Scalp EEG Findings in Temporal Lobe Epilepsy · Temporal lobe epilepsy (TLE) • The most common form of focal epilepsy worldwide. • Anterior Temporal Lobectomy (ATL) for medically

Scalp EEG Findings in

Temporal Lobe Epilepsy

EEG Course, CNSF, Ottawa, ON

Thursday, June 07, 2012

Seyed M Mirsattari M.D., Ph.D., F.R.C.P.(C)

Assistant Professor

Depts. of CNS, Medical Biophysics,

Medical Imaging, and Psychology

University of Western Ontario

[email protected]

mailto:[email protected]

Learning Objectives

• Temporal Lobe Epilepsy, a brief review

• Scalp EEG, a brief review

• EEG aspects of TLE with relevance to

surgery

Disclosure statement

• Dr. Mirsattari has nothing to disclose

Temporal lobe epilepsy (TLE) • The most common form of focal epilepsy

worldwide. • Anterior Temporal Lobectomy (ATL) for

medically refractory TLE secondary to mesial temporal sclerosis (MTS) is the most commonly performed surgical procedure in the comprehensive epilepsy management centres.

• Surgery is ideally directed towards complete seizure freedom without or with very minimal cognitive or functional deficits.

• A randomised control study demonstrated the effectiveness of surgery in adult patients with medically refractory TLE (Wiebe et al,. NEJM 2001;345:311-8.)

Jasper HH. The ten-twenty electrode system of the International Federation.

Electroenceph Clin Neurophysiol 1958;10:371- 5.

International 10-20 system of electrode placements

EEG montages

Bipolar Coronal

Common

Average

Reference

Point =

CAR

Referential

EEG scalp recording: normal, awake

Scalp EEG in TLE

• Electrophysiological assessment

remains the corner stone for

assessment of patients with TLE.

• Standard EEG recording techniques

with 10-20 system provides limited

coverage of the temporal regions.

Scalp EEG for TLE

• Additional Silverman’s electrodes (T1 and T2)

• Anterior one third and posterior two third of a

line connecting the outer canthus of the eye

and the tragus) are often used in addition to

standard 10-20 system to record from the

anterior-basal areas of temporal lobes

Silverman D. The anterior temporal electrode and the ten-twenty system.

Electroencephalograph Clin Neurophysiol 1960;12:735-737.

• May be placed between any of the principal standard positions

Additional electrodes to 10-20 system of electrode placement

Additional Localizing Electrodes

• Mandibular Notch

• Sphenoidal

• Nasopharyngeal

EEG Electrodes for TLE • Chatrian GE, et al. Modified nomenclature for

the "10%" electrode system. J Clin

Neurophysiol 1988;5(2):183-6.

• Gloor P. Preoperative electroencephalographic

investigation in temporal lobe epilepsy:

extracranial and intracranial recordings. Can J

Neurol Sci. 1991;18:554-8.

• Nowack WJ, et al. The anterior temporal

electrode in the EEG of the adult. Clin

Electroencephalogr. 1988;19:199-204.

• Blume WT. The necessity for sphenoidal

electrodes in the presurgical evaluation of

temporal lobe epilepsy: con position. J Clin

Neurophysiol 2003;20:305-10.

Interictal EEG Abnormalities in

TLE

• Focal arrhythmic slowing

• theta or delta activity

Focal Slowing in the L T Region

Interictal EEG Abnormalities in TLE

• Focal interictal epileptiform discharges

(IEDS) with after coming slow waves in

the temporal regions that are often

restricted to the anterior temporal

areas.

Interictal EEG in wakefulness (27 yrs old)

Interictal EEG in wakefulness (27 yrs old)

Interictal EEG in sleep (27 yrs old)

Interictal EEG in sleep (27 yrs old)

R MTS in MRI (27 yrs old)

Interictal EEG Abnormalities in TLE (#2) Typical EEG in a R mTLE showing R T slowing as theta-delta activity over the R T

regions and R T spikes (*) phase reversing across F8 and T4 electrodes.

