Presence but not the timing of onset of REM sleep behavior disorder distinguishes evolution patterns in Parkinson's disease.

Humans REM Sleep Behavior Disorder Parkinson Disease / pathology Cross-Sectional Studies Brain / diagnostic imaging Disease Progression
Event-based model Gray matter Neuromelanin Parkinson's disease Rapid eye movement sleep behavior disorder

Journal

Neurobiology of disease
ISSN: 1095-953X
Titre abrégé: Neurobiol Dis
Pays: United States
ID NLM: 9500169

Informations de publication

Date de publication:
05 2023
Historique:
received: 17 01 2023
revised: 09 03 2023
accepted: 14 03 2023
medline: 18 4 2023
pubmed: 18 3 2023
entrez: 17 3 2023
Statut: ppublish

Résumé

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. 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. 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). 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.

Sections du résumé

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.

Identifiants

DOI: 10.1016/j.nbd.2023.106084 PMID: 36931531
pubmed: 36931531
pii: S0969-9961(23)00098-0
doi: 10.1016/j.nbd.2023.106084
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

106084

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors have no conflict of interest to report.

Auteurs

Sijia Tan (S)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 22118579@zju.edu.cn.

Cheng Zhou (C)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 21718289@zju.edu.cn.

Jiaqi Wen (J)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 22018524@zju.edu.cn.

Xiaojie Duanmu (X)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 22118572@zju.edu.cn.

Tao Guo (T)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: taoguo0331@zju.edu.cn.

Haoting Wu (H)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 12018461@zju.edu.cn.

Jingjing Wu (J)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 21818300@zju.edu.cn.

Zhengye Cao (Z)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 0620644@zju.edu.cn.

Xiaocao Liu (X)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 21918568@zju.edu.cn.

Jingwen Chen (J)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 22018523@zju.edu.cn.

Chenqing Wu (C)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 12118575@zju.edu.cn.

Jianmei Qin (J)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: qinjm@zju.edu.cn.

Jingjing Xu (J)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: jingjingxu@zju.edu.cn.

Luyan Gu (L)

Department of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: 21918587@zju.edu.cn.

Yaping Yan (Y)

Department of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: yanyaping@zju.edu.cn.

Baorong Zhang (B)

Department of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: brzhang@zju.edu.cn.

Minming Zhang (M)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: zhangminming@zju.edu.cn.

Xiaojun Guan (X)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: xiaojunguan1102@zju.edu.cn.

Xiaojun Xu (X)

Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China. Electronic address: xxjmailbox@zju.edu.cn.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Presence but not the timing of onset of REM...
questionsmedicales.fr › Troubles mentaux › Troubles de la veille et du sommeil › Parasomnies › Parasomnies du sommeil paradoxal › Trouble du comportement en sommeil paradoxal › Presence but not the timing of onset of REM...
questionsmedicales.fr › Maladies du système nerveux › Maladies neurodégénératives › Maladie de Parkinson › Presence but not the timing of onset of REM...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Méthodes épidémiologiques › Caractéristiques des études épidémiologiques › Études épidémiologiques › Études transversales › Presence but not the timing of onset of REM...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Presence but not the timing of onset of REM...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Caractéristiques de la maladie › Évolution de la maladie › Presence but not the timing of onset of REM...