Increased neocortical spiking and surgical outcome after selective amygdalo-hippocampectomy

19.5

Epilepsy Research, 16 ( 1993) 1955206 0920-121 l/93/$06.00 11:~1993 Elsevier Science Publishers

EPIRES

B.V. All rights reserved

00607

Increased neocortical spiking and surgical outcome after selective amygdalo-hippocampectomy

F. Cendes,

F. Dubeau,

Department @Neurology

A. Olivier, A. Cukiert, F. Andermann*

E. Andermann,

L.F. Quesney,

and Neurosurgery, McGill University and the Montreal Neurological Hospital and Institute. 3801 University St., Montreal, Que.. Canada H3A 2B4 (Received

30 April

1993; revision

received

15July 1993; accepted 20 July 1993)

Abstract We studied prospectively inserted

through

interictal made

the electrocorticogram in 13 consecutive

spiking,

at the amygdala

recorded

either independently

abnormality

spikes and polyspikes,

separated in 1958.

by Niemeyer

The outcome ECoG

was comparable

and

interictal

spiking

following

and a different

background,

to that of standard

is often used to tailor the amount

after

recorded

anterior

of resection,

transcortical

selective

ECoG was performed

hippocampus.

parahippocampal

in all 16 patients

by attenuated

immediately

in three others.

Before

from the depth and surface.

This is not the case in selective amygdalo-hippocampectomy. increased

and

and anterior

amygdala

was observed

reported

before

and retrospectively

T2 aimed

in T2. The hippocampus,

epileptiform

(ECoG)

patients

gyrus

resection

the ECoG

or synchronously. were

removed

ECoG pattern

temporal

resection:

subpially.

emerged.

suggesting

62.5% class

of epileptic

that a different

and two depth electrodes

showed

a variable

A small cortical

from the most anterior

and the persistence

amygdalo-hippocampectomy,

with surface

After

It consisted temporal

incision

amount

the resection.

of repetitive,

of

(2-3 cm) was increased

high amplitude

area. Similar observations

were

I and 25% class II (Engel’s scale).

abnormalities underlying

correlates mechanism

with worse outcome. is responsible

for the

this procedure.

Key words: Electrocorticography;

1. Introduction Electrocorticography (ECoG) can be performed before epilepsy surgery to help in the localization of the epileptogenic area, using the spatial distribution of interictal spiking [ 1,4,10,17,23,27]. However, the role of ECoG in defining the region of epileptogenic tissue to be removed remains uncertain and controversial [6]. The intuitive notion that *Corresponding author. Tel.: (514) 398-1976; Fax: 514-398-8540

EEG; Temporal

lobe epilepsy

a more complete resection of the area producing spikes is associated with better outcome has been supported by several studies [4,6,18,26], but refuted by others [8,11,20]. It is also possible that the significance of remaining spikes after surgical excision differs according to the anatomic location of the focus (i.e., temporal lobe and extra-temporal), and the underlying pathological substrate (i.e., different types of structural lesions and lesions not detectable by imaging). The first report of ECoG findings after selective amygdalo-hippocampectomy was published by

196

Niemeyer who introduced this surgical approach for the treatment of temporal lobe epilepsy [Zlf. In the present study we analyzed the surgical outcome, the results of ECoGs before and immediately after selective amygdalo-hippocampectomy, and post-operative scalp EEGs in 16 patients.

