Electrophysiological study of intractable epileptogenicity in human epilepsy: clinical usefulness of ictal DC shifts and cavernous sinus EEG]

In order to clarify the clinical and electrophysiological features in intractable epileptogenicity in human epilepsy, we applied the new techniques, ictal DC shifts and cavernous sinus EEG recording, for presurgical evaluation of patients with intractable partial epilepsy. (1) Ictal DC shifts were successfully recorded with subdural electrodes in 8 patients with intractable neocortical epilepsy, and an analysis of ictal DC shifts would add useful information to delineate an epileptogenic area. Scalp-recorded ictal DC shifts were also investigated in 3 patients with intractable neocortical epilepsy. It also delineated the epileptogenic area, but it was vulnerable for artifacts. (2) By using the techniques of intravascular EEG recording, we recorded EEG from the bilateral cavernous sinus (cavernous sinus EEG) in patients with intractable temporal lobe epilepsy. Cavernous sinus EEG well sensitively recorded interictal, also ictal in selected patients, epileptiform discharges which arose from the mesial temporal structure even though they were not recorded by scalp electrodes. It is concluded that the above two techniques are clinically useful for delineating an epileptogenic area in patients with neocortical epilepsy and temporal lobe epilepsy.     

Extratemporal surface EEG features do not preclude successful surgical outcomes in drug-resistant epilepsy patients with unitemporal MRI lesions

Of 47 patients with onset of intractable partial seizures and temporal lobe MRI lesions, subjected to presurgical evaluation and temporal lobe surgery, we identified eight (mean age: 24 years; range: 7-52 years) demonstrating surface interictal and/or ictal EEG features suggestive of an extratemporal localisation. All eight patients underwent surgery aiming to predominantly resect the lesion, without extending to the extratemporal region. The patients were prospectively followed (mean follow-up duration: 38 months; range: 12-66 months) and all achieved excellent postoperative seizure control. Extratemporal surface interictal/ictal EEG features were more often encountered in tumoural and focal cortical dysplasia cases, compared with medial temporal sclerosis cases, and were most frequently localised over frontopolar and suprasylvian-pericentral locations. We postulate that propagation of interictal/ictal activity from the epileptogenic region of the temporal lobe to extratemporal neocortical areas, perhaps utilising the temporal pole and insula as intermediary nodes of a common epileptogenic network, accounts for the presence of our cohort's discordant lesion and EEG features.     

Indications and outcome of ictal recording with intracerebral and subdural electrodes in refractory complex partial seizures.

Intracranial electrophysiologic recording has often been used to localize ictal onset zones in presurgical evaluation of refractory complex partial seizures. Specific indications for intracranial ictal monitoring have not been analyzed in detail, however. The authors designed this study to test the utility of intracranial monitoring in specific indications and considered six specific indications for intracranial monitoring. They compared prospectively determined indications and outcomes of chronic intracerebral and subdural electrophysiologic recording in 50 consecutive patients whose ictal onset zones had been inadequately localized with interictal and ictal EEG using extracranial electrodes, magnetic resonance imaging, interictal[18F]fluorodeoxyglucose positron emission tomography, and neuropsychological testing. In 47 patients ictal onset zones were localized with intracranial recordings, leading to resections in 38 patients. Each indication for intracranial monitoring selected a group in which the majority went on to have efficacious epilepsy surgery (5-year follow-up). Definitive diagnosis of bilateral independent ictal onset zones in temporal lobe epilepsy required intracranial ictal EEG. Intracranial EEG localization supported efficacious resection in most patients, despite contradictory or nonlocalizing extracranial ictal EEG and neuroimaging abnormalities. Critical analysis of these specific indications for intracranial monitoring may be useful in multicenter evaluation of these techniques.     

