The spatial relationship between the MRI lesion and intraoperative electrocorticography in focal epilepsy surgery

Sven Straumann; Eline Schaft; Herke Jan Noordmans; Jan Willem Dankbaar; Willem M Otte; Josee van Steenis; Paul Smits; Willemiek Zweiphenning; Pieter van Eijsden; Tineke Gebbink; Luigi Mariani; Maryse A Van't Klooster; Maeike Zijlmans

doi:10.1093/braincomms/fcac302

The spatial relationship between the MRI lesion and intraoperative electrocorticography in focal epilepsy surgery

Brain Commun. 2022 Nov 21;4(6):fcac302. doi: 10.1093/braincomms/fcac302. eCollection 2022.

Authors

Sven Straumann^{1

2

3}, Eline Schaft¹, Herke Jan Noordmans⁴, Jan Willem Dankbaar⁵, Willem M Otte⁶, Josee van Steenis^{1

7}, Paul Smits¹, Willemiek Zweiphenning¹, Pieter van Eijsden¹, Tineke Gebbink¹, Luigi Mariani², Maryse A Van't Klooster¹, Maeike Zijlmans^{1

8}

Affiliations

¹ Department of Neurology and Neurosurgery, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands.
² Department of Neurosurgery, University Hospital Basel, 4051 Basel, Switzerland.
³ Department of Anaesthesiology and Pain Medicine, Inselspital, University Hospital Bern, 3010 Bern, Switzerland.
⁴ Department of Medical Technology and Clinical Physics, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands.
⁵ Department of Radiology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands.
⁶ Department of Child Neurology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands.
⁷ Faculty of Science and Technology, University of Twente, 7522 NB Enschede, The Netherlands.
⁸ Stichting Epilepsie Instellingen Nederland (SEIN), 2103 SW Heemstede, The Netherlands.

Abstract

MRI and intraoperative electrocorticography are often used in tandem to delineate epileptogenic tissue in resective surgery for focal epilepsy. Both the resection of the MRI lesion and tissue with high rates of electrographic discharges on electrocorticography, e.g. spikes and high-frequency oscillations (80-500 Hz), lead to a better surgical outcome. How MRI and electrographic markers are related, however, is currently unknown. The aim of this study was to find the spatial relationship between MRI lesions and spikes/high-frequency oscillations. We retrospectively included 33 paediatric and adult patients with lesional neocortical epilepsy who underwent electrocorticography-tailored surgery (14 females, median age = 13.4 years, range = 0.6-47.0 years). Mesiotemporal lesions were excluded. We used univariable linear regression to find correlations between pre-resection spike/high-frequency oscillation rates on an electrode and its distance to the MRI lesion. We tested straight lines to the centre and the edge of the MRI lesion, and the distance along the cortical surface to determine which of these distances best reflects the occurrence of spikes/high-frequency oscillations. We conducted a moderator analysis to investigate the influence of the underlying pathology type and lesion volume on our results. We found spike and high-frequency oscillation rates to be spatially linked to the edge of the MRI lesion. The underlying pathology type influenced the spatial relationship between spike/high-frequency oscillation rates and the MRI lesion (P _spikes < 0.0001, P _ripples < 0.0001), while the lesion volume did not (P _spikes = 0.64, P _ripples = 0.89). A higher spike rate was associated with a shorter distance to the edge of the lesion for cavernomas [F(1,64) = -1.37, P < 0.0001, η ² = 0.22], focal cortical dysplasias [F(1,570) = -0.25, P < 0.0001, η ² = 0.05] and pleomorphic xanthoastrocytomas [F(1,66) = -0.18, P = 0.01, η ² = 0.09]. In focal cortical dysplasias, a higher ripple rate was associated with a shorter distance [F(1,570) = -0.35, P < 0.0001, η ² = 0.05]. Conversely, low-grade gliomas showed a positive correlation; the further an electrode was away from the lesion, the higher the rate of spikes [F(1,75) = 0.65, P < 0.0001, η ² = 0.37] and ripples [F(1,75) = 2.67, P < 0.0001, η ² = 0.22]. Pathophysiological processes specific to certain pathology types determine the spatial relationship between the MRI lesion and electrocorticography results. In our analyses, non-tumourous lesions (focal cortical dysplasias and cavernomas) seemed to intrinsically generate spikes and high-frequency oscillations, particularly at the border of the lesion. This advocates for a resection of this tissue. Low-grade gliomas caused epileptogenicity in the peritumoural tissue. Whether a resection of this tissue leads to a better outcome is unclear. Our results suggest that the underlying pathology type should be considered when intraoperative electrocorticography is interpreted.

Keywords: MRI; electrocorticography; epilepsy surgery; high-frequency oscillations; spikes.