Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder
Objective: Idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD) is a prodromal stage of synucleinopathies such as Parkinson’s disease (PD). Positron emission tomography (PET) with 18F-FDG reveals metabolic perturbations, which are scored by spatial covariance analysis. However, the res...
Main Authors: | , , , , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2020-01-01
|
Series: | NeuroImage: Clinical |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158220301315 |
id |
doaj-cf45928cdb0d4da385f7c2688f49c13d |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Xianhua Han Ping Wu Ian Alberts Hucheng Zhou Huan Yu Panagiotis Bargiotas Igor Yakushev Jian Wang Guenter Höglinger Stefan Förster Claudio Bassetti Wolfgang Oertel Markus Schwaiger Sung-Cheng Huang Paul Cumming Axel Rominger Jiehui Jiang Chuantao Zuo Kuangyu Shi |
spellingShingle |
Xianhua Han Ping Wu Ian Alberts Hucheng Zhou Huan Yu Panagiotis Bargiotas Igor Yakushev Jian Wang Guenter Höglinger Stefan Förster Claudio Bassetti Wolfgang Oertel Markus Schwaiger Sung-Cheng Huang Paul Cumming Axel Rominger Jiehui Jiang Chuantao Zuo Kuangyu Shi Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder NeuroImage: Clinical REM sleep behavior disorder Parkinson’s disease PET FDG Conversion |
author_facet |
Xianhua Han Ping Wu Ian Alberts Hucheng Zhou Huan Yu Panagiotis Bargiotas Igor Yakushev Jian Wang Guenter Höglinger Stefan Förster Claudio Bassetti Wolfgang Oertel Markus Schwaiger Sung-Cheng Huang Paul Cumming Axel Rominger Jiehui Jiang Chuantao Zuo Kuangyu Shi |
author_sort |
Xianhua Han |
title |
Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder |
title_short |
Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder |
title_full |
Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder |
title_fullStr |
Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder |
title_full_unstemmed |
Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder |
title_sort |
characterizing the heterogeneous metabolic progression in idiopathic rem sleep behavior disorder |
publisher |
Elsevier |
series |
NeuroImage: Clinical |
issn |
2213-1582 |
publishDate |
2020-01-01 |
description |
Objective: Idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD) is a prodromal stage of synucleinopathies such as Parkinson’s disease (PD). Positron emission tomography (PET) with 18F-FDG reveals metabolic perturbations, which are scored by spatial covariance analysis. However, the resultant pattern scores do not capture the spatially heterogeneous trajectories of metabolic changes between individual brain regions. Assuming metabolic progression occurs as a continuum from the healthy control (HC) condition to iRBD and then PD, we investigated spatial dynamics of progressively perturbed glucose metabolism in a cross-sectional study. Methods: 19 iRBD patients, 38 PD patients and 19 HC subjects underwent 18F-FDG PET. The images were spatially normalized, scaled to the global mean uptake, and automatically parcellated. We contrasted regional metabolism by group, and allocated the inferred progression to one of several possible trajectories. We further investigated the correlations between 18F-FDG uptake and the disease duration in the iRBD and PD groups, respectively. We also explored relationships between 18F-FDG uptake and the Unified Parkinson’s Disease Rating Scale motor (UPDRS III) scores in the PD group. Results: PD patients exhibited more extensive relative hyper- and hypo-metabolism than iRBD patients. We identified three dynamic metabolic trajectories, cross-sectional hypo- or hypermetabolism, cross-sectionally unchanged hypo- or hypermetabolism, cross-sectionally late hypo- or hypermetabolism, appearing only in the contrast of PD with iRBD. No correlation was found between relative 18F-FDG metabolism and disease duration in the iRBD group. Regional hyper- and hypo-metabolism in the PD patients correlated with disease duration or clinical UPDRS III scores. Conclusion: Cerebral metabolism changes heterogeneously in a continuum extending from HC to iRBD and PD groups in this preliminary study. The distinctive metabolic trajectories point towards a potential neuroimaging biomarker for conversion of iRBD to frank PD, which should be amenable to advanced pattern recognition analysis in future longitudinal studies. |
topic |
REM sleep behavior disorder Parkinson’s disease PET FDG Conversion |
url |
http://www.sciencedirect.com/science/article/pii/S2213158220301315 |
work_keys_str_mv |
AT xianhuahan characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT pingwu characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT ianalberts characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT huchengzhou characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT huanyu characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT panagiotisbargiotas characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT igoryakushev characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT jianwang characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT guenterhoglinger characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT stefanforster characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT claudiobassetti characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT wolfgangoertel characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT markusschwaiger characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT sungchenghuang characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT paulcumming characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT axelrominger characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT jiehuijiang characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT chuantaozuo characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder AT kuangyushi characterizingtheheterogeneousmetabolicprogressioninidiopathicremsleepbehaviordisorder |
