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Epilepsia, 47(8):1300–1307, 2006Blackwell Publishing, Inc.C 2006 International League Against Epilepsy

Foramen Ovale Electrodes Can Identify a Focal Seizure Onset

When Surface EEG Fails in Mesial Temporal Lobe Epilepsy

∗Tonicarlo R. Velasco, ∗Americo C. Sakamoto, ∗Veriano Alexandre Jr., ∗Roger Walz, ∗Charles L.

Dalmagro, ∗Marino M. Bianchin, ∗†David Araujo, ∗†Antonio C. Santos, †Joao P. Leite, ‡Joao A.

Assirati, and ‡Carlos Carlotti Jr.

∗CIREP, Centro de Cirurgia de Epilepsia, Faculdade de Medicina de Ribeir ˜ ao Preto, †Departamento de Neurologia, Psiquiatria e

Psicologia M edica, and ‡Departamento de Anatomia e Cirurgia, Universidade de S ˜ ao Paulo, S ao Paulo, Brazil

Summary: Purpose: We analyze a series of patients with

mesial temporal lobe epilepsy (MTLE) associated with hip-pocampal sclerosis (HS) submitted to presurgical investigationwith scalp sphenoidal, followed by foramen ovale electrodes(FO), and, when necessary, with depth temporal electrodes. Wesought to evaluate the clinical utility of FO in patients withMTLE-HS.

Methods: We included patients who had phase I investigationwith bitemporal independent seizures, nonlateralized ictal on-sets, or ictal onset initiating in the side contralateral to the sideof hippocampal sclerosis. Patients whose implanted FO failedto demonstrate an unambiguous unilateral ictal onset were laterevaluated with depth hippocampal electrodes.

Results: Between May 1994 and December 2004, 64 patientsmet our inclusion criteria: 33 female (51.5%) and 31 male sub-

jects (48.5%). The mean age at enrollment was 37.66 ± 10.6

years (range, 12–56 years). The groups with nonlateralized sur-face ictal EEG onsets and contralateral EEG onsets had a greaterchance of lateralization with FO when compared with the groupwith bilateral independent seizures on surface EEG (p < 0.01).Foramen ovale electrodes lateralized the seizures in 60% of pa-tients. Seventy percent of patients became seizure free after tem-poral lobectomy. Five patients were implanted with depth tem-poral electrodes after FO video-EEG monitoring. The depth-electrode EEG onsets confirmed the results of FO video-EEGmonitoring in all patients, and the surgery was refused.

Conclusions: In MTLE-HS, FO is a reliable method for lat-eralization of seizures that are not clearly recorded by sur-face EEGs. Key Words: Epilepsy—Mesial temporal lobeepilepsy—Epilepsy surgery—Foramen ovale electrodes—EEG.

Mesial temporal lobe epilepsy associated with hip-

pocampal sclerosis (MTLE-HS) is the commonest type

of pharmacologically intractable epilepsy. However, after

a careful preoperative evaluation, 60–70% of MTLE-HS

patients can be rendered seizure free after temporal lobec-

tomy (1).

In many candidates for temporal lobe resection, the

seizure focus can be accurately lateralized and patients

selected for surgery by using noninvasive investiga-

tions, such as high-resolution magnetic resonance imaging

(MRI), noninvasive video-EEG monitoring, and positron

emission tomography (PET) and single-photon emission

computed tomography (SPECT) studies (2). Surface inter-

ictal and ictal EEG recordings remain an essential element

of the presurgical evaluation in patients with MTLE-HS

to demonstrate the presence of unilateral epileptogene-

Accepted February 6, 2006.

Address correspondence and reprint requests to Dr. T.R. Velasco atCIREP 4◦ andar, Hospital das Clinicas de Ribeirao Preto, Universidadede Sao Paulo 14.048-900, SP, Brasil. E-mail: [email protected]

doi: 10.1111/j.1528-1167.2006.00547.x

sis. Notably, the definition of the seizure-onset zone by

surface ictal EEG generally provides an accurate estima-

tion of the epileptogenic zone, defined as the area of cor-

tex necessary and sufficient for the generation of clinical

seizures (3).

