Neuropsychological Changes After Surgical Treatment for Temporal Lobe Epilepsy

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1 Epilepsia, 42(Suppl. 6):4 8, 2001 Blackwell Science, Inc. International League Against Epilepsy Symposium I Neuropsychological Changes After Surgical Treatment for Temporal Lobe Epilepsy *Manabu Wachi, Masaru Tomikawa, Masafumi Fukuda, Shigeki Kameyama, *Kazuhiko Kasahara, *Mutsuo Sasagawa, Seiko Shirane, Osamu Kanazawa, Mihoko Yoshino, Satsuki Aoki, and Yoshiaki Sohma Divisions of *Psychiatry, Neurosurgery, Pediatrics, and Psychology, National Nishi-Niigata-Chuo Hospital, and Department of Neurology, Brain Research Institute, Niigata University, Niigata, Japan Summary: Purpose: The effect of unilateral temporal lobectomy on seizure frequency is well recognized, but little is known about the neuropsychological changes that occur after surgical treatment. We assessed neuropsychological status in 26 patients with an average age of 35 years before and after unilateral temporal lobectomy for medically intractable TLE. Methods: Neuropsychological examination to assess cognitive function, memory, attention, visuospatial analysis, language, and emotional functions was performed preoperatively and at 1 month and 1 year after the surgery. Results: At both 1 month and 1 year after the surgery, the patients had improved scores, compared with the preoperative scores, on the Wechsler Adult Intelligence Scale Revised (WAIS-R: verbal IQ, performance IQ, and full-scale IQ), Wechsler Memory Scale Revised (WMS-R: verbal, general, and delayed paired associates memory), and Raven Colored Progressive Matrices. In the Minnesota Multiphasic Personality Inventory (MMPI), significant decreases were observed at 1 year after the surgery in the scores for infrequency, hypochondriasis, psychasthenia, and schizophrenia. Patients in whom the seizures had been relieved postoperatively also had improved scores on the WAIS-R, WMS-R, and Raven Colored Progressive Matrices. Conclusions: These data suggest that neuropsychological improvement postoperatively is influenced by the reduction in the frequency of seizures after surgery. Key Words: Intractable temporal lobe epilepsy Surgical treatment Neuropsychological assessment WAIS-R WMS-R. Unilateral anterior temporal lobectomy is widely acknowledged to be effective for entirely eliminating or reducing the frequency of intractable seizures in patients with temporal lobe epilepsy (1,2). Cognitive functions have been reported to remain stable or even to improve after successful surgery (3). However, greater deficits in learning skills and memory functions were sometimes observed (3,4). Therefore, it is important to thoroughly assess neuropsychological status, before and after epilepsy surgery. In the present investigation, patients who underwent unilateral temporal lobe surgery were interviewed preoperatively and at 1 month and 1 year after the surgery for a comprehensive neuropsychological assessment. Address correspondence and reprint requests to Dr. M. Wachi at the Division of Psychiatry, National Nishi-Niigata-Chuo Hospital, Masago , Niigata , Japan. SUBJECTS AND METHODS Subjects The subjects consisted of 26 patients aged 16 years or older who underwent anterior temporal lobectomy, including excision of the hippocampus (n 20), selective amygdalohippocampectomy (n 1), or temporolateral lesionectomy (n 5), at the National Nishi-Niigata- Chuo Hospital between 1995 and 1998, for the treatment of intractable seizures of temporal lobe origin. Table 1 summarizes the relevant preoperative characteristics of the subjects. All patients underwent comprehensive preoperative evaluation, including prolonged video-eeg scalp monitoring, neuroradiologic [computed tomography (CT), magnetic resonance imaging (MRI), singlephoton emission CT (SPECT)], and neuropsychological studies. The patients also underwent intracarotid amytal testing (IAT) to determine the cerebral dominance for speech. IAT indicated complete left hemispheric lan- 4

