Enhanced EEG functional connectivity in mesial temporal lobe epilepsy

PURPOSE: To analyze and compare spectral properties and interdependencies of intracerebral EEG signals recorded during interictal periods from mesial temporal lobe structures in two groups of epileptic patients defined according to the involvement of these structures in the epileptogenic zone (EZ). METHODS: Interictal EEG activity in mesial temporal lobe (MTL) structures (hippocampus, entorhinal cortex and amygdala) was obtained from intracerebral recordings performed in 21 patients with drug-resistant mesial temporal lobe epilepsy (MTLE group). This group was compared with a "control" group of patients (non-MTLE group) in whom depth-EEG recordings of MTL show that seizures did not start from the MTL. Comparison criteria were based on spectral properties and statistical coupling (nonlinear correlation coefficient h(2)) of MTL signals. RESULTS: Power spectral density analysis showed a significant decrease in the theta frequency sub-band (p=0.01) in the MTLE group. Nonlinear correlation (h(2)) values were found to be higher in the MTLE group than in the NMTLE group (p=0.0014). This effect was significant for theta, alpha, beta and gamma frequencies. Correlation values were not correlated with the frequency of interictal spikes (IS) and significant differences between groups were still measureable even when spikes were suppressed from analyzed EEG periods. DISCUSSION: This study shows that, during the interictal state, the EZ in MTLE is characterized by a decrease of oscillations in the theta sub-band and by a general increase of signal interdependencies. This last finding suggests that the EZ is characterized by network of neuronal assemblies with a reinforced functional connectivity.     

Ictal automatisms with preserved responsiveness in a patient with left mesial temporal lobe epilepsy

PURPOSE: To describe the possible mechanism of ictal automatisms with preserved responsiveness (APRs) in a patient with left mesial temporal lobe epilepsy, which had not been reported previously. METHODS: Ictal EEGs recorded from bilateral foramen ovale electrodes with scalp-sphenoidal electrodes were analyzed in respect to the ictal semiology. RESULTS: The patient had a right hemispheric language dominance in the dextral. Electroclinical analysis revealed that the onset of oroalimentary automatisms coincided with the involvement of the left mesial and lateral temporal structures by spreading ictal discharges. The ictal discharge spreading was limited to the ipsilateral hemisphere throughout the seizure, which explained the intact consciousness and preserved responsiveness of the patient. CONCLUSIONS: This case suggests that APRs take place in seizures originating from the nondominant temporal lobe, during which ipsilateral mesial and lateral temporal structures are diffusely involved without spreading to the contralateral side.     

Bilateral mesial temporal lobe epilepsy: comparison of scalp EEG and hippocampal MRI-T2 relaxometry

OBJECTIVE: Bilateral hippocampal abnormality is frequent in mesial temporal lobe sclerosis and might affect outcome in epilepsy surgery. The objective of this study was to compare the lateralization of interictal and ictal scalp EEG with MRI T2 relaxometry. MATERIAL AND METHODS: Forty-nine consecutive patients with intractable mesial temporal lobe epilepsy (MTLE) were studied with scalp EEG/video monitoring and MRI T2 relaxometry. RESULTS: Bilateral prolongation of hippocampal T2 time was significantly associated with following bitemporal scalp EEG changes: (i) in ictal EEG left and right temporal EEG seizure onsets in different seizures, or, after regionalized EEG onset, evolution of an independent ictal EEG over the contralateral temporal lobe (left and right temporal asynchronous frequencies or lateralization switch; P = 0.002); (ii) in interictal EEG both left and right temporal interictal slowing (P = 0.007). Bitemporal T2 changes were not, however, associated with bitemporal interictal epileptiform discharges (IED). Lateralization of bilateral asymmetric or unilateral abnormal T2 findings were associated with initial regionalization of the ictal EEG in all but one patient (P < 0.005), with lateralization of IED in all patients (P < 0.005), and with scalp EEG slowing in 28 (82,4%) of 34 patients (P = 0.007). CONCLUSION: Our data suggest that EEG seizure propagation is more closely related to hippocampal T2 abnormalities than IED. Interictal and ictal scalp EEG, including the recognition of ictal propagation patterns, and MRI T2 relaxometry can help to identify patients with bitemporal damage in MTLE. Further studies are needed to estimate the impact of bilateral EEG and MRI abnormal findings on the surgical outcome.     

