Normative brain mapping of interictal intracranial EEG to localize epileptogenic tissue.
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ABSTRACT:
SUBMITTER: Taylor PN
PROVIDER: S-EPMC9050535 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Objective:We investigated the performance of automatic spike detection and subsequent electroencephalogram (EEG) source imaging to localize the epileptogenic zone (EZ) from long-term EEG recorded during video-EEG monitoring. Methods:In 32 patients, spikes were automatically detected in the EEG and clustered according to their morphology. The two spike clusters with most single events in each patient were averaged and localized in the brain at the half-rising time and peak of the spike using EEG source imaging. On the basis of the distance from the sources to the resection and the known patient outcome after surgery, the performance of the automated EEG analysis to localize the EZ was quantified. Results:In 28 out of the 32 patients, the automatically detected spike clusters corresponded with the reported interictal findings. The median distance to the resection in patients with Engel class I outcome was 6.5 and 15 mm for spike cluster 1 and 27 and 26 mm for cluster 2, at the peak and the half-rising time of the spike, respectively. Spike occurrence (cluster 1 vs. cluster 2) and spike timing (peak vs. half-rising) significantly influenced the distance to the resection (p < 0.05). For patients with Engel class II, III, and IV outcomes, the median distance increased to 36 and 36 mm for cluster 1. Localizing spike cluster 1 at the peak resulted in a sensitivity of 70% and specificity of 100%, positive prediction value (PPV) of 100%, and negative predictive value (NPV) of 53%. Including the results of spike cluster 2 led to an increased sensitivity of 79% NPV of 55% and diagnostic OR of 11.4, while the specificity dropped to 75% and the PPV to 90%. Significance:We showed that automated analysis of long-term EEG recordings results in a high sensitivity and specificity to localize the epileptogenic focus.
| S-EPMC5862106 | biostudies-literature
Project description:Synchronized cortical activity is implicated in both normative cognitive functioning and many neurologic disorders. For epilepsy patients with intractable seizures, irregular synchronization within the epileptogenic zone (EZ) is believed to provide the network substrate through which seizures initiate and propagate. Mapping the EZ prior to epilepsy surgery is critical for detecting seizure networks in order to achieve postsurgical seizure control. However, automated techniques for characterizing epileptic networks have yet to gain traction in the clinical setting. Recent advances in signal processing and spike detection have made it possible to examine the spatiotemporal propagation of interictal spike discharges across the epileptic cortex. In this study, we present a novel methodology for detecting, extracting, and visualizing spike propagation and demonstrate its potential utility as a biomarker for the EZ. Eighteen presurgical intracranial EEG recordings were obtained from pediatric patients ultimately experiencing favorable (i.e., seizure-free, n?=?9) or unfavorable (i.e., seizure-persistent, n?=?9) surgical outcomes. Novel algorithms were applied to extract multichannel spike discharges and visualize their spatiotemporal propagation. Quantitative analysis of spike propagation was performed using trajectory clustering and spatial autocorrelation techniques. Comparison of interictal propagation patterns revealed an increase in trajectory organization (i.e., spatial autocorrelation) among Sz-Free patients compared with Sz-Persist patients. The pathophysiological basis and clinical implications of these findings are considered.
| S-EPMC5165024 | biostudies-literature
Project description:BackgroundStereotactic electroencephalography (SEEG) is a minimally invasive neurosurgical method to localize epileptogenic brain regions in epilepsy but requires days in the hospital with interventions to trigger several seizures.ObjectiveTo make initial progress in the development of network analysis methods to identify epileptogenic brain regions using brief, resting-state SEEG data segments, without requiring seizure recordings.MethodsIn a cohort of 15 adult focal epilepsy patients undergoing SEEG, we evaluated functional connectivity (alpha-band imaginary coherence) across sampled regions using brief (2 min) resting-state data segments. Bootstrapped logistic regression was used to generate a model to predict epileptogenicity of individual regions.ResultsCompared to nonepileptogenic structures, we found increased functional connectivity within epileptogenic regions (P < .05) and between epileptogenic areas and other structures (P < .01, paired t-tests, corrected). Epileptogenic areas also demonstrated higher clustering coefficient (P < .01) and betweenness centrality (P < .01), and greater decay of functional connectivity with distance (P < .05, paired t-tests, corrected). Our functional connectivity model to predict epileptogenicity of individual regions demonstrated an area under the curve of 0.78 and accuracy of 80.4%.ConclusionOur study represents a preliminary step towards defining resting-state SEEG functional connectivity patterns to help localize epileptogenic brain regions ahead of neurosurgical treatment without requiring seizure recordings.
