Biobehavioral sources of variance in presurgical neuropsychological performance among patients with temporal lobe epilepsy PDF
Preview Biobehavioral sources of variance in presurgical neuropsychological performance among patients with temporal lobe epilepsy
BIOBEHAVIORALSOURCESOFVARIANCEINPRESURGICAL NEUROPSYCHOLOGICALPERFORMANCEAMONGPATIENTSWITHTEMPORAL LOBEEPILEPSY By DAVIDJ.MOSER ADISSERTATIONPRESENTEDTOTHEGRADUATESCHOOL OFTHEUNIVERSITYOFFLORIDAINPARTIALFULFILLMENT OFTHEREQUIREMENTSFORTHEDEGREEOFDOCTOROFPHILOSOPHY UNIVERSITYOFFLORIDA 1997 ACKNOWLEDGEMENTS Completionofthisstudywouldnothavebeenpossiblewereitnotfortheimportant contributionsofmanyindividualswhodeservemyrecognitionandgratitude. Firstandforemost, Iwouldliketoextendmysincerethankstomydissertationchairperson.Dr.RussellBauer,for theenormousamountofknowledge,time,effort,patienceandhumorthathebroughttothis project. IwouldalsoliketothankDr.EileenFennellandDr.DuaneDedefortheirinsightful comments,supportandvaluableinputduringallphasesofthestudy. Theassistanceand guidanceofDr.RobinGilmoreisgreatlyappreciated,asshewasverygivingofherknowledge andexpertiseregardingepilepsyandalsoallowedmeaccesstoEpilepsyMonitoringUnit resources. IwouldalsoliketoextendmysinceregratitudetoDr.JamesAlgina,whowentto greatlengthstoprovidevaluableandtimelystatisticalguidance. Dr.ChristianaLeonardalsodeservesrecognitionandthanksforherassistanceand generosityinallowingmeaccesstotheImageProcessingLaboratory. Iwouldalsoliketothank Dr.TaraSpevackforhervaluableandthoughtfiilinputthroughoutthestudy. Dr.StevenRoper, Mr.TimothyLucas,Ms.ArleneFrank,Ms.CandaceLariz,Dr.RitaJakus,Ms.DonnaLilly,Ms. ChristieSnively,thegraduatestudentsinDr.RussellBauer'sNeuropsychologyLaboratory,and theEpilepsyMonitoringUnittechniciansalsoplayedimportantrolesintheformationand completionofthestudy. FinallyIwouldliketothankmywife,Becky,andourdaughter,Ameliafortheirconstant andunwaveringlove,supportandgoodhumor. ii TABLEOFCONTENTS page ACKNOWLEDGEMENTS ii ABSTRACT v CHAPTERS 1 OVERVIEWOFRELEVANTLITERATURE I Epilepsy:Description,Incidence,andClassification 1 NeuropsychologicalAssessmentofEpilepsyPatients 4 HippocampalPathologyandNeuropsychologicalPerformance 25 QuantitativeMRIVolumetricStudiesinEpilepsy 29 HippocampalVolumes,Pathology,andNeuropsychologicalPerformance 34 EEGLocalizationofSeizureFoci 37 NeuropsychologicalTesting,MRI,andEEG 50 EpilepsySurgeryattheUniversityofFlorida 52 PurposeofthePresentStudy 54 2 METHODS 56 Subjects 56 Measures 56 MissingNeuropsychologicalData 58 MRIVariables 59 EEGVariables 59 DataCollectionProcedures 62 ExperimentalHypotheses 68 3 RESULTS 78 DemographicandIllness-RelatedVariables 78 NeuropsychologicalVariables 78 HippocampalVolumetrics 84 EEGVariables 84 4 DISCUSSION 100 DiscussionofExperimentalandExploratoryHypotheses 100 GeneralDiscussion 113 iii DirectionsforFutureResearch 117 APPENDIX 120 REFERENCES 124 BIOGRAPHICALSKETCH 131 iv AbstractofDissertationPresentedtotheGraduateSchool oftheUniversityofFloridainPartialFulfillmentofthe RequirementsfortheDegreeofDoctorofPhilosophy BIOBEHAVIORALSOURCESOFVARIANCEINPRESURGICAL NEUROPSYCHOLOGICALPERFORMANCEAMONGPATIENTSWITHTEMPORAL LOBEEPILEPSY By DavidJ.Moser December,1997 Chairman: RussellM.Bauer,Ph.D. MajorDepartment: ClinicalandHealthPsychology Mostepilepsycentersuseelectroencephalographic(EEG),structural-anatomic(MRI), andneuropsychological(NP)datatoidentifypotentiallyresectableregionsofepileptogenictissue inepilepsysurgerycandidates. Inidealcases,thesedataareconvergentandidentifyadiscrete regiontoberesected. Sometimes,however,NPdataarelessspecificthanEEGandMRIdatain lateralizingandlocalizingseizureonset. Inthecurrentstudy,discriminantfunctionanalyses (DFA)wereusedtoevaluatethestatisticalefficacyofEEG,MRI,andNPinpredictingsideof seizurefocusandeventualsurgeryinagroupofcomplexpartialseizurepatientsundergoing unilateralanteriortemporallobectomy(ATL). Subjectswerethendividedintotwogroups dependinguponwhethertheirNPdatawereconvergentordivergentwithEEGandMRI regardingpredictionofeventualsurgicalhemisphere. Thesegroupswerethencompared