Presurgical Assessment of the Epilepsies with Clinical Neurophysiology and Functional Imaging

560 Pages·2003·14.235 MB·1-582\560

by  F. Rosenow and H.O. Luders (Eds.)

PresurgicalAssessmentoftheEpilepsieswithClinicalNeurophysiologyandFunctionalImaging
HandbookofClinicalNeurophysiology,Vol.3
FelixRosenowandHansO.Lüders(Eds.)
©2004ElsevierB.V.Allrightsreserved 3
CHAPTER1.1
Overview
Felix Rosenowa,∗ and Hans O. Lu¨dersb
aInterdisciplinaryEpilepsyCenter,DepartmentofNeurology,Philips-UniversityMarburg,D-35033Marburg,Germany
bDepartmentofNeurology,S90,ClevelandClinicFoundation,Cleveland,OH44195,USA
1. Aimsandconceptsinsurgeryforepilepsy clinical neurophysiological assessment of surgically
treatableepilepsies.
The objective of resective epilepsy surgery is the
complete resection or complete disconnection of the
2. Theconceptofcorticalzones
epileptogeniczone,whichisdefinedastheareaofcor-
texindispensableforthegenerationofclinicalseizures
2.1. Symptomatogeniczone
(CarrenoandLu¨ders,2000).Ideally,thisaimshouldbe
accomplishedwithoutdamagingthe“eloquent”cortex. The symptomatogenic zone is the area of cortex
Currently,theepileptogeniczonecannotbemeasured which, when activated by an epileptiform discharge,
directly. Therefore, a variety of diagnostic tools such produces the ictal symptomatology. It is defined by
as analysis of seizure semiology, neurophysiological carefulanalysisoftheictalsymptomatologyeitherwith
techniques, functional testing as well as structural a thorough seizure history or analysis of ictal video
and functional neuroimaging, are used to indirectly recordings.Theprecisionwithwhichwecandefinethe
definethelocationandboundariesoftheepileptogenic locationofthesymptomatogeniczonedependsonthe
zone. These diagnostic methods define different specific ictal symptomatology. For example, a highly
corticalzones(symptomatogeniczone,irritativezone, localized somatosensory aura such as paresthesias of
ictal-onset zone, stimulation-induced seizure zone, oneortwofingersatthebeginningofaseizureclearly
functional-deficit zone, and the epileptogenic lesion) localizesthesymptomatogeniczonetothecorrespond-
whichareallamoreorlesspreciseindexoftheloca- ing primary sensory area. However, a poorly defined
tionandextentoftheepileptogeniczone(Lu¨dersand bodysensationhaslittlelocalizingorlateralizingvalue.
Awad,1992;RosenowandLu¨ders,2001).Ourability There are many other ictal signs or symptoms whose
to precisely define these zones is essential to best localizing/lateralizingvaluefallsinbetweenthesetwo
appreciatethetopographyoftheepileptogeniczone. extremes(seealsoChapter2.14).
This volume is divided into four sections. The It is important to stress here that there is often no
first section describes conceptually the different overlap between the symptomatogenic zone and the
corticalzoneswhichbuildthestructureofthevolume. epileptogenic zone. The presence of ictal symptoma-
Section2dealsindetailwiththedifferentneurophys- tologymaybecausedbygenerationoftheseizurefrom
iological, functional imaging and other techniques a zone of eloquent cortex. However, in many cases,
used to define these zones in candidates for epilepsy theictalsymptomatologyisproducedbyspreadofan
surgery. In Section 3, the relative value and order epileptiformdischargefromanepileptogeniczonelo-
of application of these techniques in the presurgical cated in “silent” cortex to a distant area of eloquent
evaluation of epilepsy syndromes of different etiolo- cortex.
