Neuropsychological Evaluation in Epilepsy Surgery

Transcription

1 Epilrpsia, 38(Suppl. 4):SlS-S23, 1997 Lippincott-Raven Publishers, Philadelphia 0 International League Against Epilepsy Neuropsychological Evaluation in Epilepsy Surgery David W. Loring Department of Neurology, Medical College of Georgia, Augusta, Georgia, U.S.A. Summary: Neuropsychology has played a prominent role throughout the modern era of epilepsy surgery. Neuropsychology, including the Wada test, has been of benefit in documenting dysfunction associated with a lateralized temporal lobe seizure onset. In addition, neuropsychological results have some predicative power regarding seizure outcome following anterior temporal lobectomy. The current status of neuropsychology in patient evaluation and outcome prediction will be presented. Differences between the Wada test, an inactivation procedure, and functional magnetic resonance imaging, which is an activation procedure, will be discussed. This paper will also present preliminary information about the Wechsler Adult Intelligence Scale-111, the recent revision of the most commonly used test of intellectual function, and its effects on neuropsychological performance results. Key Words: Epilepsy- Neurosurgery-Neuropsychology-Wada test-positron emission tomography-single photon emission computer tomography-magnetic resonance imaging-temporal lobe- Intelligence. NEUROPSYCHOLOGICAL EVALUATION IN EPILEPSY SURGERY Neuropsychology has enjoyed a very special relationship with epilepsy, one that has been of mutual benefit to both. In particular, neuropsychology has been privileged to be involved with preoperative and postsurgical evaluations of patients undergoing focal resection of a variety of brain regions to control their epilepsy (1). From the neuropsychological perspective, epilepsy evaluations provide the relatively unique opportunity to positively influence patient care with the goal of significant overall improvement after amelioration of the underlying neurologic etiology. From the epileptic patient s perspective, neuropsychology has demonstrated impairments associated with both epilepsy and its medical management, and has documented the lack of significant cognitive decline in most epilepsy surgery patients (2). Like every other discipline, neuropsychology is a child of time and place (3) and has undergone evolutionary changes since the initial involvement in epilepsy surgery at the Montreal Neurological Institute. Initially, neuropsychological results were used to help determine candidacy for surgery, whether Wada testing would be necessary, and to document postoperative cognitive change (43). However, with the development of better structural Address correspondence and reprint requests to Dr. D. W. Loring at Department of Neurology, Medical College of Georgia, Augusta, GA , U.S.A. imaging capability, more sophisticated EEG and video monitoring, refinement of the Wada test, and the development of positron emission tomography (PET) and single photon emission computer tomography (SPECT), neuropsychology s role in the evaluation of epilepsy patients has shifted. This trend will continue as better functional magnetic resonance imaging (fmri) acquisition sequences and behavioral activation paradigms are developed. However, neuropsychology will continue to provide quantitative measurement of cognitive abilities and thus will contribute to the evaluation and management of epilepsy surgery patients. NEUROPSYCHOLOGY S GOALS Lezak (3) has identified four main purposes for neuropsychological assessment: diagnosis, patient care and planning, rehabilitation and treatment evaluation, and research. The current roles of neuropsychological evaluation of epilepsy patients vary across these purposes. Diagnosis Neuropsychology plays a limited role in epilepsy diagnosis. The diagnosis of epilepsy is based on clinical history, most often with EEGs. Neuropsychology does not identify cognitive profiles uniquely associated with specific etiologic brain changes, and therefore neuropsychological testing provides results that are consistent with rather than diagnostic of. However, personality testing plays more of a diagnostic role in the evaluation S18

2 NEUROPSYCHOLOGY AND EPILEPSY SURGERY S19 of seizures vs. nonepileptic seizures and is probably most useful when EEG/video monitoring fails to record any spells. Patients undergoing evaluation for epilepsy surgery receive neuropsychological evaluation, although neuropsychology results are used differently among surgery centers. Originally, neuropsychology was employed to identify patients believed to be at risk for significant postoperative memory impairment after anterior temporal lobectomy due to bilateral mesial temporal lobe dysfunction. Neuropsychological assessment is also widely employed to help in lateralizing areas of cerebral dysfunction associated with a unilateral seizure onset. In evaluation for anterior temporal lobectomy epilepsy, neuropsychology continues to emphasize