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Interictal and ictal activity recorded with subdural electrodes during preoperative evaluation for surgical treatment of epilepsy
U 1989 Demos Publications
Interictal and Ictal Activity Recorded with Subdural Electrodes During Preoperative Evaluation for Surgical Treatment of Epilepsy S. Blom, R. Flink, J . Hetta, 2 P . Hilton-Brown, 1 C. Hoffstedt, 2P. O. Osterman, and 3 B . Spannare
A total of 94 subdural strip electrodes were implanted in 22 patients during preoperative EEG evaluation for surgery of epilepsy . Eighteen patients had temporal lobe seizure onset, three had frontal lobe seizure onset, and one had occipital lobe seizure onset . Most electrodes (total, 83) were localized over the temporal lobe cortex, but in four cases additional strip electrodes (total, 11) covered the frontal, parietal, and occipital lobe cortexes. The electrodes were left in place for up to 28 days . No complications occurred . Interictally, focal spiking was recorded subtemporally, mostly without being seen in electrodes recording from the lateral temporal cortex . In three patients studied with simultaneous subdural and sphenoidal wire electrodes, spiking recorded from subdural electrodes was often not seen in the sphenoidal recording . There were 151 seizures recorded (with or without simultaneous video monitoring) . The mean number of seizures per patient was 6 .7 (range, 0-21) . The seizures were classified as having focal (80 seizures) or local (71 seizures) onset . It is concluded that subdural electrodes are safe and have a sufficient selectivity with regard to localization of interictal spiking and seizure onset in patients with mesial temporal epileptic lesions . In such cases, electrodes have to be placed subtemporally . Other cortical areas may also be explored with these electrodes . Key Words : Epilepsy- Surgery- SubduralSphenoidal- Ictal-Interictal .
Stereotactically implanted depth electrodes give precise and detailed information concerning both interictal and ictal activity during the preoperative evaluation in patients considered for surgical treatment of epilepsy. However, the implantation procedure is complicated and not free from risks (1) . Moreover, the electrodes are sometimes too selective, which can lead to misinterpretations (2) . As an alternative, sub-
From the Departments of Clinical Neurophysiology, 'Psychiatry, 2 Neurology, and 3 Neurosurgery, University Hospital, Uppsala, Sweden. Address correspondence and reprint requests to Dr . S . Blom, Department of Clinical Neurophysiology, University Hospital, S-75185 Uppsala, Sweden .
dural electrodes of different types have been used (3-6) . Since 1985, we have used Wyler subdural strip electrodes (Ad-Tech Co .) in patients with refractory simple partial seizures or partial complex seizures referred for surgical intervention . This study describes interictal and ictal findings in the patients studied with these electrodes. For comparison, EEG was simultaneously recorded with sphenoidal and scalp electrodes in three patients .
Material Since 1985, 109 patients have been referred to the Epilepsy Unit at the Neuroclinics in Uppsala for severe
I EPILEPSY, VOL. 2, NO. 1, 1989
9
Possible etiology
Seizures per month
Neurological exam
Unknown
Meningitis age 4 y; encephalitis? age 10 y
Trauma with dys- 90, most nocturphasia and nal Babinski +, age 15y
Encephalitis with 10-12 seizures, age 20 y
Probable neonatal injury
5/35/F/16
6/30/M/11
8/32/M/18
10/47/M/20
12/17/M/5
5-10
Unknown
Unknown
17/33/M/9
52/37/M/22
5-10
20-40
14/33/M/23 Trauma with GTC, age 9 y
4-10
2-15; serial seizures and GTC last 2 y
4-12 ; new seizure type and psychotic episodes last 2 y
Onset 2 weeks af- 4-6 ter childbirth
4/41/F/20
4-10
Unknown
3/31/F/26
CT : normal
CT and MRI : wide temp horn R
CT and MRI : normal
CT and MRI : normal
CT and MRI : normal
Neurological imaging
Table 1 .
Not studied
IQ normal, verbal compr subnormal
IQ normal, verbal compr subnormal
IQ normal (-), slow tapping, L (nondomin)
IQ normal, slow tapping, R (dominant)
Neuropsychology
Patient information
Normal
Normal
Clumsiness, R hand
Normal
Normal
IQ normal (+) slow performance
CT and MRI: normal
CT and MRI: normal
CT and MRI : wide temp horn R
IQ normal (-)
Not studied
IQ normal, slow tapping R (dominant)
MRI : bilat pane- IQ normal (-) tal subcortical abn
CT and MRI : normal
Minimal dyspha- CT: temp abn L ; IQ normal, verbal sia MRI : temp compr subnorand frontal abn mal L
Normal
Normal
Normal
Normal
Patients with seizures with temporal lobe onset (compare Table 2) 2/23/M/13 Unknown 15-20 Normal
Patient/age (years)/sex/ onset (years)
Sphenoidal spike focus L
Sphenoidal spike focus R
Sphenoidal spike focus R
Sphenoidal spike focus L
Temporal spike focus R
Sphenoidal spikes L
Frontotemporal spikes L > R
Sphenoidal R (+ temp L) spike focus
Sphenoidal spikes R > L
Sphenoidal R (+ temporal L) spike focus
Temporal spike tocus R
EEG (scalp + sphenoidal)
Head turning L or R, vocalization, unresp
Reports onset, vocalization, automatisms
Stare, unresp, mumbles, moves L hand
Reports onset, stare, unresp automatisms
Ictal signs (CCTV)
Reports onset, unresp, oral automatisms
Stare, unresp, head turn R
Stare, unresp, automatisms
Forced thinking, confused
Stare, unresp, automatisms
Confused, unable Stare, unresp, speak ; GTC automatisms
No perception of Stare, unresp, seizures automatisms
Nausea, taste ; GTC
Dizzy, confused
Unable to speak, confused
No perception of No seizures reseizure onset corded!
No perception of seizures
Epigastric sens, confused
No perception ; epigastric sens
Epigastric sens, confused
Ictal symptoms
No : amytal te! memory deb R
No : seizure on : R (and L) ; arr tal test: mer ory defect L
No : amytal tet memory deft R and L
L temp lobe res (gliosis?)
R temp lobe res (gliosis)
L temp lobe res (cicatrix + gliosis)
No; seizures ni recorded
No; amytal test memory clef( L
L temp lobe res (gliosis)
R temp lobe res (gliosis)
R temp lobe res (gliosis)
Surgery (PAD
Probable neonatal injury
Born prematurely (2,100 g)
Unknown
Meningitis with clonic seizure R, age 0 .5 y
Onset after vaccination, age 9 m
Unknown
58/23/M/14
64/23/M/0 .8
66/35/F/17
68/34/M/20
76/45/M/1
94/33/F/17
8-16
10-20
20-30
4-10
8-12
y 6-10
29-30; altered and increased seizures since 1
Normal
Normal
Normal
Normal
Normal
Spasticity R hand
Normal
Probable neonatal injury
Trauma with GTC, age 9 y
40/16/M/ birth
63/31/M/21
15-30; increasing rate and serial seizures last 2 y
8-10
15-20
Normal
Minimal hemianopia L
Normal
Sphenoidal spike focus R
Normal
IQ normal (+)
CT and MRI: normal
CT and MRI : frontopol small abn R
CT and MRI: occipital abn R
CR and MRI : normal
CT and MRI : parietal porencephalia L
No perception of seizure onset
Frontal spikes L and R Sphenoidal spiking R Sphenoidal spike focus R
IQ normal (-)
IQ normal (+), verbal compr subnormal IQ normal
Deja vu; sound R ear; automatisms
Sees white spot; confused
Vertigo
Nausea; confused
Deja vu; confused
Epigastric sens
No perception of seizures
No perception ; epigastric sens
No perception of seizure onset
Deja vu; can't understand
Temporal focus L
Slight mental retardation
Sphenoidal spikes R > L (+ frontal)
Normal
CT : normal; MRI : temp abn L?
