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Electroencephalographic, volumetric, and neuropsychological indicators of seizure focus lateralization in temporal lobe epilepsy.

CONTEXT: Anterior temporal lobectomy is an effective treatment for medically intractable temporal lobe seizures. Identification of seizure focus is essential to surgical success. OBJECTIVE: To examine the usefulness of presurgical electroencephalography (EEG), magnetic resonance imaging (MRI), and neuropsychological data in the lateralization of seizure focus. DESIGN: Presurgical EEG, MRI, and neuropsychological data were entered, independently and in combination, as indicators of seizure focus lateralization in discriminant function analyses, yielding correct seizure lateralization rates for each set of indicators. SETTING: Comprehensive Epilepsy Program, Shands Teaching Hospital, University of Florida, Gainesville. PATIENTS: Forty-four right-handed adult patients who ultimately underwent successful anterior temporal lobectomy. Left-handed patients, those with less-than-optimal surgical outcome, and any patients with a history of neurological insult unrelated to seizure disorder were excluded from this study. MAIN OUTCOME MEASURES: For each patient presurgical EEG was represented as a seizure lateralization index reflecting the numbers of seizures originating in the left hemisphere, right hemisphere, and those unable to be lateralized. Magnetic resonance imaging data were represented as left-right difference in hippocampal volume. Neuropsychological data consisted of mean scores in each of 5 cognitive domains. RESULTS: The EEG was a better indicator of lateralization (89% correct) than MRI (86%), although not significantly. The EEG and MRI were significantly superior to neuropsychological data (66%) (P=.02 and .04, respectively). Combining EEG and MRI yielded a significantly higher lateralization rate (93%) than EEG alone (P<.01). Adding neuropsychological data improved this slightly (95%). CONCLUSIONS: The EEG and MRI were of high lateralization value, while neuropsychological data were of limited use in this regard. Combining EEG, MRI, and neuropsychological improved focus lateralization relative to using these data independently.

Adult↗

Is impairment in set-shifting specific to frontal-lobe dysfunction? Evidence from patients with frontal-lobe or temporal-lobe epilepsy.

Frontal-lobe epilepsy (FLE), temporal-lobe epilepsy (TLE), and matched-control subjects were administered the Trail Making Test (TMT) of the Delis-Kaplan Executive Function System (D-KEFS; Delis et al., 2001), which assesses set-shifting on a visuomotor sequencing task. Results indicated that patients with FLE were impaired in both speed and accuracy on the switching condition relative to patients with TLE and controls. The two patient groups did not differ from controls on the four baseline conditions of the test, which assess visual scanning, motor speed, number sequencing, and letter sequencing. In addition, seizure-related variables (i.e., age of seizure onset, duration of epilepsy, and seizure frequency) failed to correlate with set-shifting performance in patients with FLE. These results suggest that patients with FLE can be reliably distinguished from those with TLE and control subjects on set-shifting as measured by the DKEFS TMT.

Adult↗

Relational verbal memory processing in patients with temporal lobe epilepsy.

Patients with left temporal lobe epilepsy (LTLE) have been shown to demonstrate impaired categorization in semantic memory tasks leaving open the question whether this is due to problems with active categorization or to problems with consolidation/retrieval of relations. 35 patients with left or right temporal lobe epilepsy (LTLE, RTLE) and 20 healthy controls performed three verbal learning and memory tests differing in the relational distance between the items to be learned (unrelated, low associative, high associative). In order to separate the memory component in relational memory processing, we avoided problems in active categorization and perception of semantic relations by presenting category members already clustered in the order of category membership, and by checking whether the patients had actually noticed the categories. In controls and in patients with RTLE, both semantic conditions significantly improved the test performance. LTLE-patients showed the worst test performance independent of the test condition. Their performance improved under the high associative condition, but they did not at all profit from the low associative condition. Although the semantic tasks had no demand on active clustering and although all LTLE-patients noticed the relational properties very well, they could not make use of the offered clusters. They demonstrated significantly more "item specific" than "relational" encoding than the other groups. This was pronounced in the low associative condition but became evident also in the high associative condition. In contrast to the other groups, the order in recall (clustering) deteriorated with passing time in LTLE-patients. In conclusion the data provide evidence of impaired semantic relational processing in LTLE. The impairment depends on the relational properties of the material to be learned, in that it increases with the relational distance between the memory contents. Because the tasks did not demand active clustering, we can attribute this impairment to deficits in relational encoding/retrieval which would be consistent with current opinions of the role of temporolimbic structures in relational memory processing.

Adult↗

Late-onset drop attacks in temporal lobe epilepsy: a reevaluation of the concept of temporal lobe syncope.

