021.08.020

Abstract

Recently, it was shown that patients with Parkinson's disease (PD) who exhibit an "Alzheimer's disease (AD)-like" pattern of brain atrophy are at greater risk for future cognitive decline. This study aimed to investigate whether this association is domain-specific and whether atrophy associated with brain aging also relates to cognitive impairment in PD. SPARE-AD, an MRI index capturing AD-like atrophy, and atrophy-based estimates of brain age were computed from longitudinal structural imaging data of 178 PD patients and 84 healthy subjects from the LANDSCAPE cohort. All patients underwent an extensive neuropsychological test battery. Patients diagnosed with mild cognitive impairment or dementia were found to have higher SPARE-AD scores as compared to patients with normal cognition and healthy controls. All patient groups showed increased brain age. SPARE-AD predicted impairment in memory, language and executive functions, whereas advanced brain age was associated with deficits in attention and working memory. Data suggest that SPARE-AD and brain age are differentially related to domain-specific cognitive decline in PD. The underlying pathomechanisms remain to be determined.

Keywords: Alzheimer's disease; Brain Age; MRI; Parkinson's disease; Pattern classification.

Publication types

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

MeSH terms

Aged
Aging / pathology*
Aging / psychology*
Alzheimer Disease / pathology
Atrophy
Brain / diagnostic imaging
Brain / pathology*
Cognition*
Cognitive Dysfunction / diagnostic imaging
Cognitive Dysfunction / etiology*
Cognitive Dysfunction / pathology*
Cohort Studies
Female
Humans
Magnetic Resonance Imaging / methods
Male
Middle Aged
Neuropsychological Tests
Parkinson Disease / complications
Parkinson Disease / diagnosis
Parkinson Disease / pathology*
Parkinson Disease / psychology*