CT and MRI : normal
Temporal spikes L
IQ normal, verbal compr subnormal
CT and MRI: normal Sphenoidal spike focus R
Sphenoidal spike focus R
IQ normal, verbal compr subnormal
CT : normal; MRI : temp medial abn R
Frontotemp spike focus L
Sphenoidal spike focus L
IQ normal (+), slow tapping R (dominant)
Memory and verbal fluency defect
CT and MRI : parieto-occipital atrophy L
CT : wide sulcus temporal cortex R
Abbreviations: abn, abnormality; age, age at study; compr, comprehension; F, female; L, left; M, male ; onset, age at onset of epilepsy; GTC, generalized tonic-clonic seizure ; R, right; unresp, unresponsive; y, year(s) ; sens, sensation; resec, resection .
Encephalitis?
9/19/M/1 .5
Patients with seizures with extratemporal onset (compare Table 3) 1/17/M/6 Probable neona8-16 Dystonia and tal injury hemianopia R
Trauma, unconscious one week, age 17 y
53/35/F/17
Reports onset, stare, moves R hand + pedaling; duration <30 s
Reports onset, stare, mumbles, adversive to L
Head turn R unresp, vocalization
Reports onset, stare, unresp, adversive to R
Reports onset, stare, unresp, automatisms
Reports onset, stare, unresp, chews, pedaling
Reports onset, stare, unresp, swallows
Stare, unresp, vocalization, slight pedaling
Reports onset, stare, unresp, moves hands
Deep breathing, unresp, tonic posture R
Stare, unresp, R hand to face
R frontopolar resec (cicatrix + gliosis)
R occip lobe resec (localized gliosis)
No : seizure-free after reduced medication!
No : multifocal seizure onset in language area
R temp lobe rese<
L temp lobe rese( (planned)
R temp lobe reset (gliosis)
L temp lobe rese, (gliosis)
R temp lobe res& (gliosis)
L temp lobe rese . (planned)
No: amytal test: memory defec R and L
a.
DLL/1V1 C 1 HL_
seizure problems of various kinds. There were three criteria for considering surgical intervention : (a) the seizures should be simple partial or partial complex, with or without secondary generalization ; (b) they should originate from a cortical region possible to remove without major neurological impairment ; and (c) thorough medical treatment trial with at least three major antiepileptic drugs in monotherapy had not given an acceptable result . In addition, most patients had been treated earlier with various drug combinations . Implantation of subdural electrodes was performed in 22 patients, in whom routine EEGs, including sphenoidal recordings during 12-18 h, or clinical and radiological data-computerized tomography (CT) and magnetic resonance imaging (MRI) scanninghad not provided a plausible localization of the epileptic lesion . Clinical data are summarized in Table 1 .
Methods Surgical Procedure The implantation of subdural electrodes was performed under general anesthesia with hyperventilation . Mannitol, 500 ml (150 mg/ml), was given intravenously prior to the operation . In all patients, one subdural strip electrode was placed subtemporally and one over the lateral temporal cortex bilaterally . The burr hole was made about 1 cm anterior to the external auditory meatus and just superior to the zygoma . As a guide for the strip electrode, a moistened infant feeding catheter (No . 8) was inserted 5 cm in the desired direction between the dura and the brain surface. The moistened strip electrode was then passed along this catheter . In three patients, additional electrodes were placed frontally, and one patient was also provided with electrodes over the medial and lateral occipital cortex . For electrode placements, see Fig . 1 . The total number of implanted electrodes was 94 . Before closing the wound, the electrodes were tested by recording the EEG . All the electrode wires were connected to a master cable, which was bandaged down the neck of the patient in order to reduce the risk of electrode dislocation during seizures . After electrode implantation, plain anterior-posterior and lateral skull films were taken to confirm the electrode position. Patients were not given antibiotics .
were recorded on a 17-channel Nihon Koden EEG machine with an amplification of 30 or 50 µV/mm (T .C., 0 .3; high-frequency filter, 70 Hz) . Activity from scalp and sphenoidal electrodes was recorded with an amplification of 10 µV/mm . The paper speed was 15 mm/s. Both patient and EEG were recorded with closed circuit television (CCTV), using split screen technique, which allowed detailed analysis of the electroclinical relationship . The recording started a few hours after surgery and continued daily . Sometimes the recording was also performed during the night, without video monitoring. In most cases, the monitoring was stopped when at least three seizures had been recorded . The subdural electrodes were then extracted . They were likewise extracted if the required number of seizures had not been obtained within 4 weeks . To evoke spontaneous seizures, medication was reduced after the implantation ; later, if necessary, medication was completely withdrawn. The videotapes with seizures were shown to the patients' relatives to confirm that they were the patients' habitual seizures . Analysis During the analysis of seizures, the videotapes were repeatedly replayed and relevant clinical symptoms noted on the EEG paper . The following parameters were noted : (a) seizure onset, defined as the moment when the interictal EEG activity suddenly was replaced by flattening (sometimes after an initial paroxysmal discharge), followed by a low-amplitude, high-frequency rhythm and then spikes-a seizure start was considered as focal if the onset was traced to one or two of the electrode surfaces, whereas it was classified as local if the onset was seen simultaneously in all three bipolar derivations from one strip electrode; (b) the time between EEG onset and first clinical symptom or sign ; and (c) the seizure duration, as appreciated from the EEG recording-in a few cases, the duration could not be measured, since it became necessary to disconnect the patient from the EEG machine during a seizure . Seizures with a secondary generalization are not included in the duration measurements .
Results Implantation
Recording Procedure Sequential bipolar montages from each strip electrode were used throughout the recordings . The EEGs 12
1 EPILEPSY, VOL . 2, NO. 1, 1989
The electrodes were implanted for 7-28 days . There were no complications such as bleeding, infection, or spinal fluid leakage. In two cases the strip electrodes
SUBDURAL
\/
Figure 1.
Schematic drawing of the localization
INTERICTAL
* 1i
AND ICTAL EEG RECORDING
I
20
of the 94 strip electrodes used in the study. The number ofstrips in each area is indicated
were dislocated during seizures by the patient pulling the electrode cable. However, this caused the patient no harm. The subtemporally inserted strip reached the uncus or the parahippocampal gyrus with its most me-
dial electrode. The distance from the midline to the most medial electrode was 2.2 f 0.5 cm (mean 31 1 SD; range, 1.54.2 cm) calculated from the anteriorposterior skull film (Fig. 2). Calculated from the latera1 skull film, the distance between the anterior pole
Figure 2. Frontal x-rayfilm shows electrode surfaces of the subtemporal and the lateral temporul strip, right side, in patient IO. The region of the x-ray film is indicated in the drawing (hatched area). The drawing also shows the electrode surfaces on the left side.
I EPILEPSY, VOL. 2, NO. 1. 1989
13
S. BLOM ET AL. 1
LST 1-2 2-3 3-4
/l j a
~4 , I
RST 1-2 2-3 3-4 L LTC 1-2 2-3 3-4 RLTC 1-2 2-3 3-4
Figure 3 . Patient 4, 43-year-old woman. Interictal recording, awake . Continuous sequence of spikes without clinical symptoms from electrode surface 3, left subtemporal strip electrode (channels 2 and 3) . Occasional spikes from electrode surface 1, right subtemporal strip electrode (channel 4) . Note absence of epileptiform activity in lateral temporal electrodes bilaterally . Focal onset from left subtemporal strip, surface 1 . Surgery: left anterior temporal resection, including hippocampus . Histopathology : gliosis. Seizure-free since surgery (17 months) . In this and subsequent figures the following abbreviations are used : LST, left subtemporal; RST, right subtemporal, • LLTC, left lateral temporal convexity; RLTC, right lateral temporal convexity . Note reduced paper speed (15 mm/s) in all figures .
of the temporal lobe and the medial electrode was 3 .2 ± 0 .7 cm (mean ± 1 SD ; range, 1 .7-4 .6 cm) .