Interictal EEG and ictal scalp EEG propagation are highly predictive of surgical outcome in mesial temporal lobe epilepsy

PURPOSE: Surgical outcome in patients with mesial temporal lobe sclerosis (MTS) is worse than that in patients with temporal lobe activity (TLE) with tumors. Previous studies of the ictal EEG focused on ictal EEG onset in scalp EEG or ictal EEG propagation in invasive recordings. Ictal EEG propagation with scalp electrodes has not been reported. METHODS: Ictal scalp EEG propagation patterns were studied in 347 seizures of 58 patients with MTS or nonlesional TLE. Interictal epileptiform discharges (IEDs) and the presence of unilateral mesial temporal lobe atrophy in magnetic resonance imaging (MRI) also were studied in these 58 patients. Forty-nine patients were operated on (minimal follow-up of 1 year). RESULTS: Postoperatively, seizure-free outcome was seen in (a) 82.8% of patients with regionalized EEG seizure without contralateral propagation, but in only 45.5% of patients with contralateral propagation (p = 0.007); (b) 84.6% of patients with 100% IED lateralized to one temporal lobe, but in only 52.2% with <100% unitemporal IED (p = 0.015); (c) 88.9% with 100% unitemporal IED and regionalized ictal EEG combined, 73.7% with one of both variables, and only 33.3% with <100% ipsitemporal IED combined with contralateral ictal EEG propagation (p = 0.007). CONCLUSIONS: Switch of lateralization or bitemporal asynchrony in the ictal scalp EEG and bitemporal IED are most probably an index of bitemporal epileptogenicity in MTS and are associated with a worse outcome.     

Intracranial EEG findings in patients with lesional lateral temporal lobe epilepsy

PURPOSE: Intracranial EEG in patients with lesional lateral temporal lobe epilepsy is rarely reported. Therefore, the number of patients with seizures arising independently from ipsilateral mesial structures or contralateral hemisphere has not been clarified. We analyzed the intracranial EEG of cases with localized lesion in the lateral temporal cortex. METHODS: We studied 15 patients who satisfied the following criteria: (1) MRI depicted a lesion less than 4cm in diameter located lateral to the collateral sulcus and at least 3cm posterior to the temporal pole; (2) intracranial EEG with electrodes placed on bilateral temporal lobes captured at least one complex partial seizure; and (3) postoperative follow-up period of 2 years or longer. The mean age of seizure onset was 16.6 years (range, 11-25) and that at surgery was 26.7 years (range, 16-36). RESULTS: A total of 147 complex partial seizures, 51 simple partial seizures, 16 secondarily generalized seizures, and over 80 subclinical seizures were recorded. On the lesional side, many clinical seizures were recorded from the lateral cortex. Independent of the lateral temporal onset seizures, ictal discharges originating from the mesial temporal structures were recorded in 7 of 15 patients (47%). Moreover, onset of ictal discharges from the contralateral temporal lobe was recorded in 7 of 15 patients (47%). Interictal spikes from ipsilateral mesial structures were recorded in all patients. The presence of ipsilateral mesial onset seizures was not associated with hippocampal neuron losses. CONCLUSION: Intracranial EEG analysis revealed that approximately one-half of the patients with structural lesions in the lateral cortex showed independent epileptogenic areas in ipsilateral mesial structures. Although ictal discharges originating from the contralateral temporal lobe were recorded in a half of these patients, this finding does not constitute a contraindication of resective surgery. Interictal spike is not an indicator of whether mesial structures should be resected.     

耐药性颞叶内侧癫痫发作前期海马脑电特征分析

目的 观察耐药性颞叶内侧癫痫患者发作前期海马电极脑电活动特点,为判断和切除癫痫病灶提供神经电生理学依据.方法 对16例非侵入性手段难以明确病灶的耐药性颞叶内侧癫痫患者进行双侧海马电极监测,患者停用抗癫痫药在非麻醉状态下监测48～72 h,分析癫痫发作前期海马电极脑电图资料,探讨耐药性颞叶内侧癫痫发作前期海马电极脑电活动特点.结果 16例发作间期记录到背景活动基础上出现局限于某几个电极点的阵发性高幅慢波1例、发作性快波节律1例、棘波或棘尖慢复合波14例,视为异常脑电活动;经过48～ 72 h监测,10例监测到33次临床癫痫发作,发作起始期海马电极均可记录到清晰可辨的癫痫样脑电波形.结论 颞叶内侧癫痫临床发作起始期海马电极癫痫样放电清晰可辨,部位局限,易于确定癫痫性活动起源部位.对于非侵入性手段难以判断癫痫样放电起源的颞叶内侧癫痫可采用脑立体定向技术植入海马深部电极进行脑电监测.     

