108
Electroencephalography and clinical Neurophysiology, 79 ( 1991) 108-113 ~) 1991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 ADONIS 001346499100119P
EEG 90174
E E G a n d n e u r o i m a g i n g l o c a l i z a t i o n in p a r t i a l e p i l e p s y * Bahman Jabbari a,c, Douglas Van Nostrand b,c Carl H. Gunderson a,c, David Bartoszek Michael H. Mitchell a,c, Mark Lombardo d, Charles Citrin d and John Sherman d
a,c
" Neurology Sercice, ~' Department of Radiology, Section of Nuclear Medicine, Walter Reed Army Medical Center, Washington, DC (U.S.A.), ' The Um[ormed Sercices Unicersity Of the Health Sciences, Bethesda, MD (U.S.A.), and ~tMagnetic Imaging of Washington, Washington, DC (U.S.A.)
(Accepted for publication: 10 December 199(/)
Summary We have studied cortical localization provided by surface and sphenoidal electroencephalograms (EEGs) and that of computed tomography (CT), magnetic resonance imaging (MR) and single photon emission tomography (SPECT) in 58 patients with partial epilepsy. Each patient had EEG, MR and SPECT during a hospitalization period of 1-2 weeks. CT scans were obtained either during the same period or had been performed in the preceding year. EEG evaluation consisted of 3-5 days of continuous monitoring including video-telemetry and ambulatory recording as well as conventional EEGs with special electrode placements. Additionally 33 of 58 patients (55%) who were potential surgical candidates had sphenoidal recordings. All patients had an abnormal EEG which showed evidence of epileptic hyperexcitability. EEG abnormality was localized in 43 patients (74%). Neuroimaging studies were focally abnormal in 38 patients (66%); 12 CT (21%), 29 MR (50~/~) and 24 SPECT (41%). Thirty four of 43 patients with localized EEG had at least 1 focally abnormal neuroimaging study (79%), whereas 4 of 15 (27%) patients with non-localized EEG did so. Twenty-eight of 29 patients with focal MR (97%), 11 of 12 patients with focal CT (92%) and 20 of 24 patients with focal SPECT (83%) had a concordant focal EEG. EEG and neuroimaging localization agreed in all 15 patients in whom both MR and SPECT disclosed a concordant focal abnormality. This study demonstrates a significant( P < 0.005) correlation between surface/sphenoid EEG and neuroimaging localization in partial epilepsy. Key words: EEG; Neuroimaging localization; Partial epilepsy: Computed tomography; Magnetic resonance imaging; Single photon emission tomography
Surgical resection of the e p i l e p t o g e n e t i c cortex provides significant relief from i n t r a c t a b l e partial epilepsy in 7 0 - 8 0 % of selected p a t i e n t s ( G l a s e r 1980; E n g e l 1987). E E G e v a l u a t i o n r e m a i n s essential to epilepsy surgery. In m a n y patients, p r o p e r localization requires application of s u b d u r a l or d e p t h electrodes ( S p e n c e r et
c o m p u t e d t o m o g r a p h y (CT), m a g n e t i c r e s o n a n c e imaging ( M R ) a n d single p h o t o n emission t o m o g r a p h y (SPECT).
al. 1982; Liiders et al. 1987). O t h e r p a t i e n t s do well without invasive p r o c e d u r e s if surface, s p h e n o i d a l a n d v i d e o - E E G provide consistent interictal a n d ictal localization ( S h a r b r o u g h 1987). N e u r o i m a g i n g (NI) procedures have m a d e a significant impact in this area by disclosing the site of pathology a n d s u p p o r t i n g E E G localization (Engel 1988). W e have studied the correlation b e t w e e n epileptic focus as seen in surface and
Fifty-eight consecutive p a t i e n t s with r e c u r r e n t partial seizures have b e e n studied. P a t i e n t s signed an i n f o r m e d c o n s e n t before participating. All p a t i e n t s had complex partial seizures according to the I n t e r n a t i o n a l Classification of Epileptic Seizures (ICES 19811. T w e n t y - t h r e e p a t i e n t s had initial partial simple symp-
Patients and methods
s p h e n o i d a l E E G a n d localization provided by 3 commonly available n e u r o i m a g i n g techniques, namely:
toms which evolved into complex partial seizures. Sixt e e n p a t i e n t s had o n e or more episodes of secondary g e n e r a l i z a t i o n in the p r e c e d i n g year. T h e group consisted of 43 females a n d 15 males with a m e a n age of
* The opinions and assertions expressed in this paper are the private views of the authors and should not be construed as reflecting the views of the U.S. Army, Department of Defense or Uniformed Services University of the Health Sciences.
32.9 years (range: 9 - 7 2 years). T h e i r d u r a t i o n of symptoms varied from 1 to 42 years (mean: 12). All p a t i e n t s were on a n t i c o n v u l s a n t medications, usually two of the following: p h e n y t o i n , c a r b a m a z e p i n e a n d valproic acid. T h e p a t i e n t s e n t e r e d the hospital for a period of 1-2 weeks for electrophysiological, M R a n d S P E C T stud-
Correspondence to: Bahman Jabbari, M.D., Neurology Service, Walter Reed Army Medical Center, Washington, DC 20307-5001 (U.S.A.I.
