Scalp EEG Findings in Temporal Lobe Epilepsy

Scalp EEG Findings in
Temporal Lobe Epilepsy
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]
EEG Course, CNSF, Ottawa, ON
Thursday, June 07, 2012
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.)
International 10-20 system of
electrode placements
Jasper HH. The ten-twenty electrode system of the International Federation.
Electroenceph Clin Neurophysiol 1958;10:371- 5.
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.
Additional electrodes to 10-20 system
of electrode placement
• May be placed between any of the principal standard
positions
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.
Interictal EEG Abnormalities in
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.
Interictal EEG Abnormalities in
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.
Prognostic Value of the Spike
Dipoles in TLE
• 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.
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
Ebersole Type 2 Ictal Rhythms in TLE
• Lower frequency (2-5 Hz) irregular ictal
rhythm with widespread temporal distribution.
• Is often associated with neocortical seizures.
Ebersole JS, Pacia SV.Localization of temporal lobe foci by ictal EEG patterns.
Epilepsia 1996;37:386-99.
An example of Ebersole “Type II”
Ictal Rhythm in TLE
Ebersole Type 3 Ictal Rhythms in TLE
• Diffuse ictal EEG changes or attenuation
without clear lateralization.
• Is seen both in hippocampal and temporal
neocortical seizures.
Ebersole JS, Pacia SV.Localization of temporal lobe foci by ictal EEG patterns.
Epilepsia 1996;37:386-99.
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.
Simultaneous Scalp Ictal
Rhythms with Subdural and
Depth Recordings
• Type I ictal rhythm is observed when
the seizures spread from mesial
temporal to the infero-lateral temporal
structures.
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.
Simultaneous Scalp Ictal
Rhythms with Subdural and
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.
Simultaneous Scalp Ictal
Rhythms with Subdural and
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.
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.
Simultaneous Scalp Ictal Rhythms with
Subdural and 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.
Jung KY, et al. Spatiotemporospectral characteristics of scalp ictal EEG in mesial
temporal lobe epilepsy with hippocampal sclerosis. Brain Res 2009;1287:206-19.
Invasive EEG Recordings
• 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.
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 EEG Recordings
• 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.
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.
Subdurally Recorded Seizures
•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.
Two Common Patterns of Temporal Lobe
Seizures with Invasive EEGs
• 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
Subdurally Recorded Seizures
• 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 seizureonset 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;33:86273.
Subdurally Recorded Seizures
• 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.