Ictal brain imaging in presurgical evaluation of patients with medically intractable complex partial seizures

At the Indiana University Medical Center, 99 patients with medically intractable complex partial seizures (MI-CPS) had presurgical evaluation with subsequent anterior temporal lobectomy. The majority of the patients had single photon emission tomography (SPECT) performed interictally as well as during an actual epileptic seizure (ictal scan). Decreased regional cerebral perfusion (rCP) was seen in 54/94 (57%) of the interictal scans corresponding to the eventual site of the surgery. However, ictal scans provided a higher yield; increased rCP in the temporal lobe during an actual seizure was observed in 60/82 (73%) concordant to the side of surgery. SPECT is a useful, noninvasive method of localizing the epilepti-form focus in patients with MI-CPS considered for resective surgery. Both interictal and ictal SPECT need to be performed; combined interictal hypo-perfusion and ictal hyperperfusion in the same focal area are unique to epileptogenic lesions. Ictal SPECT studies can be performed in the majority of patients during the period of continuous video/EEG monitoring with only a little additional effort. Combining the results of functional brain imaging (interictal and ictal SPECT, PET) with clinical semiology of seizures, surface and sphenoidal EEG, magnetic resonance imaging and other non-invasive tests, anterior temporal lobectomy can be recommended in approximately two-thirds of the patients without resorting to potentially dangerous intracranial EEG monitoring.     

Presurgical electroencephalographic patterns and outcome from anterior temporal lobectomy.

We reviewed data from 48 patients after anterior temporal lobe resection for medically intractable epilepsy. All had ictal electro-encephalographic (EEG) evidence of unilateral temporal lobe onset. Depth electrodes were used in 19 patients. Successful surgical outcome correlated significantly with factors that suggested a temporal lobe focus, particularly in the interictal scalp EEG. The most successful outcome occurred in patients with well-localized unilateral interictal temporal spikes (100% improved). The group with well-localized bilateral temporal spikes also did well (76% improved). Patients with extratemporal spread of the interictal spike on scalp EEG, either unilaterally or bilaterally, did less well. Only one third improved, despite extensive extracranial and intracranial monitoring, when indicated. The interictal scalp EEG may be the only EEG necessary for the presurgical evaluation of selected patients with intractable temporal lobe epilepsy.     

Association of Combined MRI, Interictal EEG, and Ictal EEG Results with Outcome and Pathology After Temporal Lobectomy

Summary: Purpose: Magnetic resonance imaging, interictal scalp EEG, and ictal scalp EEG each have been shown to localize the primaly epileptic region in most patients with mesial-basal temporal lobe epilepsy (MBTLE), but the association of surgical outcome and pathology with each combination of these test results is not known. Methods: We reviewed the MRI, interictal scalp EEG, and ictal scalp EEG results of 90 consecutive patients with MBTLE. Twelve patients were excluded from the analysis because inconclusive bitemporal intracranial EEG results precluded anterior temporal lobectomy (ATL); none had concordant MRI and interictal scalp EEG results. We compared all combinations of presurgical MRI, interictal EEG, and ictal EEG results to seizure outcome and tissue pathology in the 78 patients who underwent an ATL. Results: Forty-eight (61%) patients had concordant lateral-ized MRI and interictal EEG temporal lobe abnormalities, with no discordant ictal EEG results; 77% of these patients were seizure-free after ATL. Concordance of MRI and interictal EEG abnormalities correlated with seizure cessation (p < 0.05), compared to all combinations with discordant or nonlateralizing MRI and interictal EEG results. Mesial temporal sclerosis (MTS) was confirmed pathologically in about 80% of both groups (p = 0.5). Outcome in patients with concordant MRI and ictal EEG with nonlateralizing interictal EEG was significantly worse than combinations with concordant MRI and interictal EEG (p < 0.02). Conclusions: Compared to other combinations of test results, concordance of MRI and interictal EEG is most closely associated with surgical outcome in MBTLE. However, most selected patients have pathologic confirmation of MTS regardless of test results or outcome. This information may be useful for planning the presurgical evaluation of patients with medically intractable MBTLE.     

Spike frequency is dependent on epilepsy duration and seizure frequency in temporal lobe epilepsy.