giesarediscussed.Finally,Section4reportsindetail Electrical stimulation studies have demonstrated
on ongoing clinical and basic research studies in the thatonly“strong”enoughstimulusparametersapplied
toeloquentcortexwillelicitsymptoms.Inotherwords,
only trains of stimuli that are long enough, have ap-
∗Correspondenceto:FelixRosenow,MD. propriatefrequency,andareofsufficientdurationand
E-mailaddress:[email protected] intensitywillelicitsymptomsorsigns.Itisreasonable
Tel.:[phone];fax:[phone]. to expect also that only epileptiform discharges that
4 F.ROSENOWANDH.O.LU¨DERS
Table1
Descriptionsofzonesandlesionsofthecortex(adaptedfromLu¨dersandAwad,1992)
1.Epileptogeniczone Regionofcortexthatcangenerateepilepticseizures;bydefinition,totalremovalor
disconnectionoftheepileptogeniczoneisnecessaryandsufficientforseizurefreedom
2.Irritativezone RegionofcortexthatgeneratesinterictalepileptiformdischargesintheEEGorMEG
3.Seizure-onsetzone Regionfromwhichtheclinicalseizuresoriginate
3.1.Stimulation-inducedseizurezone Regionofcortexwhoseelectricalstimulationevokesseizures
4.Epileptogeniclesion Structurallesionthatiscausallyrelatedtotheepilepsy
5.Ictalsymptomatogeniczone Regionofcortexthatgeneratestheinitialseizuresymptomatology
6.Functional-deficitzone Regionofcortexthatintheinterictalperiodisfunctionallyabnormalasindicatedby
neurologicalexamination,neuropsychologicaltesting,functionalimaging,or
nonepileptiformEEGorMEGabnormalities
7.Eloquentcortex Regionofcortexthatisindispensableforcertaincorticalfunctions
fulfillthesecriteriawillelicitsymptomsorsigns.This 2.3. Seizure-onsetzone
explainsthefrequentobservationthatanepileptiform
The seizure-onset zone is the area of cortex from
discharge is recorded from a symptomatogenic zone
which clinical seizures are currently generated. Like
without producing the corresponding symptoms. All
the irritative zone, it is most commonly localized by
the limitations outlined above have to be considered
eitherscalporinvasiveEEGtechniques(seeChapters
whentryingtodefinetheepileptogeniczonebycareful
2.6–2.9).Unliketheirritativezone,however,theloca-
analysisofictalsymptomatology(Table1).
tionoftheseizure-onsetzonecanalsobedetermined
byictalsinglephotonemissioncomputedtomography
2.2. Irritativezone
(SPECT;seeChapter2.10).Theseizure-onsetzoneis
Theirritativezoneisdefinedastheareaofcortical usuallythatportionoftheirritativezonethatgenerates
tissue that generates interictal electrographic spikes. spikes capable of producing afterdischarges. These
Interictalspikescanbeconsideredas“mini-seizures”. consistofrepetitivespikesthathaveenough“strength”
Isolatedspikesthatareofsufficient“strength”andare to produce clinical ictal symptoms when generated
generatedwithinaneloquentcorticalareaactuallycan in eloquent cortex or when spreading into eloquent
give rise to clinical symptoms. Typical examples are cortex. For many years, it was thought that precise
myoclonicjerksthatcanbeseeninpatientswithspikes definition of the seizure-onset zone should provide
intheprimarymotorcortex.Ingeneral,however,iso- an accurate definition of the epileptogenic zone, but
lated,independentspikeswillnotgenerateanyclinical thisisnottrue.Actually,thereisnomethodologythat
symptoms regardless of whether they are located in permits precise definition of the location or extent
silent or eloquent cortex. In general, only runs of of the seizure-onset zone. Scalp electrodes give us
epileptiform discharges (afterdischarges) of sufficient an excellent overview of the electrical activity of the
“strength”inducesymptomswhentheyinvadeasymp- brainandfrequentlysuggestthesideandapproximate
tomatogeniczone.Theirritativezoneusuallyoverlaps locationoftheseizureonset.However,scalpEEGhasa
with the epileptogenic zone but is more extended. relativelylowsensitivityfortheprecisedetectionofthe
However,inmanycases,spikescanbegeneratedfrom seizureonsetbecausesurfaceelectrodesarelocatedat
areasdistantandevencontralateraltotheepileptogenic arelativelylargedistancefromthecortexandaresepa-
zone (for examples, see Chapters 3.1 and 3.2). The ratedfromthebrainbyaseriesofbarriersthatinterfere
irritativezoneisdefinedbyscalporinvasiveelectroen- significantlywiththetransmissionoftheelectricalsig-
cephalography (EEG) or magnetoencephalography nals. Usually, afterdischarges generated locally at the
(MEG;Chapters2.1–2.4).Automaticspikedetection, actualseizure-onsetzonearetoosmalltobedetected
discussed in Chapter 2.5, can help to reduce the by scalp electrodes, and therefore, scalp electrodes
review time needed to define the complete irritative areonlycapableofdetectingaseizuredischargeafter
zone but carries the potential risk of introducing it has spread considerably (see also Chapter 2.6).
aselectionbias. Invasive cortical surface electrodes, however, also
OVERVIEW 5
havesignificantlimitations.TheyrecordEEGactivity of the SISZ does not allow prediction of seizure out-
from only an extremely limited region of the brain. come(Schulzetal.,1997).Therefore,thedelineation
By eliminating distance and insulating barriers, each oftheSISZplaysarelevantroleinthedefinitionofthe
invasiveelectroderecordstheEEGactivitygenerated epileptogeniczoneonlyinaminorityofcandidatesfor
in the limited cortical area covered by that electrode. epilepsysurgery.
