Seizure: European Journal of Epilepsy
Volume 19, Issue 6 , Pages 319-323, July 2010

Outcome after cortico-amygdalo-hippocampectomy in patients with temporal lobe epilepsy and normal MRI

Epilepsy Surgery Program, Hospital Brigadeiro, São Paulo, SP, Brazil

Received 11 November 2009; received in revised form 29 March 2010; accepted 23 April 2010. published online 24 May 2010.

Article Outline

Abstract 

Rationale

We describe seizure and neuropsychological outcome obtained after CAH in patients with TLE and normal MRI evaluated in the modern imaging era.

Methods

Forty-five adult consecutive patients with TLE and normal MRI were studied. All patients had neuropsychological testing, interictal and ictal EEG recordings and MRI. They were divided into two groups: Group 1 (n=18), included patients in whom non-invasive neurophysiological evaluation was lateralizing and Group 2 (n=27) included patients with non-lateralizing neurophysiological data who were submitted to invasive recordings.

Results

Seventy-seven percent of the Group 1 patients were rated as Engel I; 11% were rated as Engel II and 11% as Engel III. In Group 2, there were 57% of patients seizure-free, 26% in Engel II and 14% in Engel III. Pre-operatively, mean general IQ was 82 and 78 in Groups1 and 2, respectively; post-operatively, mean general IQ was respectively 86 and 71. Some degree of verbal memory decline was noted in all patients submitted to dominant temporal lobe resection in both Groups 1 and 2. At last follow-up visit, 22% of Group 1 and 11% of Group 2 patients were receiving no antiepileptic drugs (AED).

Conclusions

Our data showed that patients with TLE and normal MRI could get good surgical results after CAH although 60% of them would need invasive recordings and their results regarding seizure control and cognition were worse than those obtained in patients with MRI defined temporal lobe lesions. Caution should be taken in offering dominant temporal lobe resection to this subset of patients.

Keywords: Outcome, Surgery, Temporal lobe epilepsy, Normal MRI

 

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1. Introduction 

Temporal lobe epilepsy (TLE) represents the epileptic syndrome most amenable for surgery. The presence of lesions such as mesial temporal sclerosis, cortical dysplasia, tumors and vascular malformations on MRI has been shown to be an extremely relevant post-operative prognostic factor regarding seizure freedom.1, 2, 3 In these patients, a 65–90% seizure-free rate might be expected post-operatively.4

MRI is highly effective in delineating seizure's etiology in patients with TLE but 20–30% of them present with normal imaging.5 This represents a challenging group of patients if surgical treatment is to be considered; lower post-operative seizure-free rates and higher cognitive decline were reported after temporal lobe resections in patients with normal MRI.6, 7

There are relatively few studies reporting on the outcome after cortico-amygdalo-hippocampectomy (CAH) in patients with TLE and normal MRI,8, 9, 10, 11, 12, 13 and many of them were published before modern MRI techniques came into clinical practice. Some centers would not consider this patient population as surgical candidates, but previous series showed that adequately worked-up patients might get excellent outcome, although many of them would need invasive evaluation. The likelihood of verbal memory decline after dominant temporal lobe resection in patients with TLE and normal MRI14, 15, 16 led more recently to the development and use of non-resective neuromodulatory techniques, such as vagus nerve and deep brain stimulation in these patients.

We describe seizure and neuropsychological outcome obtained after CAH in a consecutive series of patients with TLE and normal MRI evaluated in the modern imaging era.

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2. Methods 

Forty-five adult consecutive patients with TLE and normal MRI surgically treated between 1999 and 2006 at Hospital Brigadeiro Epilepsy Surgery Program were retrospectively identified within a series of 980 operated patients. Pre-operative work-up consisted of clinical history, neurological examination, interictal and ictal EEG, neuropsychological testing and MRI. There were no interspersed patients left out of the study.

Pre-operative findings as to sex, age at seizure onset, age at presentation, seizure type and frequency, antiepileptic drug (AED) regimen, and presence or not of febrile seizures, head trauma, status epilepticus, meningitis and birth injury were studied regarding final outcome.