OBJECTIVES: We wanted to investigate factors that are associated with frequency of interictal epileptiform discharges by investigating 303 patients with temporal lobe epilepsy (TLE). METHODS: We included all patients who consecutively underwent the adult presurgical evaluation program at our center and who had intractable, medial TLE with complex partial seizures due to unilateral medial temporal lobe lesions. The interictal EEG samples were automatically recorded and stored on computer. The location and frequency of interictal epileptiform discharges were assessed by visual analysis of interictal EEG samples of 2-minute duration every hour. RESULTS: There were 303 patients (aged 16-63) who met the inclusion criteria. The median interictal epileptiform discharge frequency was 15 IED/h, the median seizure frequency was 4 seizures/month. According to univariate analyses, we found that age at monitoring, epilepsy duration, and higher seizure frequency were associated with higher interictal epileptiform discharge frequency. In the logistic regression analysis, we found that higher seizure frequency (p < 0.001) and longer epilepsy duration (p = 0.007) were independently associated with higher spike frequency, while the age at monitoring was not. CONCLUSIONS: Seizure frequency and epilepsy duration (years of patient's life with seizure activity) were independently associated with IED frequency, suggesting that IED are modulated by seizures.     

Localization of epileptic foci with postictal single photon emission computed tomography

Effective surgical treatment of patients with intractable complex partial seizures depends on accurate preoperative seizure focus localization. We evaluated seizure localization with interictal and immediate postictal single photon emission computed tomographic images of cerebral perfusion using technetium-99m-hexamethyl-propyleneamineoxime (99mTc-HMPAO) in comparison with conventional ictal electroencephalographic (EEG) localization. Thirty-two patients with intractable complex partial seizures were studied. The mean delay from seizure onset to injection was 6.3 +/- 5.3 (SD) minutes. Independent blinded observers assessed the scans for interictal hypoperfusion and postictal focal hyperperfusion. Interictal scans alone were unreliable, indicating the correct localization in 17 patients (53%) and an incorrect site in 3 (9%). When interictal and postictal scans were interpreted together, the focus was correctly localized in 23 patients (72%). There was 1 false-positive study, and 8 patients had inconclusive changes, including 2 with inconclusive depth EEG studies. Postictal hyperperfusion was predominantly mesial temporal and frequently associated with hypoperfusion of lateral temporal cortex. Secondarily generalized seizures tended to show focal hyperperfusion less often than complex partial seizures did (Fisher's exact test p = 0.09). Combined interictal and immediate postictal single photon emission computed tomography with 99mTc-HMPAO is a useful noninvasive technique for independent confirmation of electrographic seizure localization. It may provide a suitable alternative to the use of depth electrode studies for confirmation of surface EEG findings in many patients with complex partial seizures.     

Clinical and Electroencephalographic Evidence for Sites of Origin of Seizures with Diffuse Electrodecremental Pattern

Summary: A diffuse electrodecremental ictal pattern with other forms of epilepsy and has been considered to reflect a generalized seizure disorder of diffuse cortical or subcortical (brainstem) origin. In some seizures associated with DEP, however, focal ictal manifestations have been observed. We reviewed the records of all patients admitted to our seizure monitoring unit for 3 years and detected 39 patients with seizures associated with DEP. In 23 of 39 patients, clinical ictal behaviors resembled seizures of unilateral supero/mesiofrontal lobe origin and interictal EEG showed a prominent unilateral frontal component. Nine of 39 had complex absences (CA)/complex partial seizures (CPS); 4 of them were of unilateral frontal lobe origin. Seven of 39 patients had tonic or atonic seizures. Seven patients were studied further with subdural electrodes. Ictal onsets showed a highfrequency frontal lobe discharge. We conclude that in a subgroup of patients a generalized electrodecremental pattern on scalp EEG results from a regional cortical high-frequency ictal discharge originating in a single frontal lobe.     

Interictal and ictal dipole modelling in patients with refractory partial epilepsy

Fifteen patients (7 men, 8 women) with mean age of 34 years and mean duration of refractory partial seizures of 17 years were included in a presurgical evaluation protocol. Neuroimaging (CAT, 1.5 T MR) demonstrated intracranial structural lesions (space-occupying: n = 9; atrophic: n = 6) and video-EEG monitoring showed complex partial seizures in all patients. Four patients underwent additional intracranial EEG monitoring that demonstrated hippocampal seizure onset in all. Voltage topography and spatiotemporal dipole mapping of interictal epileptic discharges revealed two distinct dipole types. Patients with lesions in the medial (and lateral) temporal lobe uniformly presented with a negative voltage field with a steep gradient over the inferior temporal area and a stable, combined dipole that consisted of a radial and a tangential component with a high degree of elevation relative to the axial plane. Patients with extratemporal lesions had a more diffuse, less dipolar voltage field and a corresponding dipole which was less stable and had a predominant radial component. Dipole modelling of epochs of early ictal discharges revealed a striking correspondence with the interictal findings in individual patients. Interictal spike voltage topography and corresponding dipole mapping provided additional and reliable information that was relevant in surgical candidates for refractory partial epilepsy, e.g. by suggesting in some patients that the medial temporal structures were not primarily involved. Ictal dipole modelling revealed concordant results with interictal data. It shows promising but needs further confirmation and validation in a larger patient population with intracranial EEG recordings. Despite intrinsic limitations, spike voltage topography and dipole mapping contributes to a better localisation of the underlying brain source of epileptic discharges.     