ies. All p a t i e n t s had a C T scan either d u r i n g this period or in the year p r e c e d i n g this evaluation. T h e electrophysiological assessment consisted of 3 - 5
EE(} AND NEUROIMAGING IN PARTIAL EPILEPSY days of continuous monitoring including 4 8 - ? 2 h of video-telemetry performed on 64- and 16-channel Telefactor unit, one or more 8-channel 24 h ambulatory recording and several conventional E E G s on 18channel Grass equipments. In the majority of the patients v i d e o - E E G monitoring was obtained after gradual reduction of the medications and in a few after discontinuing antiepileptic drugs. Conventional recordings were performed according to the international 10-20 system using both referential and differential montages. The recording montages included T1, T2, supraorbital (SO1, S O 2 ) a n d in some cases zygomatic electrode placements. Additionally, 33 of 58 patients (55CY~) who were considered to be potential surgical candidates had sphenoidal recordings. MR was performed on 0.5 tesla Teehnicare and 1.5 tesla Phillips equipment with comparable resolutions, A l0 mm slice thickness was employed in axial, transverse, coronal and sagittal views and in 12 patients 5 mm slices were obtained. Both T1 and T2 weighted sequences ( T R / T E in msec:500/30, 2000/80) were studied. The last 28 patients had additional gadolinium enhanced MRs. SPECT was obtained on a General Electric 400 ACT gamma camera, using an elliptical moving table, a low energy parallel hole collimator, a 20% window centered on 159 Key, 128 images through 360 ° rotation, and 10-20 s e e / f r a m e . A 64 × 64 matrix provided a resolution of 12 m m / s l i c e . Three to 5 mCi of N-isopropyl [12:~l]p-iodoamphetamine was used for the SPECT study. The imaging took place in a dimly lit, quiet room approximately l0 rain after intravenous injection. The patients kept their eyes closed during the procedure. In each patient, transaxial, coronal and sagittal views were obtained. In the last 5 patients the SPECT was performed under E E G monitoring. The SPECT study was read abnormal when a persistent tracer uptake asymmetry of more than 20% was seen in two views (i.e., transverse and coronal, transverse and sagittal). Both MR and SPECT were interpreted by neuroimaging specialists blind to the E E G findings, The CT scans were obtained on a 4th generation G E scanner. Ten millimeter transverse and coronal sections were obtained be|~)re and immediately after intravenous injection of 150 ml of diatrizoate meglumine-diatrozoate sodium. Nine patients received a double dose of 300 ml and were scanned 1 h later. For statistical evaluation of the data, we used Fisher's exact test to assess differences between binomial proportions.
109 (?4%) and 15 (26%) patients had non-localized EEGs. A localized E E G was defined as showing: (1) unilateral ictal discharge(s) corresponding to the patient's habitual seizures (35 patients); in this group, few patients had bitemporal interictal spikes but ictal episodes always occurred unilaterally; or (2) unilateral interictal spikes (more than 90% on one side) mixed with significant focal slowing or disturbance of background activity (Quesney and GIoor 1985; Sharbrough 1987) (8 patients). Thirty-four of 43 patients ( ? 9 % ) w i t h localized E E G disclosed at least one focally abnormal NI study whereas 4 of 15 (2?%) patients with non-focal E E G s did so; 3 of these 4 patients had a focally abnormal SPECT only. The incidence of abnormal scans in patients with localized E E G s was significantly higher than those patients with non-focal scans ( P < 0.005). NI studies were focally abnormal in 28 of 35 (80%) patients with ictal localization and 6 of 8 (?5%) patients with interical localization. Nine of 43 patients with localized E E G (15%) had normal or non-focal neuroimaging studies and 5 of 38 patients with positive scans (13%) had non-focal EEGs. Thirty-eight patients (66%) had at least one focally abnormal neuroimaging test. MR, SPECT and CT disclosed focal abnormalities in 29 (50%), 24 ( 4 1 % ) a n d 12 ( 2 0 % ) p a t i e n t s respectively (Table I). Gadolinium enhanced MR did not disclose any new abnormalities over T2 weighted images but in 2 patients provided better definition of the focal pathology. MR and CT showed evidence of diffuse cerebral atrophy in several older patients and MR disclosed multiple areas of increased signal in a young patient with long-tanding migraine. These diffuse and non-specific abnormalities were not considered in our analysis. Twenty-eight of 29 patients with a focal MR (97%), l l of 12 patients with focal CT (92%) and 20 of 24 patients with focal S P E C T (83%) had a concordant, localized E E G (Table II). Focal S P E C T abnormality showed an interictal pattern (decreased uptake) in 18 patients and ictal pattern (increased uptake) in 6 patients. All 6 patients with an ictal SPECT abnormality demonstrated a concordant localized EEG. Three patients with focally abnormal SPECT had non-localized EEGs. In 1 additional patient, SPECT abnormality (decreased uptake) was contralateral to the E E G foTABLE I EEG and focally abnormal NI in partial epilepsy. EEG Localized
Results
Clinical seizures were recorded on video-EEG in 35 of 58 patients (60%). Forty-three patients had localized
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B Fig. ]. From a 28-year-old female with complex partial seizures of 15 years duration. Each attack is characterized by clouding of consciousness often preceded by a smell of "bengay." A: interictal EEG shows frequent spikes over the right temporal regions maximum at T2 and SP2 electrodes. B: ictal EEG recorded on 8-channel ambulatory unit shows rhythmic high voltage 3-7 Hz discharge over the right temporal region.