Invasiveelectrodesare,therefore,extremelysensitive
for the detection of afterdischarges but will only be
2.4. Epileptogeniclesion
abletoaccuratelydefinetheseizureoriginiftheyare
implanteddirectlyintheseizure-onsetzone.Unfortu- This is a lesion visible by neuroimaging that is the
nately, since only a limited number of electrodes can causeoftheepilepticseizures.Thebestwaytoidentify
be implanted, invasive electrodes are usually located theepileptogeniclesionisbyhigh-resolutionmagnetic
intheperipheryoftheseizure-onsetzoneoronlycover resonanceimaging(MRI;seeChapter2.15).However,
aportionofthiszone(seealsoChapters2.7–2.9). some lesions identified by neuroimaging may not be
The second problem to consider is that the extent epileptogenicandbeunrelatedtotheclinicalseizures.
of the seizure-onset zone may not correspond with Forthisreason,evenwhenweseealesionintheMRI,
theextentoftheepileptogeniczone(thecorticalarea we still have to use other methods to verify (usually
from which clinical seizures may arise). In other by video/EEG monitoring and/or seizure semiology)
words, the epileptogenic zone may be either more or thatthelesionvisualizedbyneuroimagingisindeedre-
less extensive than the seizure-onset zone. When the sponsibleforthepatient’sseizures.Arelatedproblem
epileptogenic zone is smaller than the seizure-onset isthedefinitionofepileptogenicityincaseswithdual
zone, partial resection of the seizure-onset zone ormultiplepathology.Hereagain,additionaltestingis
may lead to seizure freedom because the remaining necessary to define which of the lesions are epilepto-
seizure-onsetzoneisnolongercapableofgenerating genic.Inthosecasesinwhichtwoormorelesionsare
seizures. Conversely, when the epileptogenic zone is placed in close spatial proximity, the problem of at-
greaterthantheseizure-onsetzone,wehaveasituation tributingepileptogenicitytoonelesionoranothercan
inwhicheventotalresectionoftheseizure-onsetzone frequently only be resolved with the use of invasive
will not result in seizure freedom. This phenomenon EEGtechnology(seeChapters2.7and2.8).
occurs when a patient has seizure-onset zones of The spatial relationship of the epileptogenic zone
different thresholds within a single epileptogenic withtheepileptogeniclesionissimilartoitsrelation-
zone.Theseizure-onsetzoneoflowestthresholdwill ship with the seizure-onset zone that was discussed
generate all the usual seizures and is, therefore, the above. It has been thought that complete resection of
only one we can directly measure before surgery. theepileptogeniclesionvisualizedbyneuroimagingis
Once this zone has been resected, however, another necessarytoobtainseizurefreedom.Thisisnotalways
seizure-onset zone of higher threshold may become true, however, as evidenced by cases in which only
clinically evident. The cortical area of interest now partial lesion resection (often unavoidable because of
becomes a “potential epileptogenic zone” containing partial overlap between the epileptogenic lesion and
one or more seizure-onset zones. There is no way to eloquent cortex) results in complete seizure freedom.
predictwithcurrenttechnologywhetheranyadditional However, often seizures persist in spite of complete
higherthresholdseizure-onsetzonesexist. resectionofthelesionvisibleonMRI.Thisisoftenthe
caseinpatientswithcorticaldysplasiaorposttraumatic
2.3.1. Stimulation-inducedseizurezone epilepsy (see also Chapters 3.4 and 3.5). There are
Duringelectricalstimulationofthecortex,afterdis- twopossibleexplanationsforthisphenomenon.Many
charges and seizures, including the habitual seizures lesions are not intrinsically epileptogenic but induce
of the patient, can be elicited. The area from which seizures by generating reactions in the surrounding
seizures(includingauras)areevokedisthestimulation- braintissuewithwhichtheyareincontact.Anotherex-
inducedseizurezone(SISZ).Ithasbeensuggestedthat planationaddressesthesensitivityofMRIindetecting
cortex from which seizures can be elicited has facil- the complete lesion. Brain tissue adjacent to lesions
itated pathways to a specific symptomatogenic zone visiblebyneuroimagingmayconsistoflesionaltissue
andis,therefore,likelytobepartoftheepileptogenic of a lesser pathologic severity. This tissue, while fre-
zone(seeChapter2.13).However,completeresection quently of high epileptogenicity, may be invisible on
6 F.ROSENOWANDH.O.LU¨DERS
MRI.Thisoccurrsfrequentlyinpatientswithcortical pocampalsclerosis.PETstudiesoftenrevealextensive
dysplasia in which only the “tip of the iceberg” is hypometabolic regions outside the mesial temporal
visible in MRI. Failure to resect these MRI-invisible structures (see Chapter 2.16) even when we know
lesionscanleadtopersistenceofseizuresafterepilepsy that the epileptogenic zone is usually limited to the
surgery. This is the most likely explanation for the mesialtemporalregion,andseizurefreedomisusually
relativelyhighfrequencyofsurgicalfailureinpatients achievedbyaselectiveamygdalo-hippocampectomy.