2 NEUROPSYCHOLOGICAL CHANGES AFTER TLE SURGERY 5 Characteristics TABLE 1. Patient characteristics Total (n 26) SF (n 16) NSF (n 10) Sex 12F,14M 6F,10M 6F,4M Mean age at surgery 34.7 yr (10.7) 34.1 yr (11.0) 35.6 yr (10.7) Duration of epilepsy 21.2 yr (9.2) 20.1 yr (9.0) 23.0 yr (9.8) Onset of epilepsy 13.0 yr (5.2) 13.3 yr (5.9) 12.4 yr (4.0) Hand dominance 25 right, 1 left 16 right 9 right, 1 left Side of surgery (R:L) 13:13 6:10 7:3 No. of AEDs: Preoperative 2.2 (0.7) 2.0 (0.7) 2.5 (0.5) Postoperative (1 yr) 1.8 (0.9) 1.5 (0.7) 2.4 (1.0) Values represent the means with the standard deviation indicated in parentheses. F, female; M, male; R, right; L, left, SF, seizure free; NSF, not seizure free; AEDs, antiepileptic drugs. guage dominance in 13 patients with right-sided and 13 patients with left-sided resection, complete right hemispheric language dominance in one patient with leftsided resection (the left-handed patient), and a bilateral language distribution pattern in one patient with leftsided resection. The patients were classified into two groups postoperatively on the basis of whether their neurologist determined them to be seizure free (SF; n 16) or not (NSF; n 10). The SF group included those who did not have any complex partial or grand mal seizures in the year after the surgery. Auras did not exclude patients from the SF group. Assessment of neuropsychological function The neuropsychological status was assessed in all patients preoperatively and at 1 month after surgery by the tests detailed later. Twenty-three of the 26 patients returned for a 1-year follow-up after the surgery and were assessed again with the test battery. Neuropsychological testing included Wechsler Adult Intelligence Scale Revised (WAIS-R), Wechsler Memory Scale Revised (WMS-R), Story Recall Test, Benton s visual retention test, Rey Osterreith figure test, Raven Colored Progressive Matrices, Western Aphasia Battery (WAB), and Minnesota Multiphasic Personality Inventory (MMPI). Data were analyzed for statistical significance using Student s t test to compare the differences between the preoperative and postoperative scores of the patients. RESULTS Surgical outcome The study sample included 12 female and 14 male patients, and all but one were right-handed. There were 13 right- and 13 left-sided resections. In the year after the surgery, 16 (62%) of the 26 patients were SF, but two still reported occasional auras. In 10 of the 16, anticonvulsant medication was tapered off, and eight of the 16 received only monotherapy. In six of the 10 patients in the NSF group, the seizure frequency was reduced by 90% compared with the preoperative level. In two, the seizure frequency decreased by 75 90% compared with the preoperative seizure frequency. In the remaining two, the seizure frequency remained the same as that before the surgery. None of the patients had any surgical complications. Neuropsychological function Cognitive function All 26 patients underwent intelligence testing preoperatively and 1 month after the surgery. Only 23 of the 26 underwent the testing at 1 year after the surgery. At 1 month after the surgery, we observed significant increases in the verbal IQ compared with the preoperative scores (mean, 85.1 vs. 89.3; p < 0.001). Performance IQ scores in the patients increased at 1 month and 1 year after the surgery compared with the preoperative scores (mean, 89.0 vs. 95.5; p < 0.05; and mean, 89.0 vs. 95.0; p < 0.01, respectively). Full-scale IQ scores increased at 1 month and 1 year after the surgery (mean, 85.5 vs. 91.0; p < 0.01; and mean, 85.5 vs. 88.4; p < 0.01, respectively). No statistically significant differences were observed between the verbal IQ scores determined preoperatively and those determined 1 year after the surgery (mean, 85.1 vs. 85.7) (Table 2). Verbal, performance, and full-scale IQ scores increased in the SF group at 1 year after the surgery, compared with the scores determined preoperatively (Table 3). In the NSF group, the mean scores of verbal, performance, and full-scale IQ at 1 year after surgery were not significantly different compared with the scores determined preoperatively. Memory function The preoperative and postoperative memory function data in the 26 patients are summarized in Table 2. Memory functions were assessed by use of Story Recall Test, Benton s Visual Retention Test, Rey Osterreith Complex Figure Test, and WMS-R. Student s t tests performed for all the memory function tests, except WMS- R, indicated the absence of any significant differences between the preoperatively determined scores and the scores determined at 1 month and 1 year after the surgery.

