Differentiation of tumor versus peritumoral cortex in gliomas by intraoperative electrocorticography

Abstract

Background: Brain diffuse gliomas are highly epileptic and infiltrative tumors. Glioma surgery consists of the resection of the tumor core and the maximum of the peritumoral zone, infiltrated by tumor cells, guided by the intraoperative assessment of brain functionality and connectivity. However, its electrophysiological characteristics are poorly characterized.

Methods: We studied the characteristics of electrocorticographic (ECoG) signals, in the context of glioma surgery in awake conditions on 29 patients, using EEG activity sampled on the tumor itself versus on its borders and in healthy areas. We assessed the features of frequency bands and aperiodic components (offset and slope) of ECoG power spectra during awake glioma surgery, according to cortical tumoral versus peritumoral and healthy status.

Results: We found that tumor contacts present a decrease in activity for all the frequency bands except for delta activity, which was increased. Second, the peritumoral cortex was characterized by an increase in relative beta activity and slopes between 20 and 40 Hz. Low cortical tumor cell infiltration was directly correlated with a reduction in the production of physiological brain rhythms. Finally, an automatic classifier based on neural networks allowed the classification of the electrodes based on their power spectrum characteristics.

Conclusions: This intraoperative study shows that ECoG during glioma surgery in awake condition may characterize the peritumoral cortices, key for pathophysiology and therapy, and deepens our knowledge of the effects of tumor cell infiltration on nervous tissue activity. Its assessment during the surgical procedure should better delineation of the cortical areas to be removed.

Keywords: biomarker; electrocorticography; gliomas; power spectrum; tumors.

Graphical Abstract

Figure 1.

Intraoperative ECoG recording during Glioma surgery. (A) MRI sagittal view of a left tumor and perioperative picture. (B) 3D volume rendering with the position of the contacts superimposed- tumoral (red), close peritumoral (dark blue), far peritumoral (mild blue) and healthy (pale blue). (C) ECoG traces of the 4 compartments. (D) Welch periodogram of 4 contacts, one from every location. (E) Immunohistochemistry (IDH1R132H labeling) and hematoxylin staining showed a healthy biopsy, a low infiltrated (<50 tumoral cells/250 µm²⁾, a highly infiltrated (>50 tumoral cells/250 µm²) and a tumoral biopsy (from an abnormal MRI area).

Figure 2.

Frequency bands and aperiodic components analysis of tumoral and peritumoral cortices. (A) Intraoperative picture showing the limits of the 4 compartments: tumoral (red), close peritumoral (dark blue), far peritumoral (mild blue), and healthy (pale blue). (B) Plot showing the normalized spectrum features: delta, theta, alpha, beta, low gamma, high gamma, offset, slope 1–200, 20–30, 20–40, 30–45, 40–60, and 60–120 Hz. * P < .05, *** P < .001.

Figure 3.

Phase Locking Value (PLV) of tumoral, close peritumoral, far peritumoral, and healthy compartments for each frequency band. PLV matrix represented in a heat map, with the mean values inside, for the different frequency ranges (from delta to high gamma).

Figure 4.

Correlation between glioma cells infiltration and ECoG frequency features. (A) Mirror slices immunohistochemistry using IDH1R132H labeling and hematoxylin and eosin. (B) Immunohistochemistry (IDH1R132H labeling and hematoxylin) shows tumor cells (dark brown) presence: healthy without tumoral cells, low infiltrated (<50 tumoral cells/250 µm²), and highly infiltrated (>50 tumoral cells/250 µm²). (C) Correlation between beta frequencies, low gamma, slope 40–60 and 60–120 Hz in healthy, low infiltrated, and highly infiltrated biopsies.

Figure 5.

ECoG differential frequency features between oligodendrogliomas IDH-mutant-1p19qcodeleted and astrocytomas IDH-mutant. MRI axial view of an astrocytoma and an oligodendroglioma. Plot comparing the offset and 1–200 Hz slope between astrocytomas (filled dot) and oligodendrogliomas (empty dot). * P < .05, *** P < .001.