withneocorticaldysplasia(seealsoChapter3.4). In spite of all these limitations, a good correlation
Theonlywaywecantrytopredictthepresenceof ofthefunctional-deficitzonewiththeotherzonesde-
a perilesional epileptogenic rim is by understanding finedabovegivesusadditionalsupportiveinformation
better the pathological nature of the MRI-visible regardingthelateralizationorlocationoftheepilepto-
lesion. We know, for example, that well-delineated geniczone.However,cleardiscrepanciesbetweenthe
braintumorsandcavernousangiomastendtoproduce resultsobtainedinthetestsusedtodefinethedifferent
epileptogenicity only in the MRI-visible lesion and cortical zones make accurate definition of the epilep-
its immediate surrounding. Therefore, lesionectomy togeniczoneverydifficultandarefrequentlyareason
is usually successful in these cases. However, as to request more sensitive, specific tests like invasive
mentioned above, cases with cortical dysplasia monitoring.
or posttraumatic epilepsy typically require more
extensiveresectionsforasuccessfuloutcome.
2.6. Epileptogeniczone
2.5. Functional-deficitzone The epileptogenic zone is the area of cortex that is
indispensableforthegenerationofepilepticseizures.
Thisisdefinedastheareaofcortexthatisfunction- Itmayincludeanactualepileptogeniczonethatisthe
allyabnormalintheinterictalperiod.Thisdysfunction cortical area generating seizures before surgery (see
may be a direct result of the destructive effect of the above:equivalenttoorsmallerthantheactualseizure-
lesionormaybefunctionallymediated,i.e.abnormal onsetzone)anda“potentialepileptogeniczone”,which
neuronal transmission that may affect brain function is an area of cortex that may generate seizures after
either locally or at a considerable distance from the the presurgical seizure-onset zone has been resected.
epileptogenic tissue. There are a variety of methods Thereisnodiagnosticmodalitythatcanbeusedtodi-
that can be used to measure the functional-deficit rectly measure the entire epileptogenic zone. This is
zone. Examples include neurological examination, becausewecannotexcludethepossibleexistenceofa
neuropsychological testing, EEG, positron emission “potentialepileptogeniczone”thatwouldonlybecome
tomography (PET) scan, and interictal SPECT (see clinicallyapparentpostoperatively.Theepileptogenic
Chapters2.16and2.17). zone,therefore,isatheoreticalconcept.Ifthepatientis
What is the relationship between the functional- seizure-freeaftersurgery,weconcludethattheepilep-
deficit zone defined by these different tests and the togenic zone must have been included in the surgical
location of the epileptogenic zone? Unfortunately, resection.
this relationship is very complex and difficult to Since we cannot measure the epileptogenic zone
establish even in individual cases. This is related to directly, we must infer its location indirectly by
the fact that these tests measure parameters such as definingtheotherzonesdiscussedabove.Whenallof
global brain function (general neurological exam) these data are concordant, the determination is easy.
or brain physiology (local glucose metabolism or Unfortunately, these cases are rare. In most cases,
blood perfusion), which are not directly related to there is some degree of discrepancy between the
epileptogenesis. Some of these changes may be the differentzones.Attemptsshouldthenbemadetofind
resultofanonepileptogeniclesionandmayoccurata aplausibleexplanationforthesediscrepancies,taking
considerabledistancefromtheprimaryseizurefocus. intoconsiderationthebasicprinciplesoutlinedabove.
Forthisreason,thevalueofdefiningpresurgicallythe It is difficult to accurately define the epileptogenic
functional-deficit zone is relatively limited compared zonewhennoadequateexplanationforthediscrepant
to measurement of the other zones discussed above locationand/orextentofthedifferentzonesisfound.
which are more directly related to the seizures. A Inthesecases,surgeryshouldbedeferredwhilemore
typicalexampleofthisisseeninpatientswithpurehip- precise testing like invasive video/EEG is performed.
OVERVIEW 7
As discussed earlier, however, invasive recordings thathopefullywillpermitmoredirectdefinitionofthe
are limited by their extent of cortical coverage. They epileptogeniczone.Itisverylikelythatthesedevelop-
shouldonlybeusedinthosecasesinwhichthereisa mentswillbeinfunctionalneuroimaging.Allcurrently
clearhypothesisregardingthelocationofseizureonset widely available functional neuroimaging techniques
and in which a specific question must be answered (mainlyFDG-PETandinterictalSPECT)measureonly
(seealsoChapters2.7–2.9). nonspecificbrainphysiology,likeregionalmetabolism
or blood flow. However, further developments may
2.7. “Eloquent”cortex make it possible to directly image the distribution
of neurotransmitters and receptors involved in the
Epilepsy surgery is usually an elective procedure. pathogenesisofepilepsy.Thismaynotonlyallowusto
While the complete resection of the epileptogenic definedifferenttypesofepileptogeniclesionsbasedon
zone is of paramount importance, this aim is limited neurotransmitterandreceptorphysiology,butalsogive
by one major restriction: the sparing of eloquent us a measurement of “potential epileptogenic zones”
cortex to avoid new, unacceptable deficits for the thatarecurrentlyundetectablepreoperatively.Inaddi-
patient. Eloquent cortex is cortex necessary for a tion,refinementsofthecurrentlyavailablediagnostic
given function. Methods commonly used to detect techniques may increase the accuracy with which we
such functions include electrical stimulation of the define the different zones giving us some additional
cortex, evoked potentials, MEG, functional magnetic power,eveniftheydonotsolvesomeoftheessential
resonanceimaging(fMRI),and,toalesserextent,PET theoretical limitations discussed before. In Section 4,
(see Chapters 2.17–2.24). A possible loss of function several of the newer diagnostic techniques are pre-
as a consequence of the epilepsy surgery should at sented,andtheircurrentandfuturevalueinthepresur-
least be predictable and discussed with the patient gical diagnosis of patients with epilepsy is discussed
prior to the procedure. Even today, invasive methods indetail.