However, in ∼30% of MTLE-HS patients, scalp-

sphenoidal EEG recordings fail to demonstrate an un-

ambiguous unilateral ictal onset, showing contralateral,

bitemporal independent, and nonlateralized ictalonsets, or

the surface EEG recordings are not interpretable because

of movement artifacts (4,5). Conversely, a bilateral scalp

onset is still compatible with a unilateral mesial temporal

onset and should not deter further surgical assessment (6).

When noninvasive studies remain nonconcordant or un-

certain regarding the localization of seizure onset, invasive

studies such as those with depth electrodes may be needed

(7). Nevertheless, the proportion of patients evaluated with

depth electrodes has decreased over the last decade, be-

cause of our increasing ability to localize epileptogenic

lesions such as HS with high-resolution MRI, and because

invasive electrodes carry considerable costs and risks of

complications (3).

1300



FORAMEN OVALE ELECTRODES IN TEMPORAL LOBE EPILEPSY 1301

To record from the mesiobasal aspect of the temporal

lobe, Wieser et al. (8–10) developed a subdural electrode

inserted through the foramen ovale (FO). This procedure

is safe and can be an alternative to invasive implantation

of depth electrodes in MTLE patients who are candidates

for temporal lobectomy.

Here we describe a series of patients with MTLE-HSsubmitted to a progressive presurgical investigation with

scalp sphenoidal, followedby FO anddepthtemporalelec-

trodes when necessary. Our findings agreed with previous

descriptions showing that, in patients whose surface EEG

fails to demonstrate an unequivocal unilateral ictal onset,

FO might provide relevant and sufficient information to

give an indication for resective surgery.

METHODS

Subjects

Patients with suspected MTLE-HS evaluated at the

Ribeirao Preto Epilepsy Surgery Center at University of Sao Paulo School of Medicine, between January 1996 and

June 2004, were included in the study. The presurgical

protocol was approved by our University Hospital Ethics

Committee, and an informed consent was obtained from

all subjects.

Phase I investigation for epilepsy surgery consisted

of an assessment made by a neurologist with expertise

in epileptology, structural and functional neuroimaging,

neuropsychological examination, and scalp-sphenoidal

video-EEG monitoring.

The decision to implant FO was based on the results of

the phase I investigation. Patients with a clear hypothesisregarding the location of the epileptogenic zone in mesial

temporal lobes, but whose surface EEGs failed to demon-

strate unilateral ictal onsets, were submitted to investiga-

tion with FO. When implanted FO also failed to demon-

strate an unambiguous unilateral ictal onset, patients were

further evaluated with depth temporal electrodes.

The inclusion criteria were (a) medical history and

seizure semiology consistent with intractable MTLE, usu-

ally with epigastric, autonomic, or psychic auras, followed

by behavioral arrest, progressive clouding of conscious-

ness, oroalimentary and manual automatisms, and auto-

nomic phenomena; (b) no other lesion than the presence of

atrophy or hippocampal signal changes at high-resolution

MRI; and (c) ictal EEG with bitemporal independent ic-

tal EEG onsets, nonlateralized ictal onsets, or ictal onsets

initiating contralateral to the temporal lobe with focal ab-

normalities detected on high-resolution MRI.

Vıdeo-EEG monitoring

Video-EEG analysis

EEG signals were obtained by using a digital video-

EEG system (Vangard Systems, Cleveland Clinic Foun-

dation, Cleveland, OH, U.S.A.). Surface electrodes were

placed over the scalp according to the international 10–20

system, added by temporal electrodes positioned accord-

ing to the “10–10 system” plus bilaterally placed sphe-

noidal electrodes. At least two events similar to the pa-

tient’s habitual seizures were recorded.

Interictal spikes

The frequency, lateralization ratio, and localization of

interictal spikes (ISs) were visually assessed by board-

certified electroencephalographers.For the analysis of ISs,

5-min EEG samples were collected every hour, 24 h/day.

Spikes and sharp waves were defined according to the In-

ternationalFederationof Clinical Neurophysiology guide-

lines.

