Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease
Background: Rapid eye movement (REM) sleep behavior disorder (RBD) could develop preceding or come after motor symptoms during Parkinson's disease (PD). It remains unknown that whether PD with different timing of RBD onset relative to motor symptoms suggests different spatiotemporal sequence of...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-05-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996123000980 |
| _version_ | 1797847329584185344 |
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| author | Sijia Tan Cheng Zhou Jiaqi Wen Xiaojie Duanmu Tao Guo Haoting Wu Jingjing Wu Zhengye Cao Xiaocao Liu Jingwen Chen Chenqing Wu Jianmei Qin Jingjing Xu Luyan Gu Yaping Yan Baorong Zhang Minming Zhang Xiaojun Guan Xiaojun Xu |
| author_facet | Sijia Tan Cheng Zhou Jiaqi Wen Xiaojie Duanmu Tao Guo Haoting Wu Jingjing Wu Zhengye Cao Xiaocao Liu Jingwen Chen Chenqing Wu Jianmei Qin Jingjing Xu Luyan Gu Yaping Yan Baorong Zhang Minming Zhang Xiaojun Guan Xiaojun Xu |
| author_sort | Sijia Tan |
| collection | DOAJ |
| description | Background: Rapid eye movement (REM) sleep behavior disorder (RBD) could develop preceding or come after motor symptoms during Parkinson's disease (PD). It remains unknown that whether PD with different timing of RBD onset relative to motor symptoms suggests different spatiotemporal sequence of neurodegeneration. This study aimed to explore the sequence of disease progression in crucially involved brain regions in PD with different timing of RBD onset. Method: We recruited 157 PD, 16 isolated RBD (iRBD), and 78 healthy controls. PD patients were identified as (1) PD with RBD preceding motor symptoms (PD-preRBD, n = 50), (2) PD with RBD posterior to motor symptoms (PD-postRBD, n = 31), (3) PD without RBD (PD-nonRBD, n = 75). The volumes of crucial brain regions, including the basal ganglia and limbic structures in T1-weighted imaging, and the contrast-noise-ratios of locus coeruleus (LC) and substantia nigra (SN) in neuromelanin-sensitive magnetic resonance imaging, were extracted. To simulate the sequence of disease progression for cross-sectional data, an event-based model was introduced to estimate the maximum likelihood sequence of regions' involvement for each group. Then, a statistical parameter, the Bhattacharya coefficient (BC), was used to evaluate the similarity of the sequence. Results: The model predicted that SN occupied the highest likelihood in the maximum likelihood sequence of disease progression in the all PD subgroups, while LC was specifically positioned earlier to SN in iRBD, a prodromal phase of PD. Subsequent early involvement of LC was observed in the both PD-preRBD and PD-postRBD. In contrast, atrophy in the para-hippocampal gyrus but relatively intact LC in the early stage was demonstrated in PD-nonRBD. Then, the similarity comparisons indicated higher BC between PD-postRBD and PD-preRBD (BC = 0.76) but lower BC between PD-postRBD and PD-nonRBD group (BC = 0.41). iRBD had higher BC against PD-preRBD (BC = 0.66) and PD-postRBD (BC = 0.63) but lower BC against PD- nonRBD (BC = 0.48). Conclusion: The spatiotemporal sequence of neurodegeneration between PD-pre and PD-post were similar but distinct from PD-nonRBD. The presence of RBD may be the essential factor for differentiating the degeneration patterns of PD, but the timing of RBD onset has currently proved to be not. |
| first_indexed | 2024-04-09T18:09:32Z |
| format | Article |
| id | doaj.art-ec4112d6fa884d23b57551b188aa5b72 |
| institution | Directory Open Access Journal |
| issn | 1095-953X |
| language | English |
| last_indexed | 2024-04-09T18:09:32Z |