Interictal Activity
Interictal, high-amplitude spiking was often prominent from the subdural electrodes . In several cases, interictal subtemporal spiking was recorded without simultaneous epileptiform activity from the ipsilateral temporal neocortex (Fig . 3) . In most cases with temporal lobe foci, interictal epileptiform activity was recorded from the subtemporal electrodes contralateral to the seizure-generating focus . The subdural electrodes could separate closely located spike foci (Fig. 4) . To compare the activity recorded from subdural electrodes with that recorded from simultaneous sphenoidal electrodes, bilateral sphenoidal wires were inserted in three patients . Most spikes recorded from the subdural electrodes were not detected by the sphenoidal wires (Fig . 5) . Slow background activity was, however, clearly seen in the sphenoidal recording. Recording from sphenoidal wires during implantation of subdural strip electrodes performed 14
1 EPILEPSY, VOL . 2 , NO. 1, 1989
in one case did not indicate that the intracranial strips attenuated the activity . Scalp electrodes were applied in three cases . Interictal epileptiform activity recorded only from the subdural subtemporal strip was not detected in the surface electrodes. Sharp waves and spikes recorded in the scalp leads were always recorded simultaneously with high-amplitude epileptiform potentials in the lateral temporal electrode strip .
Ictal Activity
Injuries did not occur during seizures, and status epilepticus did not occur. Secondary generalization occurred in 10 seizures in seven patients . Altogether, 151 seizures were recorded with the subdural electrodes . The results are summarized in Table 2. The number of seizures per patient was 6 .7 ± 5 .6 (mean ± 1 SD; range, 0-21) . The EEG seizure duration in seizures with clinical symptomatology was 82 ± 41 s (mean ± 1 SD; range, 30-158 s) . In one patient, no seizures were recorded in spite of daily monitoring for 4 weeks . In all but one patient (No . 9), the EEG seizure on-
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING
RST 1-2 2-3 3-4 R LT C 1-2 2-3 3-4
W
r
v'I
I500uV 1s
Patient 52, 37-year-old woman . Interictal recording asleep . Independent spiking from all electrodes in left subtemporal strip (channels 7-9) . Seizures started from left medial temporal structures . Resection not performed due to contralateral memory disturbance revealed by Wada test. Abbreviations as in Fig . 3 . Figure 4 .
L S T 1-2 2-3
Sph sin-F7 Sph sin-A1---L LTC 1-2 2-3
RST 1-2
µ
3-4 RLTC 1-2 ,,,..~,_,y`.t,,, 2-3 3-4 1300uV 1s
Patient 66, 34-year-old woman . Interictal recording awake. Simultaneous subdural and sphenoidal wire recording (channels 4 and 5) . Spiking in subdural electrodes (channels I and 2) not recorded in sphenoidal leads ; only slow components recorded . Surgery: left temporal lobectomy. Histopathology : gliosis. Abbreviations as in Fig . 3 . Figure 5 .
EPILEPSY, VOL . 2, NO. 1, 1989
15
S. BLOM ET AL.
Table 2 .
Patients with seizures with temporal lobe onset
Spread Patient
Region
Onset
Focal
Local
Unilateral
Bilateral
2 3 4 5 6 8
Right Right Left Right
Med Med Med Med
Left Right Right Left Right Left Left Right Left Left Left Right Left Right Right Left Right
Med Med Med Med Med Med Lat Lat Med Med Med Med Med Med Med Med Med
3 0 3 0 0 0 0 2 4 0 0 8 1 1 0 4 2 6 0 10 7 5
0 2 0 5 0 10 1 0 1 13 2 12 0 0 8 0 1 4 1 0 0 0
0 0 1 0 0 0 0 0 2 11 2 20 0 0 4 0 1 7 1 8 5 0
3 2 2 5 0 10 1 2 3 2 0 0 1 1 4 4 2 3 0 2 2 5
10 12 14 17 52 53 58 64 66 68 76 94
Abbreviations : Med, medial; Lat, lateral . set preceded the clinical ictal onset . Where the latency could be measured, it was 9 ± 6 s (mean ± 1 SD ; range, 4-22 s) . The onset was focal in 80 seizures (subtemporal, 47; lateral temporal, 9; frontal, 17 ; occipital, 7) . It was local in 71 seizures (subtemporal, 48; lateral temporal, 12 ; frontal, 10; parietal, 1) . Figure 6 shows a focal onset in medial temporal structures . In 17 patients, the individual seizures were clinically of almost identical appearance, and the EEG onset was confined to one side . Three of these patients have been rejected for surgery . Patient 1 had seizures that started in his dominant hemisphere . One seizure started focally from the angular gyrus, and one was confined to the Broca region . In patients 5 and 53, the amytal test contraindicated resection of the hippocampal epileptic focus . Four patients had seizures starting from alternating sides . Patients 8 and 66 were operated on, since their seizures contralateral to the side of surgery were single events and were regarded as withdrawal seizures. In patients 14 and 17, the amytal test contraindicated hippocampectomy . Short-lasting seizure activity from one electrode surface without spread to other areas was seen in some instances of seizures with 16
1 EPILEPSY, VOL. 2, NO . 1, 1989
clinical symptoms of auras . One example is patient 12 (Fig . 7), in whom the seizure activity was confined to one subtemporal electrode surface . The patient spontaneously reported his usual aura phenomenon, an unpleasant epigastric sensation . In patient 1, the seizure activity was located in the posterior part of the angular gyrus in the left dominant hemisphere . He reported a sudden dizziness. In patient 40, this type of focal seizure activity was limited to the anterior part of the lingular gyrus in the right occipital lobe . It was associated with a flickering light spot in the left visual field . In these patients, the complex partial seizures had seizure onset identical to the auras . Furthermore, when an aura was reported, there was always ongoing seizure activity. Seizure activity could spread and could involve more ipsilateral electrode surfaces (Fig. 8) . Seizure activity that spread to involve more ipsilateral, but not contralateral, electrodes-and thus remained unilateral-was usually accompanied by less pronounced clinical ictal symptoms in the patient, and no amnesia was reported . In seizures with bilateral involvement, the patients showed more severe clinical symptoms, with confusion, and were as a rule amnesic of the seizure . In the seizures with a medial subtemporal onset,
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING
Y' L
1s
Figure 6 . Patient 2, 23-year-old man . Focal seizure onset (arrow, channel 4 ; enlarged in box at bottom) inmost medial subtemporal electrode surfaces on the right side. First subjective symptom reported 9 s later ("funny feeling in my stomach') . Spread to contralateral medial temporal structures 15 s later (arrow, channel 3), then unresponsive, licking, manual automatisms . Surgery : right anterior temporal lobectomy. Seizure-free since surgery (2 years) . Histopathology : gliosis. Abbreviations as in Fig . 3 .
the immediate spread of seizure activity was either to the ipsilateral neocortex or to the contralateral medial subtemporal region before reaching the contralateral neocortex . In one patient (No . 4), the seizure activity spread from one hippocampal region via the contralateral hippocampus to the contralateral neocortex (Fig . 9) . Discussion
Gloor (2) pointed out that intracerebral wire electrodes, due to their proximity to aggregates of epileptic cells, record very high-amplitude spikes, often making a reduction of amplifier gain necessary . This can lead to a situation in which other important generators of epileptiform activity escape detection ("tunnel vision") . This was one of the reasons why we chose to use subdural electrodes . Another reason was that surgical implantation seemed much less complicated, demanding fewer resources, and was less traumatic than intracerebral electrodes . A disad-
vantage with subdural electrodes was that the available experience of their localization in some areas in the medial cortex of the hemispheres or the orbital cortex of the frontal lobe was very limited. Even if intracerebral electrodes are justified or even necessary in some cases, we found that, for example, medial parts of the occipital and frontal lobes can be examined with subdural electrodes . In recent literature concerning preoperative evaluation of patients with intractable epilepsy, there are several reports on the use of chronically implanted electrodes for seizure recording (3,5-8) . Criticism has been expressed regarding the blind insertion of subdural strip electrodes because of the risks of bleeding from bridging veins, cortical lesions, and arachnoidal adhesions (9) . In our material no complications have been noted. It was found that subdural electrode strips could be directed to the region of interest without difficulty . Most patients in the series suffered from partial complex seizures, and it was therefore important to record from the medial part of the temI
EPILEPSY, VOL. 2, NO. 1, 1989 17
S. BLOM ET AL.
LST 1-2 "I feel sick"
23^~
^
3-4 RST 1-2 2-3,r\ 3-4 q L LTC 1-2 \
W
2-3 3-4 RLTC 1-2 2-3--,,,,-
3- 4 I 30OA1V Is
Patient 12, 17-year-old boy. Short aura phenomenon (unpleasant epigastne sensation) reported during episode of repetitive spiking in channel 1 . Habitual seizures originated from the same electrode . Surgery: anterior left temporal lobectomy . Histopathology : gliosis . Postoperatively marked reduction in seizure frequency, but not completely seizure-free. Abbreviations as in Fig. 3 . Figure 7 .