Comparison of depth and subdural electrodes in recording temporal lobe seizures

Intracranial EEG recording is often required to identify an area of the brain for resective surgery for intractable epilepsy. We simultaneously compared bilaterally placed depth and limited subdural electrode EEG to determine the most effective method of recording seizures from the temporal lobes. Localized complex partial seizures usually appeared earlier in hippocampal depth electrodes and spread later to subdural recording sites. In 3 patients, hippocampal recordings showed localized seizure origin but subdural recording was nonlocalizing due to rapid bilateral seizure propagation. In 1 patient with nonlocalized seizures presumably of extratemporal origin, subdural electrodes incorrectly lateralized seizure origin to a temporal lobe. Auras and subclinical seizures detected by depth electrode recording were often not evident with subdural electrodes. We conclude that EEG recording with hippocampal depth electrodes correctly identifies and lateralizes temporal lobe seizures more often than with limited subdural electrodes.     

Scalp EEG in temporal lobe epilepsy surgery

Electroencephalography (EEG) with standard scalp and additional noninvasive electrodes plays a major role in the selection of patients for temporal lobe epilepsy surgery. Recent studies have provided data supporting the value of interictal and postictal EEG in assessing the site of ictal onset. Scalp ictal rhythms are morphologically complex but at least one pattern (a five cycles/second rhythm maximum at the sphenoidal or anterior temporal electrode) occurs in >50% of patients and has a high predictive value and interobserver reliability for temporal lobe originating seizures. Thorough interictal and ictal scalp EEG evaluation, in conjunction with modern neuroimaging, is sufficient for proceeding to surgery without invasive recordings in some patients. Further studies are required to define the scalp ictal characteristics of mesial vs. lateral temporal lobe epilepsy.     

The clinical and prognostic relevance of the postictal slow focus in the electrocorticogram

Electrocorticograms of 192 complex partial seizures which were recorded via chronically implanted subdural electrodes during presurgical evaluation of 64 patients with medically intractable epilepsy were visually analysed. The objective was to assess the diagnostic and prognostic relevance of postictal slow foci (PISF) in the electrocorticogram which were defined as focal isoelectric activity or as a focal burst-suppression pattern. The following results were obtained: (1) PISF were seen in a total of 114 of 192 seizures (59.4%), (2) 48 of 64 patients (75%) demonstrated at least 1 PISF in 3 seizures, (3) PISF were more frequent in seizures of temporal lobe origin (66%) than in those of extratemporal origin (33.3%), (4) no PISF developed if the electrographic seizure duration was < 32 sec, (5) PISF were (predominantly) localized in the lobe of seizure origin in 85%v of the seizures, (6) there was a strong correlation between frequent occurrence of temporal PISF and favourable seizure outcome following temporal lobe surgery. In conclusion, PISF contribute valuable data as to the localization of the epileptogenic zone during presurgical evaluation of epilepsy and indicate favourable seizure outcome following temporal lobe surgery.     

Spatiotemporal relationship between seizure activity and interictal spikes in temporal lobe epilepsy.

PURPOSE: To analyze the spatio-temporal relationship between seizure propagation and interictal epileptiform discharges (IEDs) in patients with bitemporal epilepsy. METHODS: We investigated 18 adult patients with intractable temporal lobe epilepsy (TLE) who had undergone continuous video-EEG monitoring during presurgical evaluation. Only those patients were selected who had independent IEDs over both temporal lobes. Two authors evaluated the ictal and interictal EEG data independently. RESULTS: We analyzed 52 lateralized seizures of 18 patients. Thirty-one seizures showed ipsilateral seizure spread exclusively, whereas in 21 seizures the contralateral hemisphere was also involved. In lateralized seizures without contralateral propagation, we found that spikes ipsilateral to the seizure onset occurred postictally in a greater ratio than preictally (P<0.001). In lateralized seizures with contralateral propagation, we found no significant changes in the postictal spike distribution. CONCLUSIONS: Our findings showed that the lateralization of IEDs may depend on the brain areas involved by the preceding seizures, suggesting that spikes can be influenced by the seizure activity, and are not independent signs of epileptogenicity.     

