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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 53  |  Issue : 1  |  Page : 41-47

Long-term scalp video-electroencephalography monitoring in the presurgical evaluation of epilepsy surgery


1 Department of Neurology, Minia University, Minia, Egypt
2 Department of Neurology, Minia University, Minia, Egypt; Department of Neurosurgery, Jichi Medical University, Tochigi, Japan
3 Department of Neurosurgery, Jichi Medical University, Tochigi, Japan

Date of Submission04-Jul-2015
Date of Acceptance01-Oct-2015
Date of Web Publication15-Feb-2016

Correspondence Address:
Nermin A Hamdy
MD, Department of Neurology, Minia University, Minia, 61111, Egypt

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-1083.176370

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  Abstract 

Background
Diagnosis of the epileptogenic zone is the main aim of the presurgical evaluation in patients with drug-resistant epilepsy. Different diagnostic tools are being used to identify it.
Objective
This study aimed at studying the value of long-term scalp video-electroencephalography (video-EEG) monitoring to diagnose laterality and locality of the epileptic focus by comparing its results with other noninvasive methods, including interictal magnetoencephalography (MEG), interictal iodine-123 iomazenil single-photon emission computed tomography ( 123 I-IMZ SPECT), and interictal fluorine-18 fluorodeoxyglucose ( 18 F-FDG) PET.
Patients and methods
A total of 24 patients with drug-resistant epilepsy were included in this study; 17 had mesial temporal lobe epilepsy, whereas the remaining seven had neocortical epilepsy. All patients were admitted to Jichi University Hospital in Japan for the presurgical evaluation and surgical intervention. All patients were subjected to clinical evaluation, brain MRI, and long-term scalp video-EEG monitoring; a total of 23 patients had interictal 123 I-IMZ SPECT, 19 had interictal MEG recording, and 10 had interictal 18 F-FDG PET. The laterality and locality of the epileptogenic area predicted by these methods were defined in relation to the resected area.
Results
Long-term scalp video-EEG monitoring was significantly superior to interictal 123 I-IMZ SPECT and interictal 18 F-FDG PET in diagnosing laterality and locality of the epileptogenic zone and superior to interictal MEG in patients with mesial temporal lobe epilepsy and patients with epileptogenic MRI findings.
Conclusion
Long-term scalp video-EEG monitoring is the cornerstone in the presurgical evaluation of epilepsy surgery.

Keywords: Epilepsy surgery, long-term scalp video-electroencephalography monitoring, presurgical evaluation


How to cite this article:
Khafagi AT, Hamdy NA, Hassan EM, Yehia MA, Ismail MM, Watanabe E. Long-term scalp video-electroencephalography monitoring in the presurgical evaluation of epilepsy surgery. Egypt J Neurol Psychiatry Neurosurg 2016;53:41-7

How to cite this URL:
Khafagi AT, Hamdy NA, Hassan EM, Yehia MA, Ismail MM, Watanabe E. Long-term scalp video-electroencephalography monitoring in the presurgical evaluation of epilepsy surgery. Egypt J Neurol Psychiatry Neurosurg [serial online] 2016 [cited 2021 Apr 23];53:41-7. Available from: http://www.ejnpn.eg.net/text.asp?2016/53/1/41/176370


  Introduction Top


Epilepsy is one of the most common neurological disorders; ∼60% of all patients with epilepsy suffer from focal epilepsy syndromes [1]. It has been estimated that about 5-10% of all incidence cases of epilepsy eventually become drug resistant [2]. Cumulatively, these patients may account for about 40% of epilepsy prevalence [3],[4]. About 50% of the patients with drug-resistant epilepsy are potential candidates for epilepsy surgical treatment [5]. The average seizure-free rate after epilepsy surgery is nearly 60% in large epilepsy centers [6]. The main aim of the presurgical evaluation in patients with drug-resistant epilepsy is the diagnosis of the epileptogenic zone [7]. Different diagnostic tools are being used by epileptologists to identify epileptogenic zone, including the following: long-term scalp video-electroencephalography (video-EEG) monitoring, MRI, interictal magnetoencephalography (MEG), interictal iodine-123 iomazenil single-photon emission computed tomography ( 123 I-IMZ SPECT), and interictal fluorine-18 fluorodeoxyglucose ( 18 F-FDG) PET [8].


