Seizure localization using ictal phase-locked high gamma: A retrospective surgical outcome study.
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ABSTRACT: Objective
To determine whether resection of areas with evidence of intense, synchronized neural firing during seizures is an accurate indicator of postoperative outcome.Methods
Channels meeting phase-locked high gamma (PLHG) criteria were identified retrospectively from intracranial EEG recordings (102 seizures, 46 implantations, 45 patients). Extent of removal of both the seizure onset zone (SOZ) and PLHG was correlated with seizure outcome, classified as good (Engel class I or II, n = 32) or poor (Engel class III or IV, n = 13).Results
Patients with good outcomes had significantly greater proportions of both SOZ and the first 4 (early) PLHG sites resected. Improved outcome classification was noted with early PLHG, as measured by the area under the receiver operating characteristic curves (PLHG 0.79, SOZ 0.68) and by odds ratios for resections including at least 75% of sites identified by each measure (PLHG 9.7 [95% CI: 2.3-41.5], SOZ 5.3 [95% CI: 1.2-23.3]). Among patients with resection of at least 75% of the SOZ, 78% (n = 30) had good outcomes, increasing to 91% when the resection also included at least 75% of early PLHG sites (n = 22).Conclusions
This study demonstrates the localizing value of early PLHG, which is comparable to that provided by the SOZ. Incorporation of PLHG into the clinical evaluation may improve surgical efficacy and help to focus resections on the most critical areas.
SUBMITTER: Weiss SA
PROVIDER: S-EPMC4464742 | biostudies-literature | 2015 Jun
REPOSITORIES: biostudies-literature
Publications
Seizure localization using ictal phase-locked high gamma: A retrospective surgical outcome study.
Weiss Shennan A SA Lemesiou Athena A Connors Robert R Banks Garrett P GP McKhann Guy M GM Goodman Robert R RR Zhao Binsheng B Filippi Christopher G CG Nowell Mark M Rodionov Roman R Diehl Beate B McEvoy Andrew W AW Walker Matthew C MC Trevelyan Andrew J AJ Bateman Lisa M LM Emerson Ronald G RG Schevon Catherine A CA
Neurology 20150513 23
<h4>Objective</h4>To determine whether resection of areas with evidence of intense, synchronized neural firing during seizures is an accurate indicator of postoperative outcome.<h4>Methods</h4>Channels meeting phase-locked high gamma (PLHG) criteria were identified retrospectively from intracranial EEG recordings (102 seizures, 46 implantations, 45 patients). Extent of removal of both the seizure onset zone (SOZ) and PLHG was correlated with seizure outcome, classified as good (Engel class I or ...[more]
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Project description:PurposeTo investigate the characteristics of intracranial ictal high-frequency oscillations (HFOs).MethodsAmong neocortical epilepsy patients who underwent intracranial monitoring and surgery, we studied patients with well-defined, unifocal seizure onsets characterized by discrete HFOs (≥70 Hz). Patients with multifocal or bilateral independent seizure onsets, electroencephalography (EEG) acquired at <1,000 Hz sampling rate, and nonresective surgery were excluded. Based on a prospectively defined protocol, we defined the seizure-onset zone (SOZ) presurgically to include only those channels with HFOs that showed subsequent sustained evolution (HFOs+ channels) but not the channels that lacked evolution (HFOs- channels). We then resected the SOZ as defined above, 1 cm of the surrounding cortex, and immediate spread area, modified by the presence of eloquent cortex in the vicinity. For purposes of this study, we also defined the SOZ based on the conventional frequency activity (CFA, <70 Hz) at seizure onset, although that information was not considered for preoperative determination of the surgical boundary. We investigated the temporal and spatial characteristics of the ictal HFOs post hoc by visual and spectral methods, and also compared them to the seizure onset