The Japanese Journal of Psychiatry and Neurology, Vol. 46, No. 2, 1992
Neuropsychological Evaluation before and after Surgical Treatment of Temporal Lobe Epilepsy Yushi Inoue, M.D., Akihiro Funakoshi,* Yutaka Watanabe, M.D.,* Tadahiro Mihara, M.D.,’ Kazumi Matsuda, M.D.,* Takayasu Tottori, M.D.,* Kazuichi Yagi, M.D.* and Masakazu Seino, M.D.* Department of Psychiatry, Kyoto University, Kyoto *National Epilepsy Center, Shizuoka Higashi Hospital, Shizuoka
Abstract: We present the results of pre- and postoperative neuropsychological evaluations of 58 patients with temporal lobe epilepsy who underwent a chronic intracranial EEG monitoring and a subsequent standard anterior temporal lobectomy. Wada’s test provided valuable information on the speech dominant side and on the focus lateralization. Some warning signs as well as verbal automatisms indicated the effect for focus localization and lateralization. The results of interictal neuropsychological tests suggested that each subgroup of TLE performed differently. A postoperative neuropsychological performance has improved in many tests that may be explained by the diminished epileptic bombardment resulting from the resection. Key Words : neuropsychological evaluation, temporal lobe epilepsy, temporal lobe resection, Wada’s test, warning signs Jpn J Psychiatr Neurol 46: 339-343, 1992
INTRODUCTION
A neuropsychological evaluation for epilepsy surgery may be performed to 1) evaluate general cognitive function, including determination of the speech/memory dominant side, 2) obtain ancillary information for focus lateralization and localization, 3) predict postoperative cognitive deficits and psychosocial outcome, and 4) assess postoperative deficits and countermeasures. The evaluation method may be invasive (e.g., Wada’s test and functional cortical mappMailing address: Yushi Inoue, M.D., National Epilepsy Center, Shizuoka Higashi Hospital, Urushiyama 886, Shizuoka 420, Japan.
ing) or noninvasive. The neuropsychological data are obtained from responses to test stimuli in addition to observation of periictal phenomena. We present the results of our experience with emphasis on four areas: Wada’s test, warning signs or auras, the standardized neuropsychological test results, and postoperative neuropsychological outcome of temporal lobe resection. SUBJECTS AND METHODS
We studied 58 patients, 38 males and 20 females, with temporal lobe epilepsy, who underwent chronic intracranial EEG monitoring, to identify the side and site of the
Y. Inoue et al.
340
epileptogenic focus or foci, and the subsequent standard anterior temporal lobectomy. Mean ( fSD) age at surgery was 26.8k 6.92 (range, 14-40 years) and mean age at seizure onset was 12.1 k5.87 (range, 426 years). In 20 patients, the focus was on the left side and in 38, it was on the right. According to the lateralization and localization of the focus, we divided the 58 patients into 4 subgroups: 13 left amygdalo-hippocampal group (LAH), 7 left lateral temporal group (LLT), 28 right amygdalo-hippocampal group (RAH), and 10 right lateral temporal group (RLT). Of 52 patients followed up for at least 1 year postoperatively, 42 (8 1 %) became free from complex partial seizures, and in 48 (93%), seizures were reduced by as much as 90% or more. A neuropsychological assessment was carried out pre- and postoperatively in all patients using the standardized neuropsychological tests, which included the Wechsler Intelligence and Memory Scale, Auditory Verbal and Visual Learning Test, Paired Associate Learning Test, Rey Complex Figure Delayed Recall, Benton Visual Test, Aphasia and Apraxia Test, Naming Test, Visual Cognition Test, Trail-Making Test, L-R Orientation Test, Stroop Test, Fluency Test, Wisconsin Card Sorting Test, and Sound Recognition Test. Wada’s test (Carotid Amytal Test for cerebral dominance of language/memory function) was done in all patients presurgically, and the verbal dichotic listening test was done in 21 patients. Subjective warning signs or auras were collected during the individual interview. RESULTS Wada’s Test
Wada’s test disclosed a left-sided speech dominance in 50 patients, a right-sided speech dominance in 7, and a bilateral speech representation in 1. Preferred hand-
Table 1: Hand Preference and Speech Dominant Side (Wada’s Test) Speech Dominant Side Handedness
Left Right N=50 N=7
Right 50 4 Left Left-right (shifted) 4 Family disposition of left handedness 14 Preference score (SD)’ 58
46a
lC 3’ 14 8.9 (5.7)
4b 2c
0
1’
0
0 4.6 (8.4)
0
a-d indicate the epileptogenic site. a : LAH RAH 21, RLT 10. b : LAH 1. R A H 2, RLT I , LAH ‘Preference of hand, foot, eye and ear was -16 to t 16, the higher the score, the right-sided preference.
.