memory function. The relationships between left medial temporal lobe and verbal memory (4,6-8), and between the right medial temporal lobe and visualhonverbal memory (5,9) are well described. However, the relationship between right temporal lobe function and visual memory is much more variable (1 0), and the inference to right temporal lobe dysfunction is necessarily less reliable. The relationship between verbal memory and the left hippocampus is robust and has been confirmed by different institutions with different approaches. Neuron loss has been associated with preoperative verbal memory performance in several studies (9,11,12) and with MRI volume (13). In contrast to traditional neuropsychological assessment, which relies on standardized tests of cognitive abilities and yields results that are easily generalizable, the Wada test differs significantly among institutions. Differences exist both procedurally (e.g., dose, type of memory stimuli, side of initial injection) and with respect to interpretation (e.g., which errors are linguistic in origin, pass/fail memory performance criteria). Since its introduction, the memory component of the Wada test has been considered a measure of mesial temporal lobe function. Patients at risk for postoperative amnesia are believed to have significant bilateral mesial temporal lobe disease. If poor Wada memory performance is obtained after injection ipsilateral to the seizure focus, the patient may be at risk for postoperative amnesia, give the presence of contralateral temporal lobe impairment. Wada memory testing is used in many of the same ways as is neuropsychological memory testing, although Wada memory testing is more controversial, in part because of its procedural heterogeneity among centers. Decreased memory performance following contralatera1 injection is a robust phenomenon reported with many different approaches to Wada testing (14-17). Given the strong relationship between Wada memory asymmetries and unilateral temporal lobe seizure onset, a current application of Wada memory testing is diagnostic, serving as one available measure to assist in seizure onset lateralization by demonstrating an associated lateralized dysfunction. Wada memory results are also associated with a variety of quantitative measures of hippocampal structure. Patients with severe hippocampal cell loss are more likely to fail the Wada memory test after injection contralateral to the seizure onset than patients with less severe hippocampal pathology (1 8-20). Some reports have noted a relationship between Wada memory performance and specific hippocampal subfields (20), but these findings have not yet been replicated (18). Similar relationships have been shown between MRI hippocampal measurements and Wada memory. Patients with greater ipsilateralkontralateral volume discrepancies are more likely to display Wada memory asymmetries (13). However, this relationship is not one-to-one. Although both hippocampal volume and Wada memory performance asymmetries are related to laterality of seizure onset, hippocampal volume asymmetries were slightly better at individual patient prediction. However, combining both the functional and structural data provided superior information on lateralization than either measure alone (1 3). Patients without hippocampal asymmetry on MRI may display ipsilateralkontralateral Wada scores that do not differ between sides (2 1). However, significant Wada asymmetries are associated with unilateral hippocampal atrophy. This relationship between Wada memory and hippocampus is unrelated to nonhippocampal temporal lobe structures, because extrahippocampal temporal lobe gray matter scores are unrelated to Wada memory performance (22). Because patients with hippocampal sclerosis tend to have better surgical outcomes (23), and given the relationship between Wada memory and hippocampal volume (1 3), the relationship between Wada memory asymmetries and surgical outcome is not surprising. Wada memory is also related to postoperative verbal memory performance. Patients who decline on verbal memory tasks (at least 1 SD) after left anterior temporal lobectomy have more symmetrical Wada memory scores (1 5). In contrast, patients with Wada memory asymmetries suggesting left unilateral temporal impairment tend to show no decline in verbal memory after left ATL. Good memory performance after amobarbital perfusion contralateral to the seizure focus has been associated with verbal memory decline after left ATL (24). As with other studies of right ATL effects employing visuospatial memory stimuli, no consistent relationship with changes in visuospatial memory after right ATL has been found. Comment Although fmri has been repeatedly and frequently touted as a potential noninvasive Wada, my personal bias is that greater changes in neuropsychological assess- Epilepsiu, Vot. 38, Suppl. 4, 1997

