Electroencephalography/functional magnetic resonance imaging responses help predict surgical outcome in focal epilepsy

Abstract

Purpose: Simultaneous electroencephalography/functional magnetic resonance imaging (EEG/fMRI) recording can noninvasively map in the whole brain the hemodynamic response following an interictal epileptic discharge. EEG/fMRI is gaining interest as a presurgical evaluation tool. This study aims to determine how hemodynamic responses related to epileptic activity can help predict surgical outcome in patients considered for epilepsy surgery.

Methods: Thirty-five consecutive patients with focal epilepsy who had significant hemodynamic responses and eventually surgical resection, were studied. The statistical map of hemodynamic responses were generated and co-registered to postoperative anatomic imaging. Patients were classified into four groups defined by the relative relationship between the location of the maximum hemodynamic response and the resection: group 1, fully concordant; group 2, partially concordant; group 3, partially discordant; and group 4, fully discordant. These findings were correlated with surgical outcome with at least 12-month follow-up.

Key findings: Ten patients in group 1 had the maximum t value (t-max) inside the resection; nine in group 2 had the t-max outside but close to the resection and the cluster with t-max overlapped the resection; five in group 3 had the t-max remote from resection, but with another less significant cluster in the resection; and 11 in group 4 had no response in the resection. The degree of concordance correlated largely with surgical outcome: a good surgical outcome (Engel's class I) was found in 7 of 10 patients of group 1, 4 of 9 of group 2, 3 of 5 of group 3, and only 1 of 11 of group 4. These results indicate that the partially concordant and partially discordant groups are best considered as inconclusive. In contrast, in the fully concordant and fully discordant groups, the sensitivity, specificity, positive predictive value, and negative predictive value were high, 87.5%, 76.9%, 70%, and 90.9%, respectively.

Significance: This study demonstrates that hemodynamic responses related to epileptic activity can help delineate the epileptogenic region. Full concordance between maximum response and surgical resection is indicative of seizure freedom, whereas a resection leaving the maximum response intact is likely to lead to a poor outcome. EEG/fMRI is noninvasive but is limited to patients in whom interictal epileptic discharges can be recorded during the 60-90 min scan.

Keywords: Electroencephalography/functional magnetic resonance imaging; Epilepsy surgery; Outcome.

Figure 1

Examples of patients from the “fully concordant” group. (A) Patient 1. Interictal EEG: equipotential over F8-T4, F10-T10 (bipolar montage). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD activation with t-max (t = 14.7) in right orbitofrontal region, which was mostly within the resection. This patient had right frontal lobe epilepsy (FLE) and negative presurgical anatomic MRI; resection in the right orbitofrontal region after an intracranial EEG (iEEG) study. Postsurgical pathology demonstrated focal cortical dysplasia (FCD) IIa. The patient was seizure-free at 24 months of follow-up (Engel’s class I). (B) Patient 13. Interictal EEG: spikes over F8, T4, F10, T10 (average reference). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD activation with t-max (t = 6.87) in right hippocampus, which was within the resection. This patient had right mesial temporal lobe epilepsy (TLE) and right mesial temporal sclerosis (MTS) on anatomic MRI. Patient underwent a right selective amygdalohippocampectomy (SeAH). The patient was seizure-free for 24 months after surgery, but seizures resumed thereafter with decreased frequency; patient was classified as Engel’s class III at 60 months of follow-up. Epilepsia © ILAE

Figure 2

Examples of patients from the “fully concordant” group. (A) Patient 10. Interictal EEG: spikes over F7, T3, T5, F9, T9 (average reference). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD activation with t-max (t = 6.29) in left amygdala and hippocampus, mostly within the resection. Patient had left TLE and presurgical anatomic MRI showing left MTS. Patient underwent a left SeAH followed by continuing seizures, and then a second surgery to extend the resection to anterior temporal lobe. The patient was seizure-free at 12 months of follow-up (Engel’s class I). (B) Patient 2. Interictal EEG: equipotential over F3-C3 and F7-T3 (bipolar montage). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD activation with t-max (t = 10.8) in the anterior part of left first frontal gyrus, which was mostly within the resection. However, there was another significant activation in the mesial frontal region with a t value of 10.5. This patient had left FLE and presurgical anatomic MRI showing FCD in the left frontal lobe. Patient had a lesionectomy in the left frontal lobe. The patient did not have any improvement after the surgery, and was classified as Engel’s class IV at 30 months of follow-up. Epilepsia © ILAE