We report the clinical, radiologic, and EEG features of six patients with temporal lobe drop attacks (TLDA), all of whom underwent temporal resection. Postoperative follow-up of at least 1 year was available in all. TLDA were never the first manifestation but followed the onset of epilepsy after a long delay ranging from 7 to 43 years (mean, 24.4 years). Seizures were of unilateral temporal origin. In one patient, stereo EEG recording of TLDA showed rapid spread of the ictal discharge away from the temporal lobe in less than 1 second. Postoperatively, three patients were seizure free; one has had no TLDA but experiences sporadic auras; another, despite a reduction of more than 50%, continues to have complex partial seizures and TLDA; and the sixth has had sporadic secondarily generalized seizures upon reduction of antiepileptic medication. In conclusion, drop attacks may occur in temporal lobe epilepsy, usually long after the onset of epilepsy. They lead to increased disability and suggest a rapid spread of the ictal discharge and possible involvement of the pontine reticular formation rather than the presence of bitemporal foci or an extratemporal origin.

Adult↗

Temporal and spatial characteristics of intracerebral seizure propagation: predictive value in surgery for temporal lobe epilepsy.

We examined the prognostic value of spatial and temporal characteristics of intracerebral propagation of seizures during temporal lobe epilepsy (TLE) surgery. Seven TLE patients resistant to standard anterotemporal lobectomy who had no known causes of resistance [e.g., extratemporal (ET), lesions, multifocal epilepsy] were matched with 7 seizure-free patients and 7 others who were almost seizure-free after operation. Intracerebral ictal propagation pathways were not different in the three groups. Propagation was multidirectional, most frequently to the frontal lobes and sometimes to the contralateral temporal lobe (CTL). ET propagation delays were significantly shorter in resistant patients than in markedly improved patients. The resistant group also had more frequent propagation delays < 1.0 s, but propagation times > 1.0 s were equally likely in all groups. The extent of ET propagation and frequency of focal onsets were not different among the groups. Results suggest that very short propagation times predict reduced efficacy of operation, and that long propagation times are not related to surgical success.

Electroencephalography↗

Increased expression of phosphate-activated glutaminase in hippocampal neurons in human mesial temporal lobe epilepsy.

Patients with mesial temporal lobe epilepsy (MTLE) have increased basal concentrations of extracellular glutamate in the epileptogenic versus the non-epileptogenic hippocampus. Such elevated glutamate levels have been proposed to underlie the initiation and maintenance of recurrent seizures, and a key question is what causes the elevation of glutamate in MTLE. Here, we explore the possibility that neurons in the hippocampal formation contain higher levels of the glutamate synthesizing enzyme phosphate-activated glutaminase (PAG) in patients with MTLE versus patients with other forms of temporal lobe epilepsy (non-MTLE). Increased PAG immunoreactivity was recorded in subpopulations of surviving neurons in the MTLE hippocampal formation, particularly in CA1 and CA3 and in the polymorphic layer of the dentate gyrus. Immunogold analysis revealed that PAG was concentrated in mitochondria. Double-labeling experiments indicated a positive correlation between the mitochondrial contents of PAG protein and glutamate, as well as between PAG enzyme activity and PAG protein as determined by Western blots. These data suggest that the antibodies recognize an enzymatically active pool of PAG. Western blots and enzyme activity assays of hippocampal homogenates revealed no change in PAG between MTLE and non-MTLE, despite a greatly (>50%) reduced number of neurons in the MTLE hippocampal formation compared to non-MTLE. Thus, the MTLE hippocampal formation contains an increased concentration and activity of PAG per neuron compared to non-MTLE. This increase suggests an enhanced capacity for glutamate synthesis-a finding that might contribute to the disrupted glutamate homeostasis in MTLE.

Adolescent↗

Feasibility of subclassification of temporal lobe epilepsy (1989): an etiological overview.

Temporal lobe epilepsy with amygdalohippocampal seizures may have episodes of severe convulsions in childhood more frequently and the onset age is significantly lower compared to epilepsy with lateral temporal seizures. To the contrary, tumorous lesions are found more frequently in epilepsy with lateral temporal seizures. In view of the presumed known etiologies in relation to the localization of epileptogenic foci, the Classification of Epileptic Syndrome (1989), subdividing temporal lobe epilepsies into 2 groups, was found to be useful.

Adult↗

Temporal lobe epilepsy and neuropathology. Histological findings in resected temporal lobes correlated to surgical results and clinical aspects.