Impaired awareness in mesial temporal lobe epilepsy: Network analysis of foramen ovale and scalp EEG

ObjectiveWe use co-registration of foramen-ovale and scalp-EEG to investigate network alterations in temporal-lobe epilepsy during focal seizures without (aura) or with impairment of awareness (SIA).MethodsOne aura and one SIA were selected from six patients. Temporal dynamic among 4 epochs, as well as the differences between aura and SIA, were analyzed through partial directed coherence and graph theory-based indices of centrality.ResultsRegarding the auras temporal evolution, fronto-parietal (FP) regions showed decreased connectivity with respect to the interictal period, in both epileptogenic (EH) and non-epileptogenic hemisphere (nEH). During SIAs, temporal dynamic showed more changes than auras: centrality of mesial temporal (mT) regions changes during all conditions, and nEH FP centrality showed the same dynamic trend of the aura (decreased centrality), until the last epoch, close to the impaired awareness, when showed increased centrality. Comparing SIA with aura, in proximity of impaired awareness, increased centrality was found in all the regions, except in nEH mT.ConclusionsOur findings suggested that the impairment of awareness is related to network alterations occurring first in neocortical regions and when awareness is still retained.SignificanceThe analysis of ‘hub’ alteration can represent a suitable biomarker for scalp EEG-based prediction of awareness impairment.     

Clinical implications of scalp ictal EEG pattern in patients with temporal lobe epilepsy

ObjectiveTo determine the clinical implications of scalp ictal EEG pattern in patients with temporal lobe epilepsy (TLE).MethodsScalp EEG ictal patterns were retrospectively determined in 27 consecutive patients with medically refractory temporal lobe epilepsy who underwent phase-1 scalp video-EEG and phase-2 simultaneous scalp and intracranial video-EEG recordings for pre-surgical evaluation.ResultsOf the 192 temporal lobe seizures recorded during phase-1 and phase-2 scalp video-EEG studies, 124 (65%) seizures were associated with theta/alpha (5–9 Hz) ictal onset pattern, and 68 (35%) seizures were associated with delta (2–5 Hz) ictal onset pattern. Fourteen (52%) patients had exclusively theta/alpha ictal onset, 3 (11%) patients had exclusively delta ictal onset, and 10 (37%) patients had mixed theta/alpha and delta ictal onsets. MTLE was observed in 26 patients who had 124 seizures with theta/alpha ictal onset and 59 seizures with delta ictal onset. LTLE was observed in one patient who had 9 seizures with delta ictal onset. Scalp ictal EEG pattern was not significantly correlated with postsurgical seizure outcomes.ConclusionsBoth scalp delta and theta/alpha ictal onset patterns can be commonly found in patients with MTLE.SignificanceScalp delta ictal onset is not a unique EEG pattern for LTLE as commonly believed.     

Prognostic factors in patients with mesial temporal lobe epilepsy

Purpose:   To disclose clinical, electrophysiologic, and neuroradiologic factors correlated to prognosis in patients with mesial temporal lobe epilepsy (MTLE).
Methods:   One hundred thirty-six MTLE patients were studied for family history, clinical characteristics, instrumental data [electroencephalography (EEG), video-EEG, neuroimaging], and outcome. The population was divided into drug-resistant (DR: 108 patients, 79.4%) and non–drug-resistant (NDR: 28 patients, 20.6%) groups; all variables were analyzed in the two groups.
Results:   The comparison between the two groups shows a relation between resistance to therapy and febrile seizures (FS) (DR 43.5% vs. NDR 17.8%, p = 0.008), mesial temporal sclerosis (MTS) (DR 64.8% vs. NDR 32.1%, p = 0.0025), early age at seizure onset (DR 23.1% vs. NDR 3.6% p = 0.0160), and epileptiform interictal abnormalities (DR 89.7% vs. NDR 68%, p = 0.010). FS were more frequent in patients with MTS than in patients without (46.28% vs. 26.3%, p = 0.0199). Sixty-nine patients underwent surgery and 85.3% of them had a good outcome.
Conclusion:   MTLE is a heterogeneous syndrome. Establishing the factors responsible for and associated with drug resistance is important for therapeutic purposes, as prompt diagnosis of drug resistance must lead to early surgical management. This study shows that FS, MTS, early age at seizure onset, and epileptiform interictal abnormalities are negative prognostic factors and that FS are related to MTS.     