vier. After exposure of the temporal neocortex, ECoG was performed with 16 carbon-tip electrodes placed on the surface of the cortex. The electrodes were about 1 cm apart in an antero-posterior direction and approximately 2 cm apart in the supero-inferior plane. After initial recording, two 5-contact depth electrodes were inserted through the second temporal gyrus (T2), approximately 4 and 5 cm from the temporal tip, aiming at the amygdala and at the anterior hippocampus respectively. After the initial ECoG a small cortical incision (2 cm) was made in T2 and a thin corridor was fashioned through the temporal subcortical white matter until the roof of the temporal horn was reached. The hippocampal formation was dissected by subpial resection with the ultrasound dissector (CUSA). The parahippocampal gyrus was then removed, the hippocampus tifted laterally and transected at the level of the tail and removed en bloc. The removal proceeded with the resection of the amygdala and uncus [24]. After this a postresection ECoG was performed with the same position of surface electrodes as before. In seven patients a flexible electrode was placed on the stump of the hippocampus. All patients were operated under general anesthe-

2. Patients and methods We studied 16 patients (mean age, 30.6 years; range 15-51 years; seven men and nine women) with medically intractable temporal lobe epilepsy who unde~ent selective transcortical amygdalohippocampectomy. Results of ECoG were analyzed prospectively in 13 consecutive patients and retrospectively in three consecutive patients who had pre- and post-resection ECoG. All patients underwent an extensive presurgical evaluation that included long-term video-EEG monitoring, neuropsychological evaluation, intracarotid sodium amytal study and MRI scans, including volumetric studies in nine patients [5,30]. The preoperative EEG recordings were reviewed, in order to assess the interictal epileptic abnormalities. The surgical technique was inspired by Niemeyer’s approach [21,22] and modified by A. Oli-

TABLE

1

Patients’

demographic

Pt. #

Sex

Age

data Age of onset

EEG lateralization

MRI

11 years 24 years 3 years

right TL right TL tight TL left TL left TL right TL right TL left TL right TL left TL left TL left TL left TL right TL right TL left TL

Rt AM + Rt AM + Lesion Rt Lt AM + Lt AM + Rt AM + Rt AM + Lt AM + NL Lt AM + Lt AM + Lt AM + NLa Lt AM + Lesion Rt Lt AM +

(years)

-

I

12 13 14 15

F M F M M F M F M F M F M F F

16

F

2 3 4 5 6 7

8 9 IO

11

“Includes

18 51 29 15 36 25 23 38 35 30 36 21 36 43 21 33

I year 8 months I year I3 years 18 years 20 years 13 years 25 years 3 years 32 years 36 years 3 years 2 months

MRI volumetric

AM = amygdala,

HF =

NA = not available,

MTS

-

HF atrophy” HF atrophya parahipp HF atrophy HF atrophy HF atrophy HF atrophy’ HF atrophy” HF atrophy + sig HF atrophya HF atrophy + sig HF atrophy” mesial TL* HF atrophy + sig

Pathology

Follow-up (months)

Outcome class

MTS Mod MTS Mild Glioma NA MTS Sev NA MTS Mod MTS Mod MTS Mild MTS Mild MTS SW NA MTS Mild MTS Mild MTS Mild MTS Sev

18 1x 13 8 19 96 18 19 16 25 16 89 18 27 12 28

fl III

I 11

I I

I I I

I II

I II III

I I

study.

hippocampalformation,NL = mesial temporal

sclerosis,

= normal, Mod

+sig

= hyperintense

= moderate,

signal in TZweighted

Sev = severe.

images.

197

sia with nitrous droperidol.

oxide, associated

The length

of ECoG

and

cal outcome

varied

post-operative

with fentanyl recordings

showed EEGs,

epileptiform but

similar

discharges

on

abnormalities

from 15 to 25 min.

were seen in the EEGs

Follow-up scalp EEGs were performed between 7 and 15 days after surgery in all patients, except in

been seizure free since surgery (Table 2). Surgical outcome was 62.5% class I (seizure

two

2

free), 25% class II (rare seizures),

1

III [9].

who

had

the

first

post-operative

months after the operation. Five patients year follow-up EEG recordings.

