Year : 2008 | Volume
: 3 | Issue : 1 | Page : 74--81
Presurgical evaluation of epilepsy
Manas Panigrahi1, Sita S Jayalakshmi2,
1 Department of Neurosurgery, Nizam's Institute of Medical Sciences, Punjagutta, Hyderabad, India
2 Department of Neurology, Nizam's Institute of Medical Sciences, Punjagutta, Hyderabad, India
Dept. of Neurosurgery, Nizam«SQ»s Institute of Medical Sciences, Punjagutta, Hyderabad
The objective of the multimodality presurgical evaluation in patients with refractory epilepsy is to establish sufficient concordance among the various investigations. There should be maximum overlap in the epileptogenic zone, the irritative zone, the ictal onset zone, the functional deficit zone and the symptomatogenic zone. The ictal and interictal electroencephalogram measures the localization of epileptiform discharges, which should be concordant with structural abnormalities noted on MRI brain and functional abnormalities in the form of a zone of hypometabolism on fluorodeoxyglucose positron emission tomography, interictal single photon emission computerized tomography (SPECT) or hyperperfusion of the epileptogenic zone on ictal SPECT for a good surgical outcome. There should be no conflicting data from any of these studies, neuropsychological evaluation or seizure semiology.
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Panigrahi M, Jayalakshmi SS. Presurgical evaluation of epilepsy.J Pediatr Neurosci 2008;3:74-81
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Panigrahi M, Jayalakshmi SS. Presurgical evaluation of epilepsy. J Pediatr Neurosci [serial online] 2008 [cited 2019 Nov 12 ];3:74-81
Available from: http://www.pediatricneurosciences.com/text.asp?2008/3/1/74/40593
Approximately 60% of all patients with epilepsy suffer from focal epilepsy syndromes. In about 15% of these patients, the seizures are not adequately controlled with anticonvulsive drugs and such patients are potential candidates for surgical treatment.  The average seizure-free rate after epilepsy surgery is ~60% in large epilepsy centers. The goals of presurgical evaluation are  1. to establish the diagnosis of epileptic seizures, 2. define the electro-clinical syndrome, 3. delineate the lesion(s) responsible for the seizures, 4. evaluate the past antiepileptic drug (AED) treatments and make sure that an adequate medical treatment had been provided, 5. select ideal surgical candidates with optimal electro-clinico-radiologic correlation, 6. ensure that the surgery will not result in disabling neuropsychological deficits.
Aim and Concept of Surgery for Epilepsy
The main aim of presurgical evaluation in patients with intractable epilepsy is the identification of the cortical area capable of generating seizures and whose removal or disconnection will result in seizure freedom. This area is called the epileptogenic zone.  Different diagnostic tools are being used by epileptologists to identify different cortical zones - symptomatogenic zone, irritative and ictal onset zones, epileptogenic lesion and functional deficit zone, each one of which is more or less a precise index of the epileptogenic zone  [Table 1]. In the ideal surgical candidate, all five zones will show a high degree of overlap, and the resection can be performed with high likelihood of seizure freedom; but in most patients, the different cortical zones are somewhat discordant in location or extent and the final decision about surgery should be taken after careful weighing of the significance of each one of these areas, based on the information provided in various investigations.
The current diagnostic techniques used in the definition of these cortical zones are video electroencephalography (EEG) monitoring, magnetic resonance imaging (MRI), ictal single photon emission computerized tomography (SPECT) and positron emission tomography (PET). A detailed neuropsychological evaluation is an indispensable tool for prognosis of neuropsychological deficits after surgery and may significantly influence the final decision about surgery.  The intracarotid amobarbital procedure (Wada test) provides additional information about lateralized deficits and may help to localize the epileptogenic zone. , Interictal SPECT is less reliable than interictal PET for identifying dysfunctional cortex with hypometabolism. 1 H magnetic resonance spectroscopy ( 1 H MRS) provides information about metabolic derangement and may be used as an adjunctive to the other data. Magnetoencephalography (MEG) can complement the scalp EEG data in defining the extent and location of the epileptogenic zone. 