defined by the CFA.Key findingsOf 14 consecutive neocortical epilepsy patients, six patients met the inclusion criteria. Magnetic resonance imaging (MRI) was normal or showed heterotopia. All had subdural electrodes, with additional intracerebral depth electrodes in some. Electrode coverage was extensive (median 94 channels), including limited contralateral coverage. Seizure onsets were lobar or multilobar. Resections were performed per protocol, except in two patients where complete resection of the SOZ could not be done due to overlap with speech area. Histology was abnormal in all patients. Postoperative outcome was class I/II (n = 5, 83%) or class III over a mean follow-up of 27 months. Post hoc analysis of 15 representative seizures showed that the ictal HFOs were widespread at seizure onset but evolved subsequently with different characteristics. In contrast to HFOs-, the HFOs+ were significantly higher in peak frequency (97.1 vs. 89.1 Hz, p = 0.001), more robust (nearly twofold higher peak power, p < 0.0001), and spatially restricted [mean 12.2 vs. 22.4 channels; odds ratio (OR) 0.51, 95% confidence interval (CI) 0.42-0.62; p < 0.0001]. The seizure onset defined by HFOs+ was earlier (by an average of 0.41 s), and occurred in a significantly different and smaller distribution (OR 0.27, 95% CI 0.21-0.34, p < 0.0001), than the seizure onset defined by the CFA. As intended, the HFOs+ channels were 10 times more likely to have been resected than the HFOs- channels (OR 9.7, 95% CI 5-17, p < 0.0001).SignificanceOur study demonstrates the widespread occurrence of ictal HFOs at seizure onset, outlines a practical method to localize the SOZ based on their restricted pattern of evolution, and highlights the differences between the SOZs defined by HFOs and CFA. We show that smaller resections, restricted mainly to the HFOs channels with evolution, can lead to favorable seizure outcome. Our findings support the notion of widespread epileptic networks underlying neocortical epilepsy.
| S-EPMC3188690 | biostudies-literature
Project description:Intracranial electroencephalography (EEG) is performed as part of an epilepsy surgery evaluation when noninvasive tests are incongruent or the putative seizure-onset zone is near eloquent cortex. Determining the seizure-onset zone using intracranial EEG has been conventionally based on identification of specific ictal patterns with visual inspection. High-frequency oscillations (HFOs, >80 Hz) have been recognized recently as highly correlated with the epileptogenic zone. However, HFOs can be difficult to detect because of their low amplitude. Therefore, the prevalence of ictal HFOs and their role in localization of epileptogenic zone on intracranial EEG are unknown.We identified 48 patients who underwent surgical treatment after the surgical evaluation with intracranial EEG, and 44 patients met criteria for this retrospective study. Results were not used in surgical decision making. Intracranial EEG recordings were collected with a sampling rate of 2,000 Hz. Recordings were first inspected visually to determine ictal onset and then analyzed further with time-frequency analysis. Forty-one (93%) of 44 patients had ictal HFOs determined with time-frequency analysis of intracranial EEG.Twenty-two (54%) of the 41 patients with ictal HFOs had complete resection of HFO regions, regardless of frequency bands. Complete resection of HFOs (n = 22) resulted in a seizure-free outcome in 18 (82%) of 22 patients, significantly higher than the seizure-free outcome with incomplete HFO resection (4/19, 21%).Our study shows that ictal HFOs are commonly found with intracranial EEG in our population largely of children with cortical dysplasia, and have localizing value. The use of ictal HFOs may add more promising information compared to interictal HFOs because of the evidence of ictal propagation and followed by clinical aspect of seizures. Complete resection of HFOs is a favorable prognostic indicator for surgical outcome.