EEG AND N E U R O I M A G I N G IN PARTIAL EPILEPSY
TABLE II Focally abnormal NI and EEG in partial epilepsy, Focally abnormal
NI CT no. 12 MR no. 29 SPECT no. 24
Localized EEG 11 (91%) 28(97%) 20(83%)
Non-localized EEG 1 (9%) 1 (3%) 4(17%)
cus. Thirteen patients with a focally abnormal MR had a normal SPECT study. Twelve of these patients (92%) demonstrated a concordant localized LEG. Nine patients had a focally abnormal SPECT but a normal MR. Five of these patients (56%) had a focally abnormal and concordant EEG. L E G and neuroimaging localizations were concordant in all 15 patients in whom both MR and SPECT were focally abnormal, There was agreement between ictal and interictal localization in all but 1 of 35 patients in whom L E G showed both focal ictal and interictal activity. This patient's interictal L E G consistently disclosed a spike focus at T1, F7 and left sphenoidal electrode whereas ictal discharges occurred on the right anterior temporal region where MR showed an area of increased T2 signal and SPECT demonstrated decreased flow. Surgery disclosed a right temporal ganglioglioma. The patient remained free of seizures over the follow-up period of 3 years. An anterior temporal lobectomy with amygdalo-hippocampectomy was performed on 15 patients based on concordance of localized L E G with habitual seizures
Fig. 1C. MR, TI weighted image discloses a distinct region of increased signal intensity over the right anterior temporal region consistent with the pathological diagnosis of an angioma,
111
and neuroimaging data. One patient had resection of a right posterior parietal lesion. All patients prior to surgery had detailed psychometric evaluation focused on language and memory functions. Fifteen of 16 patients, had concordant M R - L E G localization (Fig. 1; 6 with additional concordant SPECT abnormality), and one had concordant E E G - S P E C T (ictal) localization and a normal MR study. Electrocorticography was performed before and after cortical resection and subdural strip electrodes were used to record from inferior temporal surface. There were 5 low grade astrocytomas, 3 gangliogliomas, 5 focal cell loss and gliosis, 2 hemangiomas and 1 focal heterotopia with gliosis. All but 1 patient (93%) demonstrated either complete control or significant decrease (more than 80%) in the number of their seizures over a follow-up period of 1-5 years (mean 27 months). There were 11 patients with complete control, 4 with partial but significant control and 1 with no significant improvement. Two of 4 patients with partial control were more than 2 years out of surgery. Both had low grade astrocytomas. The patient with no significant improvement had a posterior parietal ganglioglioma. Significant social adjustment occurred in 12 of 16 patients (75%).
Discussion Even in the era of sophisticated neuroimaging electroencephalography is the only method that can sufficiently monitor an ongoing state of cerebral function (Sato and Rose 1986). Interictal spike (IS), the most common of focal epileptiform events, often correlates with the side of cerebral pathology (Hughes 1989). Presence of intermixed focal slowing or disturbance of background activity as well as wakefulness and REM sleep enhances the localizing value of interictal spikes (Montplaisir et al. 1985; Quesney and Gloor 1985; Sharborough 1987). Unilateral interictal spikes (Spencer et al. 1982) and even lateralized ictal discharges (Sammaritano et al. 1987) may provide false localization. In our study 43 of 58 (74%) patients with recurrent complex partial seizures had a localized LEG. An interical focus was falsely localizing in 1 of 43 patients (2%). We observed no false localization in patients with unilateral ictal discharges. Employment of extended montages (Morris et al. 1986) improves L E G localization. We applied T1, T2, SO1, SO2 and in some cases zygomatic electrode placements (Fig. 1). In our patients with unilateral temporal pathology (tissue diagnosis or MR), ictal and interictal discharges were higher in amplitude in ipsilateral TI or T2 electrodes compared to. F7 and F8 locations and were lower in SO1 and SO2 electrodes.
112 Sphenoidal electrodes disclosed concurrent spikes with lateral temporal electrodes in 30 of 33 patients (91%). Our experience with these electrodes agrees with Sharbrough (1987) in that they usefully demonstrate involvement of uncinate and basal temporal cortex but on a referential montage rarely disclose independent information from lateral temporal electrodes. Engel et al. (1981) reported patients with medial temporal atrophy and gliosis in whom sphenoidal electrodes localized ictal discharges incorrectly. In these patients, a rapidly propagating ictal discharge from the side of pathology showed a higher amplitude over contralateral sphenoid electrode due to ipsilateral suppression of the cortical activity. We did not encounter this phenomenon, Jasper et al. (1951) classified interictal spikes into unilateral, transmitted synchronous, truly synchronous and independent. Independent temporal spikes have been reported in 8-33% of surface EEGs of epileptic patients (Rasmussen 1975; Van Buren et al. 1975; Quesney et al. 1985). A review from the Mayo Clinic (Klass 1975), disclosed no case of brain tumor in a large number of epileptic patients with independent temporal spikes. We had the same experience with 15 patients (26%,) who showed this E E G pattern. Four of these patients (27%.) had a focally abnormal NI study, Two of 4 underwent temporal lobectomy; one in another institution and after invasive monitoring. The pathology in both patients consisted of focal gliosis and moderate cell loss with no neoplastic changes. In recent years, several communications addressed NI findings in partial epilepsy. Among different NI methods, PET has been most extensively investigated in regard to E E G localization. Focal P E T abnormalities were found in approximately 70% of the patients with partial epilepsy and focal PET hypometabolism correlated well with E E G localization (Engel 1985; Theodore et al. 1986; Abou-Khalil et al. 1987). On the other hand, most MR and SPECT reports provide the yield of the technique in partial epilepsy with sparse information on EEG-NI correlation. The following factors may explain the paucity of information in this area. (1) Non-specific abnormalities such as hydrocephalus, asymmetries of sylvian region and diffuse cortical atrophies arc lumped with specific and relevant focal findings. (2) Details of E E G evaluation and methodology of E E G localization are not provided. (3) A small number of studied patients do not allow coherent statistical assessment. (4) Late generation NI methods (especially MR) detect a considerably larger number of focal lesions than the earlier equipments (Kuzniecky et al. 1987). In our study MR was the most powerful of the 3 neuroimaging procedures. It disclosed focal abnormalities in half of the patients and demonstrated a highly significant correlation with localized EEG ( P < 0.005).