Role of Imaging in the Presurgical Evaluation of Epilepsy
The goals of neuroimaging in patients with medically refractory epilepsy are 1. delineation of structural and functional abnormalities in the suspected epileptogenic region, 2. prediction of nature of structural pathology, 3. detection of abnormalities distant from the epileptogenic region (dual pathology) and 4. identification of eloquent brain regions such as language, memory and sensorimotor areas and the relation of these regions to the epileptogenic region. , The images should be reviewed by radiologists specially interested and experienced in the evaluation of patients with epilepsy.
Magnetic resonance imaging
The common abnormalities identified by MRI in patients with refractory epilepsy are mesial temporal atrophy and sclerosis (MTS), malformations of cortical development, primary brain tumors, vascular malformations and focal atrophic lesions. The structural MRI protocol for patients with chronic epilepsy is summarized in [Table 2]. 
In mesial temporal sclerosis and atrophy, the hippocampus is best visualized by acquiring thin slices (1-3 mm) orthogonal to its long axis. The important MRI features of MTS are:
Abnormal increased signal of hippocampus and amygdala relative to other gray matter on T2 W imagesAtrophic changes in hippocampus/amygdala or temporal lobe in T1 W imagesAbnormal increased signal in gray/white matter of the temporal lobe relative to the gray matter elsewhereAtrophy of ipsilateral fornixDilatation of the temporal hornBlurring of gray and white matter margin in the temporal neocortex
In addition, there may be lesions associated with ipsilateral MTS, such as migrational disorders, porencephalic cysts and neoplasms (dual pathology). 
MTS has been classified into four groups as follows.  Group 1 - high T2 W signal and atrophy of hippocampus/amygdala with atrophy of temporal lobe [Figure 1]; Group 2 - high T2 W signal and atrophy of hippocampus/amygdala only; Group 3 - high signal in hippocampus/amygdala without atrophy; and Group 4 - hippocampal/amygdalar atrophy only without T2 W signal changes. Visual assessment may reliably detect hippocampal volume asymmetry of more than 20%; however, lesser degrees of asymmetry require quantitative volumetric analysis.  Quantification of T2 relaxation time is an objective way to assess hippocampal damage. An increased hippocampal T2 time reflects underlying gliosis and neuronal loss. Volumetric studies of entorhinal cortex may identify occult damage ipsilateral to the seizure focus that is not evident on visual inspection. In patients with bilateral MTS, volumetry helps to identify the side maximally affected.  MRI has about 90% sensitivity and specificity in detecting MTS and other abnormalities in the rest of the temporal lobe.  Malformations of cortical development are being increasingly recognized in patients with refractory epilepsy. They may be focal cortical dysplasia (FCD), lissencephalies, heterotopia, polymicrogyria, schizencephaly.  Patients with low-grade primary brain tumors frequently present with seizures. The underlying histopathologies include dysembryoplastic neuroepithelial tumors, ganglio-glioma, gangliocytoma and pilocytic and fibrillary astrocytoma. These lesions have low signal on T1 and high signal on T2 W images. Cyst formation and enhancement with gadolinium may occur. Calcification is present in some cases. Cavernous angiomas are circumscribed and have the characteristic appearance of a range of blood products on MRI. Newly developed MRI techniques, diffusion-weighted imaging (DWI), diffusion tensor imaging (DTI), tractography improve the sensitivity of MRI. ,
Role of SPECT and PET in the presurgical evaluation of epilepsy
Ictal SPECT and interictal PET remain important imaging tools in the presurgical evaluation of patients with refractory partial epilepsy. The two commonly used tracers for SPECT are 99m Tc - Hexamethylene propylene amine ( 99m Tc HMPAO) and 99m Tc-ethyl cysteinate dimer ( 99m Tc - ECD). SPECT measures blood flow; and comparing interictal and ictal SPECT studies, the increase in blood flow of certain brain regions during the ictal phase with respect to the interictal period can be evaluated. During ictal SPECT, due to epileptic activation, the neurons located in these areas are hyperactive and there is an increase in blood flow as an autoregulatory response. Thus ictal SPECT can evaluate all brain areas with similar accuracy, including deep regions of gray matter that are difficult to monitor with scalp and even with invasive EEG. , The limitations of ictal SPECT are - 1. the dye reaches the brain at least one minute after the seizure onset, a time at which significant seizure spread has already occurred; 2. the spatial resolution of the images is low. An ictal SPECT displays both the ictal onset zone and seizure propagation pathways. In common practice, the region with largest and most intense hyperperfusion is considered as the ictal onset zone [Figure 2]. However, these regions may also represent ictal propagation.  An ictal injection delay of less than 20 seconds after seizure onset significantly correlates with correct localization  . The sensitivity of ictal SPECT is 89-95% in temporal lobe epilepsy. ,, Subtraction ictal SPECT co-registered with MRI (SISCOM) improves the localization of the area of hyperperfusion. Extratemporal seizures are brief, and it is difficult to obtain an ictal SPECT. Post-ictal injections are easier to perform than ictal injections and have a sensitivity of 70% in temporal lobe seizures and 46% in extratemporal lobe epilepsy.  In conclusion ictal SPECT, as ictal EEG, can only define approximately the location and extent of the ictal onset zone and provides complementary information to the EEG data with respect to the ictal onset zone.