regardingdemographicandillness-relatedvariables. Subjectswere61surgicalcandidateswithcomplexpartialseizureswhoeventually underwenteitherright(n=26)orleft(n=35)ATL. Foreachsubject,scalpEEGonsetwas v codedandtransformedtoproduceasinglevaluereflectingdegreeofseizureonsetlaterality (SLI). Likewise,quantitativeMRIdatawereusedtoproduceavaluereflectingamountof volumetricasymmetrybetweenthetwohippocampi(DHF). Neuropsychologicalperformance wascharacterizedbycalculatingaveragez-scoresinlanguage,verbalmemory,nonverbal memory,motorandvisuoconstructivedomains. Then,SLI,DHF,andthefiveNPdomainscores wereenteredaspredictorsofsideofsurgeryandofsideofepileptogenicfocususingDFA. ResultsindicatedthatSLIwasaslightlybetterpredictorofsideofsurgeryandsideof seizurefocusthanDHF,andthatbothweresignificantlysuperiortoNPdomainscoresinthis regard. CorrectpredictionratesgenerallyimprovedwhentheseSLI,DHF,andNPdomainscores wereusedincombinationwithoneanotherratherthaninisolation. Groupcomparisonsmade betweenthosesubjectsforwhomNPdatawereconvergentwithEEGandMRIandthosefor whomthesedataweredivergentyieldednosignificantdifferencesondemographicorillness- relatedvariables. Implicationsformakingtreatmentdecisionsinepilepsyprograms,and directionsforfutureresearch,werediscussed. vi CHAPTER1 OVERVIEWOFRELEVANTLITERATURE Epilepsy:Description.Incidence,andClassification Epilepsyisaneurologicaldisordercharacterizedbyrecurrentseizures(Locharemkul, Primrose,Pilcher,Ojemann,&Ojemann,1992). Aseizureoccurswhenagroupofneurons becomes"irritable"andfiresinrepeatedbursts(Engel,1989),andmayleadtoclinically observablechangesinbehaviorifsufficientnumbersofneuronsareinvolved. Epilepsyisthe mostcommonchronicneurologicaldisorderintheUnitedStates,affectingmorethan2million adultsandchildren(Mcintosh,1992). Althoughwidelyused,theterm"epilepsy"isnotadiagnosisinitself,butisageneral term,whichsubsumesmanydifferentsyndromes(Kuzniecky&Jackson,1995). In1964,the CommissiononClassificationandTerminology(CCT)oftheInternationalLeagueagainst Epilepsy(ILAE)soughttocategorizethesevariousseizuretypesinsuchawaythatprofessionals worldwidecouldtreat,research,anddiscusstheseeventsusingconsistentcriteriaand terminology. Priortothattime,manyseparateclassificationsystemshadbeendevelopedfor differentpurposes,asituationwhichgaverisetovaryingandconfusingterminology(Wyllie& Luders,1993).TheeffortsoftheCCTweresuccessful,andtheclassificationsystemthatwas developedremainedinuseuntil1981,whenitwasrevisedintothesystemwhichiscurrentlyin use. Abriefdescriptionofthecurrentsystemfollows. Currently,allseizuresareinitiallyplacedinoneoftwolargecategories. Aseizureis definedas"generalized"ifitsonsetinvolvesactivationofalargenumberofneuronsinboth hemispheres. "Partial"or"focal"seizures,ontheotherhand,arethosethatbeginwithactivation 1 2 ofneuronsinalimitedpartofonehemisphere. Asecondmajorclassificationconcernsthe presenceorabsenceofalterationsofconsciousnessduringtheseizure. Thoseaccompaniedbyno suchalterationsaretermed"simple",whilethosethatproducechangesinconsciousnessare definedas"complex." Forthepurposesofthepresentstudy,thefollowingwillconcernonly partialseizures. Accordingtothe1981classificationsystem,partialseizuresarefiirthersubdividedinto threecategories. Ascanbeinferredfi-omtheabove,"simplepartialseizures"arethosethatbegin focallyandinvolvenoalterationofconsciousness,while"complexpartialseizures"(CPS)begin focallyanddoinvolvesuchchangeseitherimmediatelyorshortlyafteronset. Finally,thereare seizureswhicharedescribedas"secondarilygeneralized",whichbeginassimpleorcomplex partialeventsandpropagateuntillargeareasofbothhemispheresareinvolved. Simpleand complexpartialseizuresarethendescribedmorespecificallyaccordingtothepresenceor absenceofconcomitanteventssuchasmotorinvolvement,somatosensoryexperiences, autonomicsigns,andcognitiveandemotionaldisturbances(CommissiononClassificationand TerminologyoftheInternationalLeagueAgainstEpilepsy,1981). Approximately40percentof allepilepticindividualssufferfromCPS(Gastautetal.,1975),andapproximately60percentof