Ictal-onset zone

The ictal-onset zone (IOZ) was independently assessed

on ictal video-EEG by two investigators, and when the

results were discordant, they were reviewed together to

achieve agreementaboutthe localization and lateralizationof seizure onset.

Foramen ovale electrodes insertion

Commercially available FOs (AdTech) with four con-

tacts at 5-mm intervals were implanted percutaneously

with the aid of a fluoroscope under light general anesthe-

sia. Electrodes were positioned in such way that the tip

(contact 1) was located at the end of the ambient cistern,

with contact 4 placed just above the level of the foramen

ovale. Immediately after the procedure, a skull radiograph

was taken to confirm whether the FO implantation posi-

tions were adequate and bilaterally symmetrical.

MRI-guided stereotactic depth electrode implantation

A surgical plan based on an entry and target points on

axial and sagittal images was defined for the insertion of

depth electrodes. Navigational views, using three-planar

images, were performed to determine which structures the

electrodes would pass through to be correctly placed in

the amygdala and hippocampus. The correct site of depth

electrode implantation was confirmed by MRI.

Neuroimaging

Neuroimaging studies included high-resolution MRI

(1.5-T Siemens Magneton Vision, Erlangen, Germany)

with special protocols for epilepsy and interictal and ictalSPECT. Based on visual analysis of MRI, the neuro-

radiologists classified hippocampal sclerosis as (a) uni-

lateral, when hippocampal atrophy (on T1-weighted 1-

mm isotropic-voxel SPGR sequence) or increased signal

(on T2-weighted sequences: turbo-spin echo and fluid-

attenuated inversion recovery sequences) were observed

in oneside;or (b) bilateral, when thehippocampalchanges

were observed on both sides.

If the abnormality was increased signal intensity with-

out hippocampal atrophy, the radiologists did not clas-

sify it as HS. However, increased hippocampal signal

Epilepsia, Vol. 47, No. 8, 2006



1302 T. R. VELASCO ET AL.

intensities were considered abnormal for the lateraliza-

tion of neuroimaging features and for the correlation with

ictal studies.

Surgical outcome was defined according to the classi-

fication proposed by Engel (11).

Statistical analysis

The χ2 test or Fisher’s exact test was used to establish

correlation between categoric variables. A t test or Mann–

Whitney test was used to analyze numeric variables, such

as age at seizure onset, age, or epilepsy duration.

RESULTS

Clinical and demographic data

The clinical, demographic, MRI, and neurophysiologic

data are summarized in Table 1. Between 1996 and 2004,

65 patients were submitted to evaluation with FO and

were included in the analysis: 35 female (53.8%) and

30 male patients (46.2%). The mean age at enrollment

was 37.8 ± 10.1 years (range, 12–59 years). The mean

age at epilepsy onset was 12.2 ± 6.9 years (range, 1–

36 years). The epilepsy duration was 25.5 years ± 9.8

years (range, 4–45 years). The mean seizure frequency be-

fore surgery was 6.8± 7.5 seizures per month. Thirty-five

(53.8%) patients had initial precipitant insults (IPIs), and

prolonged febrile seizure was the most common type of

IPI (60%). The mean age at IPI was 3.2± 4.7 years (range,

1–28 years).

MRI findings

Thirty-one (47.6%) had bilateral abnormalities, 25 with

bilateral asymmetrical and six with bilateral symmetri-cal abnormalities. Thirty-four patients had unilateral MRI

findings: 18 (27.7%) patients had right HS, 15 (26.2%)

patients had left HS, and mild left increased hippocampus

signal intensity without hippocampal atrophy was found

in one (1.5%) patient.

EEG data

The mean duration of video-EEG monitoring (VEEG)

with scalp-sphenoidal electrodes was 6.0± 2 days (range,

2–13 days). The median of recorded seizures was five

seizures (range, 2–17 seizures). The most frequent reason

for FO implantation was independent bilateral seizures re-

vealed by surface EEG in 26 (40.0%) patients, followedbysurface EEG onsets contralateral to the side of hippocam-

pal atrophy in 23 (35.4%) patients, and nonlateralized ictal

discharge onsets in 16 (24.6%) patients. In the nonlateral-

ized group, eight (50%) patients had bilateral HS.