Interictal SPECT provides information about dysfunctional cortex with decreased blood perfusion. It is used as a baseline exam for comparison with scans obtained during the ictal phase as this method is moderately sensitive (40-50% correct localization), has high false-positive rate. 
18 F-deoxyglucose (FDG) PET measures changes in cerebral glucose metabolism and has higher spatial resolution and more reliable quantitation than SPECT, but the temporal resolution of PET with 18 FDG is unfavorable for ictal studies.  PET maps cerebral glucose metabolism using FDG PET and cerebral blood flow using 15 O-labelled water. Regional hypometabolism is best analyzed with co-registration of PET scans to MR images. The sensitivity of FDG PET is 60-90% for the detection of interictal temporal lobe hypometabolism. ,,,
18 FDG PET detects interictal glucose hypometabolism ipsilateral to the seizure focus in 60-90% of temporal lobe epilepsy (TLE) patients. Unilateral or asymmetric bilateral diffuse regional hypometabolism usually extends mesiolaterally in the temporal lobe. Some patients also have changes in extratemporal cortical areas or in the basal ganglia or thalamus. 15 OH 2 O studies generally show hypoperfusion in the same areas as glucose hypometabolism but are less sensitive and associated with more frequent false lateralization. 
18 FDG PET is more useful for lateralizing than localizing the epileptic focus. Patients with MTS have low glucose metabolism in the whole temporal lobe [Figure 3], while patients with mesiobasal temporal tumors show only a slight decrease in metabolism. There is no correlation found between the degree of hypometabolism and the location of epileptic focus. Unilateral focal temporal hypometabolism in 18 FDG PET predicts good outcome of surgery for TLE.  However, absence of unilateral hypometabolism does not preclude a favorable outcome. Symmetric bilateral temporal hypometabolism, severe extratemporal cortical or thalamic hypometabolism is associated with higher incidence of postoperative seizures. The diagnostic sensitivity of FDG PET as analyzed by statistical parametric mapping (SPM) was 44% in patients with refractory partial epilepsy and normal MRI.  18 FDG PET has lower sensitivity for lateralization of epileptic foci in extratemporal epilepsies than in TLE, and SPM improves diagnostic yield of 18 FDG PET and assists the planning of implantation of intracranial electrodes in patients with refractory partial epilepsy with nonlocalizing MRI or scalp EEG.
Magnetic resonance spectroscopy (MRS)
1 H MRS provides measurement of metabolites like N-acetylaspartate (NAA), choline, creatinine, lactate γ-aminobutyric acid (GABA) and glutamate; 31 P MRS measures phosphorus-containing compounds. 1 H MRS lateralizes seizure focus in up to 80-90% of the patients with TLE. , Patients with MTS show decrease in NAA and increase in choline, creatinine and myo-inositol signals ipsilaterally; 20-50% of patients with unilateral TLE have bilateral temporal abnormalities in 1 H MRS. The role of 1 H MRS in predicting outcome of temporal lobe epilepsy surgery is not clear, and its role in extratemporal lobe epilepsy is uncertain.