  Aim Top


The aim of the present study was to examine the role of long-term scalp video-EEG monitoring in presurgical evaluation of epilepsy surgery, and how far it is valuable in diagnosing laterality and locality of the epileptic focus by comparing its results with other noninvasive methods.


  Patients and methods Top


A total of 24 patients with drug-resistant epilepsy were included in the present study. Seventeen patients were diagnosed to have mesial temporal lobe epilepsy (MTLE), whereas seven patients had neocortical epilepsy (NE). All patients were admitted to the Department of Neurosurgery in Jichi Medical University Hospital for the presurgical evaluation and surgical intervention.

Data were collected by Dr M. M. Ismael for his MD thesis, under the supervision of the rest of authors.

We included adult patients of both sexes with surgically remediable drug-resistant epilepsy, which was defined as the failure of adequate trials of two tolerated and appropriately chosen and used anti epileptic drug (AED) schedules to achieve sustained seizure freedom. Seizure freedom was defined as the freedom from all types of seizures for 12 months or three times the preintervention interseizure interval, whichever was longer [9]. We excluded children and inoperable patients because of any cause, including patients with multiple independent epileptic foci.

Patients were subjected to history-taking, clinical examination, and phase I evaluation as follows; all patients were subjected to structural brain MRI and long-term scalp video-EEG monitoring by using the monitoring system (Neurofax EEG-1100; Nihon Kohden Corporation, Tokyo, Japan) after the withdrawal of AED medication. A total of 23 patients were subjected to interictal 123 I-IMZ SPECT, which was performed using the central benzodiazepine antagonist 123 I-iomazenil. Data acquisition was performed with a Picker PRISM 3000XP three detector rotating gamma camera (Picker International Inc., Cleveland, Ohio, USA). Nineteen patients were subjected to interictal MEG recording for 30 min using 204 channel whole-head MEG system (Neuromag Ltd, Helsinki, Finland). Ten patients were subjected to interictal 18 F-FDG PET with Biograph 16 HI-REZ PET/CT Scanner (Siemens, Hoffman Estates, Illinois, USA).

The laterality and locality of the epileptogenic area, predicted by phase I evaluation methods, were defined in relation to the laterality and locality of the resected area after a consensus was reached. For each of these methods the results were coded as follows. Regarding laterality, if the laterality of the predicted area was the same as the laterality of the resected area, the method result was coded as lateralizing (true positive+true negative). If the laterality of the predicted area was opposite to the laterality of the resected area, the method result was coded as false lateralizing (false positive+false negative). If the method predicted an epileptogenic area in both hemispheres, the method result was coded as none lateralizing (true positive+false negative). If the method did not predict any epileptogenic area, the method result was coded as negatively lateralizing (true negative+false positive).

Regarding locality, if the location of the predicted area was the same as the location of the resected area, the method result was coded as perfectly overlapping (true positive+true negative). If the location of the predicted area was more extensive (but not for more than two lobes within the same hemisphere), the method result was coded as partially overlapping (true positive+true negative). If the location of the predicted area was different from the location of the resected area, the method result was coded as none overlapping (false positive+false negative). If the location of the predicted area was much more extensive than was the location of the resected area, the method result was coded as non localizing (true positive + false positive). If the method did not predict any epileptogenic area, the method result was coded as negatively localizing (true negative+false negative).

Sensitivity of any of these methods was calculated as true positive/true positive + false negative, whereas specificity was calculated as true negative/true negative+false positive.

Ten patients were subjected to phase II evaluation with invasive intracranial EEG recording.

Statistical analysis

Data entry and analysis were carried out with an IBM compatible computer using the software SPSS (version 11; SPSS Inc., Chicago, Illinois, USA), and Microstats program (Webbsoft Technologies, Scoresby, Australia). Quantitative data were presented as mean and SD, whereas qualitative data were presented as frequency distribution. The Z-test (test of proportion), independent sample t-test and the χ2 -tests were also used. A P value of less than 0.05 was used as a cut-off point for all significant tests. A P value of less than 0.5 was considered significant.