B. JABBARI ET AL. This agrees with some earlier communications which reported E E G - M R concordance (Lesser et al. 1986; Sperling et al. 1986). Although focal CT findings also correlated well with localized EEG, the low yield of CT (22% versus 50% of MR) makes it undesirable tbr evaluation of the patients with partial epilepsy. We ignored subtle and non-specific CT findings which are commonly observed in this patient population (Janati et al. 1989). SPECT is a direct measure of cerebral blood flow and an indirect measure of cerebral metabolism. As with PET, focal decrease and increase of tracer uptake in SPECT, correlates with interictal and ictal states (Lee et al. 1988). The yield of interictal SPECT in partial epilepsy was reported to vary from 50 to 90% (Stephen et al. 1987; Lee et al. 1988; Ryding et al. 1988; LaManna et al. 1989). Employment of different SPECT technologies, tracer pharmaceuticals and different abnormality criteria accounts for this wide range of results. False positive results remain a problem with SPECT and some investigators claimed figures as high as 17% (Bluestone et al. 1989; Smith ct al. 1989). We have encountered 1 case of false positive out of 24 patients with focally abnormal SPECTs (4%). Our lower yield (41%) in this study compare to that of others might be related to employment of a more stringent abnormality criteria or our SPECT technology (using a single camera unit). The former could account for encountering less false positives and a better EEGSPECT correlation. Lee et al. (1988) emphasized the concordance between ictal SPECT and EEG localization. Our experience with 6 cases of ictal SPECT agrees with their observation. However, ictal PET or SPECT may falsely indicate a much larger area of structural pathology as blood flow and metabolic changes closely follow rapid propagation of electrical discharges (Engel 1985). In our study, 14 of 18 (77%) patients with focally abnormal interictal SPECT had a concordant localized EEG. This agrees with the figure of 81% reported in a study of 52 patients with partial epilepsy (Cordes et al. 1990). Three of our patients with independent temporal spikes had a focally abnormal SPECT (compared to 1 for MR). Is SPECT more sensetive than MR in the bilateral group? or do these cases represent false localization? Only further correlative studies can answer this question. In conclusion, surface E E G localization as described in the present study demonstrated a significant concordance ( P < 0.005) with neuroimaging localization. Significant improvement of our patients after temporal Iobectomy indicates that the lesions found in NI caused their frequent seizures. Concordance of surface E E G localization with that of MR or SPECT may eliminate the need for pre-surgical invasivc EEGs in many patients with intractable epilepsy.
EEG AND NEUROIMAGING 1N PARTIAL EPILEPSY This study was performed as a part of Project No. 7129, Departmerit of Clinical Investigation, Walter Reed Army Medical Center. Mrs. Robin Howard furnished statistical assessments and Ms. Karen Stevenson provided secretarial assistance.
References Abou-Khalil, B., Seigel, G.L., Sackellaris, C., Gilman, S., Hichwa, R. and Marshall, R. Positron emission tomography studies of cerebral glucose metabolism in chronic partial epilepsy. Ann. Neurol., 1987, 22: 480-486. Bluestone, D.L., Englestad, R.L., Barbaro, N.M. and Laxter, K.D. HMPAO SPECT imaging for intractable complex partial seizures of temporal lobe origin. Epilepsia, 1989, 30: 690. Cordes, M., Christe, W., Henkes, S., Delavier, U., Eichstadt, H., Schorner, W. et al. Focal epilepsies. HM-PAO SPECT compared with CT, MR and EEG.J. Comput. Assist. Tomogr., 1990, 14: 402-409. Engel, Jr., J. Positron emission tomography (PET) in diagnosis of epilepsy. In: R.J. Porter and P.L. Morselli (Eds.), The Epilepsies. Butterworth, Boston, MA, 1985: 243-266. Engel, J. Outcome with respect to epileptic seizures. In: J. Engel (Ed.), Surgical Treatment of Epilepsies. Raven Press, New York, 1987: 553-571. Engel, J. The role of neuroimaging in surgical treatment of epilepsy. Acta Neurol. Scand. Suppl., 1988, 117: 84-89. Engel, Jr., J., Rauch, R., Lieb, J.P., Kuhl, D.E. and Crandall. P.H. Correlation of criteria used for localizing epileptic loci in patients considered for surgical therapy of epilepsy. Ann. Neurol., 1981, 9: 215-224. Glaser, G.tt. Treatment of intractable temporal lobe-limbic epilepsy (complex partial seizuresJ by temporal Iobectomy. Ann. Neurol., t980, 8: 455-459. Hughes, J.R. The significance of the interictal spike discharge: a review. J. Clin. Neurophysiol., 1989, 3: 207-226. Janati, A., Nowack, W.J., Shah, H. and Lucy, Jr., D.D. A correlative study of electrocncephalography and computed tomography in partial complex seizures in adults. J. Epilepsy, 1989, 2: 175-179. Jasper, H.tf., Pertuiset, B. and Flannigan, H. EEG and electrocorticogram in patients with temporal lobe epilepsy. Arch. Neurol. Psychiat., t981, 65: 272-290. Klass, D.W. Electroencephalographic manifestations of partial cornplex seizures. In: J.K. Penry and D.D. Daly (Eds.), Advances of Neurology, Vol. 11. Raven Press, New York, 1975:113-140. Kuzniecky, R., Di la Sayette, V., Ethier, R., Melanson, D., Anderman, F., Berkovic, S. et al. Magnetic resonance imaging in temporal lobe epilepsy - pathological correlations. Ann. Neurol., 1987, 22: 341-347. LaManna, M.M., Sussman, N.M., Harrier, R.N. and Kaplan, L.R. Initial experience with SPECT imaging of the brain using 1 - 1 2 3 p-iodoamphetamine in focal epilepsy. Clin. Nucl. Med., 1989, 14: 428-430. Lee, B.I., Markand, O.N., Wellman, H.N., Siddiqui, A.R., Park, H.M., M6ck, B., Worth, R.M., Edwards, M.K. and Krepshaw, J. HIPDM-SPECT in patients with medically intractable complex partial seizures. Ictal study. Arch. Neurol., 1988, 45: 397-402.