Functional magnetic resonance imaging
Functional MRI (fMRI) helps to visualize regional brain activity. It provides a reliable way to lateralize language dominance and eliminates the need for invasive intracarotid amobarbital test (IAT) in 80% or more patients.  A series of related tests, such as verbal fluency and language comprehension, should be performed for functional language mapping. Language fMRI has limited correlation with the IAT, especially in patients with left TLE and with mixed speech dominance.  Functional MRI with memory paradigms may be incorporated into the presurgical assessment of TLE to minimize the adverse cognitive sequelae of anterior temporal lobe resection, and this will result in less use of IAT. fMRI of memory-induced mesial temporal lobe activation lateralizes the side of seizure onset in patients with refractory symptomatic TLE and may provide complementary information for presurgical evaluation.  fMRI may be used to identify sensorimotor cortex when planning neocortical resections.
Role of EEG in Presurgical Evaluation
Non invasive EEG monitoring
Long-term noninvasive video EEG monitoring in presurgical evaluation is performed to differentiate seizure versus nonseizure events, classification of seizure types and localization of seizure onset. It is expensive and labor intensive. At least two to five habitual seizures should be recorded after gradual AED withdrawal.
Analysis of events - Ictal semiology : The clinical features distinguishing between temporal and extratemporal complex partial seizures are given in [Table 3]. , Ictal semiology that helps to lateralize complex partial seizures (CPS) of temporal lobe origin is contralateral dystonic posturing of upper limb; ipsilateral limb automatism, associated with behavioral arrest, is seen in most cases [Table 4]. ,
Interictal EEG : Interictal epileptiform discharges (EDs) are good indices of the epileptogenic temporal lobe. , Bilateral independent EDs are seen in 15-30% of patients with intractable TLE. Excellent surgical results are obtained in patients with unilateral preponderance of EDs of 3:1, along with ipsilateral ictal onset on ictal EEG. ,,, The other interictal EEG abnormalities seen in TLE are temporal intermittent rhythmic delta activity (TIRDA) and focal delta activity and generalized EDs.
Ictal EEG : The most reliable ictal EEG pattern in TLE is a rhythmic buildup of 5-7 Hz theta activity over one temporal region preceding the clinical event  [Figure 4]. The initial pattern of ictal discharge on scalp EEG can assist in distinguishing seizures of temporal neocortical onset from those of hippocampal onset, and this information can be used to identify patients for invasive monitoring  [Table 5]; the ictal discharges in extratemporal epilepsy present as low-voltage fast activity, an incrementing or a recruiting rhythm, repetitive spikes or spikes and slow waves, rhythmic slow waves, high-voltage sharp waves or focal or widespread attenuation or a flattening of the background.  Spike and wave, paroxysmal fast and beta frequency discharges with rapid spread are more likely to be seen with extratemporal and particularly, frontal seizures. Sphenoidal electrodes have an advantage over laterally placed scalp electrodes in detecting inferiorly directed mesial temporal discharges.  They sometimes detect interictal spikes and seizures not seen with scalp electrodes. Anterior temporal electrodes detect interictal and ictal epileptiform phenomena and may replace sphenoidal electrodes as they do not require expertise for their placement and create no discomfort. 
Role of invasive EEG in presurgical evaluation : Intracranial EEG recording with seizure monitoring is indicated when exact localization of the epileptogenic zone is required to plan a precise surgical resection for treatment of medically refractory seizures or when exact localization of functional cortex is required to plan a safe resection. Stereotactically inserted depth electrodes are indicated when EEG recording is needed from buried gray matter that is not accessible with other electrodes.  Bilateral depth electrodes are indicated when the surface EEG is suggestive of bilateral independent ictal pattern and when the ictal pattern is first seen in the contralateral temporal lobe on surface EEG in a case of unilateral mesial temporal lobe epilepsy. ,, According to Mayo Clinic experience, invasive recordings in TLE were deemed necessary due to (a) inability to accurately localize the site of seizure onset by surface EEG, (b) suspected multifocal onset and (c) discrepancies between MRI findings and video EEG monitoring.  Stereotactic depth recordings, when combined with scalp EEG recording, the so-called stereo EEG (SEEG), help in well delineation of the epileptogenic zone in complex cases. The complications of depth electrodes are intracerebral hemorrhage, in 1-4% cases with rare fatalities and infection.  Subdural strip and grid electrodes, inserted through burr holes or craniotomy, are indicated when neocortical seizure onset is suspected. Foramen ovale electrode recordings from the mesial aspect of the temporal lobe are indicated in patients with temporal lobe epilepsy.  Epidural peg electrodes are now used as sentinel electrodes, often in combination with other invasive techniques, for obtaining epidural ictal recordings.
