Structural changes in the gray matter of the contralateral hemisphere and prognosis of motor function in children with pharmacoresistant epilepsy before and after hemispherotomy

IF 4.5 2区医学 Q1 NEUROIMAGING

NeuroImage Pub Date : 2025-08-25 DOI:10.1016/j.neuroimage.2025.121429

Yilin Zhao , Dezhi Cao , Fengjun Zhu , Li Chen , Zeshi Tan , Turong Chen , Hongwu Zeng

{"title":"Structural changes in the gray matter of the contralateral hemisphere and prognosis of motor function in children with pharmacoresistant epilepsy before and after hemispherotomy","authors":"Yilin Zhao , Dezhi Cao , Fengjun Zhu , Li Chen , Zeshi Tan , Turong Chen , Hongwu Zeng","doi":"10.1016/j.neuroimage.2025.121429","DOIUrl":null,"url":null,"abstract":"<div><h3>Objective</h3><div>Hemispherotomy (HS) is an effective treatment option to control seizures for children with pharmacoresistant epilepsy. We aimed to explore the alteration of the gray matter structure before and after surgery and identify the specific brain regions associated with preoperative neuropsychological development and postoperative motor development.</div></div><div><h3>Methods</h3><div>We conducted a retrospective study of magnetic resonance imaging (MRI) results, clinical parameters and follow-up data in 46 children who underwent hemispherotomy (HS) at our hospital between 2018 and 2022, and 32 controls were included. Voxel-based morphometry (VBM) and surface-based morphometry (SBM) techniques were employed to quantify the alteration of the gray matter structure. We used Spearman rank correlation and logistic regression models to analyze the influence of different factors on neuropsychological development and motor outcome.</div></div><div><h3>Results</h3><div>46 children with pharmacoresistant epilepsy undergoing hemispherotomy and 32 control subjects were recruited for this study. The patients were divided into two groups according to their surgical side: 29 patients with the left hemispherotomy (13 females, 17 months [IQR, 26 months]) and 17 patients with the right hemispherotomy (11 females, 19 months [IQR, 27.5 months]). Finally, 36 patients completed 13.80±1.54 months (LHS)/ 11.53±1.73 months (RHS) of follow-up, and 89.0 % remained completely seizure-free (outcome scale class IA). The prefrontal cortex showed a positive correlation with neuropsychological development before surgery. Cortical thickness (CT) of the anterior cingulate gyrus was an independent protective factor [OR=18.19, 95 % CI (1.56–212.43), <em>P</em> = 0.021] for motor function prognosis after surgery, while gray matter volume (GMV) of the temporal pole of the middle temporal gyrus was an independent risk factor [OR=0.07, 95 % CI (0.01–0.85), <em>P</em> = 0.037] after surgery.</div></div><div><h3>Significance</h3><div>Preoperative remodeling of prefrontal cortical gray matter structures in the contralateral hemisphere was performed for functional compensation. After surgery, the prefrontal and cingulate cortices resumed the normal developmental trajectories, with the cingulate cortex determining postoperative motor outcome. However, there is irreversible gray matter damage to the temporal lobe, leading to corresponding functional developmental deficits.</div></div>","PeriodicalId":19299,"journal":{"name":"NeuroImage","volume":"319 ","pages":"Article 121429"},"PeriodicalIF":4.5000,"publicationDate":"2025-08-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"NeuroImage","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S105381192500432X","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}

引用次数: 0

Abstract

Objective

Hemispherotomy (HS) is an effective treatment option to control seizures for children with pharmacoresistant epilepsy. We aimed to explore the alteration of the gray matter structure before and after surgery and identify the specific brain regions associated with preoperative neuropsychological development and postoperative motor development.