| S-EPMC3520059 | biostudies-other
Project description:IntroductionSurgical treatment of drug-resistant epilepsy relies on the identification of the seizure onset zone (SOZ) and often requires intracranial EEG (iEEG). We have developed a new approach for non-invasive magnetic and electric source imaging of the SOZ (MSI-SOZ and ESI-SOZ) from ictal magnetoencephalography (MEG) and EEG recordings, using wavelet-based Maximum Entropy on the Mean (wMEM) method. We compared the performance of MSI-SOZ and ESI-SOZ with interictal spike source localization (MSI-spikes and ESI-spikes) and clinical localization of the SOZ (i.e., based on iEEG or lesion topography, denoted as clinical-SOZ).MethodsA total of 46 MEG or EEG seizures from 13 patients were analyzed. wMEM was applied around seizure onset, centered on the frequency band showing the strongest power change. Principal component analysis applied to spatiotemporal reconstructed wMEM sources (0.4-1 s around seizure onset) identified the main spatial pattern of ictal oscillations. Qualitative sublobar concordance and quantitative measures of distance and spatial overlaps were estimated to compare MSI/ESI-SOZ with MSI/ESI-Spikes and clinical-SOZ.ResultsMSI/ESI-SOZ were concordant with clinical-SOZ in 81% of seizures (MSI 90%, ESI 64%). MSI-SOZ was more accurate and identified sources closer to the clinical-SOZ (P = 0.012) and to MSI-Spikes (P = 0.040) as compared with ESI-SOZ. MSI/ESI-SOZ and MSI/ESI-Spikes did not differ in terms of concordance and distance from the clinical-SOZ.ConclusionswMEM allows non-invasive localization of the SOZ from ictal MEG and EEG. MSI-SOZ performs better than ESI-SOZ. MSI/ESI-SOZ can provide important additional information to MSI/ESI-Spikes during presurgical evaluation. Hum Brain Mapp 37:2528-2546, 2016. © 2016 Wiley Periodicals, Inc.
| S-EPMC6867380 | biostudies-literature
Project description:We observed robust coupling between the high- and low-frequency bands of ongoing electrical activity in the human brain. In particular, the phase of the low-frequency theta (4 to 8 hertz) rhythm modulates power in the high gamma (80 to 150 hertz) band of the electrocorticogram, with stronger modulation occurring at higher theta amplitudes. Furthermore, different behavioral tasks evoke distinct patterns of theta/high gamma coupling across the cortex. The results indicate that transient coupling between low- and high-frequency brain rhythms coordinates activity in distributed cortical areas, providing a mechanism for effective communication during cognitive processing in humans.
| S-EPMC2628289 | biostudies-literature
Project description:BackgroundA majority of patients with insular tumors present with seizures. Although a number of studies have shown that greater extent of resection improves overall patient survival, few studies have documented postoperative seizure control after insular tumor resection.ObjectiveTo (1) characterize seizure control rates in patients undergoing insular tumor resection, (2) identify predictors of seizure control, and (3) evaluate the association between seizure recurrence and tumor progression.MethodsThe study population included adults who had undergone resection of insular gliomas between 1997 and 2015 at our institution. Preoperative seizure characteristics, tumor characteristics, surgical factors, and postoperative seizure outcomes were reviewed.ResultsOne-hundred nine patients with sufficient clinical data were included in the study. At 1 yr after surgery, 74 patients (68%) were seizure free. At final follow-up, 42 patients (39%) were seizure free. Median time to seizure recurrence was 46 mo (95% confidence interval 31-65 mo). Multivariate Cox regression analysis revealed that greater extent of resection (hazard ratio = 0.2899 [0.1129, 0.7973], P = .0127) was a significant predictor of seizure freedom. Of patients who had seizure recurrence and tumor progression, seizure usually recurred within 3 mo prior to tumor progression. Repeat resection offered additional seizure control, as 8 of the 22 patients with recurrent seizures became seizure free after reoperation.ConclusionMaximizing the extent of resection in insular gliomas portends greater seizure freedom after surgery. Seizure recurrence is associated with tumor progression, and repeat operation can provide additional seizure control.