such as subdural electrodes are still frequently used
whenthelocationandextentoftheseizure-onsetzone References
and of eloquent cortex are to be defined. Hopefully,
thesetechniqueswillhavetobeusedlessfrequentlyin Carreno, M and Lu¨ders, HO (2000) General principles of
the future when novel neurophysiology and imaging presurgical evaluation. In: HO Lu¨ders and YG Comair
techniquesdiscussedinSection4ofthisvolumewill (Eds.),EpilepsySurgery.LippincottWilliams&Wilkins,
have become more widely available as reliable tools Philadelphia,pp.185–199.
inthepresurgicaldiagnosisofepilepsy. Lu¨ders,HOandAwad,I(1992)Conceptualconsiderations.
In:HOLu¨ders(Ed.),EpilepsySurgery.RavenPress,New
York,pp.51–62.
3. Futureperspectivesinthedefinitionofthe
Rosenow,FandLu¨ders,H(2001)Presurgicalevaluationof
epileptogeniczone
epilepsy.Brain,124:1683–1700.
Schulz, R, Lu¨ders, HO, Tuxhorn, I, Ebner, A, Holthausen,
Aswementionedabove,theepileptogeniczoneisa H, Hoppe, M, Noachtar, S, Pannek, H, May, T and
theoreticalconcept.Noneoftheavailabletestspermits Wolf, P (1997) Localization of epileptic auras induced
directmeasurementoftheepileptogeniczone.Inthefu- on stimulation by subdural electrodes. Epilepsia, 38:
ture,wewillhavetolookfornewdiagnostictechniques 1321–1329.
PresurgicalAssessmentoftheEpilepsieswithClinicalNeurophysiologyandFunctionalImaging
HandbookofClinicalNeurophysiology,Vol.3
FelixRosenowandHansO.Lüders(Eds.)
©2004ElsevierB.V.Allrightsreserved 11
CHAPTER2.1
Noninvasive EEG in the definition of the irritative zone
∗
Hajo M. Hamer and Niki Katsarou
DepartmentofNeurology,UniversityofMarburg,Rudolf-Bultmann-Str.8,D-35033Marburg,Germany
1. Generalconcepts ing that a strong after-inhibition produced by IED
protects against the occurrence of ictal discharges by
The main goal of the presurgical evaluation in maintainingalowlevelofexcitationinageneralcon-
patients with medically intractable epilepsy is the dition of hyperexcitability (Binnie and Stefan, 1999;
identificationofthecorticalareacapableofgenerating DeCurtisandAvanzini,2001).Thisfinding,however,
seizures, and whose removal or disconnection will remainscontroversial(GotmanandKoffler,1989).
result in seizure freedom. This area is called the
“epileptogenic zone” (Carreno and Lu¨ders, 2001). 1.1. Limitsofscalpandsphenoidalelectrodes
The irritative zone is the area of cortex capable of comparedtointracranialelectrodes
generating interictal epileptiform discharges (IED)
Several square centimeters of synchronously
in the EEG. The irritative zone does not coincide
discharging cortex (around 6cm2) are necessary for
but frequently overlaps with the epileptogenic zone.
detectionbyoverlyingscalpelectrodes(Cooperetal.,
Extensive experience with routine extracranial EEG
1965;FernandezTorreetal.,1999b).Cerebralactivity
shows that in general, the location of IED is a good
is attenuated by the impedance of the cerebrospinal
indicator of the area of cortex from which seizures
fluid, meninges, skull, and scalp. Therefore, scalp
areoriginating(BinnieandStefan,1999;Carrenoand
EEGfailstorecordagreatnumberofIEDrecordedby
Lu¨ders, 2001). The methodology of many studies on
depthorsubduralelectrodes(Fig.1).Interictalactivity
this topic, however, is biased towards patients with
arising from deep or midline structures is usually not
medically refractory epilepsies (Foldvary, 2000; So,
reflected in scalp EEG (Carreno and Lu¨ders, 2001).
