Elsevier

NeuroImage

Volume 20, Issue 4, December 2003, Pages 2291-2301
NeuroImage

Regular article
The influence of brain tumor treatment on pathological delta activity in MEG

https://doi.org/10.1016/j.neuroimage.2003.07.030Get rights and content

Abstract

The goal of the MEG study was to investigate the influence of tumor treatment on pathological delta activity (1–4 Hz). The treatment consisted of neurosurgery, and in some of the patients, additional radiotherapy. MEG and MR recordings were made both before and after the treatment in 17 patients. The signal power in the delta frequency band was determined for each recording. The malignant tumors were associated with large tumor volumes. Furthermore, both malignant tumors and tumor volume were associated with high signal powers in the delta band, indicating a correlation of delta power with the severity of the lesions. In all patients with high grade tumors, the delta power was lower after the treatment. The sources underlying the delta signals were estimated with an automatic single dipole analysis method. Estimated sources were projected onto MR scans. Preoperatively 14 clusters of equivalent sources describing focal activity were found in 12 out of 17 patients. Thirteen of these clusters were located near the tumor, and one cluster near an edema border. The locations near tumors are plausible and suggest that in general the source estimation was reliable. After the operation, 13 such clusters were found in 12 patients. Eleven clusters were located near the lesion border and one cluster near the edema border. Furthermore a cluster contralateral to the lesion in the other hemisphere indicated that brain lesions can affect the functioning of more distant brain areas than just the peritumoral brain tissue. Of the 12 patients who had preoperatively peritumoral clusters, 11 patients had postoperatively perilesional sources. In these cases the shift in source locations was in general considerably smaller than the dimension of the preoperative tumors. This finding indicates that similar areas generate the pre- and postoperative delta activity. Furthermore, focal delta sources were found in a case without tumor recurrence, and also in cases that most tumor tissue was removed. These findings suggest that the pathology underlying the slow waves is not the presence of the tumor bulk but the structural damage done by the tumors on the surrounding white/gray matter.

Introduction

Most patients with brain tumors show pathological slow waves (1–8 Hz) in EEG/MEG recordings. Often irregularly shaped (polymorphic) slow wave activity can be observed at the sensors at the area overlying the brain tumor. Though these pathological slow waves are obviously a consequence of the tumor, the main pathological factors associated with the tumors provoking the generation of these waves are yet unknown. The fact that tumors have in general many detrimental effects on surrounding brain tissue makes a determination of the leading factor difficult. Possible factors are damage to white and gray matter, edema, raised intracranial pressure, and changed biochemical environment of neurons in the vicinity of the tumor boundary. Furthermore, it has been shown that factors as the location of the tumor, and the type (based on histology) also play a role in the generation of pathological slow waves (Fischer-Williams, 1993).

Gloor et al. (1977) examined the appearance of slow waves in brain lesions produced by thermocoagulation in cats. From their results it appeared that white matter lesions produced polymorphic delta waves localized to the cortical area overlying the lesion. Lesions limited to the gray matter did not produce slow wave activity near the lesion. High edema contents were associated with ipsilateral diffuse delta activity. The location of these slow wave generators was studied by Ball et al. (1977). Ball and colleagues found that in the case of delta activity overlying a white matter lesion, the slow waves were generated in layer 5 containing pyramidal cells. This would imply that the sources of pathological slow waves in EEG/MEG are located very close to the surface of the cortex.

To improve the understanding on the generation of slow waves in patients with brain tumors, the MEG slow waves can be studied together with structural information on the lesions based on MR scans using magnetic source imaging (MSI). With MSI, sources underlying MEG signals are overlaid on corresponding MR scans, enabling the correlation of the locations of slow wave generators with pathological features visible on the MR scan (or even other modalities as magnetic resonance spectroscopy (Kamada et al., 2001)).

MSI enables case studies of single patients, but findings in single patients cannot always be extrapolated to other patients. To reliably assess the association between MEG and MR findings, the results of each modality must be quantified systematically and subsequently correlated with each other. This implies that source analysis must be reasonably fast and standardized, to allow the data examination and analysis to be performed within reasonable limits of time. Therefore, in many studies which include large data sets of many patients, the source model is the single dipole model. The application and interpretation of research with intricate models would in general involve too much intervention of the researchers.

For pathological delta activity, this single dipole model appears adequate. Often source solutions are estimated on the margins of structural lesions and these margins are physiologically plausible areas for tumor-related activity to take place, e.g., see Lewine and Orrison (1995). Vieth et al. (1996), and De Jongh et al. (2001). Another advantageous property of single dipole solutions is that they are easily transformed into variables which can be correlated with MR scan variables, which is not so evident for extended source model solutions. Furthermore, automatic methods based on the single dipole models incorporate fever arbitrary decisions than human observers, making the comparison of the results of the source analysis between different patients more reliable.

The motivation for investigating pathological slow waves is not merely the extension of fundamental neuroelectrophysiological knowledge. The presence of focal slow waves is a possible indicator of white matter damage/cortical deafferentiation of gray matter. In patients with transient ischemic attacks or transient global amnesia, the potential use of slow wave analysis has already been investigated (Stippich et al., 2000).

There are also reports that suggest that the sources of pathological slow waves may be potentially epileptogenic; see, for example, Kamada et al. (1998). Other studies suggest that slow waves may be useful in establishing consensus about the epileptogenic area; see, for example, Gallen et al. (1997) and Panet-Raymond and Gotman (1990).

This study is the sequel of the study by Baayen et al. (2003) in which the localization of delta was investigated in preoperative patients with brain tumors. The objective of our study was to extend the previous study to postoperative data, and thereby investigate the influence of tumor treatment on pathological delta activity (1–4 Hz). Spontaneous MEG data of 17 patients were recorded before and after neurosurgery. For each recording the power in the delta frequency band was determined. An automatic single dipole analysis method was applied to estimate the sources underlying the delta signals. To our knowledge, this is the first systematic investigation of the influence of neurosurgery and radiotherapy on delta activity in patients with brain tumors.

Section snippets

Data acquisition

The patients who entered the study underwent surgery for an intracranial tumor at the Department of Neurosurgery, VU University Medical Center. All patients were older than 18 years, and had histories of epileptic seizures. The treatment consisted of surgery and antiepileptic drugs, and in patients with high graded (malignant) tumors, also radiotherapy. The histopathological diagnosis was determined according to the WHO Classification of Tumors affecting the central nervous system (Kleihues et

Patient group

Of the 17 patients nine patients had high graded gliomas, six had low graded, and two had meningiomas (Table 1). The tumors were located at temporal, parietal, and frontal areas. The postoperative registrations were made between 5 to 10 months after surgery (on average 8 months). The high graded tumors were in general larger than low graded tumors and meningiomas (Table 2) (P < 0.05, two sample t test assuming unequal variances, two-tailed). On average, the ratio of the corresponding volumes

Discussion

The goal of the present MEG study was to investigate the influence of tumor treatment on pathological delta activity (1–4 Hz) in patients with brain tumors. The signal power in the delta frequency band was determined for each recording. The malignant tumors were associated with large tumor volumes. Furthermore, both malignant tumors and tumor volume were associated with high signal powers in the delta band, indicating a correlation of delta power with the severity of the lesions. After

Acknowledgements

The research was financed by the National Epilepsy Foundation of the Netherlands (grant number 99-05).

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