Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder.,NeuroImage: Clinical

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Characterizing the heterogeneous metabolic progression in idiopathic REM sleep behavior disorder.
NeuroImage: Clinical ( IF 3.4 ) Pub Date : 2020-05-26 , DOI: 10.1016/j.nicl.2020.102294
Xianhua Han ₁ , Ping Wu ₁ , Ian Alberts ₂ , Hucheng Zhou ₃ , Huan Yu ₄ , Panagiotis Bargiotas ₅ , Igor Yakushev ₆ , Jian Wang ₄ , Guenter Höglinger ₇ , Stefan Förster ₈ , Claudio Bassetti ₉ , Wolfgang Oertel ₁₀ , Markus Schwaiger ₁₁ , Sung-Cheng Huang ₁₂ , Paul Cumming ₁₃ , Axel Rominger ₂ , Jiehui Jiang ₃ , Chuantao Zuo ₁₄ , Kuangyu Shi ₁₅

Affiliation

PET Center, Huashan Hospital, Fudan University, Shanghai, China.
Department of Nuclear Medicine, University of Bern, Switzerland.
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.
Department of Neurology, Huashan Hospital, Fudan University, Shanghai, China.
Department of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, Switzerland; Department of Neurology, Medical School, University of Cyprus, Nicosia, Cyprus.
Department of Nuclear Medicine, Technische Universität München, Munich, Germany.
Department of Neurology, Hannover Medical School, Germany.
Department of Nuclear Medicine, Technische Universität München, Munich, Germany; Department of Nuclear Medicine, Klinikum Bayreuth, Germany.
Department of Neurology, University Hospital Bern (Inselspital) and University of Bern, Bern, Switzerland.
Department of Neurology, University of Marburg, Germany.
Klinikum r. d. Isar, Technische Universität München, Munich, Germany.
Department of Molecular and Medical Pharmacology, UCLA, Los Angeles, USA.
Department of Nuclear Medicine, University of Bern, Switzerland; School of Psychology and Counselling and IHBI, Queensland University of Technology, Brisbane, Australia.
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.
Department of Nuclear Medicine, University of Bern, Switzerland; Dept. Informatics, Technische Universität München, Munich, Germany.

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.

中文翻译：

表征特发性REM睡眠行为障碍的异质代谢进程。

目的

特发性快速眼动（REM）睡眠行为障碍（iRBD）是突触性病变（如帕金森氏病（PD））的前驱阶段。具有¹⁸ F-FDG的正电子发射断层扫描（PET）揭示了代谢扰动，这些扰动通过空间协方差分析进行评分。但是，所得的模式得分未捕获单个大脑区域之间新陈代谢变化的空间异质轨迹。假设代谢进展是从健康对照（HC）到iRBD然后是PD的连续过程，我们在横断面研究中研究了逐渐扰动的葡萄糖代谢的空间动力学。

方法

19例iRBD患者，38例PD患者和19例HC患者接受了¹⁸ F-FDG PET。图像在空间上进行了归一化，缩放为整体平均摄取量，并自动进行了分类。我们按组比较了区域新陈代谢，并将推断的进展分配给了几种可能的轨迹之一。我们进一步研究了iRBD和PD组中¹⁸ F-FDG摄取与疾病持续时间之间的相关性。我们还探讨了PD组中¹⁸ F-FDG摄入量与帕金森病疾病统一评估量表运动（UPDRS III）得分之间的关系。

结果

与iRBD患者相比，PD患者表现出更广泛的相对高代谢和低代谢。我们确定了三种动态代谢轨迹：横断面低代谢或高代谢，横断面不变的低代谢或高代谢，横断面晚期低代谢或高代谢，仅在PD与iRBD的对比中出现。在iRBD组中，相对的¹⁸ F-FDG代谢与疾病持续时间之间没有相关性。PD患者的局部高代谢和低代谢与疾病持续时间或临床UPDRS III评分相关。