+
Bilat. N=l Id
-13
12, LLT 7, c : RAH, d : scored from stronger the
edness of the patient and family, as well as preference scores of hand, foot, eye and ear were inconclusive in determining the speech dominant side. Seven of 8 patients with left-handedness or shifted handedness from left to right derived from the RAH group (Table 1). The results of the verbal dichotic listening test for determination of the speech dominant side were inconsistent with the result of Wada’s test in 29% (6/21) of the patients. Memory performance conducted during Wada’s test indicated that the injection of amobarbital into the hemisphere contralateral to the focus resulted in poorer scores compared with the injection into the ipsilateral hemisphere, with the exception of the LLT group, where an ipsilateral injection was associated with poorer scores (Table 2). Warning Signs or Auras
Subjective warning signs or auras were reported by 52 patients, of whom 29 became completely free from warning signs, as well as complex partial seizures, postoperatively. We compared the individual warning signs of the seizure-free group
Neuropsychological Evaluation in Temporal Lobe Epilepsy with those who still had warning signs. Of those who were seizure free, patients in the AH group were more prone to have autonomic signs (15/19) than those in the LT group (4/10), and patients in the LT group tended to have more dysmnesic/cognitive signs (10/10) than those in the AH group (8/19). No such tendency was found in the group who had postoperative seizures. Dysphasic signs were reported in 5 patients with a left-sided focus but never in Table 2: Memory Performance during Wada's Test Left-Sided Speech Dominance
L-TLE AH LT R-TLE AH LT
N
R-Injection
L-Injection
17 11 6 32 22 10
51.2131.0 44.0f35.0 64.5f17.4 77.6f15.3 78.6f15.5 75.31'15.3
61.lrt25.0 62.1f23.5 59.3k29.9 44.4f20.8 40.6f21.5 52.7f17.5
Right-Sided Speech Dominance
L-TLE R-TLE
N
R-injection
L-injection
2 5
13.5f 9.20 38.6k35.6
90.5k 3.50 31.4f38.0 (%)
Table 3 : Principal Initial Signs at Outset of Warnings or Auras in Patients without Seizures Postoperatively N Somatosensory Autonomic Psychic Dysphasic Dysmnestichognitive Affective Illusion' * Hallucination* *
AH 19
LT 10
L* 9
R* 19
0
0
0
0 7 4 t 10 1 0 4 4 f 6 2 2 0 1 1 0
3
0 9 10 0 9
12t4
6
1 0 3
1 1
?
1 0 0
? J : p
Neuropsychological Evaluation before and after Surgical Treatment of Temporal Lobe Epilepsy Yushi Inoue, M.D., Akihiro Funakoshi,* Yutaka Watanabe, M.D.,* Tadahiro Mihara, M.D.,’ Kazumi Matsuda, M.D.,* Takayasu Tottori, M.D.,* Kazuichi Yagi, M.D.* and Masakazu Seino, M.D.* Department of Psychiatry, Kyoto University, Kyoto *National Epilepsy Center, Shizuoka Higashi Hospital, Shizuoka
Abstract: We present the results of pre- and postoperative neuropsychological evaluations of 58 patients with temporal lobe epilepsy who underwent a chronic intracranial EEG monitoring and a subsequent standard anterior temporal lobectomy. Wada’s test provided valuable information on the speech dominant side and on the focus lateralization. Some warning signs as well as verbal automatisms indicated the effect for focus localization and lateralization. The results of interictal neuropsychological tests suggested that each subgroup of TLE performed differently. A postoperative neuropsychological performance has improved in many tests that may be explained by the diminished epileptic bombardment resulting from the resection. Key Words : neuropsychological evaluation, temporal lobe epilepsy, temporal lobe resection, Wada’s test, warning signs Jpn J Psychiatr Neurol 46: 339-343, 1992
INTRODUCTION
A neuropsychological evaluation for epilepsy surgery may be performed to 1) evaluate general cognitive function, including determination of the speech/memory dominant side, 2) obtain ancillary information for focus lateralization and localization, 3) predict postoperative cognitive deficits and psychosocial outcome, and 4) assess postoperative deficits and countermeasures. The evaluation method may be invasive (e.g., Wada’s test and functional cortical mappMailing address: Yushi Inoue, M.D., National Epilepsy Center, Shizuoka Higashi Hospital, Urushiyama 886, Shizuoka 420, Japan.
