Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy

Background: The use of electrocorticography (ECoG) to avoid intraoperative stimulation-induced seizure (ISS) during awake craniotomy is controversial. Although a standard direct cortical stimulating (DCS) protocol is used to identify the eloquent cortices and subcortical structures, ISS still occurs...

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Main Authors: Shengyu Fang, Chunyao Zhou, Lei Wang, Xing Fan, Yinyan Wang, Zhong Zhang, Tao Jiang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.602716/full
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author Shengyu Fang
Shengyu Fang
Chunyao Zhou
Lei Wang
Xing Fan
Xing Fan
Yinyan Wang
Zhong Zhang
Tao Jiang
Tao Jiang
Tao Jiang
author_facet Shengyu Fang
Shengyu Fang
Chunyao Zhou
Lei Wang
Xing Fan
Xing Fan
Yinyan Wang
Zhong Zhang
Tao Jiang
Tao Jiang
Tao Jiang
author_sort Shengyu Fang
collection DOAJ
description Background: The use of electrocorticography (ECoG) to avoid intraoperative stimulation-induced seizure (ISS) during awake craniotomy is controversial. Although a standard direct cortical stimulating (DCS) protocol is used to identify the eloquent cortices and subcortical structures, ISS still occurs. Epilepsy is related to alterations in brain networks. In this study, we investigated specific alterations in brain networks in patients with ISS.Methods: Twenty-seven patients with glioma were enrolled and categorized into the ISS and non-ISS groups based on their history of ISS occurrence. A standard DCS protocol was used during awake craniotomy without ECoG supervision. Graph theoretical measurement was used to analyze resting-state functional magnetic resonance imaging data to quantitatively reveal alterations in the functional networks.Results: In the sensorimotor networks, the glioma significantly decreased the functional connectivity (FC) of four edges in the ISS group, which were conversely increased in the non-ISS group after multiple corrections (p < 0.001, threshold of p-value = 0.002). Regarding the topological properties, the sensorimotor network of all participants was classified as a small-world network. Glioma significantly increased global efficiency, nodal efficiency, and the sigma value, as well as decreased the shortest path length in the ISS group compared with the non-ISS group (p < 0.05).Conclusions: The specific alterations indicating patient susceptibility to ISS during DCS increased global and nodal efficiencies and decreased the shortest path length and FC induced by gliomas. If the patient has these specific alterations, ECoG is recommended to monitor after-discharge current during DCS to avoid ISS.
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spelling doaj.art-34249e70be904ebe8791061575eff9702022-12-21T22:21:04ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-03-011210.3389/fneur.2021.602716602716Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake CraniotomyShengyu Fang0Shengyu Fang1Chunyao Zhou2Lei Wang3Xing Fan4Xing Fan5Yinyan Wang6Zhong Zhang7Tao Jiang8Tao Jiang9Tao Jiang10Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaResearch Unit of Accurate Diagnosis, Treatment, and Translational Medicine of Brain Tumors Chinese (2019RU11), Chinese Academy of Medical Sciences, Beijing, ChinaBackground: The use of electrocorticography (ECoG) to avoid intraoperative stimulation-induced seizure (ISS) during awake craniotomy is controversial. Although a standard direct cortical stimulating (DCS) protocol is used to identify the eloquent cortices and subcortical structures, ISS still occurs. Epilepsy is related to alterations in brain networks. In this study, we investigated specific alterations in brain networks in patients with ISS.Methods: Twenty-seven patients with glioma were enrolled and categorized into the ISS and non-ISS groups based on their history of ISS occurrence. A standard DCS protocol was used during awake craniotomy without ECoG supervision. Graph theoretical measurement was used to analyze resting-state functional magnetic resonance imaging data to quantitatively reveal alterations in the functional networks.Results: In the sensorimotor networks, the glioma significantly decreased the functional connectivity (FC) of four edges in the ISS group, which were conversely increased in the non-ISS group after multiple corrections (p < 0.001, threshold of p-value = 0.002). Regarding the topological properties, the sensorimotor network of all participants was classified as a small-world network. Glioma significantly increased global efficiency, nodal efficiency, and the sigma value, as well as decreased the shortest path length in the ISS group compared with the non-ISS group (p < 0.05).Conclusions: The specific alterations indicating patient susceptibility to ISS during DCS increased global and nodal efficiencies and decreased the shortest path length and FC induced by gliomas. If the patient has these specific alterations, ECoG is recommended to monitor after-discharge current during DCS to avoid ISS.https://www.frontiersin.org/articles/10.3389/fneur.2021.602716/fullintraoperative stimulation-induced epilepsydirect cortical stimulatinggliomaseizuresensorimotor network
spellingShingle Shengyu Fang
Shengyu Fang
Chunyao Zhou
Lei Wang
Xing Fan
Xing Fan
Yinyan Wang
Zhong Zhang
Tao Jiang
Tao Jiang
Tao Jiang
Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
Frontiers in Neurology
intraoperative stimulation-induced epilepsy
direct cortical stimulating
glioma
seizure
sensorimotor network
title Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
title_full Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
title_fullStr Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
title_full_unstemmed Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
title_short Characteristic Alterations of Network in Patients With Intraoperative Stimulation-Induced Seizures During Awake Craniotomy
title_sort characteristic alterations of network in patients with intraoperative stimulation induced seizures during awake craniotomy
topic intraoperative stimulation-induced epilepsy
direct cortical stimulating
glioma
seizure
sensorimotor network
url https://www.frontiersin.org/articles/10.3389/fneur.2021.602716/full
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