Outcome after cortico-amygdalo-hippocampectomy in patients with refractory temporal lobe epilepsy and mesial temporal sclerosis without pre-operative ictal recording
Cristine Mella Baldauf
Cássio Roberto Forster
Valeria Antakli Mello
José Augusto Burattini
Pedro Paulo Mariani
Cristine Mella Baldauf
Cássio Roberto Forster
Valeria Antakli Mello
José Augusto Burattini
Pedro Paulo Mariani
Epilepsy Surgery Program, Hospital Brigadeiro, São Paulo SP.
Temporal lobe epilepsy (TLE) is the commonest epileptic syndrome and is the most frequently refractory one (Hauser et al, 1991). Mesial temporal epilepsy (MTE) is the most frequent refractory epileptic syndrome in adults and its treatment represents two-thirds of the epilepsy surgery procedures. Very good surgical outcome has been reported in patients with MTE. Engel (1996) argued that MTE was the best prototype of a “surgically remediable epileptic syndrome”. In this patient population, a 70% to 90% post-operative seizure remission rate might be expected.
More recently, many centers have reevaluated the relative value of each diagnostic procedure included in the pre-operative workup of epileptic patients (Spencer, 1994; Rhadakrishnan et al, 1998; Jeong et al, 1999). The need for video-EEG seizure recording in all patients has been extensively studied (Engel, 1999; Cendes et al, 2000) and many authors emphasized the value of MRI and interictal EEG findings in patients with TLE who were considered candidates for surgery (Chee et al, 1993; Cascino, 1995; Bronem et al, 1997). Better surgical outcome regarding seizures was found in patients with concordant MRI and interictal EEG findings, especially when MRI disclosed unilateral mesial temporal sclerosis (MTS)(Gillian et al, 1997; Cukiert et al, 2002).
We studied the surgical outcome of patients with TLE and MTS selected based on the anatomical findings provided by MRI and that were submitted to cortico-amygdalo-hippocampectomy at the side shown by imaging.
Two-hundred and twelve consecutive patients (131 women) with refractory TLE and unilateral MTS that were submitted to surgery at the Hospital Brigadeiro Epilepsy Surgery Program from 1999 to 2004 were studied. Pre-operative work-up included clinical history, neurological examination, interictal EEG, high resolution 1.5T MRI and neuropsychological testing. The following clinical variables were analyzed: sex, age at onset of seizures, weekly seizure frequency, type of seizure, pre- and post-operative AED regimen and the presence or not of febrile seizures in childhood.
All patients had clinical and semiological findings compatible with TLE. All had refractory epilepsy and had been previously unsuccessfully treated by at least two adequate antiepileptic drug (AED) regimens. All patients had unilateral MTS on MRI and at least 4 interictal EEGs performed over the last 2 years showing unilateral or bilateral temporal lobe spiking. All patients were submitted to cortico-amygdalo-hippocampectomy (CAH) at the Hospital Brigadeiro Epilepsy Surgery Program.
Patients that had been previously operated, had normal MRI, other extra-hippocampal lesions or pseudo-seizures were excluded from the study.
The clinical diagnosis was based on the International Classification of Seizures (1981) (ILAE, 1981) and Epileptic Syndromes (1989) (ILAE, 1989). The following clinical characteristics were considered as diagnostic for TLE: simple partial seizures (SPS) of the déjà vu or jamais vu type, or including epigastric or psychic manifestations (p.e., fear) followed by complex partial seizures (CPS) characterized by staring and masticatory automatisms, accompanied or not by superior limb automatisms or contralateral superior limb distonia.
All patients had 32-channels (Medelec, Profile) interictal EEG (10-20 system) recordings including zygomatic electrodes. The presence of temporal lobe interictal spiking and absence of extratemporal discharges were considered findings related to TLE. The finding of at least 90% of the discharges at one side was considered a lateralizing sign in patients with bilateral EEG findings. No patient was submitted to pre-operative video-EEG ictal recording.