2001). The term “interictal epileptiform discharges”
The distribution of IED on the scalp depends on the
includesspikesandsharpwaves,whicharewaveforms
conductive properties of the surrounding tissue, the
distinguishablefrombackgroundactivity.Bothspikes
spatialcharacteristicsofthegenerator,andthespatial
with a duration of less than 80ms and sharp waves
resolution of the surface EEG. Consequently, the
with a duration of 80–200ms have a pointed peak
distributionofinterictalepilepticdischargescanfailto
and are usually of negative polarity because they are
localizeorevenmislocalizetheregionorhemisphere
generated by depolarization of vertically oriented
of seizure origin (Foldvary, 2000). Closely spaced
neurons (Celesia and Chen, 1976; Pedley and Traub,
scalp electrodes can improve the yield of spike
1997; Foldvary, 2000). Positive IED can be seen in
detection and localization over the standard 10–20
electrocorticographyandinfrequentlyinpatientswith
system(Morris,IIIetal.,1986;Hameretal.,1999).
a breach rhythm, head trauma, or cortical dysplasia
It remains controversial whether or not sphenoidal
(Daly and Pedley, 1990; Foldvary, 2000). Spikes and
electrodes increase the detection sensitivity of IEDs.
sharpwavesconveyanincreasedriskofepilepsyand
Whereasseveralstudiesfoundthatinaminorityofpa-
mustbedifferentiatedfrombenignvariantsresembling
tients, especially those with temporal lobe epilepsies,
IED(BinnieandStefan,1999;Foldvary,2000).Some
sphenoidalelectrodescanrecordepileptiformactivity
reports suggest that spike suppression, and not an in-
whichdoesnotappearinanteriortemporalelectrodes
creaseinIEDfrequency,heraldsseizures,thuspropos-
(Fig. 2; Marks et al., 1992; Tuunainen et al., 1994;
Kanner and Jones, 1997; Pacia et al., 1998; Provini
∗Correspondenceto:HajoM.Hamer. et al., 1999), others could not verify this observation
E-mailaddress:[email protected] (FernandezTorreetal.,1999a);seealsoChapter2.6.
Tel.:[phone];fax:[phone]. Spikes with maximal amplitude at the sphenoidal
12 H.M.HAMERANDN.KATSAROU
Fig.1. Invasivevideo-EEGmonitoringwithbilateralforamenovaleelectrodesofa38-year-oldpatientwithbitemporalepilepsy.
Inaddition,scalpelectrodeswereattachedaccordingtotheInternational10–20system,andsphenoidalelectrodeswerebilaterally
inserted.NotetheIEDrecordedbythefirsttwocontactsoftheleftforamenovaleelectrodewhilethescalpandsphenoidal
electrodesfailtodetecttheseIED.FOr1,FOr2,FOr3:threecontactsoftherightforamenovaleelectrode;FOl1,FOl2,FOl3:
threecontactsoftheleftforamenovaleelectrode;Sp1:leftsphenoidalelectrode;Sp2:rightsphenoidalelectrode.
electrodescanarisefromthemesialorlateraltemporal healthy young men (Gregory et al., 1993) to 12% in
lobe or from an orbitofrontal focus (Marks et al., a study including all age groups and patients with
1992). Sphenoidal electrodes placed close to the progressive cerebral disorders (Sam and So, 2001).
foramen ovale can register higher amplitudes of IED Specificityisprobablylowerandsensitivityhigherin
thanscalpelectrodes(Morris,IIIetal.,1989;Kanner children than in adults, but reliable estimates are not
et al., 1995; Foldvary, 2000). However, sphenoidal available(BinnieandStefan,1999).Thefrequencyof
electrodesstillfailtodetectalargeproportionofIED IED in elderly patients with epilepsy is substantially
recordedbyforamenovaleelectrodes(FernandezTorre lower than that reported in epileptic populations as a
etal.,1999a)(Fig.1). whole(MarsanandZivin,1970;DruryandBeydoun,
1998). The majority of reports could not establish
a correlation between the levels of anticonvulsants
1.2. YieldofscalpEEG
and the frequency of interictal spiking, although this
The first EEG will uncover IED in about 30–50% issueremainscontroversial(MarsanandZivin,1970;
of the patients with epilepsy, but the yield increases Gotman and Marciani, 1985; Duncan, 1987; Gotman
to 60–90% by the fourth EEG (Marsan and Zivin, and Koffler, 1989; Sundaram et al., 1990; Eriksson
1970; Salinsky et al., 1987; Binnie and Stefan, 1999; etal.,2001).Overall,around10%ofthepatientswith
Blume, 2001a). This contrasts with the frequency of epilepsy would be expected to show no IED in scalp
IED in nonepileptic patients ranging from 0.5% in EEGduringwakefulnessorsleepinspiteofprolonged
NONINVASIVEEEGINTHEDEFINITIONOFTHEIRRITATIVEZONE 13
Fig.2. TwoexamplesofIEDofa39-year-oldpatientwithrightmesialtemporalepilepsyduetohippocampalsclerosis.Scalp
electrodes were attached according to the International 10–20 system, and additional sphenoidal electrodes were bilaterally
inserted(Sp2:rightsphenoidalelectrode).Thefirstfourchannelsrepresentalongitudinalbipolarmontageofscalpelectrodes
overtherighttemporalarea.Inthefollowingfivechannels,therightsphenoidalelectrodeisincludedbetweenF8andT8ina
bipolarfashion.Notethesharpwavesrecordedbythesphenoidalelectrodeandmissedbythescalpelectrodes.