| S-EPMC6454798 | biostudies-literature
Project description:Importance:Literature on ictal magnetoencephalography (MEG) in clinical practice and the relationship to other modalities is limited because of the brevity of routine studies. Objective:To investigate the utility and reliability of ictal MEG in the localization of the epileptogenic zone. Design, Setting, and Participants:A retrospective medical record review and prospective analysis of a novel ictal rhythm analysis method was conducted at a tertiary epilepsy center with a wide base of referrals for epilepsy surgery evaluation and included consecutive cases of patients who experienced epileptic seizures during routine MEG studies from March 2008 to February 2012. A total of 377 studies screened. Data were analyzed from November 2011 to October 2015. Main Outcomes and Measures:Presurgical workup and interictal and ictal MEG data were reviewed. The localizing value of using extended-source localization of a narrow band identified visually at onset was analyzed. Results:Of the 44 included patients, the mean (SD) age at the time of recording was 19.3 (14.9) years, and 25 (57%) were male. The mean duration of recording was 51.2 minutes. Seizures were provoked by known triggers in 3 patients and were spontaneous otherwise. Twenty-five patients (57%) had 1 seizure, 6 (14%) had 2, and 13 (30%) had 3 or more. Magnetoencephalography single equivalent current dipole analysis was possible in 29 patients (66%), of whom 8 (28%) had no clear interictal discharges. Sublobar concordance between ictal and interictal dipoles was seen in 18 of 21 patients (86%). Three patients (7%) showed clear ictal MEG patterns without electroencephalography changes. Ictal MEG dipoles correlated with the lobe of onset in 7 of 8 patients (88%) who underwent intracranial electroencephalography evaluations. Reasons for failure to identify ictal dipoles included diffuse or poor dipolar ictal patterns, no MEG changes, and movement artifact. Resection of areas containing a minimum-norm estimate of a narrow band at onset, not single equivalent current dipole, was associated with sustained seizure freedom. Conclusions and Significance:Ictal MEG data can provide reliable localization, including in cases that are difficult to localize by other modalities. These findings support the use of extended-source localization for seizures recorded during MEG.
| S-EPMC6233852 | biostudies-other
Project description:High frequency oscillations have been proposed as a clinically useful biomarker of seizure generating sites. We used a unique set of human microelectrode array recordings (four patients, 10 seizures), in which propagating seizure wavefronts could be readily identified, to investigate the basis of ictal high frequency activity at the cortical (subdural) surface. Sustained, repetitive transient increases in high gamma (80-150 Hz) amplitude, phase-locked to the low-frequency (1-25 Hz) ictal rhythm, correlated with strong multi-unit firing bursts synchronized across the core territory of the seizure. These repetitive high frequency oscillations were seen in recordings from subdural electrodes adjacent to the microelectrode array several seconds after seizure onset, following ictal wavefront passage. Conversely, microelectrode recordings demonstrating only low-level, heterogeneous neural firing correlated with a lack of high frequency oscillations in adjacent subdural recording sites, despite the presence of a strong low-frequency signature. Previously, we reported that this pattern indicates a failure of the seizure to invade the area, because of a feedforward inhibitory veto mechanism. Because multi-unit firing rate and high gamma amplitude are closely related, high frequency oscillations can be used as a surrogate marker to distinguish the core seizure territory from the surrounding penumbra. We developed an efficient measure to detect delayed-onset, sustained ictal high frequency oscillations based on cross-frequency coupling between high gamma amplitude and the low-frequency (1-25 Hz) ictal rhythm. When applied to the broader subdural recording, this measure consistently predicted the timing or failure of ictal invasion, and revealed a surprisingly small and slowly spreading seizure core surrounded by a far larger penumbral territory. Our findings thus establish an underlying neural mechanism for delayed-onset, sustained ictal high frequency oscillations, and provide a practical, efficient method for using them to identify the small ictal core regions. Our observations suggest that it may be possible to reduce substantially the extent of cortical resections in epilepsy surgery procedures without compromising seizure control.
| S-EPMC3859220 | biostudies-literature
Project description:Neuronal oscillations in various frequency bands have been reported in numerous studies in both humans and animals. While it is obvious that these oscillations play an important role in cognitive processing, it remains unclear how oscillations in various frequency bands interact. In this study we have investigated phase to power locking in MEG activity of healthy human subjects at rest with their eyes closed. To examine cross-frequency coupling, we have computed coherence between the time course of the power in a given frequency band and the signal itself within every channel. The time-course of the power was calculated using a sliding tapered time window followed by a Fourier transform. Our findings show that high-frequency gamma power (30-70 Hz) is phase-locked to alpha oscillations (8-13 Hz) in the ongoing MEG signals. The topography of the coupling was similar to the topography of the alpha power and was strongest over occipital areas. Interestingly, gamma activity per se was not evident in the power spectra and only became detectable when studied in relation to the alpha phase. Intracranial data from an epileptic subject confirmed these findings albeit there was slowing in both the alpha and gamma band. A tentative explanation for this phenomenon is that the visual system is inhibited during most of the alpha cycle whereas a burst of gamma activity at a specific alpha phase (e.g. at troughs) reflects a window of excitability.