Figure 3

Examples of patients from the “partially concordant” group. (A) Patient 5. Interictal EEG: sharp waves over F8, T4, F10, T10, and also Fp2, F4 (Referential montage with FCz). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD cluster with the t-max was in right orbitofrontal region and insula, which overlapped with the resection, whereas the t-max (t = 5.52) was at the edge of the resection. There was another BOLD cluster on the left side, which was considered as a rapid propagation. This patient had right FLE and negative presurgical anatomic MRI. Patient had resection in right orbitofrontal region. Postsurgical pathology demonstrated FCD IIb. The patient was seizure-free at 12 months of follow-up (Engel’s class I). (B) Patient 33. Interictal EEG: equipotential over F8-T4, F10-T10 (bipolar montage). A large part of extensive BOLD activation related to IEDs overlapped with the resection, whereas the t-max was in right superior temporal lobe (t = 9.55), which was outside the resection. This patient had right temporoparietal lobe epilepsy and polymicrogyria over the right hemisphere including temporal lobe, parietal lobe, and insula. The patient underwent two surgeries, with resections including most of the right temporal and parietal lobes. The patient still had less severe seizures with decreased frequency (Engel’s class III) 18 months after the second surgery. Epilepsia © ILAE

Figure 4

Examples of patients from the “partially discordant” group. (A) Patient 17. Interictal EEG: equipotential over F7-T3, F9-T9 (bipolar montage). (a) and (b): coregistering BOLD response with postsurgical anatomic MRI. (a) IED-related BOLD response with t-max (activation, t = 7.47) was in the right inferior temporal gyrus, remote from the resection. (b) A less significant BOLD activation (t = 5.83) was in the left hippocampus, part of the resection. This patient had left TLE and left MTS on presurgical anatomic MRI. Patient underwent left SeAH. The patient was seizure-free (Engel’s class I) at 12 months of follow-up. (B) Patient 9. Interictal EEG: bursts of generalized spike-and-waves (referential montage with FCz). (a) and (b) compared BOLD response with postsurgical anatomic MRI. (a) IED-related BOLD activation with t-max (t = 6.35) was in the left temporal pole, contralateral to the resection. (b) There were two BOLD activations with lower t value in the right frontal lobe, one of which (t = 4.75) was inside the resection. This patient had right FLE, and presurgical MRI showed FCD in right supplementary motor area. Patient underwent a lesionectomy. The patient was Engel’s class III at 14 months of follow-up. Epilepsia © ILAE

Figure 5

Examples of patients from the “fully discordant” group. (A) Patient 21. Interictal EEG: bursts of spikes over F7, T3, F9, T9 (average reference). Coregistering the t-map of BOLD response with postsurgical MRI: BOLD activation with t-max (t = 7.05) in the posterior part of left inferior temporal gyrus and a less significant BOLD cluster in the posterior part of left superior temporal gyrus. None of the clusters overlapped with the resection. This patient had left TLE and left MTS on presurgical anatomic MRI. The patient underwent a left SeAH and a second surgery extended to the anterior temporal lobe. Seizure did not improve at 13 months after the second surgery (Engel’s class IV). (B) Patient 34. Interictal EEG: equipotential over F7-T3, F9-T9 (bipolar montage). Coregistering the t-map of BOLD response with postsurgical MRI showed the BOLD activation with t-max (t = 5.45) in left mesial prefrontal region and a less significant BOLD cluster over the right homologous region. None of the clusters overlapped with the resection. This patient had left TLE and polymicrogyria over the left hemisphere including temporal lobe, parietal lobe, and insula. Patient underwent a resection in the left orbitofrontal region after iEEG recordings. The seizures did not improve at 12 months of follow-up (Engel’s class IV). Epilepsia © ILAE