Neuropsychological testing included dichotic listening, WAIS, Wechsler memory, Boston naming, Wisconsin card sorting and somesthesic (strength and two points discrimination) testing. Patients were considered to have pre-operative memory deficit when they were performing at least one standard deviation below normal. Patients were considered to have memory improvement / decline post-operatively if they performed at least one standard deviation from pre-operative baseline findings.
MRI examinations included sequences for the adequate study of the hippocampal formation: 3mm thick (0.3 mm interval) FLAIR, T2 and IR coronal slices; 6 mm thick T1, T2, gradient echo, FLAIR and IR axial slices and T1 sagittal slices. MTS was diagnosed when there was clear-cut volumetric reduction of the hippocampus as seen on T1 coronal slices and increased hippocampal signal on T2 and FLAIR coronal slices as noted by two independent observers.
All patients were submitted to CAH at the side determined by MRI. The procedure was carried out under general anesthesia and without intraoperative electrocorticography. Surgery consisted of cortical resection that included the superior, middle, and inferior temporal, parahippocampal and fusiform gyri (with its posterior border at the level of the central artery), total hippocampectomy and resection of the intratemporal portion of the amygdala. All patients were operated by the same surgeon (AC).
Engel’s scale was used to rate post-operative outcome. Data were statiscally analysed using the Student T-test.
Mean age at surgery was 26.1± 4.1years (range: 8-61 years). All patients had TLE and unilateral MTS as shown on MRI.
Men were significantly younger then women (mean=24.3±8.4 versus 32.1±6.0 years) by the time of surgery (p= 0,004). No other gender difference was noted when analyzing age at seizure onset, weekly seizure frequency or seizure type. Mean age at the onset of seizures was 8.7±7.6 years for women and 6.5±8.1 years for men. Mean weekly seizure frequency was 3.3±1,2 for women and 4.6±2.7 for men. There was no significant relationship between age of seizure onset and its weekly frequency.
SPS occurred in 189 patients (89%). The most frequent SPS types were vegetative (108 patients; 51%) or psychic (55 patients; 26%). CPS occurred in all patients. Secondarily generalized tonic-clonic (GTC) seizures occurred sporadically in 144 patients (68%) during the course of the disease. No patient presented with GTC alone.
Febrile seizures occurred in 61 patients (29%); there was a latency of 5.4 ± 7.8 years for the appearance of non-febrile seizures. There was no statistically significant relationship between the presence or not of febrile convulsion and age of non-febrile seizure onset.
Bilateral interictal EEG temporal lobe spiking was noted in 36 patients (17%). Left interictal EEG findings were noted in 91 patients (42%) and in 85 (40%) right temporal lobe spiking was noted. There was no significant gender difference.
MRI showed right MTS in 99 (46%) and left MTS in 113 (53%) patients. There was no significant gender difference.
Among the patients with bilateral interictal EEG findings, 14 (6%) had right and 22 (10%) had left MTS on MRI. There was a significant relationship between interictal EEG and MRI findings (p<0,001) (Table 1).
TABLE 1. Distribution of patients according to interictal EEG and MRI findings.
Interictal EEG MRI findings Total
Right MTS Left MTS
n % n % N %
Bilateral 14 14 22 19 36 16
Right temporal 85 85 0 0 85 40
Left temporal 0 0 91 80 91 43
Total 99 100,0 113 100,0 212 100,0
p < 0,001
MTS: Mesial temporal sclerosis.
At late follow-up (mean: 2.7±1.2 years; range: 18 months – 7 years), 163 patients (77%) had no seizure during the last follow-up year; 31 (15%) presented SPS; 11 (4%) presented CPS and GTC and 7 patients (3%) presented GTC. Thus, 92% of the patients were rated as Engel Class I and the remaining (8%) as Class II.
We noted that 38 (18%) patients had seizures during their post-operative follow-up that were related to reduction or withdrawal of AED; 30 of these patients had no seizures over the last follow-up year.
No statistically significant results were found while analyzing the surgical outcome and any clinical variable such as sex, age of seizure onset, weekly seizure frequency, type of seizure, presence or not of post-operative SPS or presence of febrile seizure in childhood.
Unilateral EEG findings did not correlate with better surgical outcome; 32 of the 36 patients with bilateral EEG findings were seizure-free after surgery.