| S-EPMC2602598 | biostudies-literature
Project description:Absence seizures are generalized, cortico-thalamo-cortical (CTC) high power electroencephalographic (EEG) or electrocorticographic (ECoG) events that initiate and terminate suddenly. ECoG recordings of absence seizures in animal models of genetic absence epilepsy show a sudden spike-wave-discharge (SWD) onset that rapidly emerges from normal ECoG activity. However, given that absence seizures occur most often during periods of drowsiness or quiet wakefulness, we wondered whether SWD onset correlates with pre-ictal changes in network activity. To address this, we analyzed ECoG recordings of both spontaneous and induced SWDs in rats with genetic absence epilepsy. We discovered that the duration and intensity of spontaneous SWDs positively correlate with pre-ictal 20-40Hz (?) spectral power and negatively correlate with 4-7Hz (Ø) power. In addition, the output of thalamocortical neurons decreases within the same pre-ictal window of time. In separate experiments we found that the propensity for SWD induction was correlated with pre-ictal ? power. These results argue that CTC networks undergo a pre-seizure state transition, possibly due to a functional reorganization of cortical microcircuits, which leads to the generation of absence seizures.
| S-EPMC5607110 | biostudies-literature
Project description:ObjectiveWe aimed to determine the rates and predictors of resection and seizure freedom after bilateral stereo-electroencephalography (SEEG) implantation.MethodsWe reviewed 184 patients who underwent bilateral SEEG implantation (2009-2015). Noninvasive and invasive evaluation findings were collected. Outcomes of interest included subsequent resection and seizure freedom. Statistical analyses employed multivariable logistic regression and proportional hazard modeling. Preoperative and postoperative seizure frequency, severity, and quality of life scales were also compared.ResultsFollowing bilateral SEEG implantation, 106 of 184 patients (58%) underwent resection. Single seizure type (P = 0.007), a family history of epilepsy (P = 0.003), 10 or more seizures per month (P = 0.004), lower number of electrodes (P = 0.02), or sentinel electrode placement (P = 0.04) was predictive of undergoing a resection, as were lack of nonlocalized (P < 0.0001) or bilateral (P < 0.0001) ictal-onset zones on SEEG. Twenty-six of 81 patients (32% with follow-up greater than 1 year) remained seizure-free. Predictors of seizure freedom were single seizure type (P = 0.01), short epilepsy duration (P = 0.008), use of 2 or fewer antiepileptic drugs (AEDs) at the time of surgery (P = 0.0006), primary localization hypothesis involving the frontal lobe (P = 0.002), sentinel electrode placement only (P = 0.02), and lack of overlap between ictal-onset zone and eloquent cortex (P = 0.04), along with epilepsy substrate histopathology (P = 0.007). Complete resection of a suspected focal cortical dysplasia showed a trend to increased likelihood of seizure freedom (P = 0.09). The 44 of 55 patients (80%) who underwent resection and experienced seizure recurrence had >50% seizure reduction, as opposed to 26 of 45 patients (58%) who continued medical therapy alone (P = 0.003). Seventy-two percent of patients had a clinically meaningful quality of life improvement (>10% decrease in the Quality of Life in Epilepsy [QOLIE-10] score) at 1 year.SignificanceA strong preimplantation hypothesis of a suspected unifocal epilepsy increases the odds of resection and seizure freedom. We discuss a tailored approach, taking into account localization hypothesis and suspected epilepsy etiology in guiding implantation and subsequent surgical strategy.
| S-EPMC6510950 | biostudies-literature