thesepatientshaveseizuredisorderswhicharerefractorytomedication(Rodin,1968). Thus, findinganalternativetreatmentforpatientswithCPSisessential. Anincreasinglyavailableandeffectivetreatmentforpatientswhoseepilepsycannotbe controlledwithmedicationissurgicalresectionofanidentified"epileptogenicfocus",whichhas beendefinedasthatbrainlocationfromwhichapatient'shabitualseizuresarise,andremovalof whichwilltheoreticallyresultincompletecessationofseizures(Risinger,1991). Ithasrecently beenestimatedthatapproximately1,000oftheseresectiveseizuresurgeriesareperformedeach year(Pilcher,Locharemkul,Primrose,Ojemann,&Ojemann,1992),andthat80to90percentof thesepatientsbenefitsignificantlyfi-omthisintervention. Inordertoprovidehealthcareprofessionalswithausefiilandconsistentindicatorof surgicaloutcome,Engel(1987)developedaclassificationsystemwherebyeachpostsurgical patientreceivesascoreofIthroughIV. Criteriaforeachclassificationareasfollows: ClassI (Seizure-free):A)Completelyseizure-freesincesurgery,excludinganyseizureswhichmayhave occurredduringthefirstfewpostoperativedays;B)Aurasonlysincesurgery;C)Someseizures aftersurgery,butseizure-freeforatleasttwoyears;orD)Atypicalgeneralizedconvulsionswith antiepilepticdrugwithdrawalonly.ClassII(RareSeizuresor"ahnostseizure-free"):A)Initially seizure-freefollowingsurgerybuthasrareseizuresnow;B)Rareseizuressincesurgery;C)More thanrareseizuresaftersurgery,butrareseizuresforatleasttwoyears;orD)Nocturnalseizures only,whichcausenodisability. ClassIII(WorthwhileImprovement):A)Worthwhileseizure reduction;orB)Prolongedseizure-freeintervalsamountingtogreaterthanhalfthefollow-up period,butnotlessthantwoyears. ClassFV(NoWorthwhileImprovement):Significantseizure reduction;B)Noappreciablechange;orC)Seizuresworse. Ascanbeinferredfromthese criteria,agivenpatient'sEngelClassificationmaychangeacrossthecourseoftimefollowing surgery. Resectivesurgeryhasbeenshowntobeparticularlysuccessfiilwhentheseizurefocus andsubsequenttargetofresectionisinthetemporallobe(Chelune,1981;Engel,VanNess, Rasmussen,&Ojemann,1993). Althoughtheaforementionedratesofsurgicalsuccessare impressive,itisimportanttonotethattheeffectivenessofsurgeryreliesheavilyontheselection ofappropriatesurgerycandidates,andmustbejudgedinthecontextofseveralfactorsinaddition toagivenpatient'sdegreeofpotentialpostoperativeseizurerelief 4 Whenevaluatinganindividualforseizuresurgery,thepotentialforseizurecontroland confidencewithwhichagivenseizurefocusisidentifiedmustbeestimatedandcomparedwith thepotentialfortheseriouscognitiveandpsychosocialimpairmentsthatmayresultfrom temporalloberesection. Thistypeof"risk-benefit"assessmentallowsboththephysicianand patienttomakewell-informeddecisionsregardingthelikelyeffectsofsurgery(Ivnik, Sharbrough,&Laws,1988). Becausesuchadeterminationiscomplexandmultifactorial,datain severaldomainsisusuallycollectedtoassistinmakingsurgerydecisions. Thosetobediscussed inthisstudyincludeneuropsychologicalevaluation,magneticresonanceimaging(MRI),and electroencephalographic(EEG)investigation. NeuropsychologicalAssessmentofEpilepsyPatients Neuropsychologicaltestingplaysauniqueroleintheassessmentoftheepilepticpatient, asitprovidesinformationwhichiscomplementarytophysiologicalandanatomicalmeasures suchasEEGandMRI. AlthoughEEGandMRIprovidevaluableinformationaboutthestateof thebrain,onlyneuropsychologicaltestingcanrevealthebrain'sactualbehavioralcapacities. In fact,properlyadministeredandinterpretedneuropsychologicaltestingmayrevealbrain dysfunctionbeforestructuralabnormalitiesareevidentusingothermeasures(Jones-Gotman, 1991). Onegoalofneuropsychologicalassessmentinthestudyofepilepsyistoidentify impairmentsthatmaysuggestthatseizureonsetislateralizedtoaparticularhemisphere,oreven morespecifically,localizedwithinthathemisphere. Suchinformation,whencombinedwithdata obtainedthroughMRI,EEG,andclinicalinterview,mayrevealanepileptogeniczone(Pilcheret al.,1992). Inadditiontoidentificationofthisareaofseizureonset,neuropsychologicaldataalso playsanimportantroleindetermininghowlikelyitisthatremovalofbraintissuewillresultina
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