7RINIIn1mll1nnmunnnnUlmnllu,mnnd 69
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4
RST 1-2
?n.,
qt 1111411 jqi
i h i . ~,r
J ~~111 ICI.If I~~'ll,~l'y ~lf,1ti l U}i~N~l'li~ f~ll
2-3 3-4
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mlil*Imn„rttlfLJ_1&. ~7,n ,ni, u ,nmti,minas,lln,IInnnnv~, nnn,L"nn,nln„im,lnn,nine,n,,,nn„,,ifi~lnm,innmn„lAnn,n'.P, : . . :,, nnm,
500AV Is
Figure 8 .
Patient 94, 32-year-old woman . EEG shown from right-sided subdural strip electrodes only . Seizure onset in most medial subtemporal electrode surface (arrow), spreading to involve the other electrodes in the same strip . Lateral temporal cortex uninvolved (as was the contralateral side, not shown in the figure) . Short-lasting epigastric unpleasant sensation, followed by unresponsiveness for a few seconds. No postictal amnesia. Surgery: right temporal lobectomy . Histopathology : presently unknown. Abbreviations as in Fig. 3 .
18
1 EPILEPSY, VOL . 2, NO. 1, 1989
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING Os
50s
LST 1-2 2-3 3-4 RST 1-2 2-3 3-4 L LTC 1-2 2-3 3-4 RLTC 1-2 2-3 3-4
is
1300 UV
Figure 9 . Patient 4, 43-year-old woman . Four sequences from a secondarily generalized seizure . Time in seconds after seizure onset (0 s) indicated above each sequence . Seizure onset in subtemporal electrode, left . Fifty seconds later, seizure spread to subtemporal leads, right side. After 53 s, seizure activity from right lateral temporal cortex After 95 s, seizure activity on the left lateral temporal cortical surface . Left anterior temporal lobectomy performed . Histopathology : gliosis . Seizure-free since surgery (17 months) . Abbreviations as in Fig . 3. EPILEPSY, VOL. 2, NO. 1, 1989 19
S. BLOM ET AL .
Table 3 .
Patients with seizures with extratemporal onset
Spread Patient
Lobe
Focal
Local
Unilateral
Bilateral
1
PL FL FL OL FL
0 0 0 7 17
1 1 6 0 3
1 1 0 5 20
0 0 6 2 0
9 40 63
Abbreviations: FL, frontal lobe; PL, parietal lobe ; OL, occipital lobe . poral lobes. The postimplantation x-ray examinations revealed that, in the majority of the cases, the most mesial electrode surface of the subtemporal strip was located over the parahippocampal gyrus . One important question was whether subdural strip electrodes were selective enough . Interictal highamplitude spikes from medial temporal structures were, as a rule, recorded from one or two electrode surfaces and not picked up by the lateral temporal strip . Moreover, in some instances it was possible to distinguish more than one spike generator in the subtemporal region . Simultaneous recordings from subtemporal, subdural, and sphenoidal electrodes showed that the latter detected considerably less epileptic activity . This was probably not due to shielding by the subdural strip. The subdural electrodes were also superior to the sphenoidal electrodes in detecting seizure onset without any problems or muscle artifact. In a study of seizure onset in temporal lobe epilepsy, where simultaneous subdural and depth electrodes were used (8), the conclusion was drawn that, since all auras and some hippocampal seizures never involved neocortex at all, the sensitivity of subdural recordings would be less efficient than that of depth electrodes for the purpose of localization . However, the number of subclinical seizures recorded by usin which the patient reported an aura and in which spread of seizure activity to contralateral hippocampus or ipsilateral neocortex did not take place-suggest sufficient sensitivity . The case of seizure spread to the contralateral neocortex prior to the ipsilateral neocortex emphasizes the necessity of a subtemporally localized electrode in order to avoid a false lateralization of seizure onset . We conclude that subtemporally located subdural electrodes have a sufficient resolution to detect interictal spikes and seizure onset in cases of partial complex epilepsy of medial temporal origin . Furthermore, in two patients we have recorded focal seizure onset in parietal and medial 20
1 EPILEPSY, VOL. 2 , NO. 1, 1989
occipital cortex, respectively, and in two patients we have recorded seizure onset in frontal foci . In seizures with a local onset (more than one electrode involved in the beginning of the seizure), the epileptic lesion could be localized in an area at some distance from the strip electrode, e .g., in the frontal lobe with a spread of seizure activity to the temporal lobe . In all such cases, a careful analysis of the videotapes was performed to make sure that the EEG onset clearly preceded any clinical symptom . EEG seizure onset prior to clinical symptoms does not rule out the possibility of a secondary spread, but the likelihood of this is considerably reduced . However, in every case of suspected partial seizures of temporal origin without neuroradiological evidence of a temporal lesion, subfrontally inserted subdural electrodes should be considered . Acknowledgment : The skillfull assistance of the technical staff at the Department of Clinical Neurophysiology is gratefully acknowledged . The authors are indebted to Catarina Farnstrand for preparing the illustrations. This work was supported by the Margaretha Foundation for Epilepsy .
References 1 . Engel J Jr, Crandall PH, Rausch R . The partial epilepsies. In : Rosenberg RN, Grossman RG, Schochet S Jr, Willis W Jr, eds . The clinical neurosciences . New York : Churchill-Livingstone, 1983 :1349-80 . 2 . Gloor P. Electroencephalography and the role of intracerebral depth electrode recordings in the selection of patients for surgical treatment of epilepsy . In : Porter RJ, Mattson RH, Ward AA, Dam M, eds . New York : Raven Press, 1984 :433-7 . (Advances in neurology; vol 15 .) 3 . Luders H, Hahn JF, Skipper GJ, et al . Chronic basal temporal arrays of subdural electrodes in the evaluation of complex partial seizures . Electroencephalogr Clin Neurophysiol 1985 ;61 :24P . 4 . Wieser HG, Elger CE, Stodieck SRG . The foramen ovale electrode : a new recording method for the preoperative evaluation of patients suffering from mesiobasal temporal lobe epilepsy . Electroencephalogr Clin Neurophysiol 1985 ;61 :314-22 . 5. Wyler AR, Ojemann GA, Lettich E, Ward AA . Subdural strip electrodes for localizing epileptogenic foci . I Neurosurg 1984;60 :1195-200 . 6 . Rosenbaum TJ, Laxer KD, Vessely M, Smith BW . Subdural electrodes for seizure focus localization . Neurosurgery 1986;19 :73-81 . 7. Laxer KD, Needleman R, Rosenbaum TJ. Subdural electrodes for seizure focus localization . Epilepsia 1984 ; 25 :651P. 8. Spencer SS, Williamson PD, Spencer DD, Mattson RH . Human hippocampal seizure spread studied by depth and subdural recording: the hippocampal commissure. Epilepsia 1987 ;28 :479-89 . 9 . Spencer SS . Surgical options for uncontrolled epilepsy. Neurol Clin 1986 ;4:669-95 .
