Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates

Chentao He; Rui Yang; Siming Rong; Piao Zhang; Xi Chen; Qi Qi; Ziqi Gao; Yan Li; Hao Li; Frank-Erik de Leeuw; Anil M. Tuladhar; Marco Duering; Rick C. Helmich; Rick van der Vliet; Sirwan K.L. Darweesh; Zaiyi Liu; Lijuan Wang; Mengfei Cai; Yuhu Zhang

NeuroImage: Clinical (Jan 2024)

Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates

Chentao He,
Rui Yang,
Siming Rong,
Piao Zhang,
Xi Chen,
Qi Qi,
Ziqi Gao,
Yan Li,
Hao Li,
Frank-Erik de Leeuw,
Anil M. Tuladhar,
Marco Duering,
Rick C. Helmich,
Rick van der Vliet,
Sirwan K.L. Darweesh,
Zaiyi Liu,
Lijuan Wang,
Mengfei Cai,
Yuhu Zhang

Affiliations

Chentao He: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China; Guangzhou Key Laboratory of Diagnosis and Treatment for Neurodegenerative Diseases, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China; Guangdong Provincial Key Laboratory of Artificial Intelligence in Medical Image Analysis and Application, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China
Rui Yang: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Siming Rong: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Piao Zhang: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Xi Chen: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Qi Qi: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Ziqi Gao: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Yan Li: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Hao Li: Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands
Frank-Erik de Leeuw: Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands
Anil M. Tuladhar: Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands
Marco Duering: Medical Image Analysis Center (MIAC AG) and Department of Biomedical Engineering, University of Basel, Basel, Switzerland; Institute for Stroke and Dementia Research (ISD), LMU University Hospital, LMU Munich, Germany
Rick C. Helmich: Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands
Rick van der Vliet: Department of Neurology, Erasmus MC, University Medical Centre Rotterdam, Rotterdam, the Netherlands
Sirwan K.L. Darweesh: Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands
Zaiyi Liu: Guangdong Provincial Key Laboratory of Artificial Intelligence in Medical Image Analysis and Application, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China; Department of Radiology, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China
Lijuan Wang: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China; Guangzhou Key Laboratory of Diagnosis and Treatment for Neurodegenerative Diseases, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China
Mengfei Cai: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China; Radboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the Netherlands; Corresponding authors at: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, No. 106 Zhongshan Er Road, Guangzhou 510080, China.
Yuhu Zhang: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, China; Guangzhou Key Laboratory of Diagnosis and Treatment for Neurodegenerative Diseases, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China; Guangdong Provincial Key Laboratory of Artificial Intelligence in Medical Image Analysis and Application, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou 510080, China; Corresponding authors at: Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, No. 106 Zhongshan Er Road, Guangzhou 510080, China.

Journal volume & issue: Vol. 44
p. 103679

Abstract

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Background: Previous research revealed differences in cerebellar white matter integrity by disease stages, indicating a compensatory role in Parkinson’s disease (PD). However, the temporal evolution of cerebellar white matter microstructure in patients with PD (PwPD) remains unclear. Objective: To unravel temporal evolution of cerebellar white matter and its dopaminergic correlates in PD. Methods: We recruited 124 PwPD from the PPMI study. The participants were divided into two subsets: Subset 1 (n = 41) had three MRI scans (baseline, 2 years, and 4 years), and Subset 2 (n = 106) had at least two MRI scans at baseline, 1 year, and/or 2 years. Free water-corrected diffusion metrics were used to measure the microstructural integrity in cerebellar peduncles (CP), the main white matter tracts connecting to and from the cerebellum. The ACAPULCO processing pipeline was used to assess cerebellar lobules volumes. Linear mixed-effect models were used to study longitudinal changes. We also examined the relationships between microstructural integrity in CP, striatal dopamine transporter specific binding ratio (SBR), and clinical symptoms. Results: Microstructural changes in CP showed a non-linear pattern in PwPD. Free water-corrected fractional anisotropy (FAt) increased in the first two years but declined from 2 to 4 years, while free water-corrected mean diffusivity exhibited the opposite trend. The initial increased FAt in CP correlated with cerebellar regional volume atrophy, striatal dopaminergic SBR decline, and worsening clinical symptoms, but this correlation varied across disease stages. Conclusions: Our findings suggest a non-linear evolution of microstructural integrity in CP throughout the course of PD, indicating the adaptive structural reorganization of the cerebellum simultaneously with progressive striatal dopaminergic degeneration in PD.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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