3 6 M. WACHI ET AL. TABLE 2. Mean test scores (and SD) in neuropsychological tests of the patients Test Presurgery 1 mo postsurgery 1 yr postsurgery WAIS-R VIQ 85.1 (13.6) 89.3 (13.8) c 85.7 (14.1) PIQ 89.0 (15.8) 95.5 (17.3) a 95.0 (18.0) b FIQ 85.5 (14.4) 91.0 (16.1) b 88.4 (15.8) b WMS-R Verbal 80.9 (15.4) 91.9 (20.5) b 90.1 (17.0) b Visual (18.3) (16.8) (15.0) General 87.4 (13.9) 97.1 (21.4) a 94.2 (17.7) a Attention 86.5 (16.6) 88.8 (18.8) 89.3 (20.4) Delayed paired associates 90.3 (14.9) 99.1 (21.1) b (17.6) c Rey complex figure 61.7 (19.4) 66.5 (20.8) 63.8 (20.9) Benton s visual retention test 7.5 (1.6) 7.4 (1.7) 6.8 (2.1) Story recall test 12.1 (4.1) 12.9 (3.4) 12.4 (3.6) Raven Progressive Matrices 32.7 (3.2) 33.7 (2.4) a 34.2 (2.1) c WAB 96.6 (4.2) 97.3 (4.6) 97.7 (3.7) Values represent the means with the standard deviation indicated in parentheses. a p < 0.05, b p < 0.01; c p < compared with the presurgical score. In 19 patients, the scores of WMS-R, including the subtests of verbal, visual, general memory, attention/ mental-tracking composite, and delayed paired association tests, were obtained both preoperatively and postoperatively. Preoperative and postoperative visual memory scores and attention/mental-tracking composite scores did not differ. Verbal memory scores of the patients at 1 month and 1 year after the surgery compared with the preoperative scores increased (mean, 80.9 vs. 91.9; p < 0.01; and mean, 80.9 vs. 90.1; p < 0.01, respectively), as did general memory scores (mean, 87.4 vs. 97.1; p < 0.05; and mean, 87.4 vs. 94.2; p < 0.05, respectively), and delayed paired associate scores (mean, 90.3 vs. 99.1; p < 0.01; and mean, 90.3 vs ; p < 0.001, respectively) (Table 2). In only the SF group were there significant increases in the verbal memory, general memory, and the delayed paired associate scores of the patients at 1 year after the surgery compared with the scores determined preoperatively (Table 3). MMPI Although all 26 patients had MMPI assessment preoperatively and at 1 month after the surgery, only 21 patients had MMPI assessment at 1 year after the surgery. In all the scales, there was a tendency toward lower scores at 1 year after the surgery (Fig. 1). Significant decreases were observed in the scores for infrequency (p < 0.05), hypochondriasis (p < 0.01), psychasthenia (p < 0.05), and schizophrenia (p < 0.05) at 1 year after the surgery compared with the scores determined preoperatively. There were no significant differences in the MMPI scores between the SF and NSF groups at 1 year after the surgery (data not shown). Other neuropsychological functions Preoperative and postoperative WAB scores did not differ. The Raven Colored Progressive Matrices scores of patients both at 1 month and 1 year increased in relation to the preoperative scores (mean, 32.7 vs. 33.7; p < 0.05; and mean, 32.7 vs. 34.2; p < 0.001, respectively). The Raven Colored Progressive Matrices scores increased in both the SF and NSF groups at 1 year after the surgery compared with the preoperative scores (Table 3). TABLE 3. Comparisons of neuropsychological results between the SF and NSF groups SF Test Presurgery 1 yr after surgery Presurgery 1 yr after surgery WAIS-R VIQ 86.1 (15.3) 87.8 (14.8) a 83.4 (10.9) 82.8 (13.3) PIQ 89.2 (16.8) 98.7 (17.8) b 88.6 (14.9) 89.7 (18.0) FIQ 86.3 (15.9) 91.4 (15.4) b 84.1 (12.5) 84.1 (16.2) WMS-R Verbal 81.4 (14.7) 91.3 (14.9) b 80.4 (17.3) 88.4 (20.6) General 88.6 (16.3) 96.1 (18.2) b 85.9 (11.2) 92.0 (18.0) Delayed paired associates 90.6 (17.7) (17.7) b 89.9 (11.0) 97.7 (18.3) Raven Progressive Matrices 32.6 (3.7) 34.3 (2.3) b 32.8 (2.4) 34.2 (1.9) b Values represent the means with the standard deviation indicated in parentheses. SF, seizure free; NSF, not seizure free. a p < 0.05, b p < 0.01 compared with the presurgical scores. NSF