FO evaluation revealedunilateral EEG onsets ipsilateral

to the side of HS in 19 patients with unilateral HS and

ipsilateral to the side of the more intense HS in 14 patients

with bilateral asymmetrical HS.

In the nonlateralized group by surface EEG, 14 (87.5%)

of 16 patients had lateralized EEGs during FO evaluation.

In the group with contralateral surface EEG onsets, the

proportion of patients with lateralized EEGs was 52.2%

(12 of 23 patients). These groups had a greater chance of

lateralization with FO when compared with the group with

bilateral independent seizures on surface EEG (34.6%,

nineof 26; p< 0.01). In eight patients, the FO EEG onsets

were unilateral but contralateral to the side of HS, and

depth electrodes were indicated.In relation to the lateralization of HS, 10 (32.2%) of 31

patients with bilateral HS revealed bilateral EEG onsets

during FO recording, and 10 (29.41%) of 34 patients with

unilateral HS had bilateral EEG onsets (p= 0.66, Fisher’s

Exact test).

Five patients were submitted to implantation of depth

temporal electrodes after FO video-EEG monitoring. The

indications for depth electrodes were bilateral EEG onsets

(four patients) and seizures contralateral to the side of HS

(one patient) revealed during FO evaluation. The depth-

electrode evaluation results yielded findings very similar

to the results of FO VEEG monitoring in all patients, and

the surgery was refused. Fifteen (23%) patients who had

bilateral or contralateral EEG onsets on FO recordings are

currently waiting for depth-electrode evaluation.

In one patient, the FO electrode had bilateral indepen-

dent EEG onsets and depth electrodes were added, allow-

ing simultaneous FO and depth-electrode recordings. MR

imaging of implanted electrodes revealed that the FO elec-

trodes were in close relation to the parahippocampal gyrus

(Fig. 1B and C). The EEG recordings in this patient re-

vealed that the time of EEG onsets in FO electrodes were

within 0.3 to 1.7 s apart from the EEG onsets in depth

hippocampal electrodes (Fig. 2A).

Complications

The complications related to FO implantation were

transitory, as follows: (a) temporary facial pain (12 pa-

tients); (b) hypoesthesia in trigeminal territory (three

patients); (c) temporomandibular joint dysfunction (two

patients); (d) recurrence of labial herpes (two patients); (e)

retromandibular hematoma (one patient); and (f) transient

complete atrioventricular block induced by FO insertion,

despite premedication with atropine (one patient). In three

patients, the insertion of FO was difficult, and the record-

ings revealed asymmetry of the background EEG.

Postsurgical dataIn 31 (47.7%) patients,the results of FO revealed unilat-

eral EEG onsets, and temporal lobectomy was performed.

Two additional patients with>90% of seizures originating

from the side of unilateral HS underwent temporal lobec-

tomy. Twenty-three(70%) of 33 patients had good postsur-

gical outcome after temporal lobectomy (Engel classes I

andII). Theproportion of patients with Engel I seizure out-

come was 80% in patients with unilateral HS in compar-

ison with 53.8% in patients with bilateral HS (p = 0.05).

In all patients who underwent temporal lobectomy, patho-

logic examination of the resected temporal tissue revealed





severe neuronal loss and gliosis in the CA1 and CA4 re-

gions, prosubiculum, and hilus, and discrete or moderate

neuronal loss of CA2 region and fascia dentata granule

cells.

Six patients refused the procedure, and three other pa-

tients with bilateral HS had the surgery contraindicated

because of risk of considerable memory deficits revealed

by intracarotid amobarbital memory testing.