  Results Top


A total of 24 patients were included in this study [10 men (41.7%) and 14 women (58.3%)]: 17 (70.8%) patients with MTLE and seven (29.2%) patients with NE. Their ages ranged from 21 to 54 years (mean: 34.2 ± 7.9 years). Complex partial seizures were shown to be the most common drug-resistant seizure type in 21 (87.5%) patients −17 (100%) patients with MTLE and four (57.1%) patients with NE - and this difference was statistically highly significant (P = 0.001). Neurological examination showed abnormality in only two patients (both were patients with NE); one patient showed motor dysphasia and Gerstmann's syndrome, whereas the other was mentally retarded with an IQ of 40.

Structural brain MRI showed epileptogenic lesions in 14 (58.3%) patients: 11 (64.7%) patients with MTLE and three (42.9%) patients with NE. In patients with MTLE, hippocampal atrophy has been shown as the most common lesion. Long-term scalp video-EEG monitoring was significantly superior to interictal MEG in diagnosing laterality and locality of the epileptogenic zone in the total number of patients. In contrast, interictal MEG was superior to long-term scalp video-EEG monitoring in diagnosing locality of the epileptogenic zone perfectly in the total number of patients and with a statistically significant difference in patients with NE [Table 1].
Table 1: Comparison between long-term scalp video-electroencephalography monitoring and interictal magnetoencephalography results

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Interictal MEG was superior to long-term scalp video-EEG monitoring in patients with normal MRI. Whereas long-term scalp video-EEG monitoring was superior to interictal MEG in patients with epileptogenic MRI findings [Table 2].
Table 2: Comparison between long-term scalp video-electroencephalography monitoring and interictal magnetoencephalography results both in patients with normal magnetic resonance imaging and epileptogenic magnetic resonance imaging findings

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Long-term scalp video-EEG monitoring was superior to interictal 123 I-IMZ SPECT regarding the diagnosis of laterality and locality in the total number of patients and in MTLE [Table 3], both in patients with normal and epileptogenic MRI findings [Table 4].
Table 3: Comparison between long-term scalp video-electroencephalography monitoring and interictal iodine-123 iomazenil single-photon emission computed tomography results

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Table 4: Comparison between long-term scalp video-electroencephalography monitoring and interictal iodine-123 iomazenil single-photon emission computed tomography results both in patients with normal magnetic resonance imaging and epileptogenic magnetic resonance imaging findings

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Long-term scalp video-EEG monitoring was superior to interictal 18 F-FDG PET with a statistically significant difference regarding the diagnosis of laterality and locality in all patients and in patients with MTLE and laterality in NE patients [Table 5]. Moreover, it was superior in the diagnosis of laterality in patients with normal MRI, both in the total number of patients and in patients with NE, and in patients with epileptogenic MRI findings, both in the total number of patients and in patients with MTLE [Table 6].
Table 5: Comparison between long-term scalp videoelectroencephalography monitoring and interictal fluorine-18 fluorodeoxyglucose positron emission tomography results

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Table 6: Comparison between long-term scalp video-electroencephalography monitoring and interictal fluorine-18 fluorodeoxyglucose positron emission tomography results both in patients with normal magnetic resonance imaging and epileptogenic magnetic resonance imaging findings

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Sensitivity and specificity of interictal MEG, interictal 123 I-IMZ SPECT, and interictal 18 F-FDG PET to measure laterality and locality of epileptogenic focus compared with long-term video-EEG are shown in [Table 7].
Table 7: Sensitivity and specificity of interictal magnetoencephalography, interictal iodine-123 iomazenil single-photon emission computed tomography and interictal fluorine-18 fl uorodeoxyglucose positron emission tomography to measure laterality and locality of epileptogenic focus compared with long-term video-electroencephalography

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  Discussion Top


Long-term scalp video-EEG monitoring allowed recording of ictal and interictal changes. In contrast, other techniques used and compared with long-term scalp video-EEG monitoring record only interictal brain activity. That was not a bias towards long-term scalp video-EEG monitoring, as MEG is performed in the outpatient setting where AEDs cannot be tapered or discontinued safely, and recording time is limited, so the chance of capturing a seizure during a study is very small [10]. The use of 123 I-IMZ as a radiotracer for interictal SPECT has been shown to delineate the epileptic focus more precisely than does ictal SPECT, with a higher sensitivity [11]. Finally, 18 F-FDG PET measures changes in cerebral glucose metabolism and has higher spatial resolution, but its temporal resolution is unfavorable for ictal studies [8].