| S-EPMC7225010 | biostudies-literature
Project description:OBJECTIVE:When considering all patients with focal drug-resistant epilepsy, as high as 40-50% of patients suffer seizure recurrence after surgery. To achieve seizure freedom without side effects, accurate localization of the epileptogenic tissue is crucial before its resection. We investigate an automated, fast, objective mapping process that uses only interictal data. METHODS:We propose a novel approach based on multiple iEEG features, which are used to train a support vector machine (SVM) model for classification of iEEG electrodes as normal or pathologic using 30 min of inter-ictal recording. RESULTS:The tissue under the iEEG electrodes, classified as epileptogenic, was removed in 17/18 excellent outcome patients and was not entirely resected in 8/10 poor outcome patients. The overall best result was achieved in a subset of 9 excellent outcome patients with the area under the receiver operating curve?=?0.95. CONCLUSION:SVM models combining multiple iEEG features show better performance than algorithms using a single iEEG marker. Multiple iEEG and connectivity features in presurgical evaluation could improve epileptogenic tissue localization, which may improve surgical outcome and minimize risk of side effects. SIGNIFICANCE:In this study, promising results were achieved in localization of epileptogenic regions by SVM models that combine multiple features from 30 min of inter-ictal iEEG recordings.
| S-EPMC6759804 | biostudies-literature
Project description:High frequency oscillations (HFOs) are very brief events that are a well-established biomarker of the epileptogenic zone (EZ) but are rare and comprise only a tiny fraction of the total recorded EEG. We hypothesize that the interictal high frequency 'background' data, which has received little attention but represents the majority of the EEG record, also may contain additional, novel information for identifying the EZ. We analysed intracranial EEG (30-500 Hz frequency range) acquired from 24 patients who underwent resective surgery. We computed 38 quantitative features based on all usable, interictal data (63-307 h per subject), excluding all detected HFOs. We assessed association between each feature and the seizure onset zone (SOZ) and resected volume (RV) using logistic regression. A pathology score per channel was also created via principle component analysis and logistic regression, using hold-out-one-patient cross-validation to avoid in-sample training. Association of the pathology score with the SOZ and RV was quantified using an asymmetry measure. Many features were associated with the SOZ: 23/38 features had odds ratios >1.3 or <0.7 and 17/38 had odds ratios different than zero with high significance (P < 0.001/39, logistic regression with Bonferroni Correction). The pathology score, the rate of HFOs, and their channel-wise product were each strongly associated with the SOZ [median asymmetry ≥0.44, good surgery outcome patients; median asymmetry ≥0.40, patients with other outcomes; 95% confidence interval (CI) > 0.27 in both cases]. The pathology score and the channel-wise product also had higher asymmetry with respect to the SOZ than the HFO rate alone (median difference in asymmetry ≥0.18, 95% CI >0.05). These results support that the high frequency background data contains useful information for determining the EZ, distinct and complementary to information from detected HFOs. The concordance between the high frequency activity pathology score and the rate of HFOs appears to be a better biomarker of epileptic tissue than either measure alone.