EEG had

Surgical outcome was assessed based on serial follow-up visits with the patient and family members. The outcome was classified according to Engel’s scale [9]. The mean post-operative follow-up was 27.5 months (ranging from 8 to 96 months). All but one patient had at least 12 months followup. 3. Results Table

1 summarizes

the

patient

demographic

data. The preoperative EEGs revealed a unilateral, or predominantly unilateral temporal lobe interictal epileptic abnormality, maximal over the mid and inferomesial temporal region. At least three of the patient’s habitual seizures were recorded. All had exclusively or predominantly unilateral seizure onset maximal over mesial temporal lobe regions (sphenoidal electrodes). MRI studies showed atrophy and/or abnormal T2 signal in the mesial temporal structures in all but two patients. The ECoG before the resection showed a variable ampunt of interictal spiking from the depth, either independently or synchronously with the surface electrodes. After the selective removal of mesial temporal structures, an increase in epileptiform abnormality was observed in all patients and a different pattern of ECoG emerged. This consisted of repetitive, high amplitude spikes and polyspikes separated by attenuated background, maximal over the anterior temporal region (see Figs. l-3). The follow-up EEGs showed no interictal epileptiform abnormalities in eight (50%) patients, and occasional epileptiform discharges in four (25%). Frequent epileptiform abnormality was recorded in the remaining four (25%) patients, and in two of them, 1 year follow-up recordings showed no epileptiform discharges. Patients with poor surgi-

of those patients

who had

and 12.5% class

4. Discussion Several studies assessed the value of ECoG in outlining the region of epileptogenic tissue to be resected during anterior temporal lobe removal and extra-temporal corticectomies, and in predicting the outcome of surgery. However, the results of studies somewhat contradictory these are [2,4,6,8,10,18,23,26,28,29]. Two important questions about ECoG are still to be answered: (a) the relation between post-resection epileptiform abnormalities and surgical outcome, and (b) when and how much additional cortex should be removed in the presence of post-resection epileptiform abnormalities. Different studies agree that patients with good surgical outcome show residual spikes less often after anterior temporal lobe resection as compared to those patients with poor surgical outcome. However, this difference is found to be statistically significant in some studies but not in others. In all studies there are patients with epileptiform abnormalities on post-resection ECoG that become seizure free after operation and vice versa. This complex issue may perhaps be explained by different underlying pathological mechanisms. This can be exemplified by an early study, in which Jasper et al. [16] found a good correlation between ECoG and operative results. The persistence of epileptiform abnormalities predicted poor surgical outcome in 75% of patients. When they described three of the exceptions, namely patients who received a poor ECoG prognosis and yet showed a good clinical result, it became apparent that one patient had had prolonged febrile convulsions, involving the right hemibody and followed by right hemiparesis at the age of 11 months, and the other two had well delimited posttraumatic lesions resected. Those two conditions are known to lead to good surgical outcome for seizure control. This illustrates that the prognostic

198

199

200

c

202

203

204

TABLE 2 ECoG and follow-up EEG results pt f#

Interietal EEG pre-operativea

EC&

1 2 3 4 5 6 7 R 9 10 11 12

right TL right TL BiT right > left left TL BiT left > right right TL right TL BiT leftlright right TL left TL left TL left TL left TL right TL BiT right z left left TL

HF AM, NC HF, NC AM, HF, NC +AM, HF, NC AM, HF. NC AM AM, f HF AM, HF, NC AM, HF. NC AM, HF, NC AM, HF, NC

few SSW Lt TL NEA very frequent EA Rt TL NEA NEA occasional EA Lt TL frequent EA Lt TL occasional EA Lt TL NEA

AM, HF. NC

NEA

AM, HF AM, HF, NC + AM, HF. NC

NEA NEA

13 14 I5 lb

(4: 1) (5: I)

(5~1)

(3:I)

before resection”

EEG post-op. (S--15 days)

Follow-up EEG (I 2 months)