| publishDate | 2023-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj.art-ec4112d6fa884d23b57551b188aa5b722023-04-14T04:18:46ZengElsevierNeurobiology of Disease1095-953X2023-05-01180106084Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's diseaseSijia Tan0Cheng Zhou1Jiaqi Wen2Xiaojie Duanmu3Tao Guo4Haoting Wu5Jingjing Wu6Zhengye Cao7Xiaocao Liu8Jingwen Chen9Chenqing Wu10Jianmei Qin11Jingjing Xu12Luyan Gu13Yaping Yan14Baorong Zhang15Minming Zhang16Xiaojun Guan17Xiaojun Xu18Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Corresponding authors at: Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, No.88 Jiefang Road, Shangcheng District, Hangzhou, China.Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Corresponding authors at: Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, No.88 Jiefang Road, Shangcheng District, Hangzhou, China.Background: Rapid eye movement (REM) sleep behavior disorder (RBD) could develop preceding or come after motor symptoms during Parkinson's disease (PD). It remains unknown that whether PD with different timing of RBD onset relative to motor symptoms suggests different spatiotemporal sequence of neurodegeneration. This study aimed to explore the sequence of disease progression in crucially involved brain regions in PD with different timing of RBD onset. Method: We recruited 157 PD, 16 isolated RBD (iRBD), and 78 healthy controls. PD patients were identified as (1) PD with RBD preceding motor symptoms (PD-preRBD, n = 50), (2) PD with RBD posterior to motor symptoms (PD-postRBD, n = 31), (3) PD without RBD (PD-nonRBD, n = 75). The volumes of crucial brain regions, including the basal ganglia and limbic structures in T1-weighted imaging, and the contrast-noise-ratios of locus coeruleus (LC) and substantia nigra (SN) in neuromelanin-sensitive magnetic resonance imaging, were extracted. To simulate the sequence of disease progression for cross-sectional data, an event-based model was introduced to estimate the maximum likelihood sequence of regions' involvement for each group. Then, a statistical parameter, the Bhattacharya coefficient (BC), was used to evaluate the similarity of the sequence. Results: The model predicted that SN occupied the highest likelihood in the maximum likelihood sequence of disease progression in the all PD subgroups, while LC was specifically positioned earlier to SN in iRBD, a prodromal phase of PD. Subsequent early involvement of LC was observed in the both PD-preRBD and PD-postRBD. In contrast, atrophy in the para-hippocampal gyrus but relatively intact LC in the early stage was demonstrated in PD-nonRBD. Then, the similarity comparisons indicated higher BC between PD-postRBD and PD-preRBD (BC = 0.76) but lower BC between PD-postRBD and PD-nonRBD group (BC = 0.41). iRBD had higher BC against PD-preRBD (BC = 0.66) and PD-postRBD (BC = 0.63) but lower BC against PD- nonRBD (BC = 0.48). Conclusion: The spatiotemporal sequence of neurodegeneration between PD-pre and PD-post were similar but distinct from PD-nonRBD. The presence of RBD may be the essential factor for differentiating the degeneration patterns of PD, but the timing of RBD onset has currently proved to be not.http://www.sciencedirect.com/science/article/pii/S0969996123000980Parkinson's diseaseRapid eye movement sleep behavior disorderEvent-based modelGray matterNeuromelanin |
| spellingShingle | Sijia Tan Cheng Zhou Jiaqi Wen Xiaojie Duanmu Tao Guo Haoting Wu Jingjing Wu Zhengye Cao Xiaocao Liu Jingwen Chen Chenqing Wu Jianmei Qin Jingjing Xu Luyan Gu Yaping Yan Baorong Zhang Minming Zhang Xiaojun Guan Xiaojun Xu Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease Neurobiology of Disease Parkinson's disease Rapid eye movement sleep behavior disorder Event-based model Gray matter Neuromelanin |
| title | Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease |
| title_full | Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease |
| title_fullStr | Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease |
| title_full_unstemmed | Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease |
| title_short | Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease |
| title_sort | presence but not the timing of onset of rem sleep behavior disorder distinguishes evolution patterns in parkinson s disease |
| topic | Parkinson's disease Rapid eye movement sleep behavior disorder Event-based model Gray matter Neuromelanin |
| url | http://www.sciencedirect.com/science/article/pii/S0969996123000980 |
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