The clinical diagnosis was based on the International Classification of Seizures17 and Epileptic Syndromes.18 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 interictal and ictal EEG recordings (10–20 system; at least three seizures recorded) 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 interictal discharges at one side was considered a lateralizing sign in patients with bilateral EEG findings.

All patients had MRI examinations including sequences for the adequate study of the hippocampal formation: 3mm thick (0.3mm interval) FLAIR, T2 and IR coronal slices perpendicular to the hippocampal axis; 6mm thick T1, T2, gradient echo, FLAIR and IR axial slices and T1 sagittal slices. Images were visually reviewed by two members of the epilepsy team independently. Patients with any hippocampal or amygdala abnormality, such as abnormal rotation, smaller hippocampus without signal increase, normal size hippocampus with increased signal or amygdala size increase or decrease were excluded from the study.

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.

Patients were divided into two groups: Group 1 (n=18; 7 males) included patients in whom non-invasive neurophysiological evaluation was localizing and lateralizing; they had more than 90% of the interictal discharges over one temporal lobe and all seizures clearly originating from the same temporal lobe and were submitted to CAH at the side defined by video-EEG recording. 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.

Group 2 (n=27; 15 males) included patients with non-lateralizing neurophysiological data; they had bilateral independent interictal temporal lobe spiking with <90% lateralization or non-lateralizing ictal video-EEG findings. All these patients were submitted to invasive recordings after bilateral subdural grids implantation. Under general anesthesia, two separate temporal craniotomies were performed and a 32-contacts (4×8) subdural grid was inserted embracing each temporal lobe. Veins were found bridging from the brain to the tentorium. In these situations, the grid was “tailored” to the patient anatomy (remodeling or cutting the plastic part of the grid) so that the vein was left in the middle of the contacts. In one patient, the grid had to be diminished to a 3×8 contacts grid. The most caudal contacts were left in contact with the parahippocampal gyrus and the more cranial ones were covering the inferior frontal gyrus. The more anterior line of electrodes covered the temporal pole while the more posterior ones were placed over the mid-temporal cortex (for details see Cukiert et al.)19; patients were then submitted to invasive video-EEG recordings, followed by CAH at the side defined by invasive neurophysiology. All patients were operated by the same surgeon (AC).

Engel's I–IV outcome scale was used for post-operative rating. Pathological examination was obtained in all patients.

All patients had at least 1 year of post-operative follow-up (mean=4.7 years). Statistical analysis was carried out when needed using the Student's T-test or univariate analysis.

The Student’ T-test was used whenever needed (p<0.05 was considered significant).

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3. Results 

Mean age at habitual seizure onset was 16.1 and 15.1 years in Groups 1 and 2, and mean age at presentation was 27.7 and 26.9 years in Groups 1 and 2, respectively. There was history of severe head trauma in one Group 1 and in two Group 2 patients and 2 patients in each Group reported severe birth injuries. Thirty-eight percent of Group 1 and 29% of Group 2 patients had history of febrile seizures and previous history of meningitis was present in one patient in each Group. There was no history of prolonged status epilepticus in either Group. Mean pre-operative seizure frequency was 8/month and 11/month in Groups 1 and 2, respectively. Pre-operatively, all patients in Groups 1 and 2 had complex partial seizures while 61% and 70% of Groups 1 and 2 patients had simple partial seizures, respectively. Three Group 1 patients and two Group 2 patients had auditory simple partial seizures. Twenty-two percent of Group 1 and 20% of Group B patients had occasional generalized tonic–clonic seizures. There were no significant differences regarding clinical demographics among Groups 1 and 2 patients. Mean follow-up time was 4.9 years for Group 1 and 3.9 years for Group 2 patients.

Invasive evaluation in Group 2 showed that seizures originated from a single temporal lobe in 21 out of 27 patients; at least 80% of the seizures originated from one temporal lobe in 5 patients and in 1 patient seizures were truly originating from both temporal lobes. This last patient was explanted and was not submitted to any resection; the other 26 patients were submitted to CAH. In 21 of these patients there was focal ictal onset comprising no more than 2 adjacent contacts and in 6 there was regional focal onset (involving at least 3 adjacent electrodes). In 20 patients there was early ipsolateral spread of the epileptic activity, but in 7 early contralateral involvement was noted. Thirty-seven percent of the patients had mesial temporal seizure onset, while 63% of them had neocortical ictal onset.

