Safety of video-EEG monitoring and surgical outcome in patients with mesial temporal sclerosis and psychosis of epilepsy

Safety

of

video-EEG

monitoring

and

surgical

outcome

in

patients

with

mesial

temporal

sclerosis

and

psychosis

of

epilepsy

Priscila

Oliveira

da

Conceic

¸

a˜o

,

Gerardo

Maria

de

Araujo

Filho

*

,

Lenon

Mazetto

,

Neide

Barreira

Alonso

,

Elza

Ma´rcia

Targas

Yacubian

a_{DepartmentofNeurologyandNeurosurgery,UniversidadeFederaldeSa˜oPaulo(UNIFESP),Sa˜oPaulo,Brazil}

b_{Laborato´rioInterdisciplinardeNeurocieˆnciasClı´nicas(LiNC),DepartmentofPsychiatry,UniversidadeFederaldeSa˜oPaulo(UNIFESP),Sa˜oPaulo,Brazil}

1. Introduction

Epilepsysurgeryhasbecomeanimportanttreatmentoptionfor patients with refractory temporal lobe epilepsy (TLE); current evidencesuggestsa60–70%remissionrateforlong-termepileptic symptomsandsignificantimprovementsinqualityoflife(QOL).1,2 Data from previous studies have demonstrated that cortico-amygdalohippocampectomy (CAH) is a safe, efficient surgical procedureforpatients withrefractoryTLEandmesialtemporal sclerosis(TLE-MTS);thelatterconditioncompromisestheprimary structuresofthelimbicsystem,particularlythehippocampusand amygdala. TLE-MTS is also one of the most common types of surgically remediable epileptic syndromes.3–5 _Prolonged video-electroencephalography(VEEG)monitoringhasbeenwidelyused inspecializedepilepsycentersforpre-surgicalevaluation.6

Oneofthemajordecisionsinepilepsysurgeryiswhetherto operate onsubjectswhohaveprevious historiesofpsychosisof epilepsy(POE).Manyepilepsycentersexcludepsychoticpatients fromtheirsurgicalprogramsduetothepossibilityofalternative psychosis, postoperative exacerbations of preexisting psychosis andtheoccurrenceofpostictaldisordersduringVEEG,which is facilitatedbythereductionofantiepilepticdrugs.Inaddition,few studieshaveaddressedthepsychiatricandseizurepost-surgical outcomes of patients withrefractory epilepsy and pre-surgical psychoses.7,8_{Thepurposeofthisstudywastoanalyzethesafety} andadverseevents(AEs)duringVEEGmonitoringandthesurgical, psychiatricandQOLoutcomesofpatientswithrefractoryTLE-MTS andaprevioushistoryofPOE.

2. Methods

2.1. Subjects

Onehundredforty-fiveTLE-MTSpatientswerefollowedinthe outpatient clinic of a tertiary center (Epilepsy Section of the UniversidadeFederaldeSa˜oPaulo,Sa˜oPaulo,Brazil)fromJanuary

ARTICLE INFO

Articlehistory:

Received29April2012

Receivedinrevisedform4June2012

Accepted5June2012

Keywords:

Mesialtemporalsclerosis

Psychosesofepilepsy

Video-EEGmonitoring

Surgicaloutcome

ABSTRACT

Purpose:Cortico-amygdalohippocampectomy (CAH)hasbecome animportanttreatmentoptionfor patientswithrefractorytemporallobeepilepsyandmesialtemporalsclerosis(TLE-MTS);ithasresulted in a 60–70% seizure remission rate and significant quality of life (QOL) improvements. Video-electroencephalography(VEEG)monitoringhasbeenwidelyusedinepilepsycentersforpre-surgical evaluation.AmajorconcerninepilepsysurgeryiswhethertoconsiderCAHtreatmentinpatientswith psychosisofepilepsy(POE).Thisstudyanalyzedthesafetyandadverseevents(AEs)ofVEEGmonitoring andthepost-surgicaloutcomesofpatientswithrefractoryTLE-MTSandPOEwhounderwentCAH. Method: Clinical,sociodemographic andVEEG datafrom 18patientswith TLE-MTSand POEwere analyzed.PsychiatricevaluationswereperformedusingDSM-IVandILAEcriteria.Theseizureoutcome wasevaluatedusingEngel’scriteria.