Interictal EEG Abnormalities in TLE (#2) Typical EEG in a R mTLE showing R T slowing as theta-delta activity over the R T

regions and R T spikes (*) phase reversing across F8 and T4 electrodes.


TLE

• Focal slowing and spikes correlate very well

with ictal onset zone:

• Focal delta (82%)

• Spikes (90%)

Blume WT, et al. Interictal indices of temporal seizure origin. Ann

Neurol 1993;34:703-9.

Pataraia E, et al. Ictal scalp EEG in unilateral mesial temporal lobe

epilepsy. Epilepsia. 1998;39:608-14.


TLE

• Focal slowing and spikes

correlated very well with the

structural abnormalities detected

by the MRI in majority of the

patients with TLE.

Cascino GD, et al. Routine EEG and temporal lobe epilepsy: relation to long-term

EEG monitoring, quantitative MRI, and operative outcome. Epilepsia 1996;37:651-6.

MRI in a patient with R mTLE: Hippocampal volume loss & signal changes (short arrows)

Poor gray white differentiation in R M T gyrus (long arrow)

Routine Outpatient EEGs in TLE

• Strong correlations for spikes and delta

may obviate the need for mandatory ictal

recordings in highly well selected

patients undergoing presurgical workup

with unilateral hippocampal atrophy on

MRI and congruent clinical and

neuropsychological data.

Cendes F, et al., Is ictal recording mandatory in temporal lobe epilepsy? Not when

the interictal electroencephalogram and hippocampal atrophy coincide. Arch Neurol.

2000;57:497-500.

Ictal EEGs in TLE

• Ictal recordings are usually essential as some

patients can have concurrent non-epileptic

attacks such as psychogenic non-epileptic

seizures (PNESs).

• Bilateral TLE or coexisting extratemporal

epilepsy may not be appreciated in routine

outpatient scalp EEGs.

Mesial TLE (mTLE) vs Neocortical TLE (nTLE)

• IEDs and clinical semiology aid to differentiate

between mTLE and nTLE.

•The interictal discharges remain lateralized to the

temporal regions in both.

•In mTLE, IEDs are dominant over the anterior

mesial temporal areas (T1/2, A1/2, F7/8, T3/4).

•In nTLE, IEDs are dominant over the lateral and

posterior temporal areas (T5/6).

Pfänder M, et al. Clinical features and EEG findings differentiating mesial from

neocortical temporal lobe epilepsy. Epileptic Disord 2002;4:189-95.

Hamer HM, et al. Interictal epileptiform discharges in temporal lobe epilepsy due to

hippocampal sclerosis versus medial temporal lobe tumors. Epilepsia 1999;40:1261-8.

mTLE vs nTLE • Mesial temporal IEDs occur infrequently in nTLE

but neocortical spikes is unlikely with mTLE.

• IEDs in MTS tend to be more localized to anterior

temporal region but with increased tendency for

bilateral expression than mTLE secondary to

tumors.

•Typical anterior temporal spikes can be seen in

association with extratemporal epilepsy (e.g.

mesial occipital lobe epilepsy which can mimic

TLE).

Pfänder M, et al. Clinical features and EEG findings differentiating mesial from neocortical temporal lobe epilepsy. Epileptic Disord 2002;4:189-95. Hamer HM, et al. Interictal epileptiform discharges in temporal lobe epilepsy due to hippocampal sclerosis versus medial temporal lobe tumors. Epilepsia 1999;40:1261-8. Aykut-Bingol C, et al. Surgical outcome in occipital lobe epilepsy: implications for pathophysiology. Ann Neurol 1998;44:60-9. Tandon N, et al. Occipital epilepsy: spatial categorization and surgical management. J Neurosurg 2009;110:306-18.