发作期录像脑电监测在15例难治性颞叶癫痫患者术前定位中的价值

目的 探讨发作期录像脑电监测（IVEEG）在难治性非病变性颞叶癫痫（TLE）致痫源术前定位中的价值。方法 对15例药物难治性TLE患者术前定位资料及术后随诊情况进行分析。结果 所有患者在行长时间IVEEG监测中均捕获到临床发作。在15例患者中，有13例IVEEG显示出一侧起源的局灶爆发性节律性电活动，该放电侧均与最终切除侧相一致，且有11例患者术后效果较好。结论 IVEEG监测不仅有助于明确诊断及发作类型，更为重要的是对于大多数难治性非病变性TLE患者可提供较可靠的致痫源定侧信息。     

Tailored resections in occipital lobe epilepsy surgery guided by monitoring with subdural electrodes: characteristics and outcome

PURPOSE: Occipital lobe epilepsy is uncommon in epilepsy surgery series and often difficult to assess due to rapid seizure propagation, misleading seizure semiology and confounding interictal epileptiform activity. Ictal recordings with surface electrodes may not define properly the seizure onset zone in surgical evaluation for intractable occipital epilepsy. Specially in dysplastic lesions, the extension of the epileptogenic zone is not well defined by neuroimaging techniques, therefore, implantation of intracranial electrodes is often indicated. In this study we present our experience with individually tailored resections of occipital lobe epileptic foci guided by monitoring with subdural electrodes. METHODS: Data from interictal and ictal surface and intracranial recordings, neuroimaging, surgical treatment, pathology and outcome of seven patients are presented. RESULTS: The most common seizure type (6/7 patients) was complex partial with temporal lobe semiology, five patients experienced visual auras as part of their complex partial seizures or as separate simple partial seizures. Two patients had seizures suggesting supplementary motor area involvement. One patient had temporal as well as frontal seizure propagation. Neuroimaging showed lesions in 6/7 patients. Pathological studies revealed cortical dysplasia and tumors as the most common causes. Intracranial recordings (6/7 patients) revealed focal onset in 2 patients, regional onset in 2, and diffuse onset in 2. Surgery was performed according to intracranial recordings restricting resections in cases with focal seizure onset (even in large dysplastic lesions) and performing wider resections in patients with regional or diffuse onset. Five of seven patients are seizure free after 12-55 months (mean 24.3). The two remaining patients may be classified as Engel 2b and 3a. CONCLUSIONS: This series of occipital lobe epilepsy surgery shows that, even in patients with cortical dysplasias, restricted resections may have a good outcome and that intracranial monitoring is usually necessary in order to design an individually tailored resection.     

Dipole Modeling in Epilepsy Surgery Candidates

Summary: Purpose : The validity and clinical significance of dipole modeling in epilepsy surgery candidates is not fully established.
Patients and Methods : Interictal and ictal dipole modeling was performed in 43 patients with refractory complex partial seizures (CPS) and intracranial structural abnormalities demonstrated with optimum magnetic resonance imaging (MRI: space–occupying, n = 15; atrophic, n = 26; dysplastic, n = 2). Video–EEG monitoring showed CPS in all patients. In 12 patients, additional intracranial EEG monitoring demonstrated hippocampal seizure onset in 11 patients and medial occipital ictal onset in 1.
Results : Spatiotemporal dipole mapping of averaged interictal spikes and epochs of early ictal discharges revealed two distinct dipole patterns. Patients with lesions located in the medial (± lateral) temporal lobe (n = 34) and medial occipital lobe (n = 1) uniformly presented a combined interictal dipole that consisted of a radial and a tangential component with a high degree of elevation relative to the axial plane. Eight of 9 patients with extratemporal lesions had a less stable dipole with a predominant radial component. Ictal dipole modeling identified the ictal onset zone correctly as compared with intracranial EEG recordings from bilateral hippocampal depth electrodes. Ictal dipoles showed a striking correspondence with the interictal dipoles in individual patients.
Conclusions : Interictal and ictal dipole mapping provided additional, reliable, and relevant localizing information in surgical candidates for refractory CPS. Ictal dipole analysis may limit the number of patients who require intracranial electrodes.     