Sex differences in patients with mesial temporal lobe epilepsy

Possible sex differences in the pattern of interictalhypometabolism were investigated, and also seizure spread in patients with mesial temporal lobe epilepsy (n=48) and hippocampal sclerosis (MTLE). Male patients (n=21) more often had a frontal lobehypometabolism ipsilateral to the seizure onset (p<0.0001) and aspread of epileptiform activity to this region (p=0.001). By contrast,female patients more often exhibited hypometabolism (p=0.0052) and anictal spread to the contralateral temporal lobe (p=0.0097). Thesefindings suggest sex differences in spatial distribution of braindysfunction in MTLE, perhaps reflecting sexual dimorphism in regionalcerebral connectivity.

     

Seizure prediction in patients with mesial temporal lobe epilepsy using EEG measures of state similarity

ObjectivesIn patients with intractable epilepsy, predicting seizures above chance and with clinically acceptable performance has yet to be demonstrated. In this study, an intracranial EEG-based seizure prediction method using measures of similarity with a reference state is proposed.Methods1565 h of continuous intracranial EEG data from 17 patients with mesial temporal lobe epilepsy were investigated. The recordings included 175 seizures. In each patient the data was split into a training set and a testing set. EEG segments were analyzed using continuous wavelet transform. During training, a reference state was defined in the immediate preictal data and used to derive three features quantifying the discrimination between preictal and interictal states. A classifier was then trained in the feature space. Its performance was assessed using testing set and compared with a random predictor for statistical validation.ResultsBetter than random prediction performance was achieved in 7 patients. The sensitivity was higher than 85%, the warning rate was less than 0.35/h and the proportion of time under warning was less than 30%.ConclusionSeizures are predicted above chance in 41% of patients using measures of state similarity.SignificanceSensitivity and specificity levels are potentially interesting for closed-loop seizure control applications.     

Automatic lateralization of temporal lobe epilepsy based on scalp EEG.

OBJECTIVE: The objective of this work is the determination of the lateralization of the epileptic seizure onset zone using the scalp EEG signal processing. METHODS: A comprehensive method based on the evaluation of the evolution of the correlation coefficients computed between bipolar channels (longitudinal montage) was applied to 43 patients (87 seizures). The correlation coefficients are estimated by a nonlinear regression analysis. The methodology that leads to the lateralization is based on several processing steps: segmentation, seizure onset determination and then lateralization. RESULTS: Results show that the mean level of the nonlinear correlation values computed between EEG channels at the seizure onset time is significantly higher on the side of the beginning of a seizure. CONCLUSIONS: The side of the seizure onset was determined for about 80-90% of the seizures studied with a satisfactory high reproducibility level. SIGNIFICANCE: Comparison of nonlinear correlation coefficients between both sides of the brain leads to the determination of the side of seizure onset.     

Benign epileptiform discharges in Rolandic region with mesial temporal lobe epilepsy: MEG, scalp and intracranial EEG features

AIM OF THE STUDY: To report benign epileptiform discharges (BEDs) in the Rolandic region, coexisting in a pediatric patient with intractable localization-related epilepsy, secondary to hippocampal sclerosis. METHODS: We describe the clinical features, MRI, scalp video EEG, magnetoencephalography (MEG) and intracranial video EEG findings, and surgical outcome in a 9-year-old boy with BEDs and intractable complex partial seizures. RESULTS: MRI showed left hippocampal sclerosis. Scalp video EEG interictally demonstrated left temporal spike and sharply contoured slow waves, and right fronto-centro-temporal spike and waves. Ictal scalp video EEG showed left temporal rhythmic sharp waves after the clinical onset of epigastric aura, followed by staring. MEG showed interictal dipoles in the bilateral Rolandic regions with a uniform orientation and right hemispheric predominance. Intracranial video EEG, with bilateral mesial temporal depth and fronto-temporo-parietal strip electrodes, interictally showed polyspikes and slow waves with superimposed low-amplitude fast waves in the left mesial and posterior lateral temporal regions, and spike and waves in the bilateral fronto-parietal regions. Ictal onset was marked by low-amplitude fast waves in the left mesial and posterior lateral temporal regions. He underwent left anterior temporal lobectomy with hippocampectomy. Pathology was hippocampal sclerosis. Predominant right fronto-centro-temporal spike and waves and MEG right Rolandic dipoles persisted after surgery. He was seizure-free 14 months after surgery. CONCLUSION: This is the first report on MEG and intracranial video EEG features of BEDs in the Rolandic region, coexisting with hippocampal sclerosis. Persistence of contralateral benign MEG Rolandic dipoles after surgery indicates that BEDs are coincidental in mesial temporal lobe epilepsy. MEG identified Rolandic dipoles, although was unable to localize the deep and focal epileptogenic dipoles from the hippocampal sclerosis.     