_version_ |
1724621623201366016 |
spelling |
doaj-cf45928cdb0d4da385f7c2688f49c13d2020-11-25T03:19:33ZengElsevierNeuroImage: Clinical2213-15822020-01-0127102294Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorderXianhua Han0Ping Wu1Ian Alberts2Hucheng Zhou3Huan Yu4Panagiotis Bargiotas5Igor Yakushev6Jian Wang7Guenter Höglinger8Stefan Förster9Claudio Bassetti10Wolfgang Oertel11Markus Schwaiger12Sung-Cheng Huang13Paul Cumming14Axel Rominger15Jiehui Jiang16Chuantao Zuo17Kuangyu Shi18PET Center, Huashan Hospital, Fudan University, Shanghai, ChinaPET Center, Huashan Hospital, Fudan University, Shanghai, ChinaDepartment of Nuclear Medicine, University of Bern, SwitzerlandKey Laboratory of Specialty Fiber Optics and Optical Access Networks, Joint International Research Laboratory of Specialty Fiber Optics and Advanced Communication ,Shanghai Institute for Advanced Communication and Data Science, Shanghai University, Shanghai, ChinaDepartment of Neurology, Huashan Hospital, Fudan University, Shanghai, ChinaDepartment of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, Switzerland; Department of Neurology, Medical School, University of Cyprus, Nicosia, CyprusDepartment of Nuclear Medicine, Technische Universität München, Munich, GermanyDepartment of Neurology, Huashan Hospital, Fudan University, Shanghai, ChinaDepartment of Neurology, Hannover Medical School, GermanyDepartment of Nuclear Medicine, Technische Universität München, Munich, Germany; Department of Nuclear Medicine, Klinikum Bayreuth, GermanyDepartment of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, SwitzerlandDepartment of Neurology, University of Marburg, GermanyKlinikum r. d. Isar, Technische Universität München, Munich, GermanyDepartment of Molecular and Medical Pharmacology, UCLA, Los Angeles, USADepartment of Nuclear Medicine, University of Bern, Switzerland; School of Psychology and Counselling and IHBI, Queensland University of Technology, Brisbane, AustraliaDepartment of Nuclear Medicine, University of Bern, SwitzerlandKey Laboratory of Specialty Fiber Optics and Optical Access Networks, Joint International Research Laboratory of Specialty Fiber Optics and Advanced Communication ,Shanghai Institute for Advanced Communication and Data Science, Shanghai University, Shanghai, China; Corresponding authors at: PET Center, Huashan Hospital, Fudan University, Shanghai, China.PET Center, Huashan Hospital, Fudan University, Shanghai, China; Human Phenome Institute, Fudan University, Shanghai, China; Institute of Functional and Molecular Medical Imaging, Fudan University, Shanghai, China; Corresponding authors at: PET Center, Huashan Hospital, Fudan University, Shanghai, China.Department of Nuclear Medicine, University of Bern, Switzerland; Dept. Informatics, Technische Universität München, Munich, GermanyObjective: Idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD) is a prodromal stage of synucleinopathies such as Parkinson’s disease (PD). Positron emission tomography (PET) with 18F-FDG reveals metabolic perturbations, which are scored by spatial covariance analysis. However, the resultant pattern scores do not capture the spatially heterogeneous trajectories of metabolic changes between individual brain regions. Assuming metabolic progression occurs as a continuum from the healthy control (HC) condition to iRBD and then PD, we investigated spatial dynamics of progressively perturbed glucose metabolism in a cross-sectional study. Methods: 19 iRBD patients, 38 PD patients and 19 HC subjects underwent 18F-FDG PET. The images were spatially normalized, scaled to the global mean uptake, and automatically parcellated. We contrasted regional metabolism by group, and allocated the inferred progression to one of several possible trajectories. We further investigated the correlations between 18F-FDG uptake and the disease duration in the iRBD and PD groups, respectively. We also explored relationships between 18F-FDG uptake and the Unified Parkinson’s Disease Rating Scale motor (UPDRS III) scores in the PD group. Results: PD patients exhibited more extensive relative hyper- and hypo-metabolism than iRBD patients. We identified three dynamic metabolic trajectories, cross-sectional hypo- or hypermetabolism, cross-sectionally unchanged hypo- or hypermetabolism, cross-sectionally late hypo- or hypermetabolism, appearing only in the contrast of PD with iRBD. No correlation was found between relative 18F-FDG metabolism and disease duration in the iRBD group. Regional hyper- and hypo-metabolism in the PD patients correlated with disease duration or clinical UPDRS III scores. Conclusion: Cerebral metabolism changes heterogeneously in a continuum extending from HC to iRBD and PD groups in this preliminary study. The distinctive metabolic trajectories point towards a potential neuroimaging biomarker for conversion of iRBD to frank PD, which should be amenable to advanced pattern recognition analysis in future longitudinal studies.http://www.sciencedirect.com/science/article/pii/S2213158220301315REM sleep behavior disorderParkinson’s diseasePETFDGConversion |