The number of patients included in this study was relatively small, but a similar number of patients has been included in other studies used to evaluate different phase I evaluation methods. A study by Debets et al. [12] included 23 patients to determine the contribution of 18 F-FDG PET, 11 C-flumazenil PET, and 123 I-IMZ SPECT in the presurgical evaluation of patients with medically intractable complex partial seizures. In their study, Tanaka et al. [11] included 10 patients to evaluate the role of interictal 123 I-IMZ SPECT in the diagnosis of the epileptogenic zone and compared its results with those of perfusion ictal SPECT and interictal 18 F-FDG PET.

The number of patients subjected to different phase I evaluation methods was not identical in our study, as not all patients were subjected to all the phase evaluation methods in their presurgical evaluation program. Other studies comparing between different phase I evaluation methods also included different number of patients in subgroups [11].

In the present study, there were 17 (70.8%) patients with MTLE and seven (29.2%) patients with NE. This was in agreement with the majority of surgical series in which the number of patients with MTLE represented between 50 and 73% of patients referred and assessed in the epilepsy surgical centers [13].

Long-term scalp video-EEG monitoring was significantly superior to interictal MEG in diagnosing laterality and locality of the epileptogenic zone with higher sensitivity and specificity, especially in patients with MTLE and patients with epileptogenic MRI findings. This may be due to the advantage of long-term video-EEG monitoring, which facilitates extensive temporal sampling across all periods of the sleep/wake cycle and recording of the ictal activity. In contrast, interictal MEG was superior to long-term scalp video-EEG monitoring in diagnosing locality of the epileptogenic zone perfectly with a statistically significant difference in patients with NE and patients with normal MRI. This was in agreement with previous studies [14],[15],[16],[17],[18],[19],[20],[21],[22],[23], which concluded that interictal MEG can localize epileptic activity accurately even to lobar subcompartments. The superiority of interictal MEG in patients with NE was in agreement with other studies [24],[25],[26], which concluded that MEG sensitivity depends mainly on the source depth with a higher sensitivity for superficial sources; the amplitude of the magnetic field depends strongly on the depth of the electrical brain activity. Its superiority in patients with normal MRI was in agreement with a study by Pataraia et al. [27],[28] who concluded that MEG is especially useful for the study of patients with nonlesional epilepsy and of patients with large lesions, where it provides unique information on the epileptogenic zone. These results showed that long-term scalp video-EEG monitoring and interictal MEG complement each other in the diagnosis of the epileptogenic zone. This was in agreement with many previous studies [16],[28],[29],[30],[31],[32],[33], which reported the complementary functions of long-term scalp video-EEG monitoring and interictal MEG.

In our study, long-term scalp video-EEG monitoring was superior to both interictal 123 I-IMZ SPECT and interictal 18 F-FDG PET in diagnosing laterality and locality of the epileptogenic zone with significantly higher sensitivities and specificities not only in patients with epileptogenic MRI findings but also in patients with normal MRI, with less significant difference in patients with NE, may be due to the relatively small number of patients in this subgroup. SPECT and PET in our study recorded brain activity in an interictal state only, whereas long-term scalp video-EEG monitoring allowed the recording of brain activity in both interictal and ictal states. This was in agreement with the studies by Wehner and Lüders [34], and Obeid et al. [35],who concluded that interictal SPECT and PET are more useful for lateralizing than localizing the epileptic focus as the area diagnosed by SPECT and PET often extends beyond the epileptogenic zone, and therefore they cannot be used to delineate surgical borders. Other studies showed that interictal SPECT and PET are mainly used to augment the diagnosis of long-term scalp video-EEG monitoring to avoid phase II evaluation [8],[36],[37],[38],[39],[40].


  Conclusion Top


Long-term scalp video-EEG monitoring is the cornerstone in the presurgical evaluation of epilepsy surgery. Interictal MEG complements long-term scalp video-EEG monitoring in the diagnosis of the epileptogenic zone, whereas interictal 123 I-IMZ SPECT and interictal 18 F-FDG PET are mainly used to augment the diagnosis of long-term scalp video-EEG monitoring to avoid phase II evaluation.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]



 

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