3 s20 D. W. LORING ment of epilepsy patients will be produced by fmri than will changes in Wada testing. This, I believe, results in significant differences in the way in which data are obtained with fmri and Wada. Functional MRI relies on cognitive activation paradigms in which patients perform cognitive tasks. Based on imaging of activated brain regions during task performance compared with a resting or control state, inferences about brain structures contributing to task performance can be made. All regions in the network involved in successful task performance, either directly or indirectly, should show some degree of activation. However, because activity relative to a control state is measured, a risk for including areas not directly involved in the task or of subtracting out the contribution of critical regions is incurred. The Wada test is an inactivation procedure. Brain regions are temporarily inactivated by amobarbital, and the effects of drug inactivation on cognitive performance are assessed. Wada testing addresses the question of whether certain tasks can be performed without the contribution of the affected brain regions, which provides a slightly different answer to a slightly different question. Although a region may be involved in task performance under ordinary circumstances, this region may not be necessary for task performance. Therefore, Wada testing potentially provides a more appropriate technique to model the effects of surgery on postoperative cognitive function. In addition, Wada testing may be more appropriate for younger patients, those who may experience significant anxiety when placed in a magnet, or those who may be unable to reliably perform activation procedures while remaining still. In contrast, functional inactivity associated with a seizure focus may start to supplant the lateralizing value of neuropsychological assessment, particularly given neuropsychology s inconsistent ability to identify memory impairments with the right temporal lobe or the frontal lobe. If procedures can be established that show lack of activation of a single mesial temporal lobe during performance of a memory task associated with a unilateral seizure focus, the lateralizing value of neuropsychology will be significantly lessened. Despite these brain-behavior associations, reliance on neuropsychology to identify lateralized temporal lobe or other regional impairment is likely to change dramatically as fmri techniques are developed and refined. Neuropsychology s contribution to surgical evaluation in epilepsy will shift somewhat, to interdisciplinary collaboration that allows development of appropriate behavioral paradigms that result in the best possible functional neuroimaging. Traditional neuropsychological test results will also be used in this context as a standard against which other functional and behavioral results are compared, for vocationalh-ehabilitation placement and for competency issues. Patient care and planning Neuropsychological testing will remain important for establishing levels of performance for issues surrounding patient competency or for job or school performance. However, no unique evaluation is needed for epilepsy patients. Although not a major goal of neuropsychological assessment at most centers, neuropsychological performance has been related to surgical outcome (25,26). Patients with more focal neuropsychological deficits and less overall cognitive impairment should be expected to have better outcomes with respect to seizure frequency, given the absence of evidence of dysfunction extending beyond the resection zone. Similarly, patients with a Wada memory asymmetry (23,27) are more likely to become seizure-free after temporal lobectomy. Because patients with hippocampal sclerosis tend to have a better surgical outcome (23), and given the relationship of neuropsychological test performance and Wada memory to hippocampal pathology and volume, the relationship between performance asymmetries and surgical outcome should not be surprising. One criticism of neuropsychological testing is that although group effects may frequently be present, it is often difficult to apply neuropsychological test results on an individual patient basis. This, of course, is a fair criticism. However, there has been a recent trend to evaluate preoperative neuropsychological test results with outcome probability estimates. Recent collaborative data from the Bozeman Epilepsy Consortium examining full-scale IQ and seizure outcome after temporal lobectomy revealed a linear relationship between seizure outcome and preoperative IQ. For patients with baseline IQ scores of 75 and below, the odds of becoming seizure-free after surgery were approximately 2: 1. These odds increased to 3: 1 among patients with IQ scores of and were 4:1 among patients with high average IQ scores and above. Knowledge of such base rate information is important if clinicians are to provide empirically derived risk-to-benefit analysis of epilepsy surgery and will undoubtedly be applied with increasing frequency in the future. The relationship between preoperative neuropsychological test performance and postoperative change is a natural area in which neuropsychology can contribute in evaluating the risk-to-benefit ratio associated with surgical resection. The robust group effect of verbal memory decline after left temporal lobectomy has also proved difficult to apply on an individual case-by-case basis. However, this relationship has also been more recently examined on a probabilistic basis (28). Greater postoperative verbal memory decline was present in patients with higher verbal memory scores. For example, 67% of patients with at least average memory performance before surgery displayed a decline of at least 10%