Prefrontal hypofunction in patients with intractable mesial temporal lobe epilepsy

We compared the cognitive functions and interictal cerebral glucose metabolism of 11 patients with mesial temporal lobe epilepsy (MTLE) with frequent seizures to those of 10 patients with MTLE with rare seizures; the groups were matched for age, sex, education, IQ, and focus side. The frequent-seizure group had more set-shifting impairment that correlated with glucose hypometabolism in the prefrontal cortices. Our results suggest that frequent seizures in MTLE are associated with hypofunction of the prefrontal cortex.     

Benign mesial temporal lobe epilepsy

Benign mesial temporal lobe epilepsy (bMTLE), which is defined as at least 24 months of seizure freedom with or without antiepileptic medication, has probably been under-recognized because of a literature bias toward refractory epilepsy cases. Seizure onset in bMTLE tends to be in adolescence or adulthood, and patients frequently have a family history of febrile seizures and epilepsy. Long-term seizure freedom is observed with or without antiepileptic medication. On brain MRI, nearly 40% of patients with long-standing bMTLE show evidence of hippocampal sclerosis, a feature usually associated with refractory temporal lobe epilepsy. Prospective studies are needed to determine the features that allow prediction of a benign course, and to clarify the significance of hippocampal MRI changes.     

Ictal stereo-electroencephalography onset patterns of mesial temporal lobe epilepsy and their clinical implications

ObjectiveThe differences in mesial temporal epilepsy (MTE) stereo-electroencephalography (SEEG) seizure-onset patterns and their clinical implications remains unclear.MethodsWe analyzed consecutive patients with MTE undergoing non-invasive workup, SEEG evaluation and resective surgery. Cases were classified into either mesial temporal sclerosis (MTS) group or non-MTS group based on magnetic resonance imaging (MRI). Seizure-onset patterns of SEEG were classified to analyze their correlation with surgical outcome and clinical subtypes.ResultsTwenty-eight patients were studied. Twenty (71.4%) patients had Engel I outcome. Thirteen patients had one seizure-onset pattern, 15 had two or more patterns. Five patterns of seizure-onset were identified and seizure-onset zones differed significantly across the 5 patterns. No difference was observed in surgical outcome between patients with single or multiple seizure-onset patterns. Periodic spike-onset pattern was associated with MTS (P = 0.003) while burst-onset was associated with non-MTS lesions (P = 0.003). Patients with seizure-onsets outside the resected temporal lobe (multiple onsets) had poorer prognosis (P = 0.0046).ConclusionWe identified 5 distinct onset patterns of MTE and correlated two of them with MRI findings. Multiple seizure-onset patterns in MTE may not necessarily suggest poor outcome. Patients with multi-focal seizure-onsets including seizures originating outside the resected temporal lobe have poorer outcome.SignificanceThis study identifies distinct onset patterns of MTE and their clinical implications.     

Correlation between temporal pole MRI abnormalities and surface ictal EEG patterns in patients with unilateral mesial temporal lobe epilepsy.

OBJECTIVE: The objective of this retrospective study is to analyze ictal patterns observed during continuous Video-EEG monitoring in patients with temporal lobe epilepsy (TLE) due to unilateral hippocampal sclerosis (HS), and to correlate these EEG patterns to temporal pole abnormalities observed on magnetic resonance imaging exams. METHODS: We analyzed 147 seizures from 35 patients with TLE and unilateral HS. Ictal patterns were classified and correlated to signal abnormalities and volumetric measures of the temporal poles. Volume differences over 10% were considered abnormal. RESULTS: The most frequent type of ictal pattern was rhythmic theta activity (RTA), encountered in 65.5% of the seizures. Rhythmic beta activity (RBA) was observed in 11% of the seizures, localized attenuation in 8%, interruption of epileptiform discharges in 6%, repetitive discharges in 5.5%, and rhythmic delta activity (RDA) in 4%. Sixty-six percent of the patients presented signal abnormalities in the temporal pole that were always ipsilateral to the HS. Sixty percent presented significant asymmetry of the temporal poles consisting of reduced volume that was also always ipsilateral to HS. Although patients with RTA as the predominant ictal pattern tended to present asymmetry of temporal poles (p=0.305), the ictal EEG pattern did not correlate with temporal pole asymmetry or signal abnormalities. CONCLUSIONS: RTA is the most frequent initial ictal pattern in patients with TLE due to unilateral HS. Temporal pole signal changes and volumetric reduction were commonly found in this group of patients, both abnormalities appearing always ipsilateral to the HS. However, neither temporal pole volume reduction nor signal abnormalities correlated with the predominant ictal pattern, suggesting that the temporal poles are not crucially involved in the process of epileptogenesis.