Methods

We conducted a retrospective study of magnetic resonance imaging (MRI) results, clinical parameters and follow-up data in 46 children who underwent hemispherotomy (HS) at our hospital between 2018 and 2022, and 32 controls were included. Voxel-based morphometry (VBM) and surface-based morphometry (SBM) techniques were employed to quantify the alteration of the gray matter structure. We used Spearman rank correlation and logistic regression models to analyze the influence of different factors on neuropsychological development and motor outcome.

Results

46 children with pharmacoresistant epilepsy undergoing hemispherotomy and 32 control subjects were recruited for this study. The patients were divided into two groups according to their surgical side: 29 patients with the left hemispherotomy (13 females, 17 months [IQR, 26 months]) and 17 patients with the right hemispherotomy (11 females, 19 months [IQR, 27.5 months]). Finally, 36 patients completed 13.80±1.54 months (LHS)/ 11.53±1.73 months (RHS) of follow-up, and 89.0 % remained completely seizure-free (outcome scale class IA). The prefrontal cortex showed a positive correlation with neuropsychological development before surgery. Cortical thickness (CT) of the anterior cingulate gyrus was an independent protective factor [OR=18.19, 95 % CI (1.56–212.43), P = 0.021] for motor function prognosis after surgery, while gray matter volume (GMV) of the temporal pole of the middle temporal gyrus was an independent risk factor [OR=0.07, 95 % CI (0.01–0.85), P = 0.037] after surgery.

Significance

Preoperative remodeling of prefrontal cortical gray matter structures in the contralateral hemisphere was performed for functional compensation. After surgery, the prefrontal and cingulate cortices resumed the normal developmental trajectories, with the cingulate cortex determining postoperative motor outcome. However, there is irreversible gray matter damage to the temporal lobe, leading to corresponding functional developmental deficits.

查看原文本刊更多论文

对侧脑半球灰质结构变化与抗药癫痫患儿运动功能预后研究

目的半脑切开术是控制儿童耐药癫痫发作的有效治疗方法。我们旨在探讨手术前后灰质结构的改变，并确定与术前神经心理发育和术后运动发育相关的特定大脑区域。方法回顾性分析2018 - 2022年在我院行半脑切开术（HS）的46例患儿的磁共振成像（MRI）结果、临床参数及随访资料，并纳入32例对照组。采用基于体素的形态测量（VBM）和基于表面的形态测量（SBM）技术来量化灰质结构的变化。采用Spearman秩相关和logistic回归模型分析不同因素对神经心理发育和运动预后的影响。结果本研究共招募了46例接受半脑切开术的耐药癫痫患儿和32例对照组。根据手术部位分为两组：左半球切除术29例（女性13例，17个月[IQR， 26个月]）和右半球切除术17例（女性11例，19个月[IQR， 27.5个月]）。最终，36例患者完成了13.80±1.54个月(LHS)/ 11.53±1.73个月（RHS）的随访，89.0%的患者完全无癫痫发作（结局量表为IA级）。手术前，前额叶皮层与神经心理发育呈正相关。扣带前回皮质厚度（CT）是术后运动功能预后的独立保护因素[OR=18.19, 95% CI (1.56 ~ 212.43), P = 0.021]，颞中回颞极灰质体积（GMV）是术后运动功能预后的独立危险因素[OR=0.07, 95% CI (0.01 ~ 0.85), P = 0.037]。术前重建对侧半球前额叶皮层灰质结构进行功能补偿。术后，前额叶和扣带皮层恢复正常发育轨迹，扣带皮层决定术后运动预后。然而，颞叶存在不可逆的灰质损伤，导致相应的功能发育缺陷。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

NeuroImage 医学-核医学

CiteScore

11.30

自引率

10.50%

发文量

809

审稿时长

63 days

期刊介绍： NeuroImage, a Journal of Brain Function provides a vehicle for communicating important advances in acquiring, analyzing, and modelling neuroimaging data and in applying these techniques to the study of structure-function and brain-behavior relationships. Though the emphasis is on the macroscopic level of human brain organization, meso-and microscopic neuroimaging across all species will be considered if informative for understanding the aforementioned relationships.