Follow-up

EEG

1 year

NEA few SSW Rt TL NEA NEA

NEA NEA

NEA

NEA

NEA

NEA occasional

EA Rt TL

occasional

EA Rt TL

few SSW Lt TL

“Interictal epiieptiform abnormalities were considered to be unilateral when occurring in one side more than 90% of the time during wakefulness. All patients had exclusively or predominantly unilateral ictal EEG onset over mid and inferomesial temporal regions. bLocalization of epileptiform spikes. The post-resection ECoG showed more intense spiking over the anterior temporal neocortex in all patients. AM = amygdata, HF = hippocampal formation, NC = neocortex, + AM = more intense spiking over the amygdata region; + HF = more intense spiking over the hippocampai region. NEA ==no epileptiform abnormality; EA = epileptiform abnormality; few SSW = EEG with fewer than five slow sharp waves, not definitely epileptifo~. Rt = right, Lt = left, TL = temporal lobe.

value of ECoG will be better defined only when analyzed in relation to underlying clinico-pathological conditions. In temporal lobe epilepsy, patients with proven mesial sclerosis should be analyzed separately from those with small cortical lesions [12] or neuronal migration disorders [25]. Patients with dual pathology [3,19] should not be included in either of these two groups. Very little has been reported about ECoG in selective amygdalo-hippocampectomy, since no cortical removal is contemplated during this procedure. Niemeyer originally described that the ECoG surprisingly worsened in patients who had a selective amygdalo-hippocampectomy, but in early post-operative scalp EEGs this abnormality then disappeared [21]. We found that all patients in the present study showed consistent worsening of ECoG, with very frequent epileptifo~ discharges. This finding, however, did not correlate with the surgical outcome. Activation of spikes after cortical resection is a

well-known phenomenon, though this is not very frequent after anterior temporal lobe removal [ 1,13,23,29]. Post-resection ECoG sharp waves and spikes may represent transient response to injury, but this alone is unlikely to explain the consistent increase in spiking following selective amygdalo-hippocampectomy, since the injury caused during this procedure is less than that due to temporal lobe removal en bloc. One possible explanation for this phenomenon is the acute disconnection of pathways between the lateral cortex and mesial structures, especially the amygdala. Suppression-burst activity from isolated cerebral cortex has been previously described [7,14,15]. In 1950 Henry [ 14] reported electrocorticograms of 25 patients before, during and after several different types of lobotomy. Following the section or undercutting there was a reduction in the amount and voltage of frontal fast activity and an increase in large slow waves, resulting in a fairly characteristic pattern of rhythmic bursts of fast activity separated by variably long periods of ‘flat’ record. In

205

a subsequent cluded judged

study

that

the

Henry

and Scoville

suppression-burst

from its continued

[15] con-

activity,

presence

as

at the time of

repeat operations, persisted over a year in the electrocorticogram of undercut cortex, but was not detected in the scalp EEG. Echlin et al. [7] reported paroxysmal high voltage discharges from isolated

and partially

isolated

human

and animal

ment of temporal 5 Cendes,

F.. Andermann,

metric measurements

experience have not fully clarified the relevance of ECoG findings in relation to outcome of surgical treatment of epilepsy.

Neurology,

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cerebral cortex. They found that this phenomenon appeared fundamentally the same in humans and animals whether from areas of frontal, parietal or temporal cortex, and that “with partial isolation the background activity became suppressed and bursts or spindles . . were more evident”. They also concluded that injury as well as ischemia may play a part but not the most important one, because one would expect more erratic discharges arising first at one cut surface, then at another. On the contrary this activity was very consistent, both in pattern and quantitatively, and was absent in the immediately neighboring cortex [7]. Although the mechanism for activation of neocortical spikes after selective amygdalo-hippocampectomy is yet to be clarified, the clinical signiticance of these spikes certainly differs from those observed after anterior temporal lobe removal en bloc or extra-temporal neocortical resection. Different underlying mechanisms, depending on the cerebral localization, type of pathology and surgical approach, may explain why 55 years of clinical

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