Zhang Xiaokang, Zhang Guobin, Wang Yonggang, Huang Huawei, Li Haoyi, Li Mingxiao, Yang Chuanwei, Li Ming, Chen Hongyan, Jing Bin, Lin Song
1Department of Neurosurgery, China National Clinical Research Center for Neurological Diseases (NCRC-ND), Beijing Tiantan Hospital, Capital Medical University.
3Beijing Key Laboratory of Brain Tumor, Beijing Tiantan Hospital, Capital Medical University.
J Neurosurg. 2022 Oct 14;138(6):1512-1521. doi: 10.3171/2022.8.JNS22591. Print 2023 Jun 1.
Patients with frontal gliomas often experience executive dysfunction (EF-D) before surgery, and the changes in brain plasticity underlying this effect remain obscure. In this study, the authors aimed to assess whole-brain structural and functional alterations by using structural MRI and resting-state functional MRI (rs-fMRI) in frontal glioma patients with or without EF-D.
Fifty-seven patients with frontal gliomas were admitted prospectively to the authors' institution and assigned to one of two groups: 1) the normal executive function (EF-N) group and 2) the EF-D group, based on patient results for the Trail Making Test, Part B and Stroop Color-Word Test, Part C. Twenty-nine baseline-matched healthy controls were also recruited. All participants underwent multimodal MRI examination. Cortical surface thickness, surface-based resting-state activity (fractional amplitude of low-frequency fluctuation [fALFF] and regional homogeneity [ReHo]), and edge-based network functional connectivity (FC) were measured with FreeSurfer and fMRIPrep. The correlation between altered MRI parameters and executive function (EF) was assessed using Pearson correlation and receiver operating characteristic (ROC) analysis.
Demographic characteristics (sex, age, and education level) and clinical characteristics (location, volume, grade of tumor, and preoperative epilepsy) were not significantly different between the groups, but the Karnofsky Performance Scale score was worse in the EF-D group. There was no significant difference in cortical surface thickness between the EF-D and EF-N groups. In both low-grade and high-grade glioma patients the fALFF value (permutation test + threshold-free cluster enhancement, p value after family-wise error correction < 0.05) and ReHo value (t-test, p < 0.001) of the left precuneus cortex in the EF-D group were greater than those in the EF-N group, which were negatively correlated with EF (p < 0.05) and enabled prediction of EF (area under the ROC curve 0.826 for fALFF and 0.855 for ReHo, p < 0.001). Compared with the EF-N group, the FCs between the default mode network (DMN) from DMN node to DMN node (DMN-DMN) and from the DMN to the central executive network (DMN-CEN) in the EF-D group were increased significantly (network-based statistics corrected p < 0.05) and negatively correlated with EF (Pearson correlation, p < 0.05).
Apart from local disruption, the abnormally activated DMN in the resting state is related to EF-D in frontal glioma patients. DMN activity should be considered during preoperative planning and postoperative neurorehabilitation for frontal glioma patients to preserve EF. Clinical trial registration no.: NCT03087838 (ClinicalTrials.gov).
额叶胶质瘤患者在手术前常出现执行功能障碍（EF-D），而这种影响背后的脑可塑性变化仍不清楚。在本研究中，作者旨在通过结构磁共振成像（MRI）和静息态功能MRI（rs-fMRI）评估有无EF-D的额叶胶质瘤患者的全脑结构和功能改变。
前瞻性纳入57例额叶胶质瘤患者，并根据患者的连线测验B部分和斯特鲁普色词测验C部分的结果分为两组：1）正常执行功能（EF-N）组和2）EF-D组。还招募了29名年龄、性别和教育程度相匹配的健康对照者。所有参与者均接受多模态MRI检查。使用FreeSurfer和fMRIPrep测量皮质表面厚度、基于表面的静息态活动（低频波动分数振幅[fALFF]和局部一致性[ReHo]）以及基于边缘的网络功能连接（FC）。使用Pearson相关性分析和受试者工作特征（ROC）分析评估MRI参数改变与执行功能（EF）之间的相关性。
两组间人口统计学特征（性别、年龄和教育水平）和临床特征（肿瘤位置、体积、分级和术前癫痫）无显著差异，但EF-D组的卡氏功能状态评分较差。EF-D组和EF-N组之间的皮质表面厚度无显著差异。在低级别和高级别胶质瘤患者中，EF-D组左侧楔前叶皮质的fALFF值（置换检验+无阈值聚类增强，家族性错误校正后的p值<0.05）和ReHo值（t检验，p<0.001）均高于EF-N组，且与EF呈负相关（p<0.05），并能够预测EF（fALFF的ROC曲线下面积为0.826，ReHo为0.855，p<0.001）。与EF-N组相比，EF-D组默认模式网络（DMN）内DMN节点之间（DMN-DMN）以及从DMN到中央执行网络（DMN-CEN）的FC显著增加（基于网络的统计校正p<0.05），且与EF呈负相关（Pearson相关性分析，p<0.05）。
除了局部破坏外，静息状态下异常激活的DMN与额叶胶质瘤患者的EF-D有关。在额叶胶质瘤患者的术前规划和术后神经康复过程中应考虑DMN的活动，以保留EF。临床试验注册号：NCT03087838（ClinicalTrials.gov）。