4 NEffROPSYCHOLOGY AND EPILEPSY SURGERY s2 I 6 months after surgery, 44% with low-average verbal memory displayed a 10% decline, whereas only 12% with borderline or below preoperative memory scores experienced a 10% memory performance reduction. Although a portion of this decline undoubtedly relates to statistical regression, it does nevertheless establish a practical approach for counseling patients. Rehabilitation and treatment evaluation As with other patients with neurologic impairment, neuropsychological testing is importact in the rehabilitation process. Accurate characterization of functional status is a requisite for appropriate rehabilitation for functional retraining. The recent interest in quality of life issues in epilepsy and epilepsy surgery has already made a significant contribution to treatment evaluation. We have always engaged in friendly dialogue with other epilepsy institutions regarding the way to code the presence of an aura with no other seizure activity in postoperative results. At the Medical College of Georgia, we consider patients with auras to be seizure-free, because without loss of consciousness and other factors associated with complex and generalized seizures they can drive and others are unaware of any auras. The counter argument, of course, is that auras are not normal events and reflect abnormal brain function in the form of simple sensory seizures. On the basis of quality of life reports, we have modified our seizure outcome scale. Epilepsy patients who are seizure-free after epilepsy surgery report a higher quality of life compared to patients who continue to have postoperative seizures (29). Similarly, significant improvement was noted in personality and psychosocial function in epilepsy surgery patients, but only in patients who were completely seizure-free (30). Patients with auras only did not report improvement in behavioral status. Research In all branches of medicine, there has been recent interest in outcomes of procedure outcomes. However, neuropsychology has been employed to characterize epilepsy surgery outcome throughout the modern era. There is no other speciality of which I am aware that has subjected itself, across the entire discipline, to the scrutiny of comprehensive pre- to postoperative comparison of a wide array of cognitive constructs. At major epilepsy surgery centers, neuropsychological testing is conducted both pre- and postoperatively. Based on epilepsy surgery s commitment to neuropsychological evaluation, we have been able to identify factors associated with cognitive change. For example, patients with good verbal memory are at greater risk for experiencing postoperative memory decline (28). Patients with normalappearing hippocampi are at greater risk for memory decline after left anterior temporal lobectomy (3 1). We also know that the risk to memory after right temporal lobectomy is small. Results of neuropsychological testing are used to evaluate the important factors leading to cognitive change for both language (32) and memory function (8,33) after surgery. Contrast the documented cognitive risk factors associated with temporal lobectomy, or even with nontemporal resections and palliative treatments, with the established risk factors for cognitive impairment after endarterectomy, one of the most common of elective operations. Beyond the gross neurologic deficits associated with surgical complications (34), the frequency and magnitude of cognitive morbidity is much less established (3 1). Consequently, the degree of informed consent is considerably less, and counseling the patient regarding the attendant risks associated with the procedure is necessarily less complete. DEVELOPMENTS IN NEUROPSYCHOLOGICAL TESTING The most commonly employed tests in neuropsychology, the Wechsler Adult Intelligence Scale and the Wechsler Memory Scale, are nearing completion of restandardization processes (WAIS-I11 and WMS-111) with the revisions anticipated in This will impact on the practice of neuropsychology and many centers will soon utilize the new tests. The implications for all consumers of neuropsychological test results will include the recentering of IQ back to 100. If recent IQ test restandardizations are a guideline, the change may be as large as 7 to 8 IQ points. Therefore, to the degree that reported