| S-EPMC8417455 | biostudies-literature
Project description:Aim: In neuroscience research, data are quite often characterized by an imbalanced distribution between the majority and minority classes, an issue that can limit or even worsen the prediction performance of machine learning methods. Different resampling procedures have been developed to face this problem and a lot of work has been done in comparing their effectiveness in different scenarios. Notably, the robustness of such techniques has been tested among a wide variety of different datasets, without considering the performance of each specific dataset. In this study, we compare the performances of different resampling procedures for the imbalanced domain in stereo-electroencephalography (SEEG) recordings of the patients with focal epilepsies who underwent surgery. Methods: We considered data obtained by network analysis of interictal SEEG recorded from 10 patients with drug-resistant focal epilepsies, for a supervised classification problem aimed at distinguishing between the epileptogenic and non-epileptogenic brain regions in interictal conditions. We investigated the effectiveness of five oversampling and five undersampling procedures, using 10 different machine learning classifiers. Moreover, six specific ensemble methods for the imbalanced domain were also tested. To compare the performances, Area under the ROC curve (AUC), F-measure, Geometric Mean, and Balanced Accuracy were considered. Results: Both the resampling procedures showed improved performances with respect to the original dataset. The oversampling procedure was found to be more sensitive to the type of classification method employed, with Adaptive Synthetic Sampling (ADASYN) exhibiting the best performances. All the undersampling approaches were more robust than the oversampling among the different classifiers, with Random Undersampling (RUS) exhibiting the best performance despite being the simplest and most basic classification method. Conclusions: The application of machine learning techniques that take into consideration the balance of features by resampling is beneficial and leads to more accurate localization of the epileptogenic zone from interictal periods. In addition, our results highlight the importance of the type of classification method that must be used together with the resampling to maximize the benefit to the outcome.
| S-EPMC8641296 | biostudies-literature
Project description:OBJECTIVE:Brain regions are localized for resection during epilepsy surgery based on rare seizures observed during a short period of intracranial electroencephalography (iEEG) monitoring. Interictal epileptiform bursts, which are more prevalent than seizures, may provide complementary information to aid in epilepsy evaluation. In this study, we leverage a long-term iEEG dataset from canines with naturally occurring epilepsy to investigate interictal bursts and their electrographic relationship to seizures. METHODS:Four dogs were included in this study, each monitored previously with continuous iEEG for periods of 475.7, 329.9, 45.8, and 451.8 days, respectively, for a total of >11,000 h. Seizures and bursts were detected and validated by two board-certified epileptologists. A published Bayesian model was applied to analyze the dynamics of interictal epileptic bursts on EEG and compare them to seizures. RESULTS:In three dogs, bursts were stereotyped and found to be statistically similar to periods before or near seizure onsets. Seizures from one dog during status epilepticus were markedly different from other seizures in terms of burst similarity. SIGNIFICANCE:Shorter epileptic bursts explored in this work have the potential to yield significant information about the distribution of epileptic events. In our data, bursts are at least an order of magnitude more prevalent than seizures and occur much more regularly. Our finding that bursts often display pronounced similarity to seizure onsets suggests that they contain relevant information about the epileptic networks from which they arise and may aide in the clinical evaluation of epilepsy in patients.
| S-EPMC4770560 | biostudies-literature
Project description:Background: Potentially curative epilepsy surgery can be offered if a single, discrete epileptogenic zone (EZ) can be identified. For individuals in whom there is no clear concordance between clinical localization, scalp EEG, and imaging data, intracranial EEG (icEEG) may be needed to confirm a predefined hypothesis regarding irritative zone (IZ), seizure onset zone (SOZ), and EZ prior to surgery. However, icEEG has limited spatial sampling and may fail to reveal the full extent of epileptogenic network if predefined hypothesis is not correct. Simultaneous icEEG-fMRI has been safely acquired in humans and allows exploration of neuronal activity at the whole-brain level related to interictal epileptiform discharges (IED) captured intracranially. Methods: We report icEEG-fMRI in eight patients with refractory focal epilepsy who had resective surgery and good postsurgical outcome. Surgical resection volume in seizure-free patients post-surgically reflects confirmed identification of the EZ. IEDs on icEEG were classified according to their topographic distribution and localization (Focal, Regional, Widespread, and Non-contiguous). We also divided IEDs by their location within the surgical resection volume [primary IZ (IZ1) IED] or outside [secondary IZ (IZ2) IED]. The distribution of fMRI blood oxygen level-dependent (BOLD) changes associated with individual IED classes were assessed over the whole brain using a general linear model. The concordance of resulting BOLD map was evaluated by comparing localization of BOLD clusters with surgical resection volume. Additionally, we compared the concordance of BOLD maps and presence of BOLD clusters in remote brain areas: precuneus, cuneus, cingulate, medial frontal, and thalamus for different IED classes. Results: A total of 38 different topographic IED classes were identified across the 8 patients: Focal (22) and non-focal (16, Regional = 9, Widespread = 2, Non-contiguous = 5). Twenty-nine IEDs originated from IZ1 and 9 from IZ2. All IED classes were associated with BOLD changes. BOLD maps were concordant with the surgical resection volume for 27/38 (71%) IED classes, showing statistical global maximum BOLD cluster or another cluster in the surgical resection volume. The concordance of BOLD maps with surgical resection volume was greater (p < 0.05) for non-focal (87.5%, 14/16) as compared to Focal (59%, 13/22) IED classes. Additionally, BOLD clusters in remote cortical and deep brain areas were present in 84% (32/38) of BOLD maps, more commonly (15/16; 93%) for non-focal IED-related BOLD maps. Conclusions: Simultaneous icEEG-fMRI can reveal BOLD changes at the whole-brain level for a wide range of IEDs on icEEG. BOLD clusters within surgical resection volume and remote brain areas were more commonly seen for non-focal IED classes, suggesting that a wider hemodynamic network is at play.
