{"title":"Cortical and Network Reorganization in Glioma-Related Epilepsy: Insights From Structural and Machine Learning Analyses","authors":"Xibiao Yang, Jingyuan Zhou, Simin Zhang, Xinke Li, Huaiqiang Sun, Qiang Yue","doi":"10.1155/ane/8965514","DOIUrl":null,"url":null,"abstract":"<p><b>Background:</b> Epilepsy is a common symptom in patients with diffuse lower-grade glioma (DLGG). However, the specific role of cortical alterations in glioma-related epilepsy (GRE) remains unclear. This study is aimed at investigating the reorganization of cortical architecture and network changes associated with GRE.</p><p><b>Materials and Methods:</b> High-resolution T1-weighted and T2-weighted images were acquired from patients with DLGG (GRE = 68, non-GRE = 79) and 94 healthy controls (HCs). Cortical thickness and myelin content were calculated using the Human Connectome Project pipeline. Characteristics of structural covariance networks were computed using graph theory and network-based statistic. Cortical thickness, myelin content, and network characteristics were compared among three groups. A GRE individual prediction model was constructed using an automated machine learning approach.</p><p><b>Results:</b> Compared with HCs, both GRE and non-GRE groups exhibited cortical thinning in the tumor ipsilateral hemisphere, whereas there was cortical thickening in the contralateral hemisphere. Regarding the connectome characteristics, both GRE and non-GRE groups showed decreased nodal efficiency and connections in multiple regions. When comparing GRE with non-GRE, the GRE group exhibited more pronounced cortical thickening and demyelination in the contralateral orbitofrontal gyrus and superior frontal gyrus, with further decreased connections in the sensorimotor network, default mode network, and salience network. Finally, an XGBoost model based on cortical features enabled classification of GRE individuals with an accuracy of 0.80 and an AUC of 0.87.</p><p><b>Conclusion:</b> These findings deepen our understanding of the comprehensive cortical alterations in patients with DLGG and simultaneously provide novel insights into the potential pathophysiological mechanisms underlying GRE.</p>","PeriodicalId":6939,"journal":{"name":"Acta Neurologica Scandinavica","volume":"2025 1","pages":""},"PeriodicalIF":2.9000,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1155/ane/8965514","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Acta Neurologica Scandinavica","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1155/ane/8965514","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Epilepsy is a common symptom in patients with diffuse lower-grade glioma (DLGG). However, the specific role of cortical alterations in glioma-related epilepsy (GRE) remains unclear. This study is aimed at investigating the reorganization of cortical architecture and network changes associated with GRE.
Materials and Methods: High-resolution T1-weighted and T2-weighted images were acquired from patients with DLGG (GRE = 68, non-GRE = 79) and 94 healthy controls (HCs). Cortical thickness and myelin content were calculated using the Human Connectome Project pipeline. Characteristics of structural covariance networks were computed using graph theory and network-based statistic. Cortical thickness, myelin content, and network characteristics were compared among three groups. A GRE individual prediction model was constructed using an automated machine learning approach.
Results: Compared with HCs, both GRE and non-GRE groups exhibited cortical thinning in the tumor ipsilateral hemisphere, whereas there was cortical thickening in the contralateral hemisphere. Regarding the connectome characteristics, both GRE and non-GRE groups showed decreased nodal efficiency and connections in multiple regions. When comparing GRE with non-GRE, the GRE group exhibited more pronounced cortical thickening and demyelination in the contralateral orbitofrontal gyrus and superior frontal gyrus, with further decreased connections in the sensorimotor network, default mode network, and salience network. Finally, an XGBoost model based on cortical features enabled classification of GRE individuals with an accuracy of 0.80 and an AUC of 0.87.
Conclusion: These findings deepen our understanding of the comprehensive cortical alterations in patients with DLGG and simultaneously provide novel insights into the potential pathophysiological mechanisms underlying GRE.
期刊介绍:
Acta Neurologica Scandinavica aims to publish manuscripts of a high scientific quality representing original clinical, diagnostic or experimental work in neuroscience. The journal''s scope is to act as an international forum for the dissemination of information advancing the science or practice of this subject area. Papers in English will be welcomed, especially those which bring new knowledge and observations from the application of therapies or techniques in the combating of a broad spectrum of neurological disease and neurodegenerative disorders. Relevant articles on the basic neurosciences will be published where they extend present understanding of such disorders. Priority will be given to review of topical subjects. Papers requiring rapid publication because of their significance and timeliness will be included as ''Clinical commentaries'' not exceeding two printed pages, as will ''Clinical commentaries'' of sufficient general interest. Debate within the speciality is encouraged in the form of ''Letters to the editor''. All submitted manuscripts falling within the overall scope of the journal will be assessed by suitably qualified referees.