Year : 2008 | Volume
: 3 | Issue : 1 | Page : 65--73
Surface and intracranial electroencephalographic in evaluation for epilepsy surgery
PD Hinduja National Hospital and MRC, GMC and JJ Group of Hospitals, Mumbai, India
PD Hinduja National Hospital and MRC, GMC and JJ Group of Hospitals, Mumbai
This review focuses on the present status of inter-ictal surface EEG, simultaneous ictal video-EEG and intracranial EEG in the evaluation of children for epilepsy surgery. This is considered in the context of high-end structural and functional neuroimaging available today. Initially the concept of the epileptogenic zone and its different components are discussed so that it is easier to understand how the EEG helps in localization. Methods of maximizing the yield of the EEG are emphasized. Abnormalities in the inter-ictal and ictal EEG are discussed in some detail. Special emphasis is given to the seizure semiology and how this helps in identifying which lobe is primarily involved. Limitations of surface EEG are then detailed, with special emphasis on young infants. Finally the discussion turns to intracranial EEG. This is used intra-operatively in one stage epilepsy surgery and more definitively extra-operatively in two stage surgery not only to define the epileptogenic zone but also to identify critical cortex.
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Udani V. Surface and intracranial electroencephalographic in evaluation for epilepsy surgery.J Pediatr Neurosci 2008;3:65-73
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Udani V. Surface and intracranial electroencephalographic in evaluation for epilepsy surgery. J Pediatr Neurosci [serial online] 2008 [cited 2020 Sep 22 ];3:65-73
Available from: http://www.pediatricneurosciences.com/text.asp?2008/3/1/65/40592
Epilepsy surgery continues to evolve as a valuable therapeutic option for approximately 7-15% of pediatric epilepsy patients who are medically refractory., To maximize favorable surgical outcomes, we must strive to improve the selection process of surgical candidates, as well as to perfect the use of available traditional and emerging diagnostic studies. In most cases, clinical experience has shown that surface video-EEG recording of habitual seizures yields the most valuable data for determining surgical candidacy and initial surgical planning. This is in part due to unique ability of video-EEG to characterize the ictal and interictal states clinically and electrographically. Video-EEG allows for the characterization of seizures, their frequency, and ictal semiology, in addition to a preliminary description of a potential epileptogenic focus. In combination with relevant clinical data, seizure semiology, neuroimaging, and other neurophysiologic studies, video-EEG recording of seizures, thus, remains a critical component of the Phase I presurgical evaluation.
The Epileptogenic and other Cortical Zones
The role of surface EEG in surgical planning is to anatomically define the epileptogenic zone (EZ). This theoretical concept describes the region of cortex responsible for generating seizures. Thus, resection or disconnection of the EZ will result in seizure freedom. The precision with which the EZ can be identified is limited with existing technology. Preserving eloquent cortical areas often limits the extent of a resection. Whether this is sufficient to provide seizure freedom depends upon the location of the other cortical zones, on whether the known ictal generator has been resected, and whether there exist other potential generators of ictal activity within the remaining EZ.
Clinically, we may define several cortical zones, which serve as markers for the EZ. The location of each of these zones may be defined by various diagnostic techniques. When these zones overlap to describe the same cortical area, they localize the EZ with increased confidence. The four generally accepted conceptual regions include ictal onset zone, irritative zone, symptomatogenic zone , and anatomic lesion/lesions .
The ictal onset zone defines the cortical region generating ictal onset. This does not include additional regions of the EZ necessary for seizure propagation and spread, nor other potential ictal generators within the EZ. Surface EEG gives an approximate localization, with more precise definition possible via intracranial EEG recording. Though limited by the lag between seizure onset and tracer transport to the ictal focus, a prompt ictal single photon emission computed tomography (SPECT) also aims to define the ictal onset zone as well. The ictal onset zone is often believed to be smaller than the EZ. For long-lasting seizure freedom, resection of the entire EZ must occur so that remaining potential ictal generators, or areas with potential epileptogenicity, are not left behind.
The irritative zone refers to the cortical region generating interictal epileptiform discharges. The irritative zone further defines the extent of the EZ. This zone may be defined by surface EEG, or more precisely by intracranial EEG. Magnetoencephalography (MEG) may also define this zone of interictal activity in deeper cortical or subcortical regions. This, however, samples a shorter time period than long-term surface video-EEG. The extent of the irritative zone often exceeds the EZ and always need not require complete resection for seizure freedom.
The symptomatogenic zone refers to the region of cortex that generates the clinical semiology of habitual clinical seizures when activated. This area may frequently be different from the EZ as ictal onset may occur in functionally "silent" regions of cortex. A seizure becomes clinically apparent only after spread has occurred to the symptomatogenic zone. Reviewing seizure semiology, by history or video-EEG capture, may localize the symptomatogenic zone. There is significant variability however in the localizing value of different ictal semiologies.
An anatomic lesion identified by MRI is the single most important predictor for surgical success. However, sometimes a lesion may not necessarily be epileptogenic. Furthermore, the EZ may include only part of a lesion, or extend to cortex beyond the anatomic boundaries of a given lesion. Also, one may have multiple lesions (for example in TS), where only one might be epileptogenic, and surface video-EEG recording would be necessary to confirm the epileptogenicity of a lesion. Also, it would help to define the EZ boundaries that may not be limited to the lesion itself.
Methods to maximize the yield of surface EEG recording
The potential information which can be gathered from surface video-EEG recording can be maximized in several ways. Regarding basic monitoring techniques, the use of collodion rather than paste improves the quality of recordings lasting several days. For more precise localization, extra electrodes should be utilized when indicated by relevant clinical and electrographic data. In addition to the standard 10-20 international system electrodes, inferior anterior temporal electrodes for presurgical evaluation are often useful. Supraorbital electrodes may aid in detecting orbital-frontal activity. Activating procedures, including hyperventilation and photic stimulation, are useful in some cases. Sleep deprivation and medication reductions often increase the probability of recording interictal and ictal epileptiform activity. Medication reduction, however, may change the electrographic and clinical features of habitual seizures. Digital EEG recordings are essential for prolonged video-EEG not only to enhance clarification of EEG phenomena by allowing the reformatting of data in different montages, and minimizing artifacts, but also to allow paperless storage for later review. Also, the ability to easily change filters, paper speed, gain, and review video simultaneously allows for clarification of electrographic activity.
Interictal EEG patterns
In identifying useful data from interictal recording, several concepts serve useful. Distortions of normal EEG rhythms may aid in localizing or lateralizing abnormalities. This may include asymmetry or poor architecture of the posterior dominant alpha rhythm or mu rhythms in waking or asymmetric spindles or vertex waves in sleep. EEG reactivity may also be impaired. Likewise, normal EEG recording may be consistent with a focus in deeper cortical regions, if suspected. Non-epileptiform abnormalities, which may help to localize the EZ, include slowing and suppression of normal activity. Focal slowing indicates dysfunction in a particular region, which may support the case for identifying the EZ zone. Persistent slowing supports an underlying structural abnormality. Rhythmic temporal theta activity supports a temporal focus. Focal background attenuation is suggestive of an epileptogenic focus. Epileptiform abnormalities such as spikes, sharp waves, and spike-wave complexes during the interictal record support epileptic dysfunction and help to localize the irritative zone. Their appearance is dependent upon the EZ being on the surface, rather than inferior or mesial. Persistent focal interictal spikes and frequent rhythmic spikes are useful in localizing the EZ. Multifocal or generalized interictal abnormalities are less helpful in localization and require additional data for the determination of the EZ.
Simultaneous video-EEG recording
To more confidently describe a patient's habitual seizures, recording at least three and preferably five seizures has been advocated. The exact number required is unclear, and appears to vary depending upon location and seizure type., The first habitual seizure recorded appears predictive of the EZ. Once recorded, seizures may then attempt to be lateralized/localized. If they cannot, then recording results may prove inconclusive and surgical candidacy thus less likely.
The manner in which a seizure evolves (seizure semiology) offers important clues to location of seizure onset. Every attempt should be made to understand the number of seizure types that a patient experiences and the precise semiology of each type. Often multiple partial seizure types are a manifestation of differing degrees of evolution and differing propagation pathways from a single focus. Precise semiology that is confirmed following successful epilepsy surgery offers the best confirmation of seizures that originate from a particular lobe. Such evidence is now available in adults, although it is still lacking in children. Seizure classification in the young child and infant are inherently problematic because alterations in mental status cannot be confirmed.,,, In an older child, however, seizure semiology often has features resembling localization-related seizures in adults. The discussion that follows examines seizure semiology originating within a cerebral lobe as described in adults and the non-infant child.
Frontal Lobe Onset
Frontal lobe seizures are generally of short duration, typically unassociated with postictal confusion, and frequently nocturnal. Differentiating nocturnal seizures from nocturnal parasomnias can be made on clinical grounds, although video-EEG may be required. Tonic or postural features are common in frontal lobe seizures and are suggestive of onset in the contralateral hemisphere. Furthermore, complex partial seizures of frontal lobe onset are more likely to be associated with thrashing, pedaling, and kicking the lower extremities. Not surprisingly, once seizures have propagated from the frontal lobe to the temporal lobe, it is not possible to determine the region of onset. Temporal lobe automatisms include simple oro-buccal or hand automatisms which help to differentiate these from frontal lobe automatisms. Leg movements are prominent in frontal lobe seizures that do not propagate to other areas, whereas hand posturing is common in seizures that remain restricted to the temporal lobe., When present, these features collectively support a finding of frontal lobe onset for seizures. Seizures originating from various regions within the frontal lobes often have unique differentiating features that help in localization., Supplementary motor seizures are associated with preservation of consciousness, tonic posturing of the extremities (often bilaterally), and are often mistaken for psychogenic seizures.
Temporal Lobe Onset
Temporal lobe seizures are often preceded by simple partial seizures that are reported as an epigastric rising sensation and may have autonomic accompaniments., The semiology of temporal lobe seizures is not clearly defined in childhood, although children older than 6 years of age seem to demonstrate a semiology similar to adults. In younger children, it may be difficult to separate typical semiology of temporal lobe onset from seizures of frontal lobe onset. Furthermore, automatisms tend to be simpler in younger children, typically limited to lip smacking and fumbling hand gestures. Behavioral arrest, oro-buccal automatism, and convulsive activity are much more commonly seen in young children. These differences may stem from differences in seizure etiology. Younger children are unlikely to have mesial temporal sclerosis and are much more likely to have tumors or dysplasia underlying temporal lobe epilepsy.,, Unlike frontal lobe epilepsy, postictal confusion is prominent particularly in patients with atrophy restricted to the amygdala. Children, like adults with temporal lobe epilepsy, may have a history of prolonged febrile seizures.
Occipital Lobe Onset
Occipital lobe seizures are usually characterized by simple visual auras (sparks, flashes, scotomata, or amaurosis) followed by contraversion of eyes and head or forced eyelid closure. Children often report a sensation of ocular oscillation., In adult patients, who had undergone successful epilepsy surgery for occipital lobe seizures, clinical features alone suggested an occipital onset in more than two-thirds of the patients. Visual auras, the most common elementary hallucinations and ictal blindness, occurred in 73% of patients. Contralateral eye deviation, blinking, a sensation of eye movement, and nystagmoid eye movements are also seen., One-third of patients exhibited another seizure type, suggesting ictal spread, with 50% having temporal lobe automatism and 38% having focal motor seizures; therefore, video-EEG monitoring is frequently required to identify region of seizure onset.
Parietal Lobe Onset
Parietal lobe epilepsy is less common than seizures originating from other lobes. Prominent sensory changes that spread in a Jacksonian march are often present. Clinical manifestations of parietal lobe epilepsy confirmed by tumoral surgery in 34 patients suggest that auras are present in 79% of patients. Somatosensory (62%), visual (12%), and aphasia were the most common auras. Localized ictal pain is a rare phenomena that when present is a strong predictor of parietal lobe seizures.
Synthesis of Seizure Semiology
Generating a hypothesis about region of seizure origin based on seizure semiology is the initial step in the strategy to localize seizures. It forms the basis for planning the remainder of the presurgical evaluation. There are several limitations with localization based on seizure semiology alone. As pointed out earlier, infants and young children often do not demonstrate localization-specific semiology. Multiple seizure types that are suggestive of multi-origin and localization areas provide important information that may suggest that surgery is not a good option for the patient being evaluated.
Propagated seizures may mislead as to site of origin and also require video-EEG. Alternatively, in patients with true multifocal seizures, it may help delineate the most disabling target seizure to tackle.
Surface ictal EEG recording has been shown to be accurate and reliable in lateralizing seizures. Electrographic onset before clinical onset of a seizure increases the confidence of localizing the epileptogenic zone before spread to the symptomatic zone. When EEG findings are seen after clinical onset, then a mesial or inferior focus not initially seen on the surface may be present. Focal rhythmic bursts of higher frequency discharges with evolution to increasing amplitude, and slowing is the most commonly observed pattern in focal seizure onset., Faster frequencies seen at ictal onset may indicate closer proximity to the ictal focus. A focal electrodecrement pattern with a reduction in interictal activity may support a deeper region of ictal onset.,, Consistent focal repetitive spikes or rhythmic slowing at ons et al so aids in localization and lateralization. Specific ictal onset patterns have been seen to occur more frequently within particular regions of cortex (e.g., temporal vs extratemporal); however, these patterns alone cannot implicate origin from a specific region. The temporal lobe ictal patterns appear to be more consistent, however, than extratemporal patterns. These specific ictal patterns include rhythmic theta activity in temporal seizures, repetitive epileptiform activity in lateral frontal seizures, suppression or paroxysmal fast activity in mesial frontal seizures, and bilateral changes and tendency towards false localization or lateralization with parietal and occipital lobe seizures.,,, Postictal focal slowing aids in lateralizing the epileptogenic zone, though is of limited localizing value within a hemisphere.,
Special Consideration in Infants
Semiology and ictal recordings in infants less than 2-3 years of age often do not follow normal rules of video-EEG interpretation and may mislead as to surgical adequacy. On analysis of seizure semiology of infants rendered seizure free by surgery, the authors suggest that "hypomotor" seizures (decrease in behavioral motor activity with indeterminate level of consciousness and minimal or no automatisms) arose mainly from temporal, parietal and occipital regions, while localized or generalized tonic, clonic and motor phenomena seem to primarily arise from frontal and central regions. Epileptic spasms, however, can arise from either frontocentral or temporo-parietal-occipital regions. The point is that often "generalized" seizures often occur from discrete lesions and hence should not be used as an argument against surgery as a therapeutic option. Interictal and ictal patterns in infancy may also be contrary to conventional wisdom The Cleveland group has shown that in early lesions, either developmental or acquired, bilateral or contralateral interictal or ictal epileptic discharges did not detract from a successful surgical outcome [Figure 1]. This suggests that an MRI lesion is probably the single most important determinant of whether surgery should be pursued.
Limitations of surface EEG recording
Though surface EEG remains fundamental in the presurgical evaluation, it has several limitations in its ability to define the epileptogenic zone. Higher than lower frequency cerebral activity is attenuated by the intervening structures between scalp and cortex, thus, limiting the sensitivity of surface EEG recording. Also, the sensitivity of detecting an epileptic discharge by surface EEG is dependent upon the depth, size, orientation, and duration of a discharge. Deeper cortical and subcortical seizure onset and propagation may not have a surface EEG correlate. Small areas of seizure activity, even if on the surface, may not have a surface correlate until larger regions of cortex are involved. It has been estimated that ictal activity must spread to approximately 6 cm 2 of cortex to be detected by surface EEG, thus, limiting definition of the precise ictal onset zone from the surface.
Another limitation of scalp EEG is that the optimal number and spacing of surface electrodes are uncertain. The currently used 19-32 electrode channels probably grossly under-samples the EEG, and a doubling would help in topographic mapping.
A low signal-to-noise ratio represents another possible limitation of scalp EEG. The noise in an EEG signal can originate from biological sources (artifacts from muscular changes, background EEG, eye movements, etc.) or electrical sources (60 or 50 Hz line noise, electrode motion, etc.). Possible solutions to correct electrical noise are notch filters, bipolar montaging, adaptive filtering, and independent component analysis (ICA). In general, notch filters are the most commonly implemented.
Factors favoring an intracranial electroencephalographic (EEG) pattern being ictal include the following: (1) a sudden change in ongoing background activity, that is (2) rhythmic rather than irregular, (3) focal rather than diffuse, (4) of higher frequency rather than lower at onset, (5) sustained for 10 seconds at the least (6) evolving in frequency, amplitude, and spatial distribution, and (7) associated with a clinical behavioral change. As always there are exceptions to the above, such as the loss or flattening of background activity often referred to as an "electrodecremental" event or seizure onset. The question here is whether the apparent absence of activity relates more to the recording characteristics of our electrodes and amplifiers rather than to an actual secession of activity. Equally important is recognizing EEG changes that are less likely to represent a seizure onset and thus should not be used to localize the focus. Irregular slowing is thought to be a change seen in cortex surrounding the focus rather than a marker of ictal activity. Similarly, regional changes in background rhythms without associated high-frequency discharges are not localizing. These include periodic sharp waves that may be recorded after a neocortical seizure onset.
Abnormal background rhythms should also be looked besidest ictal events. Sick cortex produces a different EEG background than does healthy cortex, and such areas are seizure prone. Unfortunately, the same sick cortex may generate poorly formed seizure activity, as well as background rhythms. The so-called "subtle transformation" from an abnormal background rhythm to seizure activity can be very difficult to appreciate, so it is prudent to pay particular attention to sick cortex when attempting to identify seizure onset.
Nearly everyone agrees that the earliest EEG change is the most important for localization. A frequent problem is how to interpret this change when it appears to be widespread. Is the seizure unlocalized or simply unlocalizable by the electrodes implanted? Spatial undersampling may be the culprit, and it is a major concern when interpreting intracranial EEG. As has been known for some time, the recording properties of intracranial electrodes tend to make them very "nearsighted." Local near-field cortical activity is of significantly higher amplitude than that from cortex only a few millimeters and certainly centimeters away. Successfully, identifying the epileptogenic focus is made more likely if its general location has been determined by noninvasive procedures and if sufficient numbers of electrodes are used to cover this area. ICEEG should not be considered an exploratory procedure. If one has no idea from where seizures may be coming, the limited spatial sampling of this technique is likely to lead to failure or worse, a wrong localization. This is particularly true of neocortical epilepsies which are more diverse in their location and extent than classic mesial temporal epilepsy. Given the expense, time, effort, and potential morbidity of ICEEG, it makes little sense to proceed without a reasonable expectation of obtaining adequate focus localization.
Even if the intracranial EEG changes appear to be focal from our electrode array, can we be certain it represents the seizure origin and not ictal activity that has propagated from some other region where we do not have electrodes? There is no consensus on how this can be achieved reliably. We look for behavioral alterations before EEG change to warn us of this possibility, but neocortical seizures can spread with lightning speed, making this observation less helpful. Some believe that low-voltage gamma activity or focal DC shifts are only observed at the initial focus. Less-optimistic colleagues recount the old adage among intracranial electroencephalographers that "seizures only begin where there are electrodes." Certainly, further investigations are needed to help identify distinguishing criteria or analysis techniques.
Advances in intracranial EEG recording, particularly the increase in electrode numbers, has brought with it problems as well. Appreciating the location of these electrodes relative to the underlying cortex and to each other is often very difficult. Accordingly, the spatial analysis of these intracranial EEG data is often quite confusing when looking simply at traces. In many respects, ICEEG interpretation is at a stage similar to scalp EEG analysis 10 years ago, when quantitative- and computer-assisted techniques were seldom used and localization was based principally on pattern recognition.
Since then there have been significant strides in scalp EEG interpretation using a variety of digital techniques including voltage topography, source localization (such as dipole modeling), and spectral and coherence analyses. Many of these same techniques will probably find useful applications with intracranial EEG. Except during pre-surgical evaluation, we rarely get the opportunity to record directly from the human brain. These are our most valuable data, both by providing diagnostic and localizing information for the patient and by allowing us to advance our knowledge of the electrophysiology of the brain. With these data, we can directly validate and thus more efficiently improve our noninvasive techniques.
Intracranial EEG is obtained when surgery is actively considered, not as an "exploratory procedure". It is obtained by placing strip or grid electrodes in the subdural space. Subdural electrodes measuring 2-4 mm in diameter and made of platinum alloy are embedded in polyurethane and placed either by way of a craniotomy (for grids) or under fluoroscopy through burr holes (for strips). EEG recording (electrocorticography, ECoG) and electrical stimulation (functional mapping) can be performed by way of the electrodes.
The risk for infection and hemorrhage is less than 1%.
There are two approaches to obtain intracranial EEG before resective surgery that are described here.
One-Stage Operative Strategy
A one-stage operation uses ECoG in the operating room immediately before the resection. This strategy uses interictal activity to direct the resection. Generally, ECoG is used to "fine tune" a resection in which there is already relative clarity of the relationship of the lesion to the epileptogenic zone. Interictal ECoG features used to define the epileptogenic zone include (1) consistent focality in interictal spiking, (2) rhythmic features, (3) trains of focal fast beta activity, and (4) focal attenuation of background.,,, ECoG that reveals almost continuous focal rhythmic discharges may not require ictal recordings. The one-stage strategy using ECoG is typically used to tailor resection of a tumor that manifests with seizures. It is also useful when there is congruence between the imaging lesion and the ictal onset zone. A major advantage of a one-stage procedure is the limitation of cost and risk for infection. Awake intraoperative ECoG to allow mapping of eloquent cortex, however, is particularly difficult in children. Furthermore, ECoG is performed in the operating room while the child is under the influence of general anesthesia that may suppress or occasionally paradoxically activate spikes.
Two-Stage Operative Strategy
In a two-stage operation, subdural electrodes are placed during the initial operation and the patient is then moved to a monitoring unit.,,,,, Seizures are captured and the ictal onset zone is defined. Functional mapping is performed if necessary and the relationship of eloquent cortex to the epileptogenic zone is defined. These data then allow a tailored resection at a second operation several days later., This strategy is used when the epileptogenic zone is discrete, imaging lesions are not present, or the planned resection is adjacent to eloquent cortex. Disadvantages with a two-stage strategy include the increased cost and risk for infection. Intracerebral depth electrodes seem to be of limited importance in children and are not discussed here.
Resection of regions most active on ECoG seem to be important for successful outcomes, although removal of all discharging areas may not be necessary to achieve seizure control. Surgical outcomes can be predicted by intracranial EEG.,,,, Intraoperative cortical stimulation elicited a habitual aura in 37% of 29 patients. Patients in whom stimulation elicits a habitual aura have a good prognosis for becoming seizure-free following resection. Lateralizing clinical features were seen in almost two-thirds of patients: contralateral head deviation occurred in half, 59% had visual field defects contralateral to the epileptogenic area, and 64% had abnormal imaging studies ipsilateral to the side of surgery.
Functional cortical mapping plays an important role in tailored neocortical resections., Defining the relationship between eloquent cortex and the epileptogenic zone is important in planning the resection., Typically, a margin of at least 0.5-1 cm is required to spare function. Language cortex can be mapped in children older than 4 years or more recently in children as young as 2.5 years of age.,
MEG is an increasingly utilized technology, able to map eloquent cortical areas of interest, such as language and somatosensory function, as well as to help define the irritative zone. MEG has the additional capability to detect activity from deeper cortical and subcortical structures not otherwise evident on surface EEG. However, the limited study time, compared to long-term video-EEG, may not describe the extent of the irritative zone as well as surface EEG. MEG cannot be performed in very young children, and seizures cannot be routinely captured, thus, limiting its ability to define the ictal onset zone. Nonetheless, MEG appears to be promising, and in at least one series appears to be as efficacious as surface EEG recording.
Surface EEG continues to prove indispensable in the presurgical planning of medically refractory epilepsy patients. This is largely due to its unique capability of describing seizure onset and evolution over the time. At present, newer technologies have yet to prove as effective as surface EEG in defining the epileptogenic zone. Through continued improvement of EEG techniques and newer technologies, and understanding the strengths of each, we strive to increase the power of localization by using these new methods in a complementary fashion. Intracranial EEG has an important but diminishing role in pre-surgical evaluation primarily due to the newer imaging techniques. It should be used highly selectively only in centers with a large experience and expertise. It should be hypothesis driven and should never be used as a fishing expedition. Its primary utility is when there is discordant data, when eloquent cortex is in jeopardy and in non-lesional cases.
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