Results:Twopatients(11.2%)presentedAEsthatdidnotresultinincreasedlengthsofhospitalization.Of the10patients(55.5%)whounderwentCAH,6(60%)becamefreeofdisablingseizures(EngelI).The psychiatricand QOL evaluations revealed improvements of psychotic symptoms (p=0.01) and in PhysicalHealth(p=0.01)followingsurgery.

Conclusion:Thesedata reinforce thatVEEGmonitoring isasafe methodto evaluatepatientswith refractoryTLE-MTSandPOEinepilepsycenters.

ß2012BritishEpilepsyAssociation.PublishedbyElsevierLtd.Allrightsreserved.

*Correspondingauthorat:RuaBotucatu,740,VilaClementino,Sa˜oPaulo,SP,

CEP:04023-900,Brazil.Fax:+551155493819.

E-mailaddress:filho.gerardo@gmail.com(G.M.deAraujoFilho).

ContentslistsavailableatSciVerseScienceDirect

Seizure

j o urn a lhom e pa g e :ww w . e l se v i e r. c om / l oca t e / y se i z

1059-1311/$–seefrontmatterß2012BritishEpilepsyAssociation.PublishedbyElsevierLtd.Allrightsreserved.

2002toDecember2011.AllofthepatientshadsubmittedtoVEEG monitoringandapsychiatricevaluation.After writteninformed consentwasobtained,18TLE-MTSpatientswithaprevioushistory ofPOE(12.4%)wereincludedin thestudy.To beincluded,the patients requiredan electroclinical diagnosis ofrefractory TLE-MTSandPOE,whichwasbasedontheDiagnosticandStatistical Manualformentaldisorders,4th edition(DSM-IV)and Interna-tionalLeagueAgainstEpilepsy(ILAE)classifications9,10_andanage ofatleast16years.All18patientswerefollowedforatleasttwo years,andtheyhadclearMRIfindingsconsistentwithunilateralor bilateralMTSandconcordantinterictalandictalEEGdata.Patients wereexcludediftheysufferedfromotherneurologicaldiseasesin additiontoepilepsy,cognitiveimpairmentsprecludingpsychiatric andclinicalevaluations,orwereyoungerthan16yearsold.

2.2. Procedures

Thepatientsweresubjectedto2–6daysofcontinuous video-electroencephalographic(VEEG)monitoringwith32-channelEEG recording.Electrodeswereplacedonthetemporallobeaccording tothe10–10system,includingthesphenoidalposition.MTSwas definedifatrophy,increasedT2-weightedsignal,decreased T1-weightedsignal,and/oradisruptedinternalhippocampal struc-turewerepresentandaccompaniedbyatrophyoftheamygdala and/ortemporalpolesignalalterationuponvisualinspectionof the MRI pictures. The epileptogenic zone was determined by predominantlyipsilateralinterictalepileptiformdischarges(80% cutoff)andbyseizureonsetthatwasrecordedduringprolonged VEEG monitoring. Epilepsy was considered to be resistant to medicaltreatmentwhentheseizurespersistedaftertheutilization ofat leasttwo first-linemedications for partialseizuresat the highesttolerateddoses.Initialprecipitantinjury(IPI)wasdefined astheoccurrenceofseverecerebraleventsinthefirstyearoflife beforetheappearanceofepilepsythatrequiredmedical interven-tionand/orhospitalization;sucheventsincludedfebrileseizures, meningoencephalitis,head traumaor severe perinatal hypoxia. ThewithdrawalofAEDswasmadeduringthefirstthreedaysatthe hospital,and thepatients wereobserved for24heach dayvia monitoring screens that were located outside the monitoring room; the patients were monitored by two EEG-monitoring techniciansandaspecializedepileptologistwhowasoncallfor 24h.Adverseevents(AEs)weredefinedasfalls,fractures,status epilepticus(SE),PIP,suicideattempts,anddeepvenousthrombosis duringVEEGmonitoring.PIPwasconsideredanadverseeventifit occurredwithin7daysoftheadmissiondate.TheEpilepsySurgery Inventory(ESI-55)11_{wasusedtoevaluatethepatients’QOLbefore} andaftersurgery.