Unilateral TLE • A portion of patients with unilateral TLE with

other evaluation parameters show bitemporal

IEDS.

• Most of these patients do well with epilepsy

surgery.

• However, increasing bilateral epileptiform

discharges are associated with less optimal

surgical outcomes.

Schulz R, et al. Interictal EEG and ictal scalp EEG propagation are highly predictive of surgical outcome in mesial temporal lobe epilepsy. Epilepsia 2000;41:564-70. Baumgartner C, et al. Propagation of interictal epileptic activity in temporal lobe epilepsy. Neurology 1995;45:118-22.

Prognostic Value of the Spike

Dipoles in TLE

• Ebersole Type I spikes: A relatively localized

negativity at the anterior temporal electrodes or

sphenoidal electrodes with widespread vertex

positivity.

• Localizes the abnormality to mesio-basal

temporal lobe.

• Associated with a very good surgical outcome.

How about Ebersole Type I and II. Ebersole JS, Wade PB. Spike voltage identifies two types of frontotemporal epileptic foci. Neurology 1991;41:1425-33.

• Ebersole Type II spikes: IEDs with relatively

localised negativity over the temporal regions and

widespread contralateral hemispheric positivity.

• Indicate either temporal or frontal neocortex

originating spikes.

How about Ebersole Type I and II. Ebersole JS, Wade PB. Spike voltage identifies two types of frontotemporal epileptic foci. Neurology 1991;41:1425-33.

Prognostic Value of the Spike

Dipoles in TLE

Spike Frequency in TLE

• Frequent IEDs or high spike burden (i.e. 60

spikes/hour in one study) is associated with poor

outcome after temporal lobectomy (TLY).

•Supportive of the mouse model hypothesis:

IEDs are involved with inhibitory physiology

controlling seizures (?)

Krendl R, et al. Absolute spike frequency predicts surgical outcome in TLE with unilateral hippocampal atrophy. Neurology. 2008;71:413-8. Avoli M. Do interictal discharges promote or control seizures? Experimental evidence from an in vitro model of epileptiform discharge. Epilepsia 2001;42:2-4.

TLE with Oligospikes

• TLE patients with infrequent or absent IEDs

• IEDs < 1 in an hr on several scalp EEGs

• Have a good ictal localization and excellent

surgical outcome similar to patients with

frequent IEDs.

• Associated with later onset TLE, less frequent

seizures, less SE, less MTS.

• Represents milder degree of MTS without

differences in etiological factors.

• Absence of IEDs could suggest extratemporal

seizures and would require extra care.

Rosati A, et al. Intractable temporal lobe epilepsy with rare spikes is less severe than with frequent spikes. Neurology 2003;60:1290-5. Stüve O, et al. The absence of interictal spikes with documented seizures suggests extratemporal epilepsy. Epilepsia 2001;42:778-81.

Ictal Rhythms in TLE • Can be variable even within the same patient.

• In about 90% of patients with unilateral TLE

(MRI and IEDs), the lateralization of the ictal

changes corresponds.

• Lateralization can be observed at onset in only

one third of these patients with unilateral TLE.

• Ictal EEG does not help in differentiating the

anterior from posterior lateral TLE.

Pataraia E,et al.Ictal scalp EEG in unilateral mesial temporal lobe epilepsy.Epilepsia1998;39:608-14 Lee SY, et al. Clinico-electrical Characteristics of Lateral Temporal Lobe Epilepsy; Anterior and Posterior Lateral Temporal Lobe Epilepsy. J Clin Neurol 2006;2:118-25. Ebersole JS, et al.Localization of temporal lobe foci by ictal EEG patterns.Epilepsia1996;37:386-99. Foldvary N, et al. The localizing value of ictal EEG in focal epilepsy. Neurology 2001;57:2022-8. Foldvary N, et al. Clinical and electrographic manifestations of lesional neocortical temporal lobe epilepsy. Neurology 1997;49:757-63.