113 Lesser, R.P., Modic, M.T., Weinstein, M.A.. Duchesneau, P.M. et al. Magnetic resonance imaging (1.5 tesla) in patients with intractable focal seizures. Arch. Neurol., 1986, 43: 367-37l. Liiders, H., Lesser, R.P., Dinner, D.S., Morris. H.H., Hahn, J.F., Friedman, L. et al. Chronic intracranial recording and stimulation with subdural electrodes. In: J. Engel (Ed.), Surgical Treatmerit of Epilepsies. Raven Press, New York. 1987: 297-32l. Montplaisir, J., Laverdi~re, M., St-Hilaire, J.M. and Rouleau, I. The localizing value of REM sleep recording in temporal lobe epilepsy. Sleep Res., 1985, 14: 242. Morris, lII, H.H., Liiders, H., Lesser, R.P., Dinner, D.S. and Klem, G.H. The value of closely spaced scalp electrodes in the localization of epileptiform foci: a study of 26 patients with complex partial seizures. Electroenceph. clin. Neurophysiol., 1086, 63: 107-111. Quesney, L.F. and Gloor, P. Localization of epileptic loci. In: LongTerm Monitoring of Epilepsy (EEG Suppl. 37). J. Gotman, J.R. Ires and P. Gloor (Eds.), Elsevier. Amsterdam, 1985: 165-200. Rasmussen. T. Surgical treatment of patients with partial complex seizures. In: J.K. Penry and D.D. Daly (Eds.), Advances in Neurology. Vol. 11. Partial Complex Seizures and Their Treatment. Raven Press, New York, 1975: 415-449. Ryding, E., Rosen, 1., Elmqvist, D. and lngvar, D.H. SPECT measurement with '~'~mTc-HM-PAO in focal epilepsy. J. Cereb. Blood Flow Metab., Vol. 8. Raven Press, New York, 1988: $95-S100. Sammaritano, M., De Lotbini~re, A., Andermann, F., Olivier, A., Gloor, P. and Quesney, L.F. False lateralization by surface EEG of seizure onset in patients with temporal lobe epilepsy and gross focal cerebral lesions. Ann. Neurol. 1987, 21: 215-224. Sato, S. and Rose, D.F. The electroencephalogram in the evaluation of the patients with epilepsy. In: R. Porter and W. Theodore (Eds.), Neurologic Clinics. Epilepsy. Saunders. Philadelphia, PA, 1986: 509-529. Sharbrough, F.W. Extracranial EEG evaluation. In: J. Engel (Ed.), Surgical Treatment of Epilepsies. Raven Press, New York, 1987: 167-171. Smith, M.C., Whisler, W.W. and Morrell, F. Neurosurgery of epilepsy. Sem. Neurol., 1989, 9: 231-248. Spencer, S.S., Spencer, D.D., Williamson, P.D. and Mattson, R.H. The localizing value of depth electroencephalography in 32 patients with refractory epilepsy. Ann. Neurol., 1982, 12: 248-253. Spencer, S. Surgical options for uncontrolled epilepsy, ln: R. Porter and W. Theodore (Eds.), Neurologic Clinics. Epilepsy. Saunders, Philadelpgia, PA, 1986: 669-695. Sperling, M.R., Wilson, G., Engel, Jr., J. et al. Magnetic resonance imaging partial epilepsy. Correlative studies. Ann. Neurol., 1986, 20: 57-62. Stefan, H., Khunen, C., Biersack, H.J. and Reichmann, K. Initial experience with ~gmTc-hexamethyl-propylene amine oxime (HMPAO) single photon emission computed tomography (SPECT) in patients with focal epilepsy. Epilepsy Res., 1987, 1: 134-138. Theodore, W.H., Dorwart, R., Holmes, M., Porter, R.J. and DiChiro, G. Neuroimaging in refractory partial seizures: comparison of PET, CT, and MRI. Neurology, 1986, 36: 750-759. Van Buren, J.M., Ajmone Marsan, C. Mustsuga, N. et al. In: D.P. Purpura, J.K. Penry and R.D. Walter (Eds.), Neurosurgical Management of Epilepsies. Raven Press, New York, 1975: 155.
Electroencephalography and clinical Neurophysiology, 79 ( 1991) 108-113 ~) 1991 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/91/$03.50 ADONIS 001346499100119P
EEG 90174
E E G a n d n e u r o i m a g i n g l o c a l i z a t i o n in p a r t i a l e p i l e p s y * Bahman Jabbari a,c, Douglas Van Nostrand b,c Carl H. Gunderson a,c, David Bartoszek Michael H. Mitchell a,c, Mark Lombardo d, Charles Citrin d and John Sherman d
a,c
" Neurology Sercice, ~' Department of Radiology, Section of Nuclear Medicine, Walter Reed Army Medical Center, Washington, DC (U.S.A.), ' The Um[ormed Sercices Unicersity Of the Health Sciences, Bethesda, MD (U.S.A.), and ~tMagnetic Imaging of Washington, Washington, DC (U.S.A.)
(Accepted for publication: 10 December 199(/)
Summary We have studied cortical localization provided by surface and sphenoidal electroencephalograms (EEGs) and that of computed tomography (CT), magnetic resonance imaging (MR) and single photon emission tomography (SPECT) in 58 patients with partial epilepsy. Each patient had EEG, MR and SPECT during a hospitalization period of 1-2 weeks. CT scans were obtained either during the same period or had been performed in the preceding year. EEG evaluation consisted of 3-5 days of continuous monitoring including video-telemetry and ambulatory recording as well as conventional EEGs with special electrode placements. Additionally 33 of 58 patients (55%) who were potential surgical candidates had sphenoidal recordings. All patients had an abnormal EEG which showed evidence of epileptic hyperexcitability. EEG abnormality was localized in 43 patients (74%). Neuroimaging studies were focally abnormal in 38 patients (66%); 12 CT (21%), 29 MR (50~/~) and 24 SPECT (41%). Thirty four of 43 patients with localized EEG had at least 1 focally abnormal neuroimaging study (79%), whereas 4 of 15 (27%) patients with non-localized EEG did so. Twenty-eight of 29 patients with focal MR (97%), 11 of 12 patients with focal CT (92%) and 20 of 24 patients with focal SPECT (83%) had a concordant focal EEG. EEG and neuroimaging localization agreed in all 15 patients in whom both MR and SPECT disclosed a concordant focal abnormality. This study demonstrates a significant( P < 0.005) correlation between surface/sphenoid EEG and neuroimaging localization in partial epilepsy. Key words: EEG; Neuroimaging localization; Partial epilepsy: Computed tomography; Magnetic resonance imaging; Single photon emission tomography
Surgical resection of the e p i l e p t o g e n e t i c cortex provides significant relief from i n t r a c t a b l e partial epilepsy in 7 0 - 8 0 % of selected p a t i e n t s ( G l a s e r 1980; E n g e l 1987). E E G e v a l u a t i o n r e m a i n s essential to epilepsy surgery. In m a n y patients, p r o p e r localization requires application of s u b d u r a l or d e p t h electrodes ( S p e n c e r et
c o m p u t e d t o m o g r a p h y (CT), m a g n e t i c r e s o n a n c e imaging ( M R ) a n d single p h o t o n emission t o m o g r a p h y (SPECT).
