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, 46 (7), 1086-97

Origin and Propagation of Epileptic Spasms Delineated on Electrocorticography

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Origin and Propagation of Epileptic Spasms Delineated on Electrocorticography

Eishi Asano et al. Epilepsia.

Abstract

Purpose: Ictal electrographic changes were analyzed on intracranial electrocorticography (ECoG) in children with medically refractory epileptic spasms to assess the dynamic changes of ictal discharges associated with spasms and their relation to interictal epileptiform activity and neuroimaging findings.

Methods: We studied a consecutive series of 15 children (age 0.4 to 13 years; nine girls) with clusters of epileptic spasms recorded on prolonged intracranial subdural ECoG recordings, which were being performed for subsequent cortical resection, and in total, 62 spasms were analyzed by using quantitative methods.

Results: Spasms were associated with either a "leading" spike followed by fast-wave bursts (type I: 42 events analyzed quantitatively) or fast-wave bursts without a "leading" spike (type II: 20 events analyzed quantitatively). Twenty-three of the 42 type I spasms but none of the 20 type II spasms were preceded by a focal seizure. A "leading" spike had a focal origin in all 42 type I spasms and involved the pre- or postcentral gyrus within 0.1 s in 37 of these spasms. A leading spike was associated with interictal spike activity >1/min in 40 of 42 type I spasms and originated within 2 cm from a positron emission tomography glucose hypometabolic region in all but two type I spasms. Failure to resect the cortex showing a leading spike was associated with poor surgical outcome (p = 0.01; Fisher's exact probability test). Fast-wave bursts associated with spasms involved neocortical regions extensively at least in two lobes within 1.28 s in all 62 spasms and involved the pre- or postcentral gyrus in 53 of 62 spasms.

Conclusions: Epileptic spasms may be triggered by a focal neocortical impulse in a subset of patients, and a leading spike, if present, might be used as a marker of the trigger zone for epileptic spasms. Rapidly emerging widespread fast-wave bursts might explain the clinical semiology of epileptic spasms.