Ebersole Classification of the Ictal

Rhythms in TLE (3 Types)

• Type I: rhythmic 5-9 Hz theta activity that

slowly evolves and remains localized to the

temporal or sub-temporal regions.

• The most specific pattern for seizures

originating from the hippocampal areas.

• Type 1b rhythm: a vertical dipole (mesial basal

temporal negativity and vertex positivity) results

in a rhythmic parasagittal positive ictal rhythmic

activity.

• Type 1C: a combination of Type 1 and 1b.

Ebersole JS, Pacia SV.Localization of temporal lobe foci by ictal EEG patterns. Epilepsia 1996;37:386-99.

An example of Ebersole Type I

Ictal Rhythm in TLE

• Lower frequency (2-5 Hz) irregular ictal

rhythm with widespread temporal distribution.

• Is often associated with neocortical seizures.

Ebersole Type 2 Ictal Rhythms in TLE


An example of Ebersole “Type II”

Ictal Rhythm in TLE

• Diffuse ictal EEG changes or attenuation

without clear lateralization.

• Is seen both in hippocampal and temporal

neocortical seizures.

Ebersole Type 3 Ictal Rhythms in TLE


Simultaneous Scalp Ictal

Rhythms with Subdural and

Depth Recordings

• Most subclinical electrical seizures

confined to hippocampus do not result in

surface EEG changes.

Napolitano CE, Orriols M. Two types of remote propagation in mesial temporal epilepsy: analysis with scalp ictal EEG. J Clin Neurophysiol 2008;25:69-76. Schulz R, et al. Interictal EEG and ictal scalp EEG propagation are highly predictive of surgical outcome in mesial temporal lobe epilepsy. Epilepsia 2000;41:564-70. Jung KY, et al. Spatiotemporospectral characteristics of scalp ictal EEG in mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Res 2009;1287:206-19.

• Type I ictal rhythm is observed when

the seizures spread from mesial

temporal to the infero-lateral temporal

structures.




Depth Recordings

•Type 2 ictal rhythm are often neocortical seizures

starting as fast activity (20-40 Hz) on subdural

electrodes that are either not detectable on

surface EEG or seen as attenuation pattern

followed by asynchrounous theta-delta activity

over the temporal regions. Napolitano CE, Orriols M. Two types of remote propagation in mesial temporal epilepsy: analysis with scalp ictal EEG. J Clin Neurophysiol 2008;25:69-76. Schulz R, et al. Interictal EEG and ictal scalp EEG propagation are highly predictive of surgical outcome in mesial temporal lobe epilepsy. Epilepsia 2000;41:564-70. Jung KY, et al. Spatiotemporospectral characteristics of scalp ictal EEG in mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Res 2009;1287:206-19.



Depth Recordings

•Type 3 ictal rhythm occurs when the seizures

are confined to the hippocampus, or spread

rapidly to the contralateral hippocampus where

there is little synchronization of the electrical

activity over the inferior lateral temporal

structures for expression on the surface EEG.




Depth Recordings

• Early propagation (< 10 seconds) may suggest

more widespread hyperexcitability and greater

probability of bilateral temporal epileptogenicity

and tends to occur in patients other than pure

MTS.

• Best surgical benefits can be expected in those

patients with regionalized ictal EEG activity

without contralateral spread and ipsilateral

interictal changes.

Simultaneous Scalp Ictal Rhythms with

Subdural and Depth Recordings

• Switch of lateralization or bitemporal synchrony

in the ictal scalp EEG and bitemporal IEDs are

probably indices of bitemporal epileptogenicity

and are associated with a worse outcome.

• ICA of the ictal onset patterns:

•seizures with theta rhythm are ipsilateral mesial

temporal and basal ganglia onset and then spread to

the mesial frontal regions

•Seizures with delta activity are mesial temporal with

spread to the mesial frontal and basal ganglia.