al. 1982; Liiders et al. 1987). O t h e r p a t i e n t s do well without invasive p r o c e d u r e s if surface, s p h e n o i d a l a n d v i d e o - E E G provide consistent interictal a n d ictal localization ( S h a r b r o u g h 1987). N e u r o i m a g i n g (NI) procedures have m a d e a significant impact in this area by disclosing the site of pathology a n d s u p p o r t i n g E E G localization (Engel 1988). W e have studied the correlation b e t w e e n epileptic focus as seen in surface and
Fifty-eight consecutive p a t i e n t s with r e c u r r e n t partial seizures have b e e n studied. P a t i e n t s signed an i n f o r m e d c o n s e n t before participating. All p a t i e n t s had complex partial seizures according to the I n t e r n a t i o n a l Classification of Epileptic Seizures (ICES 19811. T w e n t y - t h r e e p a t i e n t s had initial partial simple symp-
Patients and methods
s p h e n o i d a l E E G a n d localization provided by 3 commonly available n e u r o i m a g i n g techniques, namely:
toms which evolved into complex partial seizures. Sixt e e n p a t i e n t s had o n e or more episodes of secondary g e n e r a l i z a t i o n in the p r e c e d i n g year. T h e group consisted of 43 females a n d 15 males with a m e a n age of
* The opinions and assertions expressed in this paper are the private views of the authors and should not be construed as reflecting the views of the U.S. Army, Department of Defense or Uniformed Services University of the Health Sciences.
32.9 years (range: 9 - 7 2 years). T h e i r d u r a t i o n of symptoms varied from 1 to 42 years (mean: 12). All p a t i e n t s were on a n t i c o n v u l s a n t medications, usually two of the following: p h e n y t o i n , c a r b a m a z e p i n e a n d valproic acid. T h e p a t i e n t s e n t e r e d the hospital for a period of 1-2 weeks for electrophysiological, M R a n d S P E C T stud-
Correspondence to: Bahman Jabbari, M.D., Neurology Service, Walter Reed Army Medical Center, Washington, DC 20307-5001 (U.S.A.I.
ies. All p a t i e n t s had a C T scan either d u r i n g this period or in the year p r e c e d i n g this evaluation. T h e electrophysiological assessment consisted of 3 - 5
EE(} AND NEUROIMAGING IN PARTIAL EPILEPSY days of continuous monitoring including 4 8 - ? 2 h of video-telemetry performed on 64- and 16-channel Telefactor unit, one or more 8-channel 24 h ambulatory recording and several conventional E E G s on 18channel Grass equipments. In the majority of the patients v i d e o - E E G monitoring was obtained after gradual reduction of the medications and in a few after discontinuing antiepileptic drugs. Conventional recordings were performed according to the international 10-20 system using both referential and differential montages. The recording montages included T1, T2, supraorbital (SO1, S O 2 ) a n d in some cases zygomatic electrode placements. Additionally, 33 of 58 patients (55CY~) who were considered to be potential surgical candidates had sphenoidal recordings. MR was performed on 0.5 tesla Teehnicare and 1.5 tesla Phillips equipment with comparable resolutions, A l0 mm slice thickness was employed in axial, transverse, coronal and sagittal views and in 12 patients 5 mm slices were obtained. Both T1 and T2 weighted sequences ( T R / T E in msec:500/30, 2000/80) were studied. The last 28 patients had additional gadolinium enhanced MRs. SPECT was obtained on a General Electric 400 ACT gamma camera, using an elliptical moving table, a low energy parallel hole collimator, a 20% window centered on 159 Key, 128 images through 360 ° rotation, and 10-20 s e e / f r a m e . A 64 × 64 matrix provided a resolution of 12 m m / s l i c e . Three to 5 mCi of N-isopropyl [12:~l]p-iodoamphetamine was used for the SPECT study. The imaging took place in a dimly lit, quiet room approximately l0 rain after intravenous injection. The patients kept their eyes closed during the procedure. In each patient, transaxial, coronal and sagittal views were obtained. In the last 5 patients the SPECT was performed under E E G monitoring. The SPECT study was read abnormal when a persistent tracer uptake asymmetry of more than 20% was seen in two views (i.e., transverse and coronal, transverse and sagittal). Both MR and SPECT were interpreted by neuroimaging specialists blind to the E E G findings, The CT scans were obtained on a 4th generation G E scanner. Ten millimeter transverse and coronal sections were obtained be|~)re and immediately after intravenous injection of 150 ml of diatrizoate meglumine-diatrozoate sodium. Nine patients received a double dose of 300 ml and were scanned 1 h later. For statistical evaluation of the data, we used Fisher's exact test to assess differences between binomial proportions.