DISCUSSION

Available data from autopsy and surgical studies sug-

gest that patients with temporal lobe epilepsy frequently

have bilateral hippocampal damage (12,13). However, HS

FIG. 1. A: Radiography from skull of patient 29 showing symmet-rical bilateral positioning of foramen ovale (FO) electrodes. Coro-nal (B) T1 and sagittal (C) magnetic resonance imaging imagesshowing the position of depth (arrowheads ) and FO electrodes(arrows ).

is usually asymmetrical and, when preoperative evaluation

data are concordant with the side of hippocampal atro-

phy, temporal lobectomy can be indicated, and postsurgeryoutcome is usually good (1). Clinical decision making is

more complicated when neurophysiologic and neuroimag-

ing data indicate bilateral involvement of mesial structures

(1,3). Although data from the present series indicate fre-

quent bilateral involvement of mesial structures, we found

evidence that FO evaluation provide accurate neurophys-

iologic data about lateralization of seizures that were not

clearly lateralized by surface EEGs.

In other words, despite the hypothetically poor post-

surgery outcome suggested by bilateral surface EEG

onsets and the high rate of patients with bilateral HS, FO




1306 T. R. VELASCO ET AL.

FIG. 2. A: Simultaneous foramen ovale (FO)(FO1 to FO8) and depth-electrode recordingsfrom anterior hippocampus (AH1 to AH10)of patient 29, showing a right temporal lobe

seizure EEG onset in AH2 and AH4 (black arrow ), apartonly0.3 s away from FO2 and FO4EEG onset (white arrow ). B, C: Progressionof seizure 10 and 30 s after the seizure onset.





evaluation substantially affected the presurgical evalua-

tion, indicating the side of temporal lobectomy in two

thirdsof these MTLE patients.It is importantto emphasize

that this proportion was similar in patients with bilateral

and unilateral HS revealed by MRI.

The signal-to-noise ratio of FO is better than that in the

scalp-sphenoidal electrode recordings (7–10). Thereforemany electrophysiologic events with lateralizing value are

detected by FO but remainundetected by scalp-sphenoidal

contacts (14,15). In our series, this permitted the indica-

tion of temporal lobectomy in 60% of cases that were

not lateralized by scalp-sphenoidal electrodes, with the

great advantages of being nontraumatic to the brain and

of carrying much less risk for the patient than the more-

invasive depth electrodes. Moreover, even in a sample of

patients with bilateral HS on MRI and apparent bilateral

surface ictal EEG onsets, 70% of the patients had good

postsurgical outcome after temporal lobectomy, provided

that unilateral EEG onsets were defined by FO. This pro-

portion is very similar to previous descriptions of patients

with MTLE (1,10,11).

It should be stressed, however, that the FO recording

technique addresses only specific questions:if the seizures

originate in the mesiobasal temporal lobe structures and

if they are consistently lateralized. In other words, a

clear hypothesis should exist regarding the location of the

epileptogenic zone, derived from noninvasive studies. In

previous descriptions of FO, it has been stated that, in

comparison to the presurgical examination using intrac-

erebral depth recordings, the information gained by FO

electrode recording is limited, and that the FO technique

cannot substitute for a proper depth-electrode evaluation(9). However, this conclusion was drawn before the recent

advances of neuroimaging. The advent of high-resolution

MRIhas allowed theproper selectionof patients that might

benefit from FO recordings, namely MTLE patients, ex-

cluding those patients with epileptogenic lesions outside

the mesiobasal structures.

In all the five patients in whom the result of FO elec-

trodesshowed bilateral independent or nonlateralized ictal

onsets, further recordings with depth electrodesconfirmed

the findings. This can be explained by the evidence of

the intimate relation of the properly placed FO electrode

with the parahippocampal gyrus, uncus, and lingual gyrus(Fig. 1C), and by the good correlation between the ictal

onsets in FO and depth electrodes (Fig. 2A).

In conclusion, our results indicate that, in properly se-

lected patients, FO is a reliable method for lateraliza-

tion of seizures that are not clearly recorded by surface

EEGs, usually providing sufficient information to indicate

epilepsy surgery. In addition, FO implantation is relatively

simple, well tolerated, and can substantially facilitate the

presurgical evaluation of patients who are candidates for

temporal lobectomy surgery by decreasing the risks of in-

vasive neurophysiologic evaluation without excessive loss

of information.Acknowledgment: This work was supported by FAPESP/

CINAPCE Project 0556447-7. Roger Walz was supportedby CNPq (472840/2004-5 and 301379/2005-0). Marino M.Bianchin was supported by FAPESD Project (02103743-0).

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