| S-EPMC8490636 | biostudies-literature
Project description:Simultaneous collection of scalp EEG and fMRI has become an important tool for studying the hemodynamic changes associated with interictal epileptiform discharges (IEDs) in persons with epilepsy, and has become a standard presurgical assessment tool in some centres. We previously demonstrated that performing EEG-fMRI using intracranial electrodes (iEEG-fMRI) is of low risk to patients in our research centre, and offers unique insight into BOLD signal changes associated with IEDs recorded from very discrete sources. However, it is unknown whether the BOLD response corresponding to IEDs recorded by iEEG-fMRI follows the canonical hemodynamic response. We therefore scanned 11 presurgical epilepsy patients using iEEG-fMRI, and assessed the hemodynamic response associated with individual IEDs using two methods: assessment of BOLD signal changes associated with isolated IEDs at the location of the active intracranial electrode, and by estimating subject-specific impulse response functions to isolated IEDs. We found that the hemodynamic response associated with the intracranially recorded discharges varied by patient and by spike location. The observed shape and timing differences also deviated from the canonical hemodynamic response function traditionally used in many fMRI experiments. It is recommended that future iEEG-fMRI studies of IEDs use a flexible hemodynamic response model when performing parametric tests to accurately characterize these data.
| S-EPMC6869833 | biostudies-literature
Project description:Objective:Electrical source imaging (ESI) is used increasingly to estimate the epileptogenic zone (EZ) in patients with epilepsy. Directed functional connectivity (DFC) coupled to ESI helps to better characterize epileptic networks, but studies on interictal activity have relied on high-density recordings. We investigated the accuracy of ESI and DFC for localizing the EZ, based on low-density clinical electroencephalography (EEG). Methods:We selected patients with the following: (a) focal epilepsy, (b) interictal spikes on standard EEG, (c) either a focal structural lesion concordant with the electroclinical semiology or good postoperative outcome. In 34 patients (20 temporal lobe epilepsy [TLE], 14 extra-TLE [ETLE]), we marked interictal spikes and estimated the cortical activity during each spike in 82 cortical regions using a patient-specific head model and distributed linear inverse solution. DFC between brain regions was computed using Granger-causal modeling followed by network topologic measures. The concordance with the presumed EZ at the sublobar level was computed using the epileptogenic lesion or the resected area in postoperative seizure-free patients. Results:ESI, summed outflow, and efficiency were concordant with the presumed EZ in 76% of the patients, whereas the clustering coefficient and betweenness centrality were concordant in 70% of patients. There was no significant difference between ESI and connectivity measures. In all measures, patients with TLE had a significantly higher (P < 0.05) concordance with the presumed EZ than patients with with ETLE. The brain volume accepted for concordance was significantly larger in TLE. Significance:ESI and DFC derived from low-density EEG can reliably estimate the EZ from interictal spikes. Connectivity measures were not superior to ESI for EZ localization during interictal spikes, but the current validation of the localization of connectivity measure is promising for other applications.
| S-EPMC6546067 | biostudies-other