Extent of neocortical resection and surgical outcome of epilepsy: Intracranial EEG analysis

Purpose: Intracranial electroencephalography (EEG) monitoring is an important process in the presurgical evaluation for epilepsy surgery. The objective of this study was to identify the ideal resection margin in neocortical epilepsy guided by subdural electrodes. For this purpose, we investigated the relationship between the extent of resection guided by subdural electrodes and the outcome of epilepsy surgery. Methods: Intracranial EEG studies were analyzed in 177 consecutive patients who had undergone resective epilepsy surgery. We reviewed various intracranial EEG findings and resection extent. We analyzed the relationships between the surgical outcomes and intracranial EEG factors: the frequency, morphology, and distribution of ictal‐onset discharges, the propagation speed, and the time lag between clinical and intracranial ictal onset. We also investigated whether the extent of resection, including the area showing ictal rhythm and various interictal abnormalities—such as frequent interictal spikes, pathologic delta waves, and paroxysmal fast activity—influenced the surgical outcome. Results: Seventy‐five patients (42%) were seizure free. A seizure‐free outcome was significantly associated with a resection that included the area showing ictal spreading rhythm during the first 3 s or included all the electrodes showing pathologic delta waves or frequent interictal spikes. However, subgroup analysis revealed that the extent of resection did not affect the surgical outcome in lateral temporal lobe epilepsy. Conclusions: The extent of resection is closely associated with surgical outcome, especially in extratemporal lobe epilepsy. Resection that includes the area with total pathologic delta waves and frequent interictal spikes predicts a good surgical outcome.     

Ictal and Interictal Activity in Partial Epilepsy Recorded with Multichannel Magnetoelectroencephalography: Correlation of Electroencephalography/Electrocorticography, Magnetic Resonance Imaging, Single Photon Emission Computed Tomography, and Positron Emission Tomography Findings

Ictal and interictal epileptic activity was recorded for the first time by multichannel magnetoencephalography (MEG) in three patients with partial epilepsy. Pre- and intra-operative localization of the epileptogenic region was compared. The interictal epileptic activity was localized at the same region of the temporal or frontal lobe as the ictal activity. Main zones of ictal activity were shown to evolve from the tissue at the centers of interictal activity. Pre- and intra-operative electrocorticography (ECoG) as well as postoperative outcome confirmed localization in the temporal and frontal lobe. Results also correlated with findings from scalp EEG, interictal and ictal single photon emission computed tomography (SPECT), positron emission tomography (PET), and magnetic resonance imaging (MRI). Combined multichannel MEG/EEG recording permitted dipole localization of interictal and ictal activity.     

Ictal/postictal SPECT in the pre-surgical localisation of complex partial seizures.

Single photon emission computed tomography (SPECT) used in conjunction with HM-PAO (Ceretec-Amersham International) was used to image regional cerebral blood flow (rCBF) in 28 patients with medically intractable complex partial seizures during or soon after a seizure, and interictally. Changes from interictal rCBF were seen in 26/28 (93%) patients. The main findings were; 1) During the seizure--hyperperfusion of the whole temporal lobe; 2) Up to 2m postically--hyperperfusion of the hippocampus with hypoperfusion of lateral temporal structures; 3) From 2-15m postically--hypoperfusion of the whole temporal lobe. When compared with EEG and MRI data, correct localisation to one temporal lobe was obtained in 23 patients. In one further patient bilateral temporal foci, and in a further two patients frontal foci, were correctly identified. There were no disagreements between EEG and SPECT localisation. Temporal lobe surgery was successful (by the criterion of at least 90% reduction in seizure frequency) in all but one of the 23 patients operated on. It is concluded that ictal/postictal SPECT is a reliable technique for the presurgical localisation of complex partial seizures. The data indicate a likely sequence of changes in rCBF during and after complex partial seizures of temporal lobe origin.