1. Systematic review
A total of 458 studies were found initially. All studies were reviewed to exclude non-SEEG studies and those SEEG studies without SOP classification or adequate information. After screening, 8 studies were included in the present study.[3-10]. The flow of studies included in the systematic review is shown in Figure 1. Previous SOP classifications from these studies are presented in Table 1.
2. Reconsideration of terms used and conditions for SEEG interpretation
Table 2 shows the terms reconsidered in our study. We determined the EEG onset of seizure as when the EEG was seen to differ compared to the baseline of the preceding 5-second period. The type of SOP was judged in the next 5 seconds, which we considered a “period for determining the type of SOP” because we focused on the initial SOP morphology to identify one pattern in each seizure episode. If more than one SOP type was found during this period, we chose the most prominent type. Due to the propagating nature of seizures, the electrode showing the earliest change was selected as the “core electrode”, which is the electrode of primary interest. However, if the electrode with earliest change was impossible to distinguish, the electrode with the highest amplitude of SOP was selected as the core electrode as a second priority [12].
For other technical terms in SEEG, we reconsidered each term mainly according to the generally accepted consensus adapted from scalp EEG [13] and based on several studies from SEEG [8, 14]. We defined paroxysmal activity as a “spike” when a clear transient and distinguished activity with an identified peak 20–70 ms in duration was found. A “sharp wave” was defined instead when the paroxysmal activity showed a duration of 70–200 ms. “Polyspikes” was defined when two or more continuous spikes were seen in less than 0.5 seconds without an interdischarge interval, whereas “burst” was defined for a group of any continuous activities lasting more than 0.5 seconds. “Low voltage” was defined when the amplitude of the wave was less than that at baseline. We used the term “high amplitude” when the amplitude of the wave was more than 10 times that at baseline.
3. Proposal of a new classification of SOP morphology using a clear algorithm
After thoroughly reviewing all reviewed classifications, we grouped some similar SOP morphologies into fewer types that still represented the morphological characteristics previously reported in the literature. We coined the new term “periodic polyspikes” as distinguished from “burst of polyspikes” based on the periodic appearance and shorter period of polyspikes lasting less than 0.5 seconds. Our new classification comprised four major types:
1. Sharp activity
2. Burst of polyspikes, with one special subtype
2.1. Low-voltage, fast activity (LVFA)
3. Periodic polyspikes, with one special subtype
3.1. Delta brush (periodic polyspikes accompanied by delta waves)
4. Spike and wave, with one special subtype
4.1. Low-frequency, high-amplitude periodic spike (LFPS)
The algorithm for our classification is demonstrated in Figure 2. After identifying EEG onset from baseline, we look for any spikes within a period of 5 seconds to determine the SOP. If no spikes are present, the SOP type is determined as “sharp activity”. If spikes are identified, we look for any “polyspikes” with or without a “burst”. If a “burst of polyspikes” (a >0.5-s period of polyspikes) is seen, we classify that SOP as a “burst of polyspikes”. The burst of polyspikes has one special subtype, LVFA, in which the SOP shows an initial amplitude less than that at the baseline at the beginning of SOP and presents with a continuously increasing amplitude. If no burst of polyspikes is identified, “periodic polyspikes” is chosen instead. This type contains one special subtype, “delta brush”, representing when polyspikes are seen to be accompanied by a slow wave in the delta frequency (<4 Hz). Finally, if the SOP shows spikes without any polyspikes, we classify the SOP as “spike and wave”. The “spike-and-wave” pattern has one special subtype, “LFPS”, in which the amplitude of each spike is more than 10 times that at baseline. Previous studies have not determined clear definitions for LFPS, so we set a clearer definition based on amplitude.
For the three special subtypes, “LVFA”, “delta brush” and “LFPS”, if we only identify a specific characteristic in one of these special subtypes, that SOP will be chosen regardless of the duration, even if the special subtype is not present for the majority of the period for determining the type of SOP.
4. Case Illustrations
Case Illustration 1
A patient in their 50s presented with temporal lobe epilepsy. Magnetic resonance imaging (MRI) suggested left hippocampal sclerosis, but scalp EEG showed interictal and ictal discharges from bilateral temporal lobes. We evaluated the seizure origin with SEEG and confirmed seizure origin from the left hippocampus. The patient underwent selective amygdalohippocampectomy on the left side and became seizure-free.
The SOP was a burst of polyspikes. The amplitude was lower than baseline at the beginning and continuously increased in amplitude. The type of SOP was thus determined as LVFA (Figure 3A).
Case Illustration 2
A patient in their 50s presented with focal impaired awareness seizure. Right temporal lobe epilepsy was suspected from ictal and interictal EEG findings. MRI showed multiple periventricular heterotopias in bilateral temporal lobes with no findings of hippocampal sclerosis. Fluorodeoxyglucose-positron emission tomography (FDG-PET) and magnetoencephalography (MEG) failed to identify the epileptogenic area. SEEG was then performed on the right temporal lobe and insula and one of the periventricular heterotopias. The seizure origin was identified as the right hippocampus. The patient underwent right selective amygdalohippocampectomy and became seizure-free.
The patient showed two types of SOP from the same core electrode. One type was “burst of polyspikes”, since the SOP showed polyspikes lasting more than 0.5 seconds (Figure 3B). The other type showed repeated spikes without polyspikes (Figure 3C). One spike was seen with an amplitude more than 10 times baseline activity. This type of SOP was thus determined to be “LFPS”. These two distinct types of SOP showed the same habitual seizure.
Case Illustration 3
A patient in their 60s presented with focal impaired awareness seizure. Involvement of the temporal lobe or insula was suspected based on the seizure semiology. MRI suggested right hippocampal sclerosis. SEEG was then performed for the right temporal lobe and insula to evaluate seizure origin and propagation and to determine the extent of resection. We identified seizures originating from both the right anterior insula and mesial temporal lobe.
SEEG SOP showed spikes and waves without any polyspikes. We determined the SOP as “spike and wave” (Figure 3D). The patient underwent right amygdalohippocampectomy with anterior temporal lobectomy and anterior insulectomy and achieved freedom from seizures after surgery.
Case Illustration 4
A teenage patient presented with focal to bilateral tonic and clonic seizures. Left frontal lobe epilepsy was suspected from the seizure semiology. Interictal EEG showed bilateral frontal lobe spikes. Neither MRI nor FDG-PET showed obvious abnormalities.
SEEG was performed for the left frontal lobe and insula. The seizures did not have an obvious starting point due to continuous abnormal waves during baseline. However, we were able to identify abrupt distinct waves, mainly from the cingulate gyrus.
The “periodic polyspikes” were accompanied by slow waves with delta frequency, and we classified the SOP as “delta brush” (Figure 3E). The patient underwent frontal lobectomy preserving the precentral gyrus after additional evaluation with subdural grid placement for functional brain mapping.
Case Illustration 5
A patient in their 30s presented with focal to bilateral tonic and clonic seizures. Seizure started with eye opening and groaning, followed by generalized tonic and clonic seizures. Scalp EEG showed prominent interictal discharges from the left mid-to-posterior temporal area. No abnormalities were seen on MRI or FDG-PET. MEG showed dipole clustering at the left precentral operculum. SEEG was performed at the left frontal and temporal lobe, revealing the origin of seizures from the posterior part of the temporal operculum.
The SOP showed no spikes. The frequency of paroxysmal activity was 8–13 Hz, so we classified the SOP as “sharp activity” (Figure 3F). The patient underwent gyrectomy in the left posterior part of the temporal operculum after additional evaluation with subdural grid placement for functional brain mapping.