Pre- and post-operative neuropsychological data was available for 147 patients. Ninety-five of these patients (64%) were submitted to dominant temporal lobe resection. Ninety-one patients operated on the dominant temporal lobe (97%) had verbal memory deficit, and 45 (47%) had visual memory deficit, pre-operatively. After surgery, ninety-four of these patients had verbal memory deficit, and 16 visual memory deficit. Fifty-two patients submitted to neuropsychological testing were operated on the non-dominant temporal lobe. Twenty seven of these patients submitted to surgery on the non-dominant temporal lobe had visual memory deficit, and 19 had verbal memory deficit, pre-operatively. Post-operatively, 27 of these patients had visual memory deficit and 9 had verbal memory deficit. Neuropsychological decline was noted in 3 patients submitted to surgery on the dominant temporal lobe; these patients had additional post-operative posterior temporal cortical damage documented by MRI. No patient submitted to surgery on the non-dominant temporal lobe showed additional cognitive impairment. On the other hand, overall, 60% of the patients showed improvement in memory function related to the non-operated side and in 59% of them, a 10% improvement in general IQ was noted one year after seizure cessation. There was no relationship between the presence or not of memory decline and surgical outcome regarding seizures.
We noted a relevant reduction on the amount of AED post-operatively (Table 2). Before surgery, 78 (37%) patients were receiving 1 AED and the remaining 134 (62%) were under 2 or more AED. At the last follow-up visit after surgery, 67 patients (32%) were receiving no medication, 86 (40%) were receiving 1 AED and 59 (28%), 2 or more AED.
Post-operative MRI showed at least 90% resection of the hippocampus in all patients and total hippocampal removal in 94% of the patients. All surgical specimens were analyzed and MTS was found in all of them.
TABLE 2. Pre- and post-operative AED regimens.
AED Before Surgery After Surgery
N Mean daily dose (mg) N Mean daily dose (mg)
Carbamazepine 83 1100 60 600
Phenobarbital 120 115 61 90
Phenytoin 52 280 8 200
Oxcarbazepine 80 900 56 900
Valproic acid 23 750 2 1.000,0
Clonazepam 18 2 0 4,0
Lamotrigine 14 125,0 0 0
Clobazam 4 20 18 20
Topiramate 2 150 0 0
Gabapentine 2 1.200 0 0
Rigorous presurgical evaluation protocols are essential for adequate focus localization and good surgical outcome in patients with refractory epilepsy. The introduction of MRI into clinical practice and the better knowledge of the pathophysiology of epilepsy have led many centers to re-evaluate the relative role of each diagnostic technique used in the presurgical evaluation of epileptic patients.
Jeong et al (1999) considered age at surgery and duration of epilepsy as prognostic indicators of post-operative outcome. On the other hand, we (Baldauf et al, 2006) and others (McIntosh et al, 2001) showed in meta-analysis studies that gender, age of seizure onset and pre-operative weekly seizure frequency were not prognostic factors.
SPS occurred pre-operatively in 89% of our patients, as was noted by others, who reported that up to 90% of patients with MTS had SPS (Wieser and Williamson, 1993). Sporadic secondarily generalized GTC was seen in 68% of our patients. Our data, which were in agreement with those from Kilpatrick et al (1999), did not suggest that the presence of GTC would be a bad prognostic factor after surgery. On the other hand, Spencer (1994) and Henessy et al (2001) suggested that the absence of GTC would be a good prognostic factor after CAH.
Prolonged febrile seizures had been implicated in the development of MTS. Although some authors considered the presence of febrile seizures in childhood as a poor surgical outcome indicator (Kim et al, 1999), our data and those of others (Kilpatrick et al, 1999; Henessy et al, 2001) did not support this idea.