Simultaneous Scalp Ictal Rhythms with

Subdural and Depth Recordings

Jung KY, et al. Spatiotemporospectral characteristics of scalp ictal EEG in mesial

temporal lobe epilepsy with hippocampal sclerosis. Brain Res 2009;1287:206-19.

• Are required when noninvasive data are

discordant.

• The most important step prior to embarking upon

invasive recording is a proper unbiased

hypothesis.

• Indications for invasive recording in TLE include

either bitemporal epilepsy or temporal plus

syndromes.

Invasive EEG Recordings

Siegel AM, et al. Medically intractable, localization-related epilepsy with normal MRI: presurgical evaluation and surgical outcome in 43 patients. Epilepsia 2001;42:883-8. Eisenschenk S, et al. Lateralization of temporal lobe foci: depth versus subdural electrodes. Clin Neurophysiol 2001;112:836-44.

• Invasive recordings can be performed with

multiple subdural lines, subdural grids, depth

electrodes or a combination of them.

• There is a high degree of concordance between

the subdural and depth recordings in TLE

particularly if electrode placement is optimal

• recording from the surface of parahippocampal gyrus

• mesial to the collateral sulcus.

Invasive EEG Recordings

Siegel AM, et al. Medically intractable, localization-related epilepsy with normal MRI: presurgical evaluation and surgical outcome in 43 patients. Epilepsia 2001;42:883-8. Eisenschenk S, et al. Lateralization of temporal lobe foci: depth versus subdural electrodes. Clin Neurophysiol 2001;112:836-44.

Subdurally Recorded Seizures

•In general, most of the subdural seizures arise

from the same lobe showing predominant surface

IEDs and surface seizures.

•Presence of periodic IEDS prior to the seizure

onset in medial temporal lobe structures is often

specific for hippocampal onset seizures and

correlates well to reduced CA1 cell counts.

Blume WT, et al. Temporal epileptogenesis: localizing value of scalp and

subdural interictal and ictal EEG data. Epilepsia 2001;42:508-14.


•The onset in the hippocampal seizures has 13-20

Hz frequencies.

•The onset in temporal neocortical seizures has

significantly faster (20-40 Hz) frequencies.

•Mesial temporal sclerosis in comparison to

temporal lobe epilepsy not associated with MTS is

more likely to have higher seizure onset frequency

and is associated with periodic spikes prior to

seizure onset.

Blume WT, et al. Temporal epileptogenesis: localizing value of scalp and

subdural interictal and ictal EEG data. Epilepsia 2001;42:508-14.

• Hypersynchronous rhythmic high amplitude activity

(HYP)

• likely to represent more focal onset

• lesser rate of spread to contralateral mesial

temporal structures

• associated with more marked neuronal loss in the

hippocampi

• Low voltage fast activity (LVFA)

• more regionalized and neocortical in nature

• involves both hippocampal and extrahippocampal

networks

Two Common Patterns of Temporal Lobe

Seizures with Invasive EEGs

• Subdural patterns may be substrate specific and

prognostic.

• Seizures with LVFA and rhythmic sinusoidal ictal

patterns are associated with better outcomes after

surgery.


Ogren JA, et al. Three-dimensional hippocampal atrophy maps distinguish two common temporal lobe seizure-onset patterns. Epilepsia 2009;50:1361-70. King D, Spencer S. Invasive electroencephalography in mesial temporal lobe epilepsy J Clin Neurophysiol 1995;12:32-45. Velasco AL, et al. Functional and anatomic correlates of two frequently observed temporal lobe seizure-onset patterns. Neural Plast 2000;7:49-63. Bragin A, et al. Analysis of seizure onset on the basis of wideband EEG recordings. Epilepsia 2005;46:59-63. Lee SA, et al. Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia2000;41:297-307. Gloor P, et al. The human dorsal hippocampal commissure: an anatomically identifiable and functional pathway. Brain 1993;116:1249-73. Spanedda F, et al. Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in bitemporal epilepsy. Epilepsia 1997;38:1300-14. Spencer SS, et al. Anatomic correlates of interhippocampal seizure propagation time. Epilepsia 1992;33:862-73.

