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ClinicalStudy

Safetyandfeasibilityofcombinedcoilingandneuroendoscopyforbetteroutcomesinthetreatmentofseveresubarachnoidhemorrhageaccompaniedbymassiveintraventricularhemorrhage

MitsutoshiIwaasa,TetsuyaUeba?,MasaniNonaka,MasakazuOkawa,HiroshiAbe,ToshioHigashi,TooruInoue

DepartmentofNeurosurgery,FacultyofMedicine,FukuokaUniversity,7-45-1Nanakuma,Jounan-ku,FukuokaCity,Fukuoka814-0180,Japan

articleinfoabstract

Subarachnoidhemorrhage(SAH)withintraventricularhemorrhage(IVH)isassociatedwithpoorout-comes.Theaimofthisstudywastoevaluatethesafetyandfeasibilityofcombinedcoilingandneuroen-doscopyfortreatingsevereSAHwithmassiveIVH.BetweenