Electroencephalography and clinical Neurophysiology, 1989, 73:381-388 Elsevier Scientific Publishers Ireland, Ltd.
The evaluation of patients with intractable complex partial seizures R o n a l d P. L e s s e r
a,b,c, R o b e r t
S. F i s h e r a,b,c a n d P e t e r K a p l a n a,b,d
a Johns Hopkins Epilepsy Center, and Departments of b Neurology and ¢ Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, AID 21205 (U.S.A.), and d Department of Neurology, Francis Scott Key Hospital, Baltimore, MD 21205 (U.S.A.) (Accepted for publication: 5 June 1989)
Summary Conceptual advantages, together with advances in both technique and technology, have considerably altered the approach to intractable epilepsy over the past two decades. Appropriate utilization of these advances allows our evaluation of patients with intractable seizures to be much more precise and specific than was once the case and allows us to improve considerably our ability to treat patients with intractable epilepsy. We propose an algorithm for the evaluation and treatment of patients with intractable complex partial seizures. Other forms of intractable epilepsy may benefit from similar diagnostic and therapeutic approaches.
Key words: Complex partial seizures; EEG evaluation
Epilepsy is a disorder requiring clinical diagnosis. Although the best initial diagnostic methodology is the evaluation by an experienced clinician of a well-described set of behaviors, epilepsy monitoring techniques extend the eyes and ears of the clinician. Over the past two decades enormous progress has been made in our ability to acquire and evaluate data regarding patients with seizure disorders. Recently developed microprocessor based techniques can further serve to usefully reduce, analyze and present massive volumes of EEG data. Prolonged EEG monitoring has many other purposes, including the evaluation of candidates with other seizure types who may require other surgical procedures. This discussion, however, will focus on the evaluation of the candidate for surgery for the control of intractable complex partial seizures. Intensive EEG monitoring is a new technique, and several questions can be raised about its use.
Correspondence to: Ronald P. Lesser, M.D., The Johns Hopkins Hospital, Department of Neurology, Meyer 2-147, 600 N. Wolfe Street, Baltimore, MD 21205 (U.S.A.).
First, who is a suitable candidate for intensive video-EEG monitoring? Second, what is the best method for staging non-invasive and invasive monitoring studies? Third, what are the likely outcomes from monitoring? Video/EEG is an expensive and time consuming procedure, but several studies (Porter et al. 1977, 1985; Theodore et al. 1984) have shown a significant decrease in seizure frequency following discharge from intensive inpatient monitoring and treatment. Drug toxicity and social adjustments also were much improved at follow-up. Whereas the evaluation of intractable seizures once occurred by means of EEG recordings of relatively short duration using techniques varying little from those utihzed in the routine outpatient laboratory, contemporary technology allows us to prolong the monitoring of patients over days or weeks, obtaining continuous clinical and video information (Frost 1979; Kamp and Lopes da Silva 1982; Gotman 1985; Principe and Smith 1985; Samson-Dollfus and Senant 1985). There is also considerable interest, and some evidence of progress, in developing microprocessor based techniques to help in the acquisition and interpre-
0013-4649/89/$03.50 © 1989 Elsevier Scientific Publishers Ireland, Ltd.
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tation of this information. These successes permit us the opportunity to reexamine progress made, determine ways in which this progress may be directed towards improving patient care, and develop plans for improving current methods and implementing new techniques for the future.
Who is a candidate for intensive monitoring? It is important to keep in mind that although we now often emphasize the 'high tech' aspects of medical care, the cornerstone of the care of patients initially should be decidedly 'low tech.' The crucial first step in the evaluation of patients with intractable seizures therefore must be the taking of a history and performance of a physical and neurological examination so that an initial diagnosis can be made or confirmed. A routine E E G may
HISTORY, EXAMINATION,INITIAL DIAGNOSIS
T ROUTINE EEG CONFIRM DX
MONITOR DIAGNOSE EPISODES
MONITOR SURGICAL CANDIDATE? EEG LOCALIZATION INTERICTAL/ICTAL
NOT A SURGICAL CANDIDATE
VIDEO/EEG TIMESUCING SPATIAL DEFINITION
FUNCTIONALASSESSMENT NEUROPSYCHOLOGY BATTERY
BEHAVIORALOBSERVATION AMOBARBITAL (WADA) TEST IMAGING CT, MRI, PET
SURGICAL CANDIDATE NO EXCISION
NO IMPLANTED ELECTRODES IMPLANTED ELECTRODES DEPTH/SUBDURAL,/EPIDURAL STANDARD VS TAILORED PLACEMENT EEG LOCALIZATION FUNCTIONAL ASSESSMENT
Fig. 1. Flow diagram of the decision processes involved in evaluating patients with a history of intractable complex partial seizures.
confirm the clinical impression, help document the seizure type, and therefore help determine the appropriate anticonvulsants. ]-he clinician can then decide whether these medications have been exploited to the fullest. When the routine recordings confirm the clinical impression of epilepsy and support the diagnosis of a particular seizure type. then management usually may proceed without intensive monitoring. It is particularly important to keep in mind that only definite epileptiform discharges spikes, sharp waves, and spike-andwave complexes as well as specific ictal patterns can confirm the diagnosis of epilepsy. Non-specific patterns such as irregular sioux activity should not be taken to confirm such a diagnosis. It also i,, very important that the electroencephalographer be aware that normal variant discharges can be, and often are, confused with patterns of trul~ epileptiform character (Reiher and Lebel 1977: White et al. 1977: Klass and Westmoreland 1985: Westmoreland and Klass 1986: Santamaria and Chiappa 1987). Imitators of epilepsy include: psychogenic events, hyperventilation attacks, atypical migraine, syncope, transient ischemic attacks, sleep disorders, hypoglycemia and intermittent movement disorders. Some of these diagnoses may at times be suggested by the findings in the routine EEG but, in other cases, intensive monitoring is necessary to document the etiology of the clinical episode. For example, routine recording may suggest the presence of a syncopal disorder if a cardiac arrhythmia is noted (Gastaut and Fischer-Williams 1957: Fisher 1979: Kapoor et al. 1983). Another possibility is that psychogenic seizures will be demonstrated (either in the routine record or during intensive monitoring) because of the occurrence of a clinically typical episode of unresponsiveness in association with a normal EEG during the episode (Gates et al. 1983, 1985: Krumhoitz and Niedermeyer 1983: Lesser et al. 1983: Lesser 1986). When a diagnostic alternative to epilepsy suggests itself in the initial history, physical, or electroencephalogram these possibilities should be thoroughly explored. It is particularly important to keep in mind that, while at one time it was felt all or at least most patients with psychogenic seizures had epilepsy, more recent evidence has
COMPLEX PARTIALSEIZURE EVALUATION suggested that this occurs in only 10-20% of such patients (Krumholtz and Niedermeyer 1983; Lesser et al. 1983; Lesser 1986). There are several implications of this. First, a patient who is noted to have psychogenic seizures does not necessarily need to remain on anticonvulsants if there is no evidence to definitely support the presence of epilepsy. Second, however, the possibility of an additional diagnosis must always be considered. Third, specific confirmatory information should be sought, and if possible found, before pursuing the treatments for this second diagnosis. Although situations of course exist where the diagnosis remains uncertain and where it may be appropriate to treat for a diagnosis in a presumptive fashion, in most situations continued treatment for epilepsy when this is not present may, in fact, complicate the management of the patient's psychogenic seizures. When the possible presence of two diagnoses presents an important patient management issue, prolonged monitoring can be obtained in an effort to definitely support, or definitely exclude, the diagnosis of a second illness (Kaplan and Lesser 1990). Monitoring may further be useful when the seizure type is uncertain. Atypical absence can be difficult to distinguish by history from complex partial seizures. Institution of proper medication, for example valproic acid for absence and carbamazepine or phenytoin for complex partial seizures, may depend upon video-EEG documentation and then categorization of a clinical event. Once a diagnosis has been confirmed in a patient, anticonvulsants can be given in the appropriate sequence. It is important to keep in mind that epilepsy evaluation units often have had patients referred for surgery who are found, on reflection, to have seizures controllable by medication. There is no question, however, that a great many patients with complex partial seizures have episodes which cannot be controlled by anticonvulsants. Because of this, a fourth reason for intensive monitoring is to evaluate patients for whom epilepsy surgery is a potential therapeutic option. For these individuals it is crucial to secure a diagnosis of epilepsy, classify the seizure type, and localize the focus for the neurosurgeon. An important reason for performing prolonged monitor-
383 ing is the need to record and evaluate not only interictal activity but also actual seizure episodes. Interictal and ictal EEGs do not always coincide and, when properly evaluated, provide complementary information regarding appropriate clinical interventions and their likely efficacy. Video documentation is necessary so one can be certain that one treats the spells that are causing the patient's clinical problems. As in other branches of medicine, evaluation should proceed from the less invasive to the more invasive investigative modalities, as guided by clinical judgment. For example, some patients benefit from outpatient ambulatory cassette monitoring, particularly in circumstances where diagnosis of a cryptogenic loss of awareness or alteration of consciousness is needed (Ebersole and Bridges 1986). Such ambulatory monitoring is generally not sufficient for presurgical evaluation because of limitations in numbers of leads and difficulty in interpreting artifacts in ambulatory recordings. In candidates for surgery a further role of the electroencephalogram comes into play: seizure focus localization in order to guide a surgical approach (Engel 1987).
Issues in methodology of monitoring (1) Although the eventual goal may be an invasive procedure, the initial approach can and should be intensive non-invasive monitoring (Kaplan and Lesser 1990). (2) Video-EEG monitoring is of clear value in correlating the clinical behaviors of patients during seizures with the electroencephalographic changes which accompany them (Ives et al. 1976; Porter et al. 1985). (3) Time slicing allows precise correlations between ictal clinical behaviors and EEG changes. One can determine whether the EEG changes precede the clinical changes and how the two correlate with one another. These correlations often provide clues regarding the site of origin of clinical ictal phenomena. Time slicing may also be of value, when assessing the 24 h record, in determining whether there is an clinically relevant cyclicality of epileptiform activity.
(4) Increased spatial definition of a patient's seizure focus may be of similar value. During non-invasive evaluations this can be accomplished by adding additional basal electrodes to patients with temporal or basal-frontal lobe epilepsy (examples include the so-called Silverman or T 1 / T 2 electrodes and sphenoid electrodes). Additional electrodes placed between and below the standard electrodes of the international 10-20 system are of value in confirming epileptiform activity over additional channels, thus increasing the certainty of event definition (Lueders et al. 1982; Chatrian et al. 1985; Lesser et al. 1987a). The recording of such activity with additional electrodes gives greater spatial definition of the distribution of this activity over the scalp and, therefore, a greater possibility of inferring what the likely source of the activity might be (Morris et al. 1986). Electrodes such as sphenoid leads (Rovit et al. 1960; lves and Gloor 1977) may be particularly useful since they are more clearly subcortical. It is important to keep in mind that they remain outside of the skull, however. Moreover, recordings from sphenoid leads often remain relatively unchanged as the wires are gradually pulled back from their initial position near the foramen ovale and therefore move towards the skin surface (Wilkus and Thomson 1985); and similar recordings often can be obtained from the skin surface itself at the usual site of sphenoid electrode insertion (Sadler and Goodwin 1986). This is not meant to detract from the usefulness of sphenoid electrodes but rather to remind us that we must put this usefulness into its appropriate perspective: a prime value of these electrodes is their basal position; a second value may derive from their basal-mesial position. An alternative electrode therefore has been proposed by Wieser. who places leads within the foramen ovale itself (Wieser and Moser 1988). These have the advantage of recording activities less attenuated by bone and by distance from the cortical base, but placement carries a higher risk of morbidity. Finally, magnetoencephalography (Sutherling et al. 1988) is currently an investigative technique. If perfected, however, it may be able to assess intracranial activity, including from deep areas such as the hippocampus and amygdala, non-invasively.
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There has been discussion regarding what the best lead may be for the assessment of certain kinds of seizures. An alternative formulation in terms of the preceding discussion however is: how can we best and most safely use the available electrodes to assess the specific problems of specific patients. This search for greater diagnostic accuracy often results in a need for an increasing number of channels to monitor the activity found. Because of this, monitoring units now increasingly have available 32, 64, or even more channels to permit increased spatial definition of a patient's seizure focus. Interictal spike maps are extremely useful in localizing seizure foci and are also helpful in determining the extent of the potentially epileptogenic field (Lueders et al. 1982). However, occasional individuals will have seizure origin remote from the site of maximal interictal discharge. Since consistency of origin of seizures is an important predictor of surgical success, several seizures should be recorded. There is no unanimity on the numbers of seizures and a goal of a specific number of seizures is not always feasible, because patients' seizure frequencies vary. Overall, consistency of localization of interictal and ictal data may be the best confirmation of the site of seizure onset. It is a common experience for individuals not to have seizures when in a monitoring unit. Activation techniques such as sleep deprivation and withdrawal of anticonvulsant medication may provoke seizures for analysis in these situations. Withdrawal seizures may occasionally arise from an atypical location (Engel and Crandall 1983), but this occurrence appears to be relatively rare; generally withdrawal seizures appear to be predictive of the site of the spontaneous seizure focus (Spencer et al. 1981; Marciani and G o t m a n 1986)~ (5) A second concern relates to 'functional localization.' Neuropsychological testing, including intracarotid sodium amobarbitol (Wada) testing, helps in determining overall levels of cortical functioning and in determining whether specific cortical regions are functioning optimally. This information can sometimes be used to infer that the area which is not functioning optimally may also be, or be near, an area of epileptogenesis. Also, the presence of functional impairment of
COMPLEX PARTIAL SEIZURE EVALUATION
one area of the brain (e.g., possible memory impairment in the hippocampus) often cautions us to avoid tissue removals from homologous areas on the opposite side. (6) There are several possible results of this monitoring. (a) One possibility is that the epileptogenic focus will be found to reside clearly in an area which is resectable and not contiguous with any crucial cortical regions which one would wish to avoid during resective surgery. In such cases cortical resection can take place without any further EEG investigations. (b) A second possibility occurs when a focus appears to be mesial in origin but the precise mesial site or side is uncertain. In this situation there is a clear need to perform electrode implants. For many years invasive studies were done by implantation of depth electrodes through burr holes or twist drill holes (stereoelectroencephalography), as pioneered by Talaraich and Bancaud (Talairach et al. 1958; Talairach and Bancaud 1973, 1974; Spencer 1981; Engel and Crandall 1986). Depth wires may show seizure origin in deep limbic structures or in the supplementary motor area, when scalp recordings are relatively unimpressive. Because of this, depth electrodes are able to lateralize activity when origin is unclear from scalp electrodes (Spencer et al. 1981; Sammaritano et al. 1987). Complications of depth electrodes are few, but hematomas and infections can result. The main practical limitation is a sampiing problem, since only a relatively small number of sites may be assayed by penetrating wires. Additionally, it is more difficult to stimulate and perform detailed physiologic studies on cerebral cortex with depth wires. The advantage of depth electrodes is that they can be placed through relatively small burr holes, under stereotaxis and under local anesthesia. Their disadvantages relate to problems attendant to penetration of brain tissues by electrodes and issues related to the relatively small area of tissue sampled by any one depth electrode. An additional theoretical concern relates to whether normal variant discharges in the hippocampus may more closely resemble epileptiform discharges than is the case in neocortex, making interictal activity in this area difficult to
utilize for localization of the epileptogenic focus (Suzuki and Smith 1987). Another useful technique employs epidural or subdural electrode strips or arrays (Goldring 1978; Lesser et al. 1984a, b; Wyler et al. 1985; Liaders et al. 1987). Subdural strips inserted through burr holes can allow considerable neocortical sampling on each side, but may not provide as extensive spatial coverage of cortex in any one area as can occur with the larger subdural grids. In addition, although both strips and grids can be placed on the floor of the middle fossa in order to sample perilimbic neocortex, they do not directly assess the hippocampus. Despite this potential disadvantage, experience has shown that abundant epileptiform activity occurs in perilimbic neocortex (Burnstine in prep.; Ltiders et al. 1989) and that such activity can be utilized to determine the location of epileptogenic cortex. In addition, the normal variant discharges which, in hippocampus, can be confused with interictal-spikes seem to be less common in neocortex. For all