Network topology in brain tumor patients with and without structural epilepsy: a prospective MEG study

Barbara Ladisich; Stefan Rampp; Eugen Trinka; Nathan Weisz; Christoph Schwartz; Theo Kraus; Camillo Sherif; Franz Marhold; Gianpaolo Demarchi

doi:10.1177/17562864231190298

Network topology in brain tumor patients with and without structural epilepsy: a prospective MEG study

Ther Adv Neurol Disord. 2023 Aug 29:16:17562864231190298. doi: 10.1177/17562864231190298. eCollection 2023.

Authors

Barbara Ladisich^{1

2

3}, Stefan Rampp^{4

5}, Eugen Trinka^{6

7}, Nathan Weisz^{8

9}, Christoph Schwartz¹, Theo Kraus¹⁰, Camillo Sherif¹¹, Franz Marhold¹¹, Gianpaolo Demarchi^{8

9}

Affiliations

¹ Department of Neurosurgery, Christian Doppler University Hospital, Paracelsus Medical University, Salzburg, Austria.
² Department of Neurosurgery, University Hospital St. Poelten, Dunant-Platz 1, St Polten 3100 Austria.
³ Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.
⁴ Department of Neurosurgery, Department of Neuroradiology, University Hospital Erlangen, Germany.
⁵ Department of Neurosurgery, University Hospital Halle (Saale), Germany.
⁶ Department of Neurology, Center for Cognitive Neuroscience Salzburg, Member of the European Reference Network, EpiCARE, Neuroscience Institute, Christian Doppler University Hospital, Paracelsus Medical University, Salzburg, Austria.
⁷ Karl Landsteiner Institute of Neurorehabilitation and Space Neurology, Salzburg, Austria.
⁸ Neuroscience Institute, Christian Doppler University Hospital, Salzburg, Austria.
⁹ Center for Cognitive Neuroscience & Department of Psychology, Paris Lodron University, Salzburg, Austria.
¹⁰ Institute of Pathology, University Hospital Salzburg, Paracelsus Medical University, Salzburg, Austria.
¹¹ Department of Neurosurgery, University Hospital St. Poelten, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Abstract

Background: It was proposed that network topology is altered in brain tumor patients. However, there is no consensus on the pattern of these changes and evidence on potential drivers is lacking.

Objectives: We aimed to characterize neurooncological patients' network topology by analyzing glial brain tumors (GBTs) and brain metastases (BMs) with respect to the presence of structural epilepsy.

Methods: Network topology derived from resting state magnetoencephalography was compared between (1) patients and controls, (2) GBTs and BMs, and (3) patients with (PSEs) and without structural epilepsy (PNSEs). Eligible patients were investigated from February 2019 to March 2021. We calculated whole brain (WB) connectivity in six frequency bands, network topological parameters (node degree, average shortest path length, local clustering coefficient) and performed a stratification, where differences in power were identified. For data analysis, we used Fieldtrip, Brain Connectivity MATLAB toolboxes, and in-house built scripts.

Results: We included 41 patients (21 men), with a mean age of 60.1 years (range 23-82), of those were: GBTs (n = 23), BMs (n = 14), and other histologies (n = 4). Statistical analysis revealed a significantly decreased WB node degree in patients versus controls in every frequency range at the corrected level (p_1-30Hz = 0.002, p_γ = 0.002, p_β = 0.002, p_α = 0.002, p_θ = 0.024, and p_δ = 0.002). At the descriptive level, we found a significant augmentation for WB local clustering coefficient (p_1-30Hz = 0.031, p_δ = 0.013) in patients compared to controls, which did not persist the false discovery rate correction. No differences regarding networks of GBTs compared to BMs were identified. However, we found a significant increase in WB local clustering coefficient (p_θ = 0.048) and decrease in WB node degree (p_α = 0.039) in PSEs versus PNSEs at the uncorrected level.

Conclusion: Our data suggest that network topology is altered in brain tumor patients. Histology per se might not, however, tumor-related epilepsy seems to influence the brain's functional network. Longitudinal studies and analysis of possible confounders are required to substantiate these findings.

Keywords: brain metastasis; brain tumor; epilepsy; magnetoencephalography; network topology; resting-state.