Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients

Introduction: Functional coupling of the tumor to extralesional brain areas and the pretherapeutic cognitive performance status have each independently been identified as prognostically relevant in glioma patients. It is however unclear, whether tumor-connectivity correlates with cognitive performan...

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Main Authors: Chuh-Hyoun Na, Hans Clusmann, Martin Wiesmann, Kerstin Jütten, Verena Mainz
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Brain and Spine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772529425000219
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author Chuh-Hyoun Na
Hans Clusmann
Martin Wiesmann
Kerstin Jütten
Verena Mainz
author_facet Chuh-Hyoun Na
Hans Clusmann
Martin Wiesmann
Kerstin Jütten
Verena Mainz
author_sort Chuh-Hyoun Na
collection DOAJ
description Introduction: Functional coupling of the tumor to extralesional brain areas and the pretherapeutic cognitive performance status have each independently been identified as prognostically relevant in glioma patients. It is however unclear, whether tumor-connectivity correlates with cognitive performance or the cognitive outcome. Research question: To investigate potential associations between pre- and postoperative resting-state fMRI connectivity (FC) and cognitive functions in glioma patients compared to healthy controls. Material and methods: 18 patients and 18 age-matched, healthy controls underwent resting-state fMRI and neuropsychological testing pre- and 4.5 months (mean) postoperatively. FC of the tumor to extralesional brain (Tu-EL) was determined, as well as FC of extralesional brain (EL) and the contralesional hemisphere (conEL). Groups were compared with regard to behavioral and FC measures. Results: Patients showed deficits in all cognitive domains tested. While postoperative performance tended to be worse, deterioration was not statistically significant between timepoints. EL FC did not differ between groups, but conEL FC (p < .045) was increased in patients as compared to controls. Tu-EL FC was significantly associated with worse attention performance (p < .001), and, by trend (p < .058), with worse attentional outcome in patients. Discussion and conclusion: Intrinsic functional coupling to the rest of the brain was associated with worse cognitive performance and might relate to pathological tumor-neuron interaction on the macroscale, reflecting the invasive nature of diffusely infiltrating glioma. Deepening our understanding of FC measures at the connectomic level in the context of cancer neuroscience may aid in identifying neurophysiological correlates of cognitive impairment and in prognosticating cognitive outcome in glioma patients.
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spelling doaj-art-cde9ba62e8cf437b933114758995471d2025-02-08T05:01:40ZengElsevierBrain and Spine2772-52942025-01-015104202Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patientsChuh-Hyoun Na0Hans Clusmann1Martin Wiesmann2Kerstin Jütten3Verena Mainz4Department of Neurosurgery, RWTH Aachen University, Pauwelsstraße 30, 52074, Aachen, Germany; Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf (CIO ABCD)Department of Neurosurgery, RWTH Aachen University, Pauwelsstraße 30, 52074, Aachen, Germany; Center for Integrated Oncology Aachen Bonn Cologne Duesseldorf (CIO ABCD)Department of Diagnostic and Interventional Neuroradiology, RWTH Aachen University, Pauwelsstraße 30, 52074, Aachen, GermanyDepartment of Neurosurgery, RWTH Aachen University, Pauwelsstraße 30, 52074, Aachen, Germany; Corresponding author. Department of Neurosurgery, RWTH Aachen University, Pauwelsstraße 30, 52074, Aachen, Germany.Institute of Medical Psychology and Medical Sociology, RWTH Aachen University, Pauwelsstraße 19, 52074, Aachen, GermanyIntroduction: Functional coupling of the tumor to extralesional brain areas and the pretherapeutic cognitive performance status have each independently been identified as prognostically relevant in glioma patients. It is however unclear, whether tumor-connectivity correlates with cognitive performance or the cognitive outcome. Research question: To investigate potential associations between pre- and postoperative resting-state fMRI connectivity (FC) and cognitive functions in glioma patients compared to healthy controls. Material and methods: 18 patients and 18 age-matched, healthy controls underwent resting-state fMRI and neuropsychological testing pre- and 4.5 months (mean) postoperatively. FC of the tumor to extralesional brain (Tu-EL) was determined, as well as FC of extralesional brain (EL) and the contralesional hemisphere (conEL). Groups were compared with regard to behavioral and FC measures. Results: Patients showed deficits in all cognitive domains tested. While postoperative performance tended to be worse, deterioration was not statistically significant between timepoints. EL FC did not differ between groups, but conEL FC (p < .045) was increased in patients as compared to controls. Tu-EL FC was significantly associated with worse attention performance (p < .001), and, by trend (p < .058), with worse attentional outcome in patients. Discussion and conclusion: Intrinsic functional coupling to the rest of the brain was associated with worse cognitive performance and might relate to pathological tumor-neuron interaction on the macroscale, reflecting the invasive nature of diffusely infiltrating glioma. Deepening our understanding of FC measures at the connectomic level in the context of cancer neuroscience may aid in identifying neurophysiological correlates of cognitive impairment and in prognosticating cognitive outcome in glioma patients.http://www.sciencedirect.com/science/article/pii/S2772529425000219Resting-state fMRICognitive outcomeGliomaFunctional connectivityConnectome
spellingShingle Chuh-Hyoun Na
Hans Clusmann
Martin Wiesmann
Kerstin Jütten
Verena Mainz
Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
Brain and Spine
Resting-state fMRI
Cognitive outcome
Glioma
Functional connectivity
Connectome
title Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
title_full Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
title_fullStr Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
title_full_unstemmed Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
title_short Tumor resting-state fMRI connectivity to extralesional brain is associated with cognitive performance in glioma patients
title_sort tumor resting state fmri connectivity to extralesional brain is associated with cognitive performance in glioma patients
topic Resting-state fMRI
Cognitive outcome
Glioma
Functional connectivity
Connectome
url http://www.sciencedirect.com/science/article/pii/S2772529425000219
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