Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates
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 u...
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Elsevier
2024-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158224001207 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Chentao He |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-5fb3e90d29704159a84acee1fd9f177f |
| institution | OA Journals |
| issn | 2213-1582 |
| language | English |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj-art-5fb3e90d29704159a84acee1fd9f177f2025-08-20T01:54:12ZengElsevierNeuroImage: Clinical2213-15822024-01-014410367910.1016/j.nicl.2024.103679Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlatesChentao He0Rui Yang1Siming Rong2Piao Zhang3Xi Chen4Qi Qi5Ziqi Gao6Yan Li7Hao Li8Frank-Erik de Leeuw9Anil M. Tuladhar10Marco Duering11Rick C. Helmich12Rick van der Vliet13Sirwan K.L. Darweesh14Zaiyi Liu15Lijuan Wang16Mengfei Cai17Yuhu Zhang18Department 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, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaDepartment of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, Guangdong Province 510080, ChinaRadboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the NetherlandsRadboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the NetherlandsRadboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the NetherlandsMedical 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, GermanyRadboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the NetherlandsDepartment of Neurology, Erasmus MC, University Medical Centre Rotterdam, Rotterdam, the NetherlandsRadboud University Medical Center, Nijmegen, Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, the NetherlandsGuangdong 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, ChinaDepartment 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, ChinaDepartment 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.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.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.http://www.sciencedirect.com/science/article/pii/S2213158224001207Parkinson’s diseaseCerebellar pedunclesMicrostructural integrityCompensationDopaminergic degeneration |
| spellingShingle | 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 Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates NeuroImage: Clinical Parkinson’s disease Cerebellar peduncles Microstructural integrity Compensation Dopaminergic degeneration |
| title | Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates |
| title_full | Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates |
| title_fullStr | Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates |
| title_full_unstemmed | Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates |
| title_short | Temporal evolution of microstructural integrity in cerebellar peduncles in Parkinson’s disease: Stage-specific patterns and dopaminergic correlates |
| title_sort | temporal evolution of microstructural integrity in cerebellar peduncles in parkinson s disease stage specific patterns and dopaminergic correlates |
| topic | Parkinson’s disease Cerebellar peduncles Microstructural integrity Compensation Dopaminergic degeneration |
| url | http://www.sciencedirect.com/science/article/pii/S2213158224001207 |
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