Aerobic glycolysis imaging of epileptic foci during the inter-ictal period

Miao Zhang; Qikai Qin; Shuning Zhang; Wei Liu; Hongping Meng; Mengyang Xu; Xinyun Huang; Xiaozhu Lin; Mu Lin; Peter Herman; Fahmeed Hyder; Raymond C. Stevens; Zheng Wang; Biao Li; Garth J. Thompson

EBioMedicine (May 2022)

Aerobic glycolysis imaging of epileptic foci during the inter-ictal period

Miao Zhang,
Qikai Qin,
Shuning Zhang,
Wei Liu,
Hongping Meng,
Mengyang Xu,
Xinyun Huang,
Xiaozhu Lin,
Mu Lin,
Peter Herman,
Fahmeed Hyder,
Raymond C. Stevens,
Zheng Wang,
Biao Li,
Garth J. Thompson

Affiliations

Miao Zhang: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Qikai Qin: iHuman Institute, ShanghaiTech University, Shanghai 201210, China; School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China; University of Chinese Academy of Sciences, Beijing 100049, China
Shuning Zhang: iHuman Institute, ShanghaiTech University, Shanghai 201210, China; School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China; University of Chinese Academy of Sciences, Beijing 100049, China
Wei Liu: Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Hongping Meng: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Mengyang Xu: iHuman Institute, ShanghaiTech University, Shanghai 201210, China; School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, Shanghai 200031, China
Xinyun Huang: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Xiaozhu Lin: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Mu Lin: MR Collaboration, Siemens Healthineers Ltd., Shanghai 201318, China
Peter Herman: Magnetic Resonance Research Center (MRRC), Yale University, New Haven 06520, USA; Quantitative Neuroscience with Magnetic Resonance (QNMR) Core Center, Yale University, New Haven 06520, USA; Radiology and Biomedical Imaging, Yale University, New Haven 06520, USA
Fahmeed Hyder: Magnetic Resonance Research Center (MRRC), Yale University, New Haven 06520, USA; Quantitative Neuroscience with Magnetic Resonance (QNMR) Core Center, Yale University, New Haven 06520, USA; Radiology and Biomedical Imaging, Yale University, New Haven 06520, USA; Biomedical Engineering, Yale University, New Haven 06520, USA
Raymond C. Stevens: iHuman Institute, ShanghaiTech University, Shanghai 201210, China; School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China
Zheng Wang: School of Psychological and Cognitive Sciences; Beijing Key Laboratory of Behavior and Mental Health; IDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China
Biao Li: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; Collaborative Innovation Center for Molecular Imaging of Precision Medicine, Ruijin Center, Shanghai 200025, China; Corresponding author: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, No.197 Rui Jin 2nd Road, Shanghai, 200025, China.
Garth J. Thompson: iHuman Institute, ShanghaiTech University, Shanghai 201210, China; Corresponding author. Garth J. Thompson iHuman Institute, ShanghaiTech University, 393 Middle Huaxia Road, Pudong, Shanghai, 201210, China.

Journal volume & issue: Vol. 79
p. 104004

Abstract

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Summary: Background: In drug-resistant epilepsy, surgical resection of the epileptic focus can end seizures. However, success is dependent on the ability to identify foci locations and, unfortunately, current methods like electrophysiology and positron emission tomography can give contradictory results. During seizures, glucose is metabolized at epileptic foci through aerobic glycolysis, which can be imaged through the oxygen-glucose index (OGI) biomarker. However, inter-ictal (between seizures) OGI changes have not been studied, which has limited its application. Methods: 18 healthy controls and 24 inter-ictal, temporal lobe epilepsy patients underwent simultaneous positron emission tomography (PET) and magnetic resonance imaging (MRI) scans. We used [18F]fluorodeoxyglucose-PET (FDG-PET) to detect cerebral glucose metabolism, and calibrated functional MRI to acquire relative oxygen consumption. With these data, we calculated relative OGI maps. Findings: While bilaterally symmetrical in healthy controls, we observed, in patients during the inter-ictal period, higher OGI ipsilateral to the epileptic focus than contralateral. While traditional FDG-PET results and temporal lobe OGI results usually both agreed with invasive electrophysiology, in cases where FDG-PET disagreed with electrophysiology, temporal lobe OGI agreed with electrophysiology, and vice-versa. Interpretation: As either our novel epilepsy biomarker or traditional approaches located foci in every case, our work provides promising insights into metabolic changes in epilepsy. Our method allows single-session OGI measurement which can be useful in other diseases. Funding: This work was supported by ShanghaiTech University, the Shanghai Municipal Government, the National Natural Science Foundation of China Grant (No. 81950410637) and Shanghai Municipal Key Clinical Specialty (No. shslczdzk03403). F. H. and P. H. were supported by USA National Institute of Health grants (R01 NS-100106, R01 MH-067528).Z. W. was supported by the Key-Area Research and Development Program of Guangdong Province (2019B030335001), National Natural Science Foundation of China (No. 82151303), and National Key R&D Program of China (No. 2021ZD0204002).

Published in EBioMedicine

ISSN: 2352-3964 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General)
Website: http://www.journals.elsevier.com/ebiomedicine/

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