The surgical results reported for patients with MTS varied among centers, and seemed to be better when there was agreement among the clinical, EEG and imaging pre-operative findings. The presence of MTS on MRI had been related to a better surgical outcome after CAH (Jack et al, 1992). Radhakrishnan et al (1998) found excellent outcome in patients with MRI-defined MTS submitted to CAH and worse results in patients without MTS. In this study, they also pointed out that exclusively unilateral interictal EEG discharges were as important as MR findings as positive prognostic factor. Gilliam et al (1997) reported good surgical outcome in patients with concordant MRI and interictal EEG findings, in contrast to those results in patients with non-concordant or non-localizatory findings. In our sample, patient selection was essentially based on anatomical MRI data, and the majority of them got excellent results (92%). In our series patients with bilateral interictal EEG findings did not have a worst post-operative prognosis. This finding suggests that the presence of MTS on MRI would be the most important positive post-operative prognostic factor after CAH (Cukiert et al, 2002). We found that all patients with MTS on MRI had favorable post-operative outcome (Engel I or II). We did not analyze the impact of other (non-MTS) temporal lobe MRI findings.
EEG recordings have always been included as part of the presurgical evaluation of epileptic patients. On the other hand, the introduction of new technological tools in the diagnosis of epilepsy led to the need to re-evaluate its role in this setting. By the time epilepsy surgery was introduced all patients were submitted to invasive recordings for adequate focus localization, which is clearly not the present situation. Presently, we submit all patients with temporal lobe epilepsy and bilateral mesial temporal sclerosis or normal MRI to video-EEG monitoring. No patient with unilateral mesial temporal sclerosis or typically epileptogenic lesions (such as brain tumors) is currently submitted to ictal recording. Williamson et al (1993) found that patients with temporal lobe epilepsy almost always had focal interictal EEG abnormalities. In our study, anterior temporal lobe spikes were present in all patients and bilateral interictal findings were seen in 17% of them. Cascino et al (1996) evaluated the relative role of routine interictal EEG, vídeo-EEG and MRI findings in the post-operative prognosis of patients with TLE and found that interictal EEG abnormalities were unilateral in most of them. Bilateral findings were less frequent, similarly to what was found in our data. There was a statistically significant relationship between MRI and interictal EEG findings.
Prataria et al (1998) concluded that congruent clinical history, unilateral MTS on MRI and unilateral interictal EEG were highly sensitive for focus localization and that ictal recordings did not bring additional useful information in this patient population. Actually, almost all centers around the world, even those which are used to record every patient, would in some cases go ahead with surgery in patients with MTS and congruent clinical information in whom ictal recording was not fully lateralizatory.
Cendes et al (2000) evaluated MRI, ictal and interictal EEG findings and concluded that almost all patients with unilateral MTS had congruent ictal and interictal EEG findings and in only 3% of them interictal and ictal EEG were not concordant. They suggested that, in this patient population, serial routine interictal EEG would be sufficient for focus localization. Our findings are in agreement with the latter and, additionally, suggest that MRI findings might be isolately efficacious for focus localization and good post-operative outcome forecast.
We noted that some of our patients had GTC after surgery that was related to reduction or withdrawal of AED. Williamson et al (1993) also reported that GTC comprised the majority of the post-operative ictal events, that they usually occurred during the first 2 years of follow-up and were related to inadequate management of AED.
Potential neuropsychological decline has always been a major concern in patients submitted to cortical resection. MRI-defined MTS has been correlated to higher degrees of pre-operative memory deficits and significantly lower post-operative morbidity (Hermann et al, 1992; Bell et al, 1998). Our series suggested that in patients with clinically suspected refractory temporal lobe epilepsy with MRI-well defined MTS, post-operative memory function decline is not a major issue. The most likely explanation for this is that we were dealing with an extremely homogeneous population of patients with clear-cut mesial temporal sclerosis as seen on visual inspection of MRI. All these patients have severe hippocampal lesion and its removal would very unlikely cause additional deficit (Paglioli et al, 2006). All patients who had verbal memory decline after surgery were operated on the dominant temporal lobe, and had unpredicted posterior temporal cortical damage, supposedly caused by venous infarction at the posterior border of resection. There is an ongoing discussion on the relative role of the cortex and mesial structures in memory function in these patients. A significant portion of the literature might have neglected the role of the cortex. The widespread use of tests such as the Wada’s test, as a way of predicting post-operative memory deficits, remains controversial. The most commonly used protocols for Wada’s testing include the injection of the drug in the internal carotid artery. In this setting, only a small part of the head of the hippocampus is perfused by the anterior choroidal artery. The rest of the hippocampus is fed by the posterior cerebral artery and is not usually perfused. On the other hand, internal carotid artery injections of amobarbital lead to extensive fronto-temporal cortical inactivation. Wada’s procedure is possibly testing mainly the cortical and not the hippocampal role in memory function in this type of patient. We used to submit all patients with temporal lobe epilepsy to Wada test at the beginning of our series. Presently, none of the patients with unilateral mesial temporal sclerosis undergo this procedure. We (Caner-Cukiert et al, 1985) and others (Kanemoto et al, 1999) have already shown that patients with MTS most invariably pass an amobarbital injection ipsolateral to the lesion seen on MRI. Additionally, patients with MTS who have been denied surgery previously based on Wada’s finding (despite all other congruent additional information) were subsequently submitted to surgery and got results similar to those who passed the test.
