Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy

BackgroundGlioma-related epilepsy (GRE) is a common symptom in patients with prefrontal glioma. Epilepsy onset is associated with functional network alterations. This study investigated alterations of functional networks in patients with prefrontal glioma and GRE.MethodsSixty-five patients with pref...

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Main Authors: Shengyu Fang, Lianwang Li, Shimeng Weng, Yuhao Guo, Zhong Zhang, Lei Wang, Xing Fan, Yinyan Wang, Tao Jiang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-02-01
Series:Frontiers in Oncology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2022.840871/full
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author Shengyu Fang
Shengyu Fang
Lianwang Li
Shimeng Weng
Yuhao Guo
Zhong Zhang
Lei Wang
Xing Fan
Yinyan Wang
Tao Jiang
Tao Jiang
Tao Jiang
author_facet Shengyu Fang
Shengyu Fang
Lianwang Li
Shimeng Weng
Yuhao Guo
Zhong Zhang
Lei Wang
Xing Fan
Yinyan Wang
Tao Jiang
Tao Jiang
Tao Jiang
author_sort Shengyu Fang
collection DOAJ
description BackgroundGlioma-related epilepsy (GRE) is a common symptom in patients with prefrontal glioma. Epilepsy onset is associated with functional network alterations. This study investigated alterations of functional networks in patients with prefrontal glioma and GRE.MethodsSixty-five patients with prefrontal lobe gliomas were retrospectively assessed and classified into GRE and non-GRE groups. Additionally, 25 healthy participants were enrolled after matching for general information. Imaging data were acquired within 72 h in pre-operation. The sensorimotor network was used to delineate alterations in functional connectivity (FC) and topological properties. One-way analysis of variance and post-hoc analysis with Bonferroni correction were used to calculate differences of FC and topological properties.ResultsAll significant alterations were solely found in the sensorimotor network. Irrespective of gliomas located in the left or right prefrontal lobes, the edge between medial Brodmann area 6 and caudal ventrolateral Brodmann area 6 decreased FC in the GRE group compared with the non-GRE group [p < 0.0001 (left glioma), p = 0.0002 (right glioma)]. Moreover, the shortest path length decrease was found in the GRE group compared with the non-GRE group [p = 0.0292 (left glioma) and p = 0.0129 (right glioma)].ConclusionsThe reduction of FC between the medial BA 6 (supplementary motor area) and caudal ventrolateral BA 6 in the ipsilateral hemisphere and the shortening of the path length of the sensorimotor network were characteristics alterations in patients with GRE onset. These findings fill in the gap which is the relationship between GRE onset and the alterations of functional networks in patients with prefrontal glioma.Significance StatementGlioma related epilepsy is the most common symptom of prefrontal glioma. It is important to identify characteristic alterations in functional networks in patients with GRE. We found that all significant alterations occurred in the sensorimotor network. Moreover, a decreased FC in the supplementary motor area and a shortening of the path’s length are additional characteristics of glioma-related epilepsy. We believe that our findings indicate new directions of research that will contribute to future investigations of glioma-related epilepsy onset.
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spelling doaj.art-b084347837db45e0b94bfeaa88ba02432022-12-22T00:01:03ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2022-02-011210.3389/fonc.2022.840871840871Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related EpilepsyShengyu Fang0Shengyu Fang1Lianwang Li2Shimeng Weng3Yuhao Guo4Zhong Zhang5Lei Wang6Xing Fan7Yinyan Wang8Tao Jiang9Tao Jiang10Tao Jiang11Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaBeijing Neurosurgical Institute, 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, ChinaBeijing Neurosurgical Institute, Capital Medical University, Beijing, ChinaResearch Unit of Accurate Diagnosis, Treatment, and Translational Medicine of Brain Tumors, Chinese Academy of Medical Sciences, Beijing, ChinaBackgroundGlioma-related epilepsy (GRE) is a common symptom in patients with prefrontal glioma. Epilepsy onset is associated with functional network alterations. This study investigated alterations of functional networks in patients with prefrontal glioma and GRE.MethodsSixty-five patients with prefrontal lobe gliomas were retrospectively assessed and classified into GRE and non-GRE groups. Additionally, 25 healthy participants were enrolled after matching for general information. Imaging data were acquired within 72 h in pre-operation. The sensorimotor network was used to delineate alterations in functional connectivity (FC) and topological properties. One-way analysis of variance and post-hoc analysis with Bonferroni correction were used to calculate differences of FC and topological properties.ResultsAll significant alterations were solely found in the sensorimotor network. Irrespective of gliomas located in the left or right prefrontal lobes, the edge between medial Brodmann area 6 and caudal ventrolateral Brodmann area 6 decreased FC in the GRE group compared with the non-GRE group [p < 0.0001 (left glioma), p = 0.0002 (right glioma)]. Moreover, the shortest path length decrease was found in the GRE group compared with the non-GRE group [p = 0.0292 (left glioma) and p = 0.0129 (right glioma)].ConclusionsThe reduction of FC between the medial BA 6 (supplementary motor area) and caudal ventrolateral BA 6 in the ipsilateral hemisphere and the shortening of the path length of the sensorimotor network were characteristics alterations in patients with GRE onset. These findings fill in the gap which is the relationship between GRE onset and the alterations of functional networks in patients with prefrontal glioma.Significance StatementGlioma related epilepsy is the most common symptom of prefrontal glioma. It is important to identify characteristic alterations in functional networks in patients with GRE. We found that all significant alterations occurred in the sensorimotor network. Moreover, a decreased FC in the supplementary motor area and a shortening of the path’s length are additional characteristics of glioma-related epilepsy. We believe that our findings indicate new directions of research that will contribute to future investigations of glioma-related epilepsy onset.https://www.frontiersin.org/articles/10.3389/fonc.2022.840871/fullgliomaglioma-related epilepsyfunctional networkgraph theoryhuman
spellingShingle Shengyu Fang
Shengyu Fang
Lianwang Li
Shimeng Weng
Yuhao Guo
Zhong Zhang
Lei Wang
Xing Fan
Yinyan Wang
Tao Jiang
Tao Jiang
Tao Jiang
Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
Frontiers in Oncology
glioma
glioma-related epilepsy
functional network
graph theory
human
title Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
title_full Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
title_fullStr Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
title_full_unstemmed Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
title_short Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy
title_sort decreasing shortest path length of the sensorimotor network induces frontal glioma related epilepsy
topic glioma
glioma-related epilepsy
functional network
graph theory
human
url https://www.frontiersin.org/articles/10.3389/fonc.2022.840871/full
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