2.3. Psychiatricevaluation

Asinglepsychiatrist(GMAF)conductedtheclinicalinterviews usingtheDSM-IVaxisIandILAEcriteria.10,12–14_{IIPwasdefinedas} achronicpsychoticstatethatoftenincludedaninsidiousonsetof paranoiddelusions andhallucinations thatmay be present in clearconsciousnessandnottemporallyrelatedtoseizures.PIP was defined as episodes of psychosis within 1 week after a seizure(s), psychosis lasting >15h and<3 months, delusions,

hallucinations in clear consciousness, bizarre or disorganized behavior,formalthoughtdisorder,oraffectivechanges,withno evidence of antiepileptic drug (AED) toxicity, non-convulsive

status epilepticus, recent head trauma, alcohol and/or drug intoxication/withdrawal,orpriorchronicpsychoticdisorder.13,14 InformationregardingthefamilyhistoryofepilepsyandPDwas obtainedfromthepatientsthroughbroadquestionsthatasked whetheranyfirst-degreerelativewasreceivingtreatmenteither forepilepsyorforanyPDatthemomentoftheclinicalinterview.

The psychiatric evaluations occurred pre-surgically and were thenheldeverythreemonthsbythesamepsychiatrist(GMAF). The Brazilian version of the Brief Psychiatric Rating Scale anchored (BPRS-A)15_{wasalso usedtomeasurethe severityof} psychoticsymptomsbeforeandaftersurgery,andthescoresthat wereusedforthestatisticalanalysiswereobtainedatoneandtwo yearsaftersurgery.

2.4. Surgeryandpost-surgicalevaluation

After the VEEG evaluation, the patients without a surgical indicationwerefollowed atthree-month intervalsby thesame neurologist,andthepatientswithasurgicalindicationunderwent CAH within 2 months of the initial evaluation. The surgical procedure consisted of en block resectioning of the superior, middle,inferiortemporalandfusiformgyri,withaposteriorlimit of 4.5cm from thetip ofthe temporal lobe. After opening the temporal horn, the mesial temporal structures (hippocampus, amygdalaandparahippocampalgyrus)werealsoresected.3 _The patientswereevaluatedone,three,sixand12monthsaftersurgery and then every six months by two neurosurgeons. Engel’s classificationsystemwasutilizedtomeasurethepatients’seizure outcomesoneandtwoyearsafterthesurgery.16_{TheQOLofallof} thepatientssubmittedtoCAHwasalsoevaluatedafterthefirstand secondyearsaftersurgery.

2.5. Statisticalanalysis

Thestatisticalanalyseswereperformedusingtheversion10.0 of Statistical Package for Social Sciences (SPSS 10.0, Chicago, Illinois).Somesocio-demographiccharacteristicswerepresented asone-sampleproportionsthatincludedconfidenceintervals.The McNemarandWilcoxontestswereusedtoanalyzetheclinicaland socio-demographic data, and corrections were used for the multiplestatisticalcomparisons.pvalues of<0.05were

consid-eredtobestatisticallysignificant.

3. Results

Thedatafrom18patients(12women,6men,meanageof40.4 years,standarddeviation[SD]=8.97,rangeof26–65years,mean ofdurationofepilepsyof29.7years,SD=11.13)wereanalyzed. ThemeanlengthoftheVEEGmonitoringwas94h.Ninepatients (50%) presented with left-sidedMTS, eight (44.4%)were right-sidedandone(5.6%)hadbilateralMTS.Threepatients(16.8%)had a positive psychiatric familyhistory, while four (22.2%)had a positivepsychicaurahistory,andeight(44.4%)hadanIPIintheir epilepsy history. The patients’ clinical and sociodemographic characteristicsaresummarizedinTable1.