Neuropathological findings were studied in 74 patients with drug-resistant temporal lobe epilepsy who underwent unilateral temporal lobe resection in 1960-1969 in Denmark. In 60 per cent of the patients a well-defined neuropathological abnormality was revealed (i.e. 13 cases of focal lesions, including four small tumours, 21 cases of gliosis, and 10 cases of perivascular infiltration), in 23 per cent the findings were either questionably abnormal or without structural abnormality, while in the last 18 per cent sequelae of a previous operation dominated the histology. The general trend was for the postoperative clinical outcome to be better, the more specific and circumscribed the histological abnormality. There was no correlation between the neuropathological findings and the preoperative types of seizures. Postoperative recurrence of seizures was more often observed in patients with gliosis than in those with other histological diagnoses. A positive correlation existed between a history of cerebral infection and the presence of perivascular lymphocytic and histiocytic infiltration, and gliosis was a frequent finding in patients with epilepsy of unknown aetiology. No other significant correlation was found between the neuropathological abnormalities and the clinical, hereditary, aetiological, and social aspects.

Adolescent↗

Clinical features and EEG findings differentiating mesial from neocortical temporal lobe epilepsy.

We evaluated whether mesial temporal lobe epilepsy (MTE) and neocortical temporal lobe epilepsy (NTE) can be distinguished on electroclinical grounds. One hundred and twenty-two consecutive MTE (n = 86) and NTE (n = 36) patients were included in this prospective study. All patients underwent prolonged EEG-video monitoring and high resolution magnetic-resonance imaging (MRI). MTE was defined as epilepsy with purely mesial temporal lesion in the absence of extramesial temporal pathology, based on pre-operative MRI or post-operative histology. NTE was defined as neocortical temporal MRI lesions, depth recorded neocortical temporal seizure onset and lack of mesial temporal lesions on MRI or histology. One thousand two hundred and fourty-nine epileptic seizures were analyzed. Congenital malformation (NTE 19% versus MTE 3%, P < 0.01), nonspecific auras (NTE 25% versus MTE 8%, P < 0.001) and early clonic activity following automatisms (NTE 22% versus MTE 8%, P < 0.03) were more frequent in NTE. In contrast, a history of febrile seizures (MTE 29% versus NTE 3%, P < 0,001), abdominal auras (MTE 62% versus NTE 33%, P < 0.005) and contralateral hand dystonia (MTE 43% versus NTE 22%, P < 0.03) were more often documented in MTE. Interictal epileptiform discharges in MTE occurred predominantly (> 67%) over the ipsilateral mesial temporal regions (MTE 65% versus NTE 33%, P < 0.001). No MTE patient had lateral neocortical temporal spike predominance (NTE 22%, P < 0.001). Multiple logistic regression revealed that a history of febrile seizures, abdominal auras, contralateral dystonic posturing and predominance of ipsilateral mesial temporal spikes point to MTE, with an accuracy of 73% (PPV 81%, NPV 70%). Analyzing clinical and EEG features, particularly the distribution of interictal epileptiform discharges, helps to differentiate between MTE and NTE.

Adult↗

[Is visual assessment of MRI adequate in the investigation of patients with temporal lobe epilepsy? Evaluation of the diagnostic accuracy of the visual assessment of MRI in mesial temporal sclerosis].

INTRODUCTION: Is visual assessment of MRI adequate in patients with temporal lobe epilepsy? Visual versus quantitative MRI assessment of mesial temporal sclerosis (hippocampal gliosis (HG) and hippocampal atrophy (HA)). MATERIAL AND METHODS: The MRIs of 25 patients with temporal lobe epilepsy were assessed visually by three radiologists with different levels of neuroradiological MRI experience (expert, trained, and inexperienced). Diagnosis obtained earlier by T2-relaxometry and volume measurements were considered to be the gold standard. RESULTS: The diagnostic accuracy of visual assessment was high for unilateral HA, but low for bilateral HA and unilateral and bilateral HG, and it was not better for the expert eye than for the inexperienced. Interobserver agreement on the visual diagnosis of HG and HA (Cohen's Kappa coefficient): 0.49 (HG) and 0.84 (HA). Intraobserver reliability for the expert/trained/inexperienced observer for visual diagnosis (Kappa): 0.83/0.64/0.47 (HG) and 0.88/0.69/0.73 (HA). DISCUSSION: Reproducibility and diagnostic accuracy of visual assessment varied unacceptably from the quantitative MRI-based diagnosis. Quantitative measurements are recommended in patients suspected of MTS.

Atrophy↗

Temporal lobe epilepsy. Follow-up investigation of 74 temporal lobe resected patients.