4 NEUROPSYCHOLOGICAL CHANGES AFTER TLE SURGERY 7 FIG. 1. Mean MMPI profiles before (diamonds), 1 month (squares), and 1 year (triangles) after the surgery. The scales are denoted by L, Lie; F, Infrequency; K, Defensiveness; Hs, Hypochondriasis; D, Depression; Hy Hysteria; Pd, Psychopathic; Mf, Masculine-Feminine; Pa, Paranoia; Pt, Psychasthenie; Sc, Schizophrenia; Ma, Hypomania; and Si, Social Introversion. *p < 0.05, **p < DISCUSSION We found the following: (a) temporal lobe surgery in our patients effectively eliminated seizures in the majority; (b) the postoperative IQ scores, including those on the tests of verbal, performance, and full-scale IQ, increased compared with the preoperative scores; (c) verbal memory, general memory, and delayed paired associate scores of the WMS-R increased at both 1 month and 1 year after the surgery; (d) the Raven Colored Progressive Matrices scores showed significant improvement at both 1 month and 1 year after the surgery compared with the preoperative scores; (e) in the MMPI, decreased scores were observed for infrequency, hypochondriasis, psychasthenia, and schizophrenia at 1 year after the surgery; and (f) patients in the SF group had improved postoperative WAIS-R, WMS-R, and Raven Colored Progressive Matrices scores. The seizure-relief rates in our patients (62%) were compatible with the 21 65% previously reported for epilepsy patients who had temporal lobe resections (5 7). Moreover, the majority of the patients with continuing seizures also experienced significant improvement. In general, the available literature (8 12) suggests that patients undergoing anterior temporal lobectomy may be expected, as a group, not to deteriorate but to show a modest increase in their intelligence scores, especially if they become SF. Despite the relatively small number of patients in the present study, our findings are consistent with previous reports (11,12) of apparent increases in intellectual status. Furthermore, in our study, patients who became essentially free of seizures after the surgery showed a corresponding postoperative increase in intelligence scores, which also is consistent with previous reports (12,13). The F scales on the MMPI, which measure psychological distress and frustration, were decreased at 1 year after the surgery, compared with the presurgical scores. According to this measure, many patients were experiencing less distress and frustration by 1 year after the surgery. This might have provided stronger motivation for these patients to pursue their goals. In all clinical scales of the MMPI but the Mf scale, scores declined at 1 year. Our data are consistent with the hypothesis that removal of an active epileptogenic lesion in the temporal lobe is associated with psychological test indications of improved personality functioning (14). Many factors, such as reduced seizure frequency, alleviated stress associated with vocational maladjustment, altered environmental demands, and modified external attitudes toward these patients could contribute to the observed postoperative changes (14). Learning and memory functions were studied in detail both before and after temporal lobectomy (3,4,13). A risk of decline in verbal learning and recall ability after surgery on the left side has often been reported previously (3,4,13,15). In this study, patients showed improvements after the surgery on some subtests of WMS-R. Thus, our findings are not consistent with previous reports (3,4,13, 15) of the occurrence of specific memory deficits after temporal lobe surgery. Because the sample size was too small, statistical before-and-after comparisons could not be performed separately for patients with left- and rightsided resection. We propose to investigate larger samples to determine clearly and precisely the changes in memory function after surgery. In conclusion, the effects of surgery in patients with temporal lobe epilepsy were studied with a selected set of tests for neuropsychological assessment. Significant improvements in cognitive and memory functions were detected in several of these patients. We agree with other investigators (16,17) that the seizure relief after the surgery seems to play an important role in determining the neuropsychological outcome in these patients.

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