ing) or noninvasive. The neuropsychological data are obtained from responses to test stimuli in addition to observation of periictal phenomena. We present the results of our experience with emphasis on four areas: Wada’s test, warning signs or auras, the standardized neuropsychological test results, and postoperative neuropsychological outcome of temporal lobe resection. SUBJECTS AND METHODS
We studied 58 patients, 38 males and 20 females, with temporal lobe epilepsy, who underwent chronic intracranial EEG monitoring, to identify the side and site of the
Y. Inoue et al.
340
epileptogenic focus or foci, and the subsequent standard anterior temporal lobectomy. Mean ( fSD) age at surgery was 26.8k 6.92 (range, 14-40 years) and mean age at seizure onset was 12.1 k5.87 (range, 426 years). In 20 patients, the focus was on the left side and in 38, it was on the right. According to the lateralization and localization of the focus, we divided the 58 patients into 4 subgroups: 13 left amygdalo-hippocampal group (LAH), 7 left lateral temporal group (LLT), 28 right amygdalo-hippocampal group (RAH), and 10 right lateral temporal group (RLT). Of 52 patients followed up for at least 1 year postoperatively, 42 (8 1 %) became free from complex partial seizures, and in 48 (93%), seizures were reduced by as much as 90% or more. A neuropsychological assessment was carried out pre- and postoperatively in all patients using the standardized neuropsychological tests, which included the Wechsler Intelligence and Memory Scale, Auditory Verbal and Visual Learning Test, Paired Associate Learning Test, Rey Complex Figure Delayed Recall, Benton Visual Test, Aphasia and Apraxia Test, Naming Test, Visual Cognition Test, Trail-Making Test, L-R Orientation Test, Stroop Test, Fluency Test, Wisconsin Card Sorting Test, and Sound Recognition Test. Wada’s test (Carotid Amytal Test for cerebral dominance of language/memory function) was done in all patients presurgically, and the verbal dichotic listening test was done in 21 patients. Subjective warning signs or auras were collected during the individual interview. RESULTS Wada’s Test
Wada’s test disclosed a left-sided speech dominance in 50 patients, a right-sided speech dominance in 7, and a bilateral speech representation in 1. Preferred hand-
Table 1: Hand Preference and Speech Dominant Side (Wada’s Test) Speech Dominant Side Handedness
Left Right N=50 N=7
Right 50 4 Left Left-right (shifted) 4 Family disposition of left handedness 14 Preference score (SD)’ 58
46a
lC 3’ 14 8.9 (5.7)
4b 2c
0
1’
0
0 4.6 (8.4)
0
a-d indicate the epileptogenic site. a : LAH RAH 21, RLT 10. b : LAH 1. R A H 2, RLT I , LAH ‘Preference of hand, foot, eye and ear was -16 to t 16, the higher the score, the right-sided preference.
.
+
Bilat. N=l Id
-13
12, LLT 7, c : RAH, d : scored from stronger the
edness of the patient and family, as well as preference scores of hand, foot, eye and ear were inconclusive in determining the speech dominant side. Seven of 8 patients with left-handedness or shifted handedness from left to right derived from the RAH group (Table 1). The results of the verbal dichotic listening test for determination of the speech dominant side were inconsistent with the result of Wada’s test in 29% (6/21) of the patients. Memory performance conducted during Wada’s test indicated that the injection of amobarbital into the hemisphere contralateral to the focus resulted in poorer scores compared with the injection into the ipsilateral hemisphere, with the exception of the LLT group, where an ipsilateral injection was associated with poorer scores (Table 2). Warning Signs or Auras
Subjective warning signs or auras were reported by 52 patients, of whom 29 became completely free from warning signs, as well as complex partial seizures, postoperatively. We compared the individual warning signs of the seizure-free group
Neuropsychological Evaluation in Temporal Lobe Epilepsy with those who still had warning signs. Of those who were seizure free, patients in the AH group were more prone to have autonomic signs (15/19) than those in the LT group (4/10), and patients in the LT group tended to have more dysmnesic/cognitive signs (10/10) than those in the AH group (8/19). No such tendency was found in the group who had postoperative seizures. Dysphasic signs were reported in 5 patients with a left-sided focus but never in Table 2: Memory Performance during Wada's Test Left-Sided Speech Dominance
L-TLE AH LT R-TLE AH LT
N
R-Injection
L-Injection
17 11 6 32 22 10
51.2131.0 44.0f35.0 64.5f17.4 77.6f15.3 78.6f15.5 75.31'15.3
61.lrt25.0 62.1f23.5 59.3k29.9 44.4f20.8 40.6f21.5 52.7f17.5
Right-Sided Speech Dominance
L-TLE R-TLE
N
R-injection
L-injection
2 5
13.5f 9.20 38.6k35.6
90.5k 3.50 31.4f38.0 (%)
Table 3 : Principal Initial Signs at Outset of Warnings or Auras in Patients without Seizures Postoperatively N Somatosensory Autonomic Psychic Dysphasic Dysmnestichognitive Affective Illusion' * Hallucination* *
AH 19
LT 10
L* 9
R* 19
0
0
0
0 7 4 t 10 1 0 4 4 f 6 2 2 0 1 1 0
3
0 9 10 0 9
12t4
6
1 0 3
1 1
?
1 0 0
? J : p
