Neurocognitive and Resting-State Functional Magnetic Resonance Imaging Changes in Patients With Diffuse Gliomas After Chemoradiation Therapy

Zhihua Liu PhD , Timothy J. Mitchell PhD , Chongliang Luo PhD , Ki Yun Park BS , Joshua S. Shimony MD, PhD , Robert Fucetola PhD , Eric C. Leuthardt MD, MBA , Stephanie M. Perkins MD , Abraham Z. Snyder MD, PhD , Tong Zhu PhD, DABR , Jiayi Huang MD, MSCI
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Abstract

Purpose

This prospective observational study employed resting-state functional magnetic resonance imaging (rs-fMRI) to investigate network-level disturbances associated with neurocognitive function (NCF) changes in patients with gliomas following partial-brain radiation therapy (RT).

Methods and Materials

Adult postoperative patients with either isocitrate dehydrogenase (IDH)–wild-type or IDH-mutant gliomas underwent computerized NCF testing and rs-fMRI at baseline and 6 months post-RT. rs-fMRI data were assessed using seed-based functional connectivity (FC). NCF changes were quantified by the percent change in age-normalized composite scores from baseline (ΔNCFcomp). Connectivity regression analysis assessed the association between network FC changes and NCF changes, using a split-sample approach with a 26-patient training set and a 6-patient validation set, iterated 200 times. Permutation tests evaluated the significance of network selection.

Results

Between September 2020 and December 2023, 43 patients were enrolled, with 32 completing both baseline and follow-up evaluations. The mean ΔNCFcomp was 2.9% (SD, 13.7%), with 38% experiencing a decline. Patients with IDH-mutant glioma had similar NCF changes compared with those with IDH–wild-type glioma. Intrahemispheric FC was similar between ipsilateral and contralateral hemispheres for 91% of patients at baseline, and 69% had similar intrahemispheric FC change posttreatment. FC changes accounted for a moderate fraction of variance in NCF changes (mean R2, 0.301; SD, 0.249), with intranetwork FC of the parietal memory network (PMN-PMN, P = .001) and internetwork FC between the PMN and the visual network (PMN-VN, P = .002) as the most significant factors. Similar findings were obtained by sensitivity analyses using only the FC data from the hemisphere contralateral to the tumor.

Conclusions

Post-RT rs-fMRI changes significantly reflected NCF decline, highlighting rs-fMRI as a promising imaging biomarker for neurocognitive decline after RT.
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放化疗后弥漫性胶质瘤患者的神经认知和静息状态功能MRI改变。
背景:这项前瞻性观察研究采用静息状态功能MRI (rs-fMRI)研究神经胶质瘤患者部分脑放射治疗(RT)后神经认知功能(NCF)变化相关的网络水平紊乱。方法:idh野生型或idh突变型胶质瘤的成年术后患者在基线和rt后6个月进行计算机化NCF测试和rs-fMRI。rs-fMRI数据采用基于种子的功能连接(FC)进行评估。NCF变化通过年龄标准化综合评分与基线的百分比变化来量化(ΔNCFcomp)。连接回归分析评估了网络FC变化和NCF变化之间的关联,使用了26例患者训练集和6例患者验证集的分样本方法,迭代200次。排列测试评估了网络选择的重要性。结果:在2020年9月至2023年12月期间,纳入了43例患者,其中32例完成了基线和随访评估。平均值ΔNCFcomp为2.9% (SD: 13.7%),其中38%出现下降。与idh野生型胶质瘤患者相比,idh突变型胶质瘤患者的NCF变化相似。91%的患者在基线时同侧和对侧半球的半球内FC相似,69%的患者在治疗后半球内FC变化相似。在NCF变化中,FC变化占了中等程度的方差(平均R2: 0.301, SD: 0.249),其中顶叶记忆网络的网络内FC (PMN-PMN, p=0.001)和顶叶记忆网络与视觉网络之间的网络间FC (PMN- vn, p=0.002)是最显著的影响因素。通过敏感性分析,仅使用肿瘤对侧半球的FC数据获得了类似的结果。结论:RT后rs-fMRI的变化显著反映了NCF的下降,突出了rs-fMRI作为RT后神经认知功能下降的一种有希望的成像生物标志物。
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来源期刊
CiteScore
11.00
自引率
7.10%
发文量
2538
审稿时长
6.6 weeks
期刊介绍: International Journal of Radiation Oncology • Biology • Physics (IJROBP), known in the field as the Red Journal, publishes original laboratory and clinical investigations related to radiation oncology, radiation biology, medical physics, and both education and health policy as it relates to the field. This journal has a particular interest in original contributions of the following types: prospective clinical trials, outcomes research, and large database interrogation. In addition, it seeks reports of high-impact innovations in single or combined modality treatment, tumor sensitization, normal tissue protection (including both precision avoidance and pharmacologic means), brachytherapy, particle irradiation, and cancer imaging. Technical advances related to dosimetry and conformal radiation treatment planning are of interest, as are basic science studies investigating tumor physiology and the molecular biology underlying cancer and normal tissue radiation response.
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