of these reasons, subdural electrode arrays appear to be a very accurate method of determining the spatial relationships of epileptogenic foci in some detail. Subdural electrodes also have the advantage of not penetrating cerebral tissue but, as with depth electrodes, infections may result from their implantation. Indications for subdural versus depth electrodes versus a combination of these two modalities have not clearly been established and each of these different invasive approaches shows good results in the hands of teams experienced in their use (Ojemann and Engel 1987). In our monitoring unit we employ subdural arrays to map out the lateral or peri-hippocampal extent of a seizure focus and to map functional regions. We employ depth wires, or at times subdural strips or small subdural grids, to answer lateralization questions, and to differentiate certain instances of anterior temporal versus deep frontal seizure origin. Either depth and subdural electrodes could be utilized to clarify issues related to mesial or basal-mesial temporal or frontal discharges. In part the best electrode to select may depend upon the exact presumed site of epileptogenesis with related mechanical concerns about the best way ' t o get to
the area' which must be monitored. (c) The third possibility is that the focus is, or appears to be, near a region controlling, for example, important motor, sensory or speech functions. In such an instance, it is often important to determine exactly what the relationship between the epileptogenic region and the functional region might be. Both intraoperative stimulation and extraoperative stimulation can be utilized for this purpose. Penfield and Rasmussen (Penfield and Jasper 1954; Penfield and Rasmussen 1957; Ojemann 1978, 1983) and their collaborators pioneered the use of this technique in the operating room. The advantages of intraoperative monitoring are those of a resection decision made under direct cortical visualization at the time of surgery as well as those of avoiding a second operation, and of avoiding the potential risks of implanted electrodes. However, a relatively short time which can be devoted to functional assessments due to surgical and anesthetic considerations. Issues also exist regarding (a) whether patient cooperation can be optimal when the patient must be assessed on the operating table under local anesthesia, and (b) whether the testing methodologies can always be optimized in this setting. As a corollary to these concerns, certain patients may not do well under local anesthesia in the operating room and may therefore be best considered for subdural electrode implantation. On the other hand, some patients who may not be optimally cooperative in the operating room also might not be the best candidates for subdural or depth electrode implantation because of their inability to cooperate with postoperative electrode care. With subdural electrodes, relationships among epileptogenic regions and between these and functionally important regions of cortex can be determined in an extraoperative setting (Liiders et al. 1987; Lesser et al. 1987b). In this respect, stimulation via subdural electrodes represents an extension into chronic recordings of techniques previously employed in an acute setting. Goldring (1978) pioneered developments in this area, using epidural electrodes. These can map epileptogenic tissue in a manner similar to subdural arrays (for
R.P. LESSER ET A t .
epidural stimulation, dura must be denervated or the studies are painful), but extraoperative stimulation is now more commonly performed using subdural arrays. One advantage of stimulation in a chronic setting is that stimulation parameters can be optimized at each electrode site: there is evidence that, for example, the intensities needed can vary from site to site and from one stimulation period to another when using this technique (Ajmone Marsan 1972: Lesser et al. 1984a.b. 1987b). It is important to keep in mind that electrode diameters are generally larger when subdural electrodes are utilized than is the case when stimulating with intraoperative techniques. Because of this, at a given current setting, current densities will be smaller (Gordon in prep.). A second advantage is that the patient is in a hospital bed or in a testing room, either of which is likely to be a more comfortable setting than the operating room table. The chronic setting can be a more relaxed one for the patient: the patient can take a break when necessary, for example if he or she becomes tired or hungry. The patient can ask questions about the procedures during the testing session. Finally, crucial findings can be verified during a separate testing period. (d) A fourth possibility is that the general focus localization is known but its site appears to be unusual. Subdural or epidural electrodes can be of value in this situation as well since the large number of electrodes which can be placed allows spatial mapping in considerable detail (Lesser et al. 1987b; Blom et al. 1989). (7) Both electrode implantation and cortical resections can occur in either a tailored or standard manner. Although both have their proponents, there are reasons to believe that seizure producing areas may in fact vary somewhat among individuals so that some tailoring of electrode placement and surgical resection may be of benefit to the patient. Moreover, the removal of cortical tissue can have cognitive consequences and these may be greater when more is removed (Ojemann and Dodrill 1985). Either smaller (Wieser 1988) or larger resections may be appropriate in a given patient.
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