109 (?4%) and 15 (26%) patients had non-localized EEGs. A localized E E G was defined as showing: (1) unilateral ictal discharge(s) corresponding to the patient's habitual seizures (35 patients); in this group, few patients had bitemporal interictal spikes but ictal episodes always occurred unilaterally; or (2) unilateral interictal spikes (more than 90% on one side) mixed with significant focal slowing or disturbance of background activity (Quesney and GIoor 1985; Sharbrough 1987) (8 patients). Thirty-four of 43 patients ( ? 9 % ) w i t h localized E E G disclosed at least one focally abnormal NI study whereas 4 of 15 (2?%) patients with non-focal E E G s did so; 3 of these 4 patients had a focally abnormal SPECT only. The incidence of abnormal scans in patients with localized E E G s was significantly higher than those patients with non-focal scans ( P < 0.005). NI studies were focally abnormal in 28 of 35 (80%) patients with ictal localization and 6 of 8 (?5%) patients with interical localization. Nine of 43 patients with localized E E G (15%) had normal or non-focal neuroimaging studies and 5 of 38 patients with positive scans (13%) had non-focal EEGs. Thirty-eight patients (66%) had at least one focally abnormal neuroimaging test. MR, SPECT and CT disclosed focal abnormalities in 29 (50%), 24 ( 4 1 % ) a n d 12 ( 2 0 % ) p a t i e n t s respectively (Table I). Gadolinium enhanced MR did not disclose any new abnormalities over T2 weighted images but in 2 patients provided better definition of the focal pathology. MR and CT showed evidence of diffuse cerebral atrophy in several older patients and MR disclosed multiple areas of increased signal in a young patient with long-tanding migraine. These diffuse and non-specific abnormalities were not considered in our analysis. Twenty-eight of 29 patients with a focal MR (97%), l l of 12 patients with focal CT (92%) and 20 of 24 patients with focal S P E C T (83%) had a concordant, localized E E G (Table II). Focal S P E C T abnormality showed an interictal pattern (decreased uptake) in 18 patients and ictal pattern (increased uptake) in 6 patients. All 6 patients with an ictal SPECT abnormality demonstrated a concordant localized EEG. Three patients with focally abnormal SPECT had non-localized EEGs. In 1 additional patient, SPECT abnormality (decreased uptake) was contralateral to the E E G foTABLE I EEG and focally abnormal NI in partial epilepsy. EEG Localized
Results
Clinical seizures were recorded on video-EEG in 35 of 58 patients (60%). Forty-three patients had localized
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B Fig. ]. From a 28-year-old female with complex partial seizures of 15 years duration. Each attack is characterized by clouding of consciousness often preceded by a smell of "bengay." A: interictal EEG shows frequent spikes over the right temporal regions maximum at T2 and SP2 electrodes. B: ictal EEG recorded on 8-channel ambulatory unit shows rhythmic high voltage 3-7 Hz discharge over the right temporal region.
EEG AND N E U R O I M A G I N G IN PARTIAL EPILEPSY
TABLE II Focally abnormal NI and EEG in partial epilepsy, Focally abnormal
NI CT no. 12 MR no. 29 SPECT no. 24
Localized EEG 11 (91%) 28(97%) 20(83%)
Non-localized EEG 1 (9%) 1 (3%) 4(17%)
cus. Thirteen patients with a focally abnormal MR had a normal SPECT study. Twelve of these patients (92%) demonstrated a concordant localized LEG. Nine patients had a focally abnormal SPECT but a normal MR. Five of these patients (56%) had a focally abnormal and concordant EEG. L E G and neuroimaging localizations were concordant in all 15 patients in whom both MR and SPECT were focally abnormal, There was agreement between ictal and interictal localization in all but 1 of 35 patients in whom L E G showed both focal ictal and interictal activity. This patient's interictal L E G consistently disclosed a spike focus at T1, F7 and left sphenoidal electrode whereas ictal discharges occurred on the right anterior temporal region where MR showed an area of increased T2 signal and SPECT demonstrated decreased flow. Surgery disclosed a right temporal ganglioglioma. The patient remained free of seizures over the follow-up period of 3 years. An anterior temporal lobectomy with amygdalo-hippocampectomy was performed on 15 patients based on concordance of localized L E G with habitual seizures
Fig. 1C. MR, TI weighted image discloses a distinct region of increased signal intensity over the right anterior temporal region consistent with the pathological diagnosis of an angioma,
111
and neuroimaging data. One patient had resection of a right posterior parietal lesion. All patients prior to surgery had detailed psychometric evaluation focused on language and memory functions. Fifteen of 16 patients, had concordant M R - L E G localization (Fig. 1; 6 with additional concordant SPECT abnormality), and one had concordant E E G - S P E C T (ictal) localization and a normal MR study. Electrocorticography was performed before and after cortical resection and subdural strip electrodes were used to record from inferior temporal surface. There were 5 low grade astrocytomas, 3 gangliogliomas, 5 focal cell loss and gliosis, 2 hemangiomas and 1 focal heterotopia with gliosis. All but 1 patient (93%) demonstrated either complete control or significant decrease (more than 80%) in the number of their seizures over a follow-up period of 1-5 years (mean 27 months). There were 11 patients with complete control, 4 with partial but significant control and 1 with no significant improvement. Two of 4 patients with partial control were more than 2 years out of surgery. Both had low grade astrocytomas. The patient with no significant improvement had a posterior parietal ganglioglioma. Significant social adjustment occurred in 12 of 16 patients (75%).