• Following seizure onset and initial recruitment of the

surrounding area, the ictal rhythm propagates variably.

• The spread can be to the ipsilateral temporal lobe,

contralateral mesial temporal or temporal neocortex.

• Long interhemispheric propagation times are

associated with good surgical outcomes in MTS.

• Time to propagation of the seizure to the contralateral

hippocampus is lengthened in direct proportion to

Cornu Ammonis (CA) subfield 4 (CA4, a.k.a. the hilar

region of the dentate gyrus) cell loss, suggesting a role

for CA4 in this process.


“Wasted Hippocampal Syndrome” • Relatively rare

• Patients with severe unilateral hippocampal

atrophy with contralateral ictal onset of seizures.

• In the majority of these patients, invasive

recordings show seizures arising from the atrophic

side and have very good seizure outcomes with

surgery.

• Interictal epileptiform discharges are more likely to

correlate with the lateralization of the seizures in

this situation.

• It is debatable if these subset of patients need

invasive study. In selected patients, noninvasive

tests such as SPECT or PET may aid resective

surgery without invasive monitoring.

Case 1 • A 30 YO man with medically refractory CPSs and R MTS

• Interictal EEG: R T interictal slowing and spikes localized

to the R T regions.

• Six CPSs were captured during video-EEG recordings

with rhythmic (Type 1) EEG changes that evolved but

remained localized to the R T regions.

• Postictal: slowing and spikes in the R T region.

• Neuropsychology: mild R T dysfunction.

• Rx: R TLY

• Outcome: Seizure free.

• Histopathology: severe R HS in addition to incidentally

detected cortical dysplasia in the R T neocortex.

MRI in a patient with R mTLE: Hippocampal volume loss & signal changes (short arrows)

Poor gray white differentiation in R M T gyrus (long arrow)

Interictal EEG shows right temporal slowing

and anterior and mid temporal spikes.

Ictal R T rhythm in one of the CPSs recorded

during video-EEG.

Histopathology of the R ATL: marked neuronal loss in CA1,

CA3 and CA4 (NeuN stain) with relative preservation of CA2

neurons and subiculum(S).

Temporal neocortex (corresponding to long arrow on MRI) shows

focal widening of cortex with blurring of gray white junction (arrows)

on NeuN stain. Higher magnification view shows dyslamination and

disorientation with accumulation of phosphorylated neurofilament

with the dysplastic neurons.

Case 2 • An otherwise healthy and high functioning 60 YO man

developed stereotyped CPSs that began at the age of 41 yrs.

• Neurological and neuropsychological examinations: normal.

MRI: Cavernous hemangioma in the R T neocortex.

• EEG: Infrequent broad IEDs in the R anterior-mid temporal

regions in sleep and normal background activity.

• Ictal EEG: High amplitude IEDS in the R anterior-mid T region

with ipsilateral hemispheric generalization in 4 seconds. It

only minimally spread to the contralateral FP region and lasted

65 seconds without postictal changes.

• Rx: Limited right temporal lobe corticectomy.

• Pathology: Cavernous angioma.

• Outcome: Seizure free for over 10 years on no meds.

Cranial MRI: A. Coronal gradient echo shows susceptibility

change (arrow) in R middle T gyrus, abutting on grey matter.

B. Axial FLAIR shows the lesion in the R T neocortex.

A typical R T IED involving F8, A2 and T4 during sleep.

R hemispheric seizure onset in the R T region (F8, A2,

T4) with minimal involvement of the R FP2 region.

Documents

Scalp EEG Findings in Temporal Lobe Epilepsy · Temporal lobe epilepsy (TLE) • The most common form of focal epilepsy worldwide. • Anterior Temporal Lobectomy (ATL) for medically