Figures

FIG. 1
FIG. 1
A 7-year-old girl with intractable epileptic spasms associated with tuberous sclerosis complex. A: Ictal electrocorticogram (ECoG) showed a focal periodic spike-and-wave activity in the left temporooccipital region. The focal periodic spike-and-wave discharges were followed by focal fast-wave bursts in the same region. The focal seizure discharges gradually propagated to the left subtemporal region with minimal clinical correlation, and the focal seizure discharges subsided 5 s before the initiation of cluster of spasms. Each spasm was associated with a single giant spike followed by widespread fast-wave bursts. A low-frequency filter of 4.0 Hz and a high-frequency filter of 100 Hz were applied. B: The magnitude of averaged focal periodic spike-and-wave activity was highest in the left temporooccipital region. C: The magnitude of leading spike activity associated with a spasm was also highest in the left temporooccipital region. According to the ictal voltage mapping (see Supplementary Video), the leading spike originated from the left temporooccipital region and propagated to the left parietal, temporal, and frontal regions within 100 ms. D: The subtraction ictal ECoG magnitude coregistered to MRI revealed increased fast-wave magnitude (24–100 Hz) associated with a spasm in the left temporooccipital, parietal, subtemporal, and sensory-motor cortex.
FIG. 2
FIG. 2
A 1-year-old boy with intractable epileptic spasms associated with a tumor in the left postcentral gyrus. A: Ictal electrocorticogram (ECoG) showed a focal fast-wave discharge confined to the postcentral gyrus (electrode B5), which was followed by a single giant spike and subsequently followed by widespread fast-wave bursts in the left parietal, temporal, and frontal regions. Widespread fast-wave bursts were associated with a clinical spasm. A low-frequency filter of 4.0 Hz and a high-frequency filter of 100 Hz were applied. B: The subtraction ictal ECoG magnitude coregistered to MRI revealed an increase of fast-wave magnitude (16–32 Hz) in the left postcentral gyrus. White broken line, The resection margin. C: The magnitude of leading spike activity associated with a spasm also was highest in the left postcentral gyrus. D: The subtraction ictal ECoG magnitude coregistered to MRI showed increase of fast-wave magnitude (16–64 Hz) associated with a spasm in the left temporal, parietal, and frontal regions.
FIG. 3
FIG. 3
A 5-month-old boy with intractable epileptic spasms and a cortical tuber in the right precentral gyrus. A: Frequent interictal epileptiform activity was noted in the right medial precentral gyrus. Red line, The location of central sulcus. B: Ictal electrocorticogram (ECoG) showed a focal leading spike activity in the right medial frontal region with the maximal amplitude at electrode 4 on the precentral gyrus. After the spike activity, regional fast-wave bursts emerged from the right medial and lateral frontal region as well as the right parietal region. It should be noted that the fast-wave discharges minimally involved the left medial frontal region, which was correlated with milder spasm-related movement of the right-sided limbs compared with the left. A low-frequency filter of 4.0 Hz and a high-frequency filter of 100 Hz were applied. C: The magnitude of leading spike activity associated with a spasm was highest in the right medial precentral gyrus. D: The subtraction ictal ECoG magnitude coregistered to MRI revealed increase of fast-wave magnitude (16–64 Hz) associated with a spasm in the right medial and lateral frontal regions, as well as the right parietal region.
FIG. 4
FIG. 4
A 13-year-old girl with nonlesional intractable epileptic spasms. A: Glucose hypometabolic regions [blue-coded areas; >10% decrease of fluorodeoxyglucose (FDG) uptake compared with the homotopic region] involved the left temporoparietal-frontal regions. B: Very frequent interictal epileptiform activity was noted in the left parietal, frontal, and temporal regions, independently. C: Ictal electrocorticogram (ECoG) associated with spasm 2 showed widespread fast-wave bursts over the left hemisphere without a leading spike activity. A low-frequency filter of 8.0 Hz and a high-frequency filter of 100 Hz were applied. D: The subtraction ictal ECoG magnitude coregistered to MRI for this spasm showed increase of fast-wave magnitude (32–100 Hz) extensively in the left parietal, temporal, and frontal regions, including the postcentral gyrus. E: Another spasm event (Spasm 3) showed increase of fast-wave magnitude (32–100 Hz) in the left parietal, frontal, and temporal regions, but the distribution of increased fast-wave magnitude is different from that for Spasm 2. F: The distribution of increased fast-wave magnitude for Spasm 5 is different from Spasms 2 or 3.
FIG. 5
FIG. 5
A 4-year-old girl with intractable epileptic spasms associated with subcortical heterotopia. A: Glucose hypometabolic regions (blue-coded areas; >10% decrease of fluorodeoxyglucose uptake compared with the homotopic region) involved the left frontal region as well as the pre- and postcentral gyri. Red line, The location of central sulcus; white broken line, the resection margin (frontal lobectomy). B: Frequent interictal epileptiform activity was noted in the left precentral gyrus and frontal region. C: Ictal electrocorticogram (ECoG) findings for Spasm 1 consisted of a preceding focal seizure characterized by periodic spike-and-wave discharges in the left frontal region, followed by a regional leading spike activity in the left frontal region, and subsequently followed by widespread fast-wave bursts associated with a spasm. D: Ictal ECoG findings for Spasm 2 also consisted of a preceding focal seizure characterized by periodic spike-and-wave discharges in the left frontal region, followed by a regional leading spike activity in the left frontal region, and subsequently followed by widespread fast-wave bursts associated with a spasm. E: Ictal ECoG findings for Spasm 4 consisted of a focal leading spike activity in the precentral gyrus followed by widespread fast-wave bursts associated with a spasm. It should be noted that the origin of leading spike for Spasm 4 was not resected because of the proximity to the motor cortex. F: Ictal ECoG findings for Spasm 5 consisted of widespread fast-wave bursts without a leading spike.

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