or repeated recordings (Chung et al., 1991; Adachi (Sammaritano et al., 1991; Malow et al., 1997, 1998;
etal.,1998;BinnieandStefan,1999).Theyieldfrom MendezandRadtke,2001;CarrenoandLu¨ders,2001).
a single EEG is substantially increased in patients Increased neuronal synchronization within thalam-
investigated within 1 or 2 days after a seizure, and is ocortical projection neurons during non-REM sleep
greaterinpatientswithmonthlyseizuresthaninthose may contribute to the activation process in epileptic
who had been seizure-free for a year (Marsan and cortex (Adachi et al., 1998). The predictive accuracy
Zivin,1970;Sundarametal.,1990;Kingetal.,1998). inlateralizationofepileptogenesisisimprovedduring
Thedurationofrecordingmayalsoaffectthedetection non-REM sleep in patients who showed bilateral
rateofinterictalspiking(GotmanandKoffler,1989). or no discharges in wakefulness because unilateral
Moreover, the yield can be significantly increased, discharges arising de novo in sleep were always
and new abnormalities found, if the EEG includes correctlylateralizing(Adachietal.,1998).Inpatients
sleeprecordings(Kingetal.,1998;BinnieandStefan, who had unilateral discharges in the awake state,
1999). IED are seen more commonly during sleep, whetheripsilateralorcontralateraltotheepileptogenic
with the greatest activation during non-REM sleep zone, the findings were generally unchanged during
14 H.M.HAMERANDN.KATSAROU
sleep. Sleep may also alter IED morphology and Chapter2.4).Severalstudiesfoundanassociationbe-
distribution (Mendez and Radtke, 2001). Spikes can tweenpostresectionIEDinthistestandalessfavorable
be more widespread during non-REM sleep than outcome (So et al., 1989; Fiol et al., 1991; McBride
duringwakefulnessorREMsleep,suggestingthatthe et al., 1991; Salanova et al., 1996; Wennberg et al.,
localizationofinterictaldischargesinREMsleepmay 1998),whileothersdidnot(Godoyetal.,1992;Shih
beabetterindicatoroftheepileptogeniczonethanin etal.,1994;Tuunainenetal.,1994;Tranetal.,1995;
non-REM sleep (Sammaritano et al., 1991). Hyper- Radhakrishnan et al., 1998; Ficker et al., 1999;
ventilation or photic stimulation rarely activates IED McIntosh et al., 2001). The lack of agreement of
in patients with focal epilepsies (Celesia et al., 1975; these studies may be due to differences in the patient
Miley and Forster, 1977; Kasteleijn-Nolst Trenite, populations (e.g. lesional versus nonlesional cases),
1989;Shiraishietal.,2001;Kleinetal.,2003). recording techniques, and anesthetic agents used
during surgery. Even in the studies confirming the
association of postresection IED and seizure contin-
1.3. SpecificityofinterictalscalpEEG
uation, the percentage of patients with postresection
In general, the frequency, repetition rate, morpho- persistenceofIEDbutstillafavorableoutcomevaried
logiccharacteristics,andstatedependenceofinterictal from 26 to 47% (So et al., 1989; Fiol et al., 1991;
epileptiform activity cannot be used to predict the Salanova et al., 1996), which can make it difficult to
etiology of the disorder (Foldvary, 2000). However, estimatetheprognosisinindividualcases.
rhythmic spiking on a slow background activity and
not associated with behavioral changes has been 2. Temporallobeepilepsy(TLE)
foundtobecharacteristicforfocalcorticaldysplastic
lesions(Palminietal.,1995;Gambardellaetal.,1996; Asmentionedabove,severalstudieshaveindicated
Rosenowetal.,1998).Tumorstendedtocausewider that the majority of mesial and neocortical temporal
distributedIEDascomparedtodevelopmentalabnor- IEDcannotberecordedbysurfaceelectrodes(Cooper
malitiesorhippocampalsclerosis(Aykut-Bingoletal., et al., 1965; Alarcon et al., 1994; So, 2001; see
1998; Hamer et al., 1999; Kameyama et al., 2001), also Chapter 3.1). The IED which are recorded in
which was also true for seizure patterns (Bo¨sebeck the extracranial EEG, however, may show a better
et al., 2002). This may be caused by local neuronal correlationwiththeseizureoriginascomparedtoIED
injury,edema,ischemiaorotherelectricaland/orbio- recorded by depth electrodes (Blume et al., 1993).
chemicaleffectsofthestructurallesiononsusceptible This suggests that widely synchronous interictal
neighboring brain tissue or homologous contralateral spikes more likely rise from the epileptogenic area
areas(Spenceretal.,1984;Awadetal.,1991). thanspikeswithsmallerfields.