Interictal and Ictal Activity Recorded with Subdural Electrodes During Preoperative Evaluation for Surgical Treatment of Epilepsy S. Blom, R. Flink, J . Hetta, 2 P . Hilton-Brown, 1 C. Hoffstedt, 2P. O. Osterman, and 3 B . Spannare
A total of 94 subdural strip electrodes were implanted in 22 patients during preoperative EEG evaluation for surgery of epilepsy . Eighteen patients had temporal lobe seizure onset, three had frontal lobe seizure onset, and one had occipital lobe seizure onset . Most electrodes (total, 83) were localized over the temporal lobe cortex, but in four cases additional strip electrodes (total, 11) covered the frontal, parietal, and occipital lobe cortexes. The electrodes were left in place for up to 28 days . No complications occurred . Interictally, focal spiking was recorded subtemporally, mostly without being seen in electrodes recording from the lateral temporal cortex . In three patients studied with simultaneous subdural and sphenoidal wire electrodes, spiking recorded from subdural electrodes was often not seen in the sphenoidal recording . There were 151 seizures recorded (with or without simultaneous video monitoring) . The mean number of seizures per patient was 6 .7 (range, 0-21) . The seizures were classified as having focal (80 seizures) or local (71 seizures) onset . It is concluded that subdural electrodes are safe and have a sufficient selectivity with regard to localization of interictal spiking and seizure onset in patients with mesial temporal epileptic lesions . In such cases, electrodes have to be placed subtemporally . Other cortical areas may also be explored with these electrodes . Key Words : Epilepsy- Surgery- SubduralSphenoidal- Ictal-Interictal .
Stereotactically implanted depth electrodes give precise and detailed information concerning both interictal and ictal activity during the preoperative evaluation in patients considered for surgical treatment of epilepsy. However, the implantation procedure is complicated and not free from risks (1) . Moreover, the electrodes are sometimes too selective, which can lead to misinterpretations (2) . As an alternative, sub-
From the Departments of Clinical Neurophysiology, 'Psychiatry, 2 Neurology, and 3 Neurosurgery, University Hospital, Uppsala, Sweden. Address correspondence and reprint requests to Dr . S . Blom, Department of Clinical Neurophysiology, University Hospital, S-75185 Uppsala, Sweden .
dural electrodes of different types have been used (3-6) . Since 1985, we have used Wyler subdural strip electrodes (Ad-Tech Co .) in patients with refractory simple partial seizures or partial complex seizures referred for surgical intervention . This study describes interictal and ictal findings in the patients studied with these electrodes. For comparison, EEG was simultaneously recorded with sphenoidal and scalp electrodes in three patients .
Material Since 1985, 109 patients have been referred to the Epilepsy Unit at the Neuroclinics in Uppsala for severe
I EPILEPSY, VOL. 2, NO. 1, 1989
9
Possible etiology
Seizures per month
Neurological exam
Unknown
Meningitis age 4 y; encephalitis? age 10 y
Trauma with dys- 90, most nocturphasia and nal Babinski +, age 15y
Encephalitis with 10-12 seizures, age 20 y
Probable neonatal injury
5/35/F/16
6/30/M/11
8/32/M/18
10/47/M/20
12/17/M/5
5-10
Unknown
Unknown
17/33/M/9
52/37/M/22
5-10
20-40
14/33/M/23 Trauma with GTC, age 9 y
4-10
2-15; serial seizures and GTC last 2 y
4-12 ; new seizure type and psychotic episodes last 2 y
Onset 2 weeks af- 4-6 ter childbirth
4/41/F/20
4-10
Unknown
3/31/F/26
CT : normal
CT and MRI : wide temp horn R
CT and MRI : normal
CT and MRI : normal
CT and MRI : normal
Neurological imaging
Table 1 .
Not studied
IQ normal, verbal compr subnormal
IQ normal, verbal compr subnormal
IQ normal (-), slow tapping, L (nondomin)
IQ normal, slow tapping, R (dominant)
Neuropsychology
Patient information
Normal
Normal
Clumsiness, R hand
Normal
Normal
IQ normal (+) slow performance
CT and MRI: normal
CT and MRI: normal
CT and MRI : wide temp horn R
IQ normal (-)
Not studied
IQ normal, slow tapping R (dominant)
MRI : bilat pane- IQ normal (-) tal subcortical abn
CT and MRI : normal
Minimal dyspha- CT: temp abn L ; IQ normal, verbal sia MRI : temp compr subnorand frontal abn mal L
Normal
Normal
Normal
Normal
Patients with seizures with temporal lobe onset (compare Table 2) 2/23/M/13 Unknown 15-20 Normal
Patient/age (years)/sex/ onset (years)
Sphenoidal spike focus L
Sphenoidal spike focus R
Sphenoidal spike focus R
Sphenoidal spike focus L
Temporal spike focus R
Sphenoidal spikes L
Frontotemporal spikes L > R
Sphenoidal R (+ temp L) spike focus
Sphenoidal spikes R > L
Sphenoidal R (+ temporal L) spike focus
Temporal spike tocus R
EEG (scalp + sphenoidal)
Head turning L or R, vocalization, unresp
Reports onset, vocalization, automatisms
Stare, unresp, mumbles, moves L hand
Reports onset, stare, unresp automatisms
Ictal signs (CCTV)
Reports onset, unresp, oral automatisms
Stare, unresp, head turn R
Stare, unresp, automatisms
Forced thinking, confused
Stare, unresp, automatisms
Confused, unable Stare, unresp, speak ; GTC automatisms
No perception of Stare, unresp, seizures automatisms
Nausea, taste ; GTC
Dizzy, confused
Unable to speak, confused
No perception of No seizures reseizure onset corded!
No perception of seizures
Epigastric sens, confused
No perception ; epigastric sens
Epigastric sens, confused
Ictal symptoms
No : amytal te! memory deb R
No : seizure on : R (and L) ; arr tal test: mer ory defect L
No : amytal tet memory deft R and L
L temp lobe res (gliosis?)
R temp lobe res (gliosis)
L temp lobe res (cicatrix + gliosis)
No; seizures ni recorded
No; amytal test memory clef( L
L temp lobe res (gliosis)
R temp lobe res (gliosis)
R temp lobe res (gliosis)
Surgery (PAD
Probable neonatal injury
Born prematurely (2,100 g)
Unknown
Meningitis with clonic seizure R, age 0 .5 y
Onset after vaccination, age 9 m
Unknown
58/23/M/14
64/23/M/0 .8
66/35/F/17
68/34/M/20
76/45/M/1
94/33/F/17
8-16
10-20
20-30
4-10
8-12
y 6-10
29-30; altered and increased seizures since 1
Normal
Normal
Normal
Normal
Normal
Spasticity R hand
Normal
Probable neonatal injury
Trauma with GTC, age 9 y
40/16/M/ birth
63/31/M/21
15-30; increasing rate and serial seizures last 2 y
8-10
15-20
Normal
Minimal hemianopia L
Normal
Sphenoidal spike focus R
Normal
IQ normal (+)
CT and MRI: normal
CT and MRI : frontopol small abn R
CT and MRI: occipital abn R
CR and MRI : normal
CT and MRI : parietal porencephalia L
No perception of seizure onset
Frontal spikes L and R Sphenoidal spiking R Sphenoidal spike focus R
IQ normal (-)
IQ normal (+), verbal compr subnormal IQ normal
Deja vu; sound R ear; automatisms
Sees white spot; confused
Vertigo
Nausea; confused
Deja vu; confused
Epigastric sens
No perception of seizures
No perception ; epigastric sens
No perception of seizure onset
Deja vu; can't understand
Temporal focus L
Slight mental retardation
Sphenoidal spikes R > L (+ frontal)
Normal
CT : normal; MRI : temp abn L?