IQ may be used as a criterion for surgery, the difference associated with a new IQ measure will need to be considered. However, these data have not been presented, and the average difference between the WAIS-R and WAIS-I11 is presently unknown. The floor of the WAIS-111 has also been extended downward. Where the lowest scores with the WAIS-R were generally in the 40s, scores from the WAIS-111 extend down to the 30s. Therefore, lower IQ scores will be present for patients in the lower end of the distribution, although these only reflect the difference in standardization employed between the two test versions. Although there will be many similarities between the WMS 111 and its progenitors, some difference in specific item content (e.g., new stories) may produce changes in test sensitivity (better or worse), and greater confidence in interpreting test results will require reestablishing the expected relationships with new patient series. One major strength of these two new tests will be co-norming, in which a portion of the standardization sample receives both tests. One limitation of previous versions of the Wechsler scales, and of many neuropsychological tests in general, has been the formulation of standardized norms based on different samples. Thus, for

5 s22 D. W. LORING example, the 50th percentile on one test may not necessarily correspond to the same absolute performance level associated with the 50th percentile of another test. What is sacrificed with this approach will be novelty and diversity of approaches to memory assessment. To paraphrase an old statement made about intelligence, memory will become that quantity assessed by the WMS-111. Furthermore, with the increasing regulation of the American health care market place, other approaches to assessment may ultimately not be reimbursed if a single approach to assessment becomes the accepted standard of practice. Neuropsychology may become homogenized at the expense of innovative approaches to characterize cognitive abilities as clinical research is forced into a dichotomy of pure clinical vs. pure research. FUTURE DIRECTIONS There has been heightened sensitivity to how a meaningful decline in memory function is characterized, and this shift will continue. Although acknowledged by authors, postoperative declines of lo%, or 1 SD, represent arbitrary choices used to begin to characterize change with respect to an objective criterion. However, effort will continue to be exerted to determine at what point psychometric change is meaningful on a day-today basis. In addition, the degree of change will not be the same for all individuals or necessarily for all levels of baseline performance. These will be areas that will be more carefully explored in the near future. The other area that is ripe for investigation is the longterm cognitive outcome of temporal lobectomy. Memory impairment associated with epilepsy surgery continues to improve for as long as 5 to 10 years (35). What is not known, however, is the long-term affect of temporal lobectomy on memory. Many patients who had surgery at age 20 or 30 are entering senescence without knowing if there may be a possible negative interaction of temporal lobectomy effects with normal age-related memory changes. Similarly, the effects of remote seizure activity on age-related memory change have not been addressed. SUMMARY Neuropsychological testing and Wada evaluation will continue to play a prominent role in the evaluation of epilepsy surgery patients. In many patients, these techniques not only assess functional deficits with known cerebral lesions but also contribute to establishing laterality of seizure onset and provide an estimate of the risk to memory after anterior femoral lobectomy. With both approaches, however, there will continue to be procedural refinements based on correlations with MRI volumetry, fmri, and MRI spectroscopy, and also correla- tions with long-term cognitive, vocational, and seizure outcome. New noninvasive measures of brain function, including fmri, are eventually likely to provide much of the same information as currently derived from Wada testing. However, it remains to be established if a procedure that relies on activation of cognitive functions can provide comparable data to the Wada test, which is an inactivation procedure and therefore more directly models the effects of surgery on cognition. Nevertheless, there continues to be an important need for further refinement in the ability to predict and avoid significant postoperative cognitive deficits. Greater understanding of the interaction between cognitive, psychiatric, and quality of life variables, and how these factors contribute to the overall outcome of epilepsy surgery, will provide a richer description of postsurgical results than simply reporting postoperative seizure frequency. Delineation of these issues will contribute to improved care of patients undergoing epilepsy surgery. 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