In addition to IED, temporal intermittent rhythmic
1.4. PrognosticrelevanceofpostoperativeIED delta activity (TIRDA) was also strongly correlated
withaclinicaldiagnosisofTLEandcouldberecorded
In both temporal and extratemporal epilepsy, inalargenumberofpatientswithmedicallyrefractory
absenceofIEDinthe6-monthor1-yearpostoperative TLE (Fig. 3; Reiher et al., 1989; Blume et al., 1993;
scalp EEG was associated with good postoperative Normand et al., 1995; Gambardella et al., 1996).
outcome (Godoy et al., 1992; Patrick et al., 1995; However, temporal intermittent polymorphic delta
Morris et al., 1998; Aronica et al., 2001). The prog- activity was recorded in patients with temporal and
nosticvalueofa3-monthpostoperativeEEGremains extratemporalepilepsies(Geyeretal.,1999).
controversial(Cascinoetal.,1992;Kirkpatricketal.,
1993; Tuunainen et al., 1994; Radhakrishnan et al., 2.1. DistributionofIEDinTLE
1998). The presence of IED in the early extracranial
postoperative EEG (within 1 or 2 weeks) was not In TLE, IED tend to produce a stereotyped pattern
foundtobeofprognosticvalueinmostofthestudies onthescalpwiththehighestamplitudesattheanterior
(Soetal.,1989;Salanovaetal.,1992;Radhakrishnan temporal electrodes. This may be due to the location
et al., 1998; Ficker et al., 1999). There are conflict- of the neuronal generators within the temporal lobe
ing results on the prognostic value of IED in the and anatomical characteristics of the brain coverings,
postresection electrocorticography (ECoG; see also such as skull discontinuities (Fernandez Torre et al.,
NONINVASIVEEEGINTHEDEFINITIONOFTHEIRRITATIVEZONE 15
Fig.3. InterictalEEGofa21-year-oldpatientwithlefttemporallobeepilepsyduetohippocampalsclerosis.Scalpelectrodes
areattachedaccordingtotheInternational10–20system.NoteTIRDAinthelefttemporalregion.
1999b). Children may have a more widespread irrita- and can reflect bilateral damage, dysfunction at a
tive zone, which may be caused by a high frequency distance, or secondary epileptogenesis (Margerison
of dual pathology (Mohamed et al., 2001). Most and Corsellis, 1966; Morrell, 1985; Sammaritano
(Bengzon et al., 1968; Dodrill et al., 1986; Barry etal.,1987).
etal.,1992;Keoganetal.,1992;Salanovaetal.,1996; InextracranialEEGrecordings,interictaldischarges
McIntosh et al., 2001), but not all, studies (Chung can have a more reliable lateralizing value than ictal
etal.,1991;Cascinoetal.,1996)confirmedthefinding changesintemporallobeepilepsy(Sammaritanoetal.,
that IED confined to the anterior temporal region 1987), and they almost always predict seizure origin
are predictive of a good postoperative outcome in inTLEandgoodpostoperativeoutcomeiftheyareex-
TLEsurgery. clusiveorclearlypreponderantonthesideofsurgery
(Blume et al., 1993; Chee et al., 1993; Hufnagel
et al., 1994; Salanova et al., 1994, 1996; Steinhoff
2.2. LateralizingvalueofIED
etal.,1995;Holmesetal.,1996;Pataraiaetal.,1998;
TheincidenceofbilateralIEDinTLEisestimated Radhakrishnanetal.,1998;Serlesetal.,1998;Malow
to be between 20 and 44% and may be more when et al., 1999; Blume, 2001a; McIntosh et al., 2001;
investigated with invasive EEG (So, 2001). The So, 2001). In a study of 59 candidates for temporal
probability of bilateral IED was positively correlated lobectomy, 92% of patents with >90% lateralization
with the duration of the EEG monitoring (Cascino hadagoodsurgicaloutcome,whereasonly50%with
et al., 1996; Ergene et al., 2000). Bitemporal IED <90%hadafavorableoutcome(Chungetal.,1991).
increase the likelihood that seizures are arising In addition to IED, lateralization of delta activity
independendlyfrombothsides(Steinhoffetal.,1995) also indicates the side of temporal seizure origin in