Magnetoencephalography (MEG) in presurgical evaluation : Whole-head MEG facilitates simultaneous recording from the entire brain surface. Localizations of interictal spike zone with MEG showed excellent agreement with invasive EEG recordings. MEG is useful for the study of patients with nonlesional neocortical epilepsy and in patients with large lesions; it provides unique information on the epileptogenic zone. MEG can be used to map the sensorimotor cortex and language cortex. Both EEG and MEG yield complementary and confirmatory information. 
Neuropsychology and psychiatry workup in presurgical evaluation : The primary goal for neuropsychological evaluation is to characterize the patient's intellectual level, intelligence quotient (IQ) with the Wechsler Adult Intelligence Scale (WAIS) or a revision of it (WAIS-R), the Minnesota Multiphasic Personality Inventory (MMPI) and the Washington Psychosocial Seizure Inventory (WPSI).  An epileptic dysfunction in a silent cortical area will have less influence on IQ area. Discriminative neuropsychology has several tests in store, as reviewed by Jones Gotman et al.  Neuropsychology provides information about size, location and degree of epileptic dysfunction. Preoperative evaluation assists in predicting epilepsy surgery outcome and thus helps in selecting ideal candidates for surgery.  Epilepsy surgery can be performed without any neuropsychology at all, but it helps in the preoperative counseling of the patients and their caregivers. It provides baseline values against which the postoperative values can be compared.
Epilepsy, especially TLE, is often associated with psychiatric disorders such as behavioral changes, major mood disorders or psychosis. Presurgical psychiatric workup is a must for documentation of psychiatric disorders. This should be followed by postsurgical psychiatric documentation.  It is important to determine whether the association is casual and when postoperatively new psychiatric disorders occur, what the casual mechanism is. 
The role of Wada's test in the presurgical evaluation: The intracarotid amobarbital test (IAT) (or Wada's test) is commonly used to assess the hemispheric functions in patients being evaluated for epilepsy surgery. It helps in lateralization of language and to identify temporal lobe surgical candidates at risk for global amnesia and lateralization of the epileptic zone. , Memory assessment during Wada's test produces a state of temporary, reversible dysfunction ipsilateral to the side of surgery; it thus helps to know the effect of temporal lobectomy on memory before surgical resection. However, a relative failure of a side in Wada's memory test does not reliably predict postoperative amnesia. Wada's test involves selective internal carotid artery catheterization through transfemoral route. Selective posterior cerebral artery amobarbital test can reliably predict postoperative memory function in patients with TLE. , A practice test is performed prior to actual Wada's test one day before. A transfemoral intercarotid angiogram is performed and sodium amobarbital 125 mg is injected. The patient will develop hemiplegia on the contralateral side and global aphasia if speech-dominant hemisphere is injected. Memory for the items presented during the period of hemiparesis is tested approximately ten minutes after the time of injection, when the strength and language functions have returned to normal. The Wada's test is most commonly performed in patients who are candidates for temporal lobectomy, for the evaluation of language and memory and for language lateralization in patients with extratemporal lobe epilepsy. The Wada's test is used mostly in left-handed patients or in those who demonstrate bilateral or contralateral hemisphere damage or with confusing findings on neuropsychological testing. fMRI is a promising noninvasive technique to replace IAT for language lateralization as several studies which compared language lateralization by fMRI and IAT have shown a strong correlation between Wada testing and fMRI. ,,
Successful epilepsy surgery requires a multidisciplinary team approach with discussion of individual patient presurgical evaluation data in detail in a patient management conference. It will improve patient care and communication among members of the team.
In conclusion, none of the currently available preoperative workups can exactly delineate the epileptogenic zone. However, with the multimodality presurgical evaluation approach, sufficient concordance should be established among various independent investigations, thus identifying location and extent of the epileptogenic zone with a high degree of confidence. This will result in a good surgical outcome.
Words/Group of words/Corrections that need to be checked/verified have been highlighted or commented upon. Those abbreviations used for the first time in the article but not spelt out are highlighted; along with the abbreviations, their expanded forms need to be given at the place where the abbreviations are first used.
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