MEG Network Differences between Low- and High-Grade Glioma Related to Epilepsy and Cognition

Edwin Van Dellen,Linda Douw,Demetrios N Velis,Cornelis J Stam,Jaap C Reijneveld,Martin Klein,Arjan Hillebrand,Jan J Heimans,Philip C De Witt Hamer,Johannes C Baayen,Irene H M Ris-Hilgersom,Menno M Schoonheim

doi:10.1371/journal.pone.0050122

Edwin Van Dellen, Linda Douw + Show 10 more

Open Access

https://doi.org/10.1371/journal.pone.0050122

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Abstract

ObjectiveTo reveal possible differences in whole brain topology of epileptic glioma patients, being low-grade glioma (LGG) and high-grade glioma (HGG) patients. We studied functional networks in these patients and compared them to those in epilepsy patients with non-glial lesions (NGL) and healthy controls. Finally, we related network characteristics to seizure frequency and cognitive performance within patient groups.MethodsWe constructed functional networks from pre-surgical resting-state magnetoencephalography (MEG) recordings of 13 LGG patients, 12 HGG patients, 10 NGL patients, and 36 healthy controls. Normalized clustering coefficient and average shortest path length as well as modular structure and network synchronizability were computed for each group. Cognitive performance was assessed in a subset of 11 LGG and 10 HGG patients.ResultsLGG patients showed decreased network synchronizability and decreased global integration compared to healthy controls in the theta frequency range (4–8 Hz), similar to NGL patients. HGG patients’ networks did not significantly differ from those in controls. Network characteristics correlated with clinical presentation regarding seizure frequency in LGG patients, and with poorer cognitive performance in both LGG and HGG glioma patients.ConclusionLesion histology partly determines differences in functional networks in glioma patients suffering from epilepsy. We suggest that differences between LGG and HGG patients’ networks are explained by differences in plasticity, guided by the particular lesional growth pattern. Interestingly, decreased synchronizability and decreased global integration in the theta band seem to make LGG and NGL patients more prone to the occurrence of seizures and cognitive decline.

Highlights

Symptoms in patients with brain tumors and in other lesional epilepsy patients are to some extent correlated with histological characteristics of the lesion
There was a difference in age between groups (F (3,67) = 6.59; p = 0.001); non-glial lesions (NGL) patients were significantly younger than patients in the other groups
No significant differences regarding epilepsy duration and seizure frequency were found between low-grade glioma (LGG) and high-grade gliomas (HGG) patients (Mann-Whitney U = 44.5; p = 0.069 and U = 64.5; p = 0.473, respectively), epilepsy duration tended to be longer in LGG patients

Summary

Introduction

Symptoms in patients with brain tumors and in other lesional epilepsy patients are to some extent correlated with histological characteristics of the lesion. Patients with cerebral lesions suffer from cognitive deficits, for example in the attention domain, that cannot be explained by local disturbance due to infiltration of the lesion [3]. Cerebral lesions such as brain tumors can lead to global alterations in functional interactions, even between brain regions remote from the tumor [4,5]. This recent insight may increase our understanding of the symptoms in these patients. Several studies have shown that small-world networks, which combine local segregation with global integration, facilitate optimal (brain) network functioning [6,9,10,11]

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