Eight out of 18 patients in Group 1 and 15 out of 26 patients in Group 2 were operated on the dominant side.

Seventy-seven percent of the Group 1 patients were seizure-free after surgery (Engel I); 11% were rated as Engel II and 11% as Engel III. In Group 2, there were 57% of patients seizure-free, 26% in Engel II and 14% in Engel III. Six out of 8 and 7 out of 15 patients operated on the dominant side were rendered seizure-free after surgery in Groups 1 and 2, respectively. This was true for 8 out of 10 (Group 1) and 8 out of 11 (Group 2) of the patients who got non-dominant temporal lobe resection (Table 1).

Table 1. Summary of the post-operative seizure outcome findings. D-CAH, dominant CAH; ND-CAH, non-dominant CAH.
NEngel 1 (%)Engel II (%)Engel III (%)Engel IV (%)
Group 1D-CAH 87512120
Group 1ND-CAH108010100
Group 2D-CAH15464670
Group2 ND-CAH11729180

Total446623110

Pathological findings in Group 1 included 27% of the specimens with mesial temporal sclerosis and 38% with non-specific gliosis. In Group 2, there was one patient with mesial temporal sclerosis (3%) and seven with non-specific gliosis (26%). Except for one patient in Group 1, mesial temporal sclerosis was of the end-folium type.

A summary of the neuropsychological findings can be seen in Table 2. Pre-operatively, mean general IQ was 82 and 78 in Groups 1 and 2, respectively; post-operatively, mean general IQ was respectively 86 and 71.

Table 2. Summary of the pre- and post-operative neuropsychological findings. D-CAH, dominant CAH; ND-CAH, non-dominant CAH; VeM, verbal memory; ViM, visual memory; Def, deficit; Imp, improvement; pre-op, pre-operative; post-op, post-operative.
NPre-op VeM def (%)Pre-op ViM def (%)Post-op VeM def (%)Post-op ViM def (%)Post-op VeM imp (%)Post-op ViM imp (%)
Group 1D-CAH85012100000
Group 1ND-CAH102020030500
Group 2D-CAH156027100000
Group 2ND-CAH113636036360

Total4443225216200

Visual memory deficit was noted in 30% and 27% of patients in Groups 1 and 2 before surgery, respectively.

Some degree of verbal memory decline was noted in all patients submitted to dominant temporal lobe resection in both Groups 1 and 2; there was no significant difference between Groups 1 and 2 patients. Overall, 68% of those patients submitted to dominant temporal lobe resection complained about their newly acquired deficits; this was true for 30% of these patients who got seizure-free and 90% of those who did not get seizure-free after surgery. Two Group 2 patients who were not rendered seizure-free after dominant temporal lobe resection mentioned they would have preferred having seizures to the new verbal memory deficits. Although patients submitted to dominant temporal lobe resection who were ultimately found to have mesial temporal sclerosis (end-folium type) complained less of memory loss compared to those with no pathological finding (32%×71%), this was not statistically significant.

On the other hand, verbal memory improvement was noted in 50% of the patients who underwent non-dominant temporal lobe resection in Group 1 and in 36% of those patients in Group 2. The qualitative improvement in verbal memory was more marked in patients with non-dominant temporal lobe resections and who were seizure-free post-operatively, compared to those who were not seizure-free, although quantitatively it did not reach statistical significance.

We did not notice any improvement in visual memory post-operatively in any Group 1 or 2 patients; 30% of Group 1 patients who underwent non-dominant temporal resection and 36% of those of Group 2 got additional visual memory deficits. Only one Group 1 and two Group 2 patients complained about their new visual memory deficits.

At last follow-up visit, 22% of Group 1 and 11% of Group 2 patients were receiving no antiepileptic drugs (AED). Twenty-seven percent of Group 1 and 19% of Group 2 patients were receiving a more modest AED regimen while 51% and 70% were under a drug regimen similar to the pre-operative one, respectively.

There was no surgical morbidity or mortality.