CT and MRI : normal
Temporal spikes L
IQ normal, verbal compr subnormal
CT and MRI: normal Sphenoidal spike focus R
Sphenoidal spike focus R
IQ normal, verbal compr subnormal
CT : normal; MRI : temp medial abn R
Frontotemp spike focus L
Sphenoidal spike focus L
IQ normal (+), slow tapping R (dominant)
Memory and verbal fluency defect
CT and MRI : parieto-occipital atrophy L
CT : wide sulcus temporal cortex R
Abbreviations: abn, abnormality; age, age at study; compr, comprehension; F, female; L, left; M, male ; onset, age at onset of epilepsy; GTC, generalized tonic-clonic seizure ; R, right; unresp, unresponsive; y, year(s) ; sens, sensation; resec, resection .
Encephalitis?
9/19/M/1 .5
Patients with seizures with extratemporal onset (compare Table 3) 1/17/M/6 Probable neona8-16 Dystonia and tal injury hemianopia R
Trauma, unconscious one week, age 17 y
53/35/F/17
Reports onset, stare, moves R hand + pedaling; duration <30 s
Reports onset, stare, mumbles, adversive to L
Head turn R unresp, vocalization
Reports onset, stare, unresp, adversive to R
Reports onset, stare, unresp, automatisms
Reports onset, stare, unresp, chews, pedaling
Reports onset, stare, unresp, swallows
Stare, unresp, vocalization, slight pedaling
Reports onset, stare, unresp, moves hands
Deep breathing, unresp, tonic posture R
Stare, unresp, R hand to face
R frontopolar resec (cicatrix + gliosis)
R occip lobe resec (localized gliosis)
No : seizure-free after reduced medication!
No : multifocal seizure onset in language area
R temp lobe rese<
L temp lobe rese( (planned)
R temp lobe reset (gliosis)
L temp lobe rese, (gliosis)
R temp lobe res& (gliosis)
L temp lobe rese . (planned)
No: amytal test: memory defec R and L
a.
DLL/1V1 C 1 HL_
seizure problems of various kinds. There were three criteria for considering surgical intervention : (a) the seizures should be simple partial or partial complex, with or without secondary generalization ; (b) they should originate from a cortical region possible to remove without major neurological impairment ; and (c) thorough medical treatment trial with at least three major antiepileptic drugs in monotherapy had not given an acceptable result . In addition, most patients had been treated earlier with various drug combinations . Implantation of subdural electrodes was performed in 22 patients, in whom routine EEGs, including sphenoidal recordings during 12-18 h, or clinical and radiological data-computerized tomography (CT) and magnetic resonance imaging (MRI) scanninghad not provided a plausible localization of the epileptic lesion . Clinical data are summarized in Table 1 .
Methods Surgical Procedure The implantation of subdural electrodes was performed under general anesthesia with hyperventilation . Mannitol, 500 ml (150 mg/ml), was given intravenously prior to the operation . In all patients, one subdural strip electrode was placed subtemporally and one over the lateral temporal cortex bilaterally . The burr hole was made about 1 cm anterior to the external auditory meatus and just superior to the zygoma . As a guide for the strip electrode, a moistened infant feeding catheter (No . 8) was inserted 5 cm in the desired direction between the dura and the brain surface. The moistened strip electrode was then passed along this catheter . In three patients, additional electrodes were placed frontally, and one patient was also provided with electrodes over the medial and lateral occipital cortex . For electrode placements, see Fig . 1 . The total number of implanted electrodes was 94 . Before closing the wound, the electrodes were tested by recording the EEG . All the electrode wires were connected to a master cable, which was bandaged down the neck of the patient in order to reduce the risk of electrode dislocation during seizures . After electrode implantation, plain anterior-posterior and lateral skull films were taken to confirm the electrode position. Patients were not given antibiotics .
were recorded on a 17-channel Nihon Koden EEG machine with an amplification of 30 or 50 µV/mm (T .C., 0 .3; high-frequency filter, 70 Hz) . Activity from scalp and sphenoidal electrodes was recorded with an amplification of 10 µV/mm . The paper speed was 15 mm/s. Both patient and EEG were recorded with closed circuit television (CCTV), using split screen technique, which allowed detailed analysis of the electroclinical relationship . The recording started a few hours after surgery and continued daily . Sometimes the recording was also performed during the night, without video monitoring. In most cases, the monitoring was stopped when at least three seizures had been recorded . The subdural electrodes were then extracted . They were likewise extracted if the required number of seizures had not been obtained within 4 weeks . To evoke spontaneous seizures, medication was reduced after the implantation ; later, if necessary, medication was completely withdrawn. The videotapes with seizures were shown to the patients' relatives to confirm that they were the patients' habitual seizures . Analysis During the analysis of seizures, the videotapes were repeatedly replayed and relevant clinical symptoms noted on the EEG paper . The following parameters were noted : (a) seizure onset, defined as the moment when the interictal EEG activity suddenly was replaced by flattening (sometimes after an initial paroxysmal discharge), followed by a low-amplitude, high-frequency rhythm and then spikes-a seizure start was considered as focal if the onset was traced to one or two of the electrode surfaces, whereas it was classified as local if the onset was seen simultaneously in all three bipolar derivations from one strip electrode; (b) the time between EEG onset and first clinical symptom or sign ; and (c) the seizure duration, as appreciated from the EEG recording-in a few cases, the duration could not be measured, since it became necessary to disconnect the patient from the EEG machine during a seizure . Seizures with a secondary generalization are not included in the duration measurements .
Results Implantation
Recording Procedure Sequential bipolar montages from each strip electrode were used throughout the recordings . The EEGs 12
1 EPILEPSY, VOL . 2, NO. 1, 1989
The electrodes were implanted for 7-28 days . There were no complications such as bleeding, infection, or spinal fluid leakage. In two cases the strip electrodes
SUBDURAL
\/
Figure 1.
Schematic drawing of the localization
INTERICTAL
* 1i
AND ICTAL EEG RECORDING
I
20
of the 94 strip electrodes used in the study. The number ofstrips in each area is indicated
were dislocated during seizures by the patient pulling the electrode cable. However, this caused the patient no harm. The subtemporally inserted strip reached the uncus or the parahippocampal gyrus with its most me-
dial electrode. The distance from the midline to the most medial electrode was 2.2 f 0.5 cm (mean 31 1 SD; range, 1.54.2 cm) calculated from the anteriorposterior skull film (Fig. 2). Calculated from the latera1 skull film, the distance between the anterior pole
Figure 2. Frontal x-rayfilm shows electrode surfaces of the subtemporal and the lateral temporul strip, right side, in patient IO. The region of the x-ray film is indicated in the drawing (hatched area). The drawing also shows the electrode surfaces on the left side.
I EPILEPSY, VOL. 2, NO. 1. 1989
13
S. BLOM ET AL. 1
LST 1-2 2-3 3-4
/l j a
~4 , I
RST 1-2 2-3 3-4 L LTC 1-2 2-3 3-4 RLTC 1-2 2-3 3-4
Figure 3 . Patient 4, 43-year-old woman. Interictal recording, awake . Continuous sequence of spikes without clinical symptoms from electrode surface 3, left subtemporal strip electrode (channels 2 and 3) . Occasional spikes from electrode surface 1, right subtemporal strip electrode (channel 4) . Note absence of epileptiform activity in lateral temporal electrodes bilaterally . Focal onset from left subtemporal strip, surface 1 . Surgery: left anterior temporal resection, including hippocampus . Histopathology : gliosis. Seizure-free since surgery (17 months) . In this and subsequent figures the following abbreviations are used : LST, left subtemporal; RST, right subtemporal, • LLTC, left lateral temporal convexity; RLTC, right lateral temporal convexity . Note reduced paper speed (15 mm/s) in all figures .
of the temporal lobe and the medial electrode was 3 .2 ± 0 .7 cm (mean ± 1 SD ; range, 1 .7-4 .6 cm) .
