Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder

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

NeuroImage: Clinical (Jan 2020)

Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder

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

Affiliations

Xianhua Han: PET Center, Huashan Hospital, Fudan University, Shanghai, China
Ping Wu: PET Center, Huashan Hospital, Fudan University, Shanghai, China
Ian Alberts: Department of Nuclear Medicine, University of Bern, Switzerland
Hucheng Zhou: Key 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
Huan Yu: Department of Neurology, Huashan Hospital, Fudan University, Shanghai, China
Panagiotis Bargiotas: Department of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, Switzerland; Department of Neurology, Medical School, University of Cyprus, Nicosia, Cyprus
Igor Yakushev: Department of Nuclear Medicine, Technische Universität München, Munich, Germany
Jian Wang: Department of Neurology, Huashan Hospital, Fudan University, Shanghai, China
Guenter Höglinger: Department of Neurology, Hannover Medical School, Germany
Stefan Förster: Department of Nuclear Medicine, Technische Universität München, Munich, Germany; Department of Nuclear Medicine, Klinikum Bayreuth, Germany
Claudio Bassetti: Department of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, Switzerland
Wolfgang Oertel: Department of Neurology, University of Marburg, Germany
Markus Schwaiger: Klinikum r. d. Isar, Technische Universität München, Munich, Germany
Sung-Cheng Huang: Department of Molecular and Medical Pharmacology, UCLA, Los Angeles, USA
Paul Cumming: Department of Nuclear Medicine, University of Bern, Switzerland; School of Psychology and Counselling and IHBI, Queensland University of Technology, Brisbane, Australia
Axel Rominger: Department of Nuclear Medicine, University of Bern, Switzerland
Jiehui Jiang: Key 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.
Chuantao Zuo: 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.
Kuangyu Shi: Department of Nuclear Medicine, University of Bern, Switzerland; Dept. Informatics, Technische Universität München, Munich, Germany

Journal volume & issue: Vol. 27
p. 102294

Abstract

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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.

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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