This survey covers 74 patients with temporal lobe epilepsy, resistant to medication, who underwent unilateral temporal lobectomy during the years 1960-1969 at Rigshospitalet, Copenhagen. Preoperatively all patients were socially incapacitated. In all patients a unilateral or predominantly unilateral temporal EEG focus was found. No tumour or gross vascular malformation had been recognized before or during operation. At follow-up 45 patients were free from seizures. A further 15 had obtained a reduction in their seizure frequencies by at least 75%, while the remaining 10 survivors, only obtained a slight improvement or remained unchanged. There were four deaths. The operation also favourably influenced the psychiatric status, which was found closely related to relief from seizures. Prognostically favourable factors were: i) preoperative presence of a single type of seizure, ii) duration of epilepsy of less than four years, iii) operation in or before early adulthood, iv) an anterior temporal or sphenoidal electrode focus, or both, on the EEG. The prognostically unfavourable factors regarding complete relief from seizures were: i) preoperative presence of grand mal, ii) age at onset of epilepsy or of the first grand mal seizure between 5 and 19 years of age, iii) preoperative duration of epilepsy of over ten years and of grand mal of over one year. Prognostically unfavourable factors regarding psychiatric normalization were: i) preoperative presence of psychosis, ii) ictal-affective attacks or automatisms of a complex nature, iii) impairment of intellectual functions. The eventual neuropathological conclusion was that the more specific and circumscribed the histological abnormality the better the final outcome. The social rehabilitation was found to be significantly improved by operation at an early age.

Adolescent↗

Developmental abnormalities of the medial temporal lobe in patients with temporal lobe epilepsy.

PURPOSE: To evaluate MR temporal lobe malformations and their frequency in patients with temporal lobe epilepsy. METHODS: Two hundred twenty-two consecutive adult patients with temporal lobe epilepsy of varying severity were investigated with 1.0-T or 1.5-T MR units using three-dimensional T1-weighted acquisition protocol. RESULTS: Sixteen patients (7.2%) presented with malformations of the temporal lobe. Four patterns of malformations were encountered: (a) heterotopia (n = 1), lining the temporal horn of the lateral ventricle; (b) focal neocortical dysgenesis (n = 6), which consisted of cortical thickening, poor gray/white matter demarcation, abnormal gyration (n = 5), or limited schizencephaly (n = 1); (c) hippocampal malformations (n = 5), which presented as abnormal hippocampal formation associated with a cyst (n = 2), isolated malformation of the subiculum (n = 1), or bilateral hippocampal malformation (n = 2) consisting of an abnormal shape and a misplaced fimbria; (d) complex malformations of the temporal lobe, combining categories a, b, and c (n = 4). The age at onset, severity of the disease, and occurrence of generalized tonicoclonic seizures were not significantly different between patients with malformations and the entire population of patients with temporal lobe epilepsy. CONCLUSION: MR analysis of temporal lobe malformations allowed a precise determination of the extent of the malformations and the presence or absence of associated hippocampal disease, all of which are of great help in the preoperative evaluation of patients with intractable epilepsy.

Adolescent↗

The orienting reflex in cats with experimental temporal lobe epilepsy.

Aluminum-induced temporal lobe epilepsy in 24 cats showed marked interictal intensification of somatic and EEG components of the orienting reaction and increase in their resistance to habituation. The greatest disturbances of the orienting response were noted in cases of bitemporal foci, of foci situated in the allocortex (hippocampus and amygdala) and of foci inducing generalized or generalized and partial seizures.

Animals↗

Hypergraphia in epilepsy: is there a specificity to temporal lobe epilepsy?

The purpose of this investigation was to determine the specificity of hypergraphia to temporal lobe epilepsy using the paradigm developed by Sachdev and Waxman (1981). One hundred and thirty-eight patients were sent a standard stimulus letter and the response rates were examined for the patient groups with temporal lobe epilepsy (N = 80), and without (N = 31), and mixed seizure types (N = 13). For those patients who responded, additional analyses involved the number of words per response and the presence/absence of any qualitative indices of the postulated interictal behavioural syndrome of temporal lobe epilepsy. The results were interpreted in the light of the contemporary definitions of hypergraphia and were related to the larger literature concerned with personality and behavioural change in temporal lobe epilepsy.

Adult↗

Temporal pole hypometabolism may be linked to a reduction of grey matter in temporal lobe epilepsy.

In order to gain further insight into the pathophysiology of temporal pole hypometabolism, we decided to perform a voxel-based automated analysis of structural MRI in epileptic patients with or without temporal pole hypometabolism. After fully automated segmentation of cerebral grey matter from structural T1-weighted MRI scans, we applied the automated technique of statistical parametric mapping (SPM) to the analysis of grey matter of nine control subjects, and 18 patients with right medial temporal lobe epilepsy with (n = 13) or without (n = 5) significant temporal pole hypometabolism. Group comparisons between subject controls and epileptic patients with temporal pole hypometabolism showed a reduction of grey matter located into the superior part of the right temporal pole, the right hippocampus and the left parahippocampal gyrus. Epileptic patients without temporal pole hypometabolism did not exhibit temporal pole grey matter abnormalities. These findings suggest that a reduction of temporal pole neocortical grey matter might contribute to temporal pole hypometabolism in temporal lobe epilepsy.

Adult↗