Interictal Activity
Interictal, high-amplitude spiking was often prominent from the subdural electrodes . In several cases, interictal subtemporal spiking was recorded without simultaneous epileptiform activity from the ipsilateral temporal neocortex (Fig . 3) . In most cases with temporal lobe foci, interictal epileptiform activity was recorded from the subtemporal electrodes contralateral to the seizure-generating focus . The subdural electrodes could separate closely located spike foci (Fig. 4) . To compare the activity recorded from subdural electrodes with that recorded from simultaneous sphenoidal electrodes, bilateral sphenoidal wires were inserted in three patients . Most spikes recorded from the subdural electrodes were not detected by the sphenoidal wires (Fig . 5) . Slow background activity was, however, clearly seen in the sphenoidal recording. Recording from sphenoidal wires during implantation of subdural strip electrodes performed 14
1 EPILEPSY, VOL . 2 , NO. 1, 1989
in one case did not indicate that the intracranial strips attenuated the activity . Scalp electrodes were applied in three cases . Interictal epileptiform activity recorded only from the subdural subtemporal strip was not detected in the surface electrodes. Sharp waves and spikes recorded in the scalp leads were always recorded simultaneously with high-amplitude epileptiform potentials in the lateral temporal electrode strip .
Ictal Activity
Injuries did not occur during seizures, and status epilepticus did not occur. Secondary generalization occurred in 10 seizures in seven patients . Altogether, 151 seizures were recorded with the subdural electrodes . The results are summarized in Table 2. The number of seizures per patient was 6 .7 ± 5 .6 (mean ± 1 SD; range, 0-21) . The EEG seizure duration in seizures with clinical symptomatology was 82 ± 41 s (mean ± 1 SD; range, 30-158 s) . In one patient, no seizures were recorded in spite of daily monitoring for 4 weeks . In all but one patient (No . 9), the EEG seizure on-
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING
RST 1-2 2-3 3-4 R LT C 1-2 2-3 3-4
W
r
v'I
I500uV 1s
Patient 52, 37-year-old woman . Interictal recording asleep . Independent spiking from all electrodes in left subtemporal strip (channels 7-9) . Seizures started from left medial temporal structures . Resection not performed due to contralateral memory disturbance revealed by Wada test. Abbreviations as in Fig . 3 . Figure 4 .
L S T 1-2 2-3
Sph sin-F7 Sph sin-A1---L LTC 1-2 2-3
RST 1-2
µ
3-4 RLTC 1-2 ,,,..~,_,y`.t,,, 2-3 3-4 1300uV 1s
Patient 66, 34-year-old woman . Interictal recording awake. Simultaneous subdural and sphenoidal wire recording (channels 4 and 5) . Spiking in subdural electrodes (channels I and 2) not recorded in sphenoidal leads ; only slow components recorded . Surgery: left temporal lobectomy. Histopathology : gliosis. Abbreviations as in Fig . 3 . Figure 5 .
EPILEPSY, VOL . 2, NO. 1, 1989
15
S. BLOM ET AL.
Table 2 .
Patients with seizures with temporal lobe onset
Spread Patient
Region
Onset
Focal
Local
Unilateral
Bilateral
2 3 4 5 6 8
Right Right Left Right
Med Med Med Med
Left Right Right Left Right Left Left Right Left Left Left Right Left Right Right Left Right
Med Med Med Med Med Med Lat Lat Med Med Med Med Med Med Med Med Med
3 0 3 0 0 0 0 2 4 0 0 8 1 1 0 4 2 6 0 10 7 5
0 2 0 5 0 10 1 0 1 13 2 12 0 0 8 0 1 4 1 0 0 0
0 0 1 0 0 0 0 0 2 11 2 20 0 0 4 0 1 7 1 8 5 0
3 2 2 5 0 10 1 2 3 2 0 0 1 1 4 4 2 3 0 2 2 5
10 12 14 17 52 53 58 64 66 68 76 94
Abbreviations : Med, medial; Lat, lateral . set preceded the clinical ictal onset . Where the latency could be measured, it was 9 ± 6 s (mean ± 1 SD ; range, 4-22 s) . The onset was focal in 80 seizures (subtemporal, 47; lateral temporal, 9; frontal, 17 ; occipital, 7) . It was local in 71 seizures (subtemporal, 48; lateral temporal, 12 ; frontal, 10; parietal, 1) . Figure 6 shows a focal onset in medial temporal structures . In 17 patients, the individual seizures were clinically of almost identical appearance, and the EEG onset was confined to one side . Three of these patients have been rejected for surgery . Patient 1 had seizures that started in his dominant hemisphere . One seizure started focally from the angular gyrus, and one was confined to the Broca region . In patients 5 and 53, the amytal test contraindicated resection of the hippocampal epileptic focus . Four patients had seizures starting from alternating sides . Patients 8 and 66 were operated on, since their seizures contralateral to the side of surgery were single events and were regarded as withdrawal seizures. In patients 14 and 17, the amytal test contraindicated hippocampectomy . Short-lasting seizure activity from one electrode surface without spread to other areas was seen in some instances of seizures with 16
1 EPILEPSY, VOL. 2, NO . 1, 1989
clinical symptoms of auras . One example is patient 12 (Fig . 7), in whom the seizure activity was confined to one subtemporal electrode surface . The patient spontaneously reported his usual aura phenomenon, an unpleasant epigastric sensation . In patient 1, the seizure activity was located in the posterior part of the angular gyrus in the left dominant hemisphere . He reported a sudden dizziness. In patient 40, this type of focal seizure activity was limited to the anterior part of the lingular gyrus in the right occipital lobe . It was associated with a flickering light spot in the left visual field . In these patients, the complex partial seizures had seizure onset identical to the auras . Furthermore, when an aura was reported, there was always ongoing seizure activity. Seizure activity could spread and could involve more ipsilateral electrode surfaces (Fig. 8) . Seizure activity that spread to involve more ipsilateral, but not contralateral, electrodes-and thus remained unilateral-was usually accompanied by less pronounced clinical ictal symptoms in the patient, and no amnesia was reported . In seizures with bilateral involvement, the patients showed more severe clinical symptoms, with confusion, and were as a rule amnesic of the seizure . In the seizures with a medial subtemporal onset,
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING
Y' L
1s
Figure 6 . Patient 2, 23-year-old man . Focal seizure onset (arrow, channel 4 ; enlarged in box at bottom) inmost medial subtemporal electrode surfaces on the right side. First subjective symptom reported 9 s later ("funny feeling in my stomach') . Spread to contralateral medial temporal structures 15 s later (arrow, channel 3), then unresponsive, licking, manual automatisms . Surgery : right anterior temporal lobectomy. Seizure-free since surgery (2 years) . Histopathology : gliosis. Abbreviations as in Fig . 3 .
the immediate spread of seizure activity was either to the ipsilateral neocortex or to the contralateral medial subtemporal region before reaching the contralateral neocortex . In one patient (No . 4), the seizure activity spread from one hippocampal region via the contralateral hippocampus to the contralateral neocortex (Fig . 9) . Discussion
Gloor (2) pointed out that intracerebral wire electrodes, due to their proximity to aggregates of epileptic cells, record very high-amplitude spikes, often making a reduction of amplifier gain necessary . This can lead to a situation in which other important generators of epileptiform activity escape detection ("tunnel vision") . This was one of the reasons why we chose to use subdural electrodes . Another reason was that surgical implantation seemed much less complicated, demanding fewer resources, and was less traumatic than intracerebral electrodes . A disad-
vantage with subdural electrodes was that the available experience of their localization in some areas in the medial cortex of the hemispheres or the orbital cortex of the frontal lobe was very limited. Even if intracerebral electrodes are justified or even necessary in some cases, we found that, for example, medial parts of the occipital and frontal lobes can be examined with subdural electrodes . In recent literature concerning preoperative evaluation of patients with intractable epilepsy, there are several reports on the use of chronically implanted electrodes for seizure recording (3,5-8) . Criticism has been expressed regarding the blind insertion of subdural strip electrodes because of the risks of bleeding from bridging veins, cortical lesions, and arachnoidal adhesions (9) . In our material no complications have been noted. It was found that subdural electrode strips could be directed to the region of interest without difficulty . Most patients in the series suffered from partial complex seizures, and it was therefore important to record from the medial part of the temI
EPILEPSY, VOL. 2, NO. 1, 1989 17
S. BLOM ET AL.
LST 1-2 "I feel sick"
23^~
^
3-4 RST 1-2 2-3,r\ 3-4 q L LTC 1-2 \
W
2-3 3-4 RLTC 1-2 2-3--,,,,-
3- 4 I 30OA1V Is
Patient 12, 17-year-old boy. Short aura phenomenon (unpleasant epigastne sensation) reported during episode of repetitive spiking in channel 1 . Habitual seizures originated from the same electrode . Surgery: anterior left temporal lobectomy . Histopathology : gliosis . Postoperatively marked reduction in seizure frequency, but not completely seizure-free. Abbreviations as in Fig. 3 . Figure 7 .