Regardingthe psychiatricevaluations,according totheILAE criteria,10_{tenpatients (55.5%)had a diagnosisof IIP,andeight} patients(45.5%)hadadiagnosisofPIP.AllofthepatientswithIIP also presented with the diagnosis of paranoid schizophrenia accordingtotheDSM-IVcriteria.12_{Allofthepatientsweretaking} oneantipsychoticdrug;Risperidone(RIS)wasthemostcommon drug(tenpatients),whichwasfollowedbyHaloperidol(HAL)(five patients)and Olanzapine (OLZ) (threepatients).Themean pre-surgicaldosesofRIS,HALandOLZwere3mg/day,7.5mg/dayand 10mg/day,respectively,andthedosesdidnotdiffersignificantly betweenthePIPandIIPpatients(p=0.89).

VEEGmonitoring,andlateralizedEEGorMRIasymmetrieswere notassociatedwiththeAEs.

Tenpatients(55.5%)underwentCAH;fivepatientshadPIPand fivehadIIP.Aftertwoyearsofpost-surgicalfollow-up,sixofthe patients(60%)werefreeofdisablingseizures(EngelClassI),three (30%)hadraredisablingseizures(EngelClassII),andonepresented withaworthwhileseizureimprovement(EngelClassIII)(Fig.1). Thedifferencesinthepost-surgicaloutcomesbetweenthefirstand secondyear werenotsignificant(p=1.00). Antipsychoticdrugs werediscontinuedinallfiveCAHpatientswithPIPbecausethey presentedwithacompleteremissionofpsychoticsymptomsafter surgeryandlackedanyrecurrencewithintwoyearsoffollow-up.A reductionofthemeanantipsychoticdoseswasobservedintheIIP patientsaftersurgery(2mg/dayforRISand5mg/dayforHAL),but performingstatistical comparisons ofthe patients who didnot undergosurgery wasunfeasible due tothereduced number of subjects involved. Among thepatients who underwent CAH, a meanBPRS-Ascoreof39.95.36(range26–44)wasobserved pre-surgically;thisscorewasreducedto26.76.21(range18–36)inthe firstyearandto22.34.47(range18–32)inthesecondyearafter surgery. A significant difference was observed between the pre-surgical andfirst-year scores (p=0.012),butno differences were observedbetweenthePIPandIIPpatients(p=0.87).

TheESI-55wasusedtomeasurethepatients’QOLbeforeand aftersurgery.AlthoughQOLimprovementswereobservedinallof thepatients’domainsaftersurgery(Fig.2),significantdifferences wereobservedonlyinthephysicalhealthsphere(p=0.01).Thep -valuewasapproximately0.05intheoverallqualityoflife(p=0.07) and psychosocial health (p=0.12) spheres, and it was not significantinthecognitiveandfunctionalsphere(p=0.23).

4. Discussion

Thedatafrompreviousstudieshavedemonstratedthat30–40% of patients withepilepsy present with a medically intractable disease with available AEDs. CAH is a safe, efficient surgical procedureforpatientswithrefractoryTLE-MTS,whichisoneofthe mostcommontypesofsurgicallyremediableepilepticsyndromes; it confers an approximately 70% chance of long-term seizure freedom.3–5 However, one of the most important decisions in epilepsysurgeryiswhethertooperateonpatientswithaprevious history of POE. The prevalence of psychoses in hospital-based

Fig.1.EngelandILAEclassificationsoneandtwoyearsafterepilepsysurgeryof

patientswithmesialtemporalsclerosisandpsychosesofepilepsy.