Discussion Even in the era of sophisticated neuroimaging electroencephalography is the only method that can sufficiently monitor an ongoing state of cerebral function (Sato and Rose 1986). Interictal spike (IS), the most common of focal epileptiform events, often correlates with the side of cerebral pathology (Hughes 1989). Presence of intermixed focal slowing or disturbance of background activity as well as wakefulness and REM sleep enhances the localizing value of interictal spikes (Montplaisir et al. 1985; Quesney and Gloor 1985; Sharborough 1987). Unilateral interictal spikes (Spencer et al. 1982) and even lateralized ictal discharges (Sammaritano et al. 1987) may provide false localization. In our study 43 of 58 (74%) patients with recurrent complex partial seizures had a localized LEG. An interical focus was falsely localizing in 1 of 43 patients (2%). We observed no false localization in patients with unilateral ictal discharges. Employment of extended montages (Morris et al. 1986) improves L E G localization. We applied T1, T2, SO1, SO2 and in some cases zygomatic electrode placements (Fig. 1). In our patients with unilateral temporal pathology (tissue diagnosis or MR), ictal and interictal discharges were higher in amplitude in ipsilateral TI or T2 electrodes compared to. F7 and F8 locations and were lower in SO1 and SO2 electrodes.
112 Sphenoidal electrodes disclosed concurrent spikes with lateral temporal electrodes in 30 of 33 patients (91%). Our experience with these electrodes agrees with Sharbrough (1987) in that they usefully demonstrate involvement of uncinate and basal temporal cortex but on a referential montage rarely disclose independent information from lateral temporal electrodes. Engel et al. (1981) reported patients with medial temporal atrophy and gliosis in whom sphenoidal electrodes localized ictal discharges incorrectly. In these patients, a rapidly propagating ictal discharge from the side of pathology showed a higher amplitude over contralateral sphenoid electrode due to ipsilateral suppression of the cortical activity. We did not encounter this phenomenon, Jasper et al. (1951) classified interictal spikes into unilateral, transmitted synchronous, truly synchronous and independent. Independent temporal spikes have been reported in 8-33% of surface EEGs of epileptic patients (Rasmussen 1975; Van Buren et al. 1975; Quesney et al. 1985). A review from the Mayo Clinic (Klass 1975), disclosed no case of brain tumor in a large number of epileptic patients with independent temporal spikes. We had the same experience with 15 patients (26%,) who showed this E E G pattern. Four of these patients (27%.) had a focally abnormal NI study, Two of 4 underwent temporal lobectomy; one in another institution and after invasive monitoring. The pathology in both patients consisted of focal gliosis and moderate cell loss with no neoplastic changes. In recent years, several communications addressed NI findings in partial epilepsy. Among different NI methods, PET has been most extensively investigated in regard to E E G localization. Focal P E T abnormalities were found in approximately 70% of the patients with partial epilepsy and focal PET hypometabolism correlated well with E E G localization (Engel 1985; Theodore et al. 1986; Abou-Khalil et al. 1987). On the other hand, most MR and SPECT reports provide the yield of the technique in partial epilepsy with sparse information on EEG-NI correlation. The following factors may explain the paucity of information in this area. (1) Non-specific abnormalities such as hydrocephalus, asymmetries of sylvian region and diffuse cortical atrophies arc lumped with specific and relevant focal findings. (2) Details of E E G evaluation and methodology of E E G localization are not provided. (3) A small number of studied patients do not allow coherent statistical assessment. (4) Late generation NI methods (especially MR) detect a considerably larger number of focal lesions than the earlier equipments (Kuzniecky et al. 1987). In our study MR was the most powerful of the 3 neuroimaging procedures. It disclosed focal abnormalities in half of the patients and demonstrated a highly significant correlation with localized EEG ( P < 0.005).
B. JABBARI ET AL. This agrees with some earlier communications which reported E E G - M R concordance (Lesser et al. 1986; Sperling et al. 1986). Although focal CT findings also correlated well with localized EEG, the low yield of CT (22% versus 50% of MR) makes it undesirable tbr evaluation of the patients with partial epilepsy. We ignored subtle and non-specific CT findings which are commonly observed in this patient population (Janati et al. 1989). SPECT is a direct measure of cerebral blood flow and an indirect measure of cerebral metabolism. As with PET, focal decrease and increase of tracer uptake in SPECT, correlates with interictal and ictal states (Lee et al. 1988). The yield of interictal SPECT in partial epilepsy was reported to vary from 50 to 90% (Stephen et al. 1987; Lee et al. 1988; Ryding et al. 1988; LaManna et al. 1989). Employment of different SPECT technologies, tracer pharmaceuticals and different abnormality criteria accounts for this wide range of results. False positive results remain a problem with SPECT and some investigators claimed figures as high as 17% (Bluestone et al. 1989; Smith ct al. 1989). We have encountered 1 case of false positive out of 24 patients with focally abnormal SPECTs (4%). Our lower yield (41%) in this study compare to that of others might be related to employment of a more stringent abnormality criteria or our SPECT technology (using a single camera unit). The former could account for encountering less false positives and a better EEGSPECT correlation. Lee et al. (1988) emphasized the concordance between ictal SPECT and EEG localization. Our experience with 6 cases of ictal SPECT agrees with their observation. However, ictal PET or SPECT may falsely indicate a much larger area of structural pathology as blood flow and metabolic changes closely follow rapid propagation of electrical discharges (Engel 1985). In our study, 14 of 18 (77%) patients with focally abnormal interictal SPECT had a concordant localized EEG. This agrees with the figure of 81% reported in a study of 52 patients with partial epilepsy (Cordes et al. 1990). Three of our patients with independent temporal spikes had a focally abnormal SPECT (compared to 1 for MR). Is SPECT more sensetive than MR in the bilateral group? or do these cases represent false localization? Only further correlative studies can answer this question. In conclusion, surface E E G localization as described in the present study demonstrated a significant concordance ( P < 0.005) with neuroimaging localization. Significant improvement of our patients after temporal Iobectomy indicates that the lesions found in NI caused their frequent seizures. Concordance of surface E E G localization with that of MR or SPECT may eliminate the need for pre-surgical invasivc EEGs in many patients with intractable epilepsy.
EEG AND NEUROIMAGING 1N PARTIAL EPILEPSY This study was performed as a part of Project No. 7129, Departmerit of Clinical Investigation, Walter Reed Army Medical Center. Mrs. Robin Howard furnished statistical assessments and Ms. Karen Stevenson provided secretarial assistance.
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