7RINIIn1mll1nnmunnnnUlmnllu,mnnd 69
,a,m .in nn : : :,,, :u,, :, : n :mnm~ • :, :: : • : . • ; ,,,,I]]
.
r. :c : .=m„n,nmv, .
4
RST 1-2
?n.,
qt 1111411 jqi
i h i . ~,r
J ~~111 ICI.If I~~'ll,~l'y ~lf,1ti l U}i~N~l'li~ f~ll
2-3 3-4
3-4 -A. .-.
mlil*Imn„rttlfLJ_1&. ~7,n ,ni, u ,nmti,minas,lln,IInnnnv~, nnn,L"nn,nln„im,lnn,nine,n,,,nn„,,ifi~lnm,innmn„lAnn,n'.P, : . . :,, nnm,
500AV Is
Figure 8 .
Patient 94, 32-year-old woman . EEG shown from right-sided subdural strip electrodes only . Seizure onset in most medial subtemporal electrode surface (arrow), spreading to involve the other electrodes in the same strip . Lateral temporal cortex uninvolved (as was the contralateral side, not shown in the figure) . Short-lasting epigastric unpleasant sensation, followed by unresponsiveness for a few seconds. No postictal amnesia. Surgery: right temporal lobectomy . Histopathology : presently unknown. Abbreviations as in Fig. 3 .
18
1 EPILEPSY, VOL . 2, NO. 1, 1989
SUBDURAL INTERICTAL AND ICTAL EEG RECORDING Os
50s
LST 1-2 2-3 3-4 RST 1-2 2-3 3-4 L LTC 1-2 2-3 3-4 RLTC 1-2 2-3 3-4
is
1300 UV
Figure 9 . Patient 4, 43-year-old woman . Four sequences from a secondarily generalized seizure . Time in seconds after seizure onset (0 s) indicated above each sequence . Seizure onset in subtemporal electrode, left . Fifty seconds later, seizure spread to subtemporal leads, right side. After 53 s, seizure activity from right lateral temporal cortex After 95 s, seizure activity on the left lateral temporal cortical surface . Left anterior temporal lobectomy performed . Histopathology : gliosis . Seizure-free since surgery (17 months) . Abbreviations as in Fig . 3. EPILEPSY, VOL. 2, NO. 1, 1989 19
S. BLOM ET AL .
Table 3 .
Patients with seizures with extratemporal onset
Spread Patient
Lobe
Focal
Local
Unilateral
Bilateral
1
PL FL FL OL FL
0 0 0 7 17
1 1 6 0 3
1 1 0 5 20
0 0 6 2 0
9 40 63
Abbreviations: FL, frontal lobe; PL, parietal lobe ; OL, occipital lobe . poral lobes. The postimplantation x-ray examinations revealed that, in the majority of the cases, the most mesial electrode surface of the subtemporal strip was located over the parahippocampal gyrus . One important question was whether subdural strip electrodes were selective enough . Interictal highamplitude spikes from medial temporal structures were, as a rule, recorded from one or two electrode surfaces and not picked up by the lateral temporal strip . Moreover, in some instances it was possible to distinguish more than one spike generator in the subtemporal region . Simultaneous recordings from subtemporal, subdural, and sphenoidal electrodes showed that the latter detected considerably less epileptic activity . This was probably not due to shielding by the subdural strip. The subdural electrodes were also superior to the sphenoidal electrodes in detecting seizure onset without any problems or muscle artifact. In a study of seizure onset in temporal lobe epilepsy, where simultaneous subdural and depth electrodes were used (8), the conclusion was drawn that, since all auras and some hippocampal seizures never involved neocortex at all, the sensitivity of subdural recordings would be less efficient than that of depth electrodes for the purpose of localization . However, the number of subclinical seizures recorded by usin which the patient reported an aura and in which spread of seizure activity to contralateral hippocampus or ipsilateral neocortex did not take place-suggest sufficient sensitivity . The case of seizure spread to the contralateral neocortex prior to the ipsilateral neocortex emphasizes the necessity of a subtemporally localized electrode in order to avoid a false lateralization of seizure onset . We conclude that subtemporally located subdural electrodes have a sufficient resolution to detect interictal spikes and seizure onset in cases of partial complex epilepsy of medial temporal origin . Furthermore, in two patients we have recorded focal seizure onset in parietal and medial 20
1 EPILEPSY, VOL. 2 , NO. 1, 1989
occipital cortex, respectively, and in two patients we have recorded seizure onset in frontal foci . In seizures with a local onset (more than one electrode involved in the beginning of the seizure), the epileptic lesion could be localized in an area at some distance from the strip electrode, e .g., in the frontal lobe with a spread of seizure activity to the temporal lobe . In all such cases, a careful analysis of the videotapes was performed to make sure that the EEG onset clearly preceded any clinical symptom . EEG seizure onset prior to clinical symptoms does not rule out the possibility of a secondary spread, but the likelihood of this is considerably reduced . However, in every case of suspected partial seizures of temporal origin without neuroradiological evidence of a temporal lesion, subfrontally inserted subdural electrodes should be considered . Acknowledgment : The skillfull assistance of the technical staff at the Department of Clinical Neurophysiology is gratefully acknowledged . The authors are indebted to Catarina Farnstrand for preparing the illustrations. This work was supported by the Margaretha Foundation for Epilepsy .
References 1 . Engel J Jr, Crandall PH, Rausch R . The partial epilepsies. In : Rosenberg RN, Grossman RG, Schochet S Jr, Willis W Jr, eds . The clinical neurosciences . New York : Churchill-Livingstone, 1983 :1349-80 . 2 . Gloor P. Electroencephalography and the role of intracerebral depth electrode recordings in the selection of patients for surgical treatment of epilepsy . In : Porter RJ, Mattson RH, Ward AA, Dam M, eds . New York : Raven Press, 1984 :433-7 . (Advances in neurology; vol 15 .) 3 . Luders H, Hahn JF, Skipper GJ, et al . Chronic basal temporal arrays of subdural electrodes in the evaluation of complex partial seizures . Electroencephalogr Clin Neurophysiol 1985 ;61 :24P . 4 . Wieser HG, Elger CE, Stodieck SRG . The foramen ovale electrode : a new recording method for the preoperative evaluation of patients suffering from mesiobasal temporal lobe epilepsy . Electroencephalogr Clin Neurophysiol 1985 ;61 :314-22 . 5. Wyler AR, Ojemann GA, Lettich E, Ward AA . Subdural strip electrodes for localizing epileptogenic foci . I Neurosurg 1984;60 :1195-200 . 6 . Rosenbaum TJ, Laxer KD, Vessely M, Smith BW . Subdural electrodes for seizure focus localization . Neurosurgery 1986;19 :73-81 . 7. Laxer KD, Needleman R, Rosenbaum TJ. Subdural electrodes for seizure focus localization . Epilepsia 1984 ; 25 :651P. 8. Spencer SS, Williamson PD, Spencer DD, Mattson RH . Human hippocampal seizure spread studied by depth and subdural recording: the hippocampal commissure. Epilepsia 1987 ;28 :479-89 . 9 . Spencer SS . Surgical options for uncontrolled epilepsy. Neurol Clin 1986 ;4:669-95 .