T able 1 Clinical and sociodemographic characteristics of in psychotic patients with refractory temporal lobe epilepsy and mesial temporal sclerosis. Patient no./ gender POE Age of epilepsy onset (y) Age at VEEG (y) IPI

Psychiatric family history Psychic aura TCS during life Dominant side MTS side Interictal foci % of laterality at VEEG

Secondary generalization at

epilepsyservicesisestimatedtobeapproximately9%,17_andthe prevalenceratesareevenhigher(19–27%)inspecializedcenters.18 Despitethis highprevalence,patients withthis condition have frequentlybeenexcluded(forpsychiatricreasons)fromacomplete evaluationoftheir epilepsysyndromes.Somereasonstojustify thisattitudearetheoccurrenceofpostictaldisordersduringVEEG, thepossibilityofalternativepsychosisandpostoperative exacer-bationsofpreexistingpsychosis.6,19,20

PreviousstudieshavesuggestedthatPOErecurrencemaybe closelylinkedtoseizureexacerbationduringVEEG.6,19_Theyearly incidenceofpostictalpsychiatricdisordershasbeenreportedas 7.9% among patients with partial epilepsy who undergo VEEG monitoring,andepisodesofPIPrepresentthemajorityofthese disorders(6.4%).20_{PIPwastheonlyAEobservedinthepresent} study,anditoccurredinaslightlyhigherproportionthanhadbeen reportedinpreviousstudies.6,19,20_{However,theseeventsdidnot} alter the length of hospitalization for the two patients who presentedthisAE,andneitherAEnegativelyinfluencedthe post-surgicaloutcomeofthepatientswhounderwentCAH.

Fewstudies,however,haveadequatelyaddressedthepsychiatric andseizurepost-surgicaloutcomesofpatientswithpreoperative POE.7,8 _{Although some studies have reported a post-surgical} remissionofpsychoticsymptoms,20,21_{othershaveconcludedthat} IIPdoes not change after surgery, whilePIP symptomsmay be diminished and even remitted after patients become free of disablingseizures.22,23_{ThepossiblesignificanceofbehavioralAEs} duringVEEGmonitoringandpost-surgicalpsychiatricoutcomehas alsobeen amatter ofinterest inpaststudies.Kanemotoetal.23 reportedpreoperativeepisodesofPIP,left-sidedsurgeriesandauras ofictalfearaspsychopathologicalriskfactorsofpostoperativemood disorders.Inthepresentstudy,allofthePIPpatientswhounderwent CAHdisplayedacompleteremissionoftheirpsychoticsymptoms aftersurgery.AEsweremorelikelytobeassociatedwithmorethan 100tonic–clonicseizuresduringthepatients’livesand withthe patients’previousPIPhistories.Althoughasmallnumberofpatients enrolled,thepresenceofIPI,psychiatricfamilyhistory,psychicaura, MTSlaterality,interictalfocisideandgeneralizationduringVEEG monitoringdidnotinfluenceeithertheoccurrenceofAEsorthe post-surgicaloutcomes.Inaddition,alternativepsychosesdidnot occurinthepsychiatricfollow-upevaluations.

Patients with epilepsy havea lower QOLand higher ratesof comorbiditiescomparedwiththegeneralpopulation.11_Therefore, seizureimprovementorcessationisofgreatclinicalsignificancefor

patients’QOL eveninthepresence of persistingpsychosis.7,24_Surgery is abetter treatmentoptionthanprolongedmedical therapyfor patients with refractory TLE-MTS.25_{In addition, seizure control can be} associatedwithimprovementsinthepsychiatricconditionofPIP patients.7,8,14_{Althoughsignificantdifferenceswereobservedonlyin} thephysicalhealthspheredomain,thepatientspresentedimportant QOL improvements in mostoftheESI-55 domains atthepost-surgical follow-up;suchnon-significantdifferencescouldbecausedbythe smallnumberofenrolledpatients.

Toconclude,thepresentdataconfirmthatVEEGmonitoringcan beconsideredtobeasafeprocedureforevaluatingthepossibilityof surgicalinterventioninpatientswithrefractoryTLE-MTSandPOE. DespitethepossibleoccurrenceofAEsandthesmallnumberof patientsenrolled,wedidnotobservesubstantialmorbidityoran increasedlengthofhospitalizationinoursample.Inaddition,the post-surgical outcomedata revealed anoverall improvement of psychoticsymptomsandQOLamongthesepatients.

Acknowledgments

ThisworkwassupportedbyCAPESandFAPESPfromBrazil.

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