The most consistent neuropsychological finding was cognitive function improvement, and not decline. In 60% of the patients there was improvement in memory function related to the non-operated temporal lobe. This has already been described in the literature and is related to improved contralateral temporal lobe function after seizure cessation. Furthermore, 59% of the patients had at least 10% of improvement in general IQ. This fact is easily recognized by the family and caregivers and is generally accompanied by improvement in quality of life. We (Frayman et al, 1999) and others (Lowe et al, 2004) have already approached this issue, and it is probably a consensus that quality of life improves after surgery in those patients who were rendered seizure-free. If QOL improves in patients who got better (Engel II) but were not seizure free is not yet clear. Additionally, QOL improvement is not always related to better employment, marital status or physical capability. The absence of surgically induced memory deficits is not so surprising in this group of patients, in whom pre-operative deficits were already noted, especially in patients with dominant temporal lobe epilepsy.
In this study, we reported a significant reduction on the amount of AED during the post-operative period. It is our policy to initiate clobazam post-operatively in Class II patients; thus, clobazan was the only AED which was added post-operatively. Clobazan is a 1-5 benzodiazepine which has good anti-epileptic activity and small sedative effect. It is not usually included in the first line of anti-epileptic drugs but we and others (Montenegro et al, 2005) have already noted its apparently selective effect in patients with mesial temporal sclerosis. It is simple to use (once daily), with minimal side effects. The main objective after epilepsy surgery would be to have a seizure-free patient under no AED. On the other hand, improvement in quality of life was easily documented in those patients who were not AED-free but were seizure-free under a more modest AED regimen. These patients showed less side effects and lower AED-related costs.
We found persistent SPS (auras) in 10 patients, as reported by others. SPS are often thought as “benign” by most authors. On the other hand, this is not true in some patient’s perception, although the majority of them feel comfortable about them in the long term follow-up.
In most series that attempted to investigate the importance of ictal and interictal EEG findings in predicting prognosis after mesial temporal lobe resections for refractory mesial temporal lobe epilepsy, the population was skewed because most or many of the patients underwent ictal EEG recording which was part of their work-up. In our study, with a large number of contemporary patients and excellent seizure outcome, ictal recording was never done and cannot therefore bias the outcome or the conclusion. Patients were selected entirely on the basis of outpatient interictal EEG findings and MRI evidence of mesial temporal sclerosis. Accordingly, this is the most compelling information yet that suggests ictal recording may not be necessary in this special situation to predict excellent seizure control after resective surgery of medial temporal structures.
Although other papers addressed the relative usefulness of each pre-operative test, this is the largest series presented so far studying seizure and neuropsychological outcome after cortico-amygdalo-hippocampectomy using this pre-operative work-up paradigm. Our study included only patients with unilateral MTS who presumably had the best surgical outcome prognosis. The number of patients who were not rendered seizure-free was very low. This fact made it difficult to further analyze predictive factors in Class II patients. The finding of unilateral MTS on MRI is the single most important positive predictive factor for good surgical outcome after CAH.
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Disclosure of Conflicts of Interest
None of the authors has any conflict of interest to disclose.