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4. Discussion 

Our data showed that patients with TLE and normal MRI could get good surgical results after CAH although 60% of them would need invasive recordings and their results regarding seizure control were worse than those obtained in patients with MRI defined temporal lobe lesions.20 Many of our patients did undergo thinner and volumetric MRI acquisition and 3T examinations as well. Since we did not want to mix patients with different MRI quality in this subset of patients, we used the minimal common MRI definition/quality among them. On the other hand, although we do agree that these are not the state-of-the-art parameters for hippocampal visualization, we noticed very little improvement in visual analysis diagnosis of MTS with thinner slices (or even 3T). Only one-quarter of the patients had MTS on the pathological specimen in this series, mainly of the end-folium type, which might not be recognized even with higher resolution MRI.

Previous studies reporting on patients with TLE and normal MRI included a lower percentage of patients undergoing invasive evaluation.21 This is likely related to the fact that many of these patients might have been considered not suitable for surgery based on their initial non-invasive work-up in these centers. Other authors published series in which they evaluated patients using exclusively non-invasive or invasive protocols.22, 23, 24 We analyzed a series of consecutive patients; there were no patients in the series that were denied surgery before invasive evaluation was carried out. The number of patients that required invasive evaluation in our series most likely represents the actual need for invasive investigation in this patient population.

Although PET and SPECT were available in some of our patients, these evaluations were not regularly performed. Some authors suggested that these functional studies might add to our ability to delineate foci in these patients,2, 11, 25, 26 but the results of these evaluations were not included in the final decision-making process in the present series. All patients underwent invasive recordings if non-invasive video-EEG evaluation was not localizing and lateralizing irrespective to any findings on PET or SPECT. The prominent predictor role regarding seizure outcome of ictal video-EEG in this patient population has already been reported.12

Wada test has been used to try to anticipate post-operative memory deficits in patients submitted to temporal lobe resection, although its importance, reliability and reproducibility was challenged in the recent years.27, 28 We used to submit all our patients that were candidates for temporal lobe resection to Wada testing (1992–1996), but this practice has been discontinued and we abandoned this type of evaluation. We have shown that it was not necessary in patients with mesial temporal sclerosis.20 Moreover, by that earlier time, patients with normal looking hippocampi consistently passed both injections of sodium amytal (personal communication), which did not generate much useful additional data in patients with normal MRI.

Few papers discussing surgical outcome in patients with TLE and normal MRI addressed neuropsychological outcome findings. This is somewhat unusual since the most prominent result in our series was the consistent neuropsychological decline after dominant temporal lobe resection in those patients with TLE and normal MRI, as noted by others.13 One standard deviation (for deterioration or improvement) is the usual standard practice in general neuropsychological testing. It might be considered “generous” while reporting cognitive improvement. On the other hand, in our patients with normal MRI, in whom we expected eventual deterioration (and not improvement) of cognitive functions, it might be considered strict, since patients with minimal impairment would be rated as having new deficits. Many of our patients performed within normal range on memory tests pre-operatively, despite the presence of medically intractable seizures. Although some of the patients would agree to trade seizure control for some degree of verbal memory loss, this was not true for many of them; some of them clearly stated post-operatively that they would prefer to keep seizing than having to cope with the new neuropsychological deficits. We were not able to define any clinical variable that could forecast the severity of verbal memory loss, although all patients were counselled to consider that they would get some verbal memory decline after surgery during the informed consenting procedure. We have been very reluctant to offer dominant temporal lobe resection to patients with suspected TLE and normal MRI over the last three years and had preferred the use of neuromodulatory techniques such as vagus nerve or deep brain hippocampal stimulation in this subset of patients. Non-dominant temporal lobe resections were not associated with major neurological or neuropsychological morbidity. The post-operative neuropsychological findings in the present series were in contrast to findings after CAH in patients with MTS. In the latter, cognitive decline is very rare and cognitive improvement is often seen.20, 29, 30, 31

Our findings suggested that patients with TLE and normal MRI could get good surgical outcome regarding seizures as far as there was at least 90% lateralization of the interictal discharges and ictal recordings clearly documented an unilateral seizure onset.32, 33, 34 We commonly use 90% of interictal discharges restricted to one hemisphere as a lateralizing sign in all our patients. This approach derived from our pre-MRI series, by the time we had to heavily rely on scalp EEG findings for localization and lateralization. The percentage of lateralized interictal discharges needed for correct lateralization of temporal lobe foci ranged from 70% to 95% in different series. In this sense, our 90% rate would be actually strict. Although extensively studied, there is no clinical or surface EEG characteristic to fully differentiate between neocortical and mesial temporal lobe epilepsy. Auditory simple partial seizures are thought to be characteristically neocortical in origin, but they were present in only 11% of our patients.

Our patients submitted to invasive recordings were implanted bilaterally with subdural grids. All patients underwent CT scanning to confirm electrode's position and post-operative status. The most caudal line of electrodes was implanted over the parahippocampus under direct microscopic vision. This was easily performed since the procedure was carried out through a temporal craniotomy. In many centers, strips and small grids might be implanted through burr holes and the exact position of the electrodes might be more difficult to ascertain; additionally, it might be more difficult to perform symmetric bilateral strips implantation through burr holes. This technique proved to be safe and effective in localizing foci in this patient population. It could be argued that we were not sampling the hippocampus directly, since no depth electrode was inserted together with the grids. On the other hand, the most caudal electrodes were lying under the parahippocampal gyrus yielding exactly the same type of recording as in patients with foramen ovale electrodes, which have been shown to adequately sample the hippocampal structures that are just nearby. We felt that the most important issue in this patient population would be to adequately cover the temporal neocortex since mesial structures looked normal on MRI and these patients were suspected of having neocortical TLE. Our findings that 86% of the patients did not have mesial lesions gave support to this initial notion. Some authors used strips35 instead of grids while implanting these patients. Strips could be inserted through burr holes obviating the need of a craniotomy (as is the case with grids), but it is extremely difficult to position strips bilaterally in a symmetric way and non-sampled cortical areas would always remain intermingled with the strip's electrodes. Others have preferred the use of depth electrodes to evaluate these patients,36 but depth electrodes would yield an even worse cortical coverage and additional epidural or subdural coverage would be needed. An association of subdural grids/strips and depth electrodes was also tried37; unfortunately, there was no adequate comparative study of these different invasive techniques.

Seventy-seven percent of our Group 1 patients were rendered seizure-free. Although this did not reach the seizure-free rate obtained in patients with mesial temporal sclerosis (MTS) (85–90%,20 this rate was significantly higher than that obtained in Group 2 patients. This might suggest that Group 1 patients behaved more like MTS patients regarding seizure control, although their neuropsychological outcome was worse. Although it might appear surprising, the absence of Engel class IV patients post-operatively in this series might be related to careful clinical, semiological and scalp interictal and ictal EEG pre-operative evaluation, which need to be highly suggestive of temporal lobe epilepsy, as noted by others38; surgical failure in this type of patient is usually related to misdiagnosis of temporal lobe epilepsy. On the other hand, our findings do suggest that good surgical outcome can be obtained in well-selected patients with normal MRI and TLE. It is not clear if further refinement of MRI technique would make it possible to disclose previously unnoticed temporal lobe lesions in this patient population or if these patients with normal MRI that failed surgery would prove not to have TLE at all. Forty percent of our patients were able to reduce their AED intake, and 12% of them were receiving no AED. These results were also inferior to those obtained in patients with MTS, but were superior to optimal medical therapy alone.

The only discrete pathological finding in this series was end-folium sclerosis. It is not possible at this point to establish if this finding would represent a precursor type of MTS or not.39, 40

Temporal lobe resection has been shown to be superior to optimal medical treatment in patients with mesial temporal sclerosis.41 Although our results in patients with normal MRI are worse than those obtained in lesional patients, they are superior to those obtained with medical therapy alone. Patients with TLE and normal MRI might get good surgical outcome as far as they are adequately investigated and counselled.

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Conflicts of interest 

None of the authors has any conflict of interest to disclose.

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References 

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PII: S1059-1311(10)00087-7

doi:10.1016/j.seizure.2010.04.012

Seizure: European Journal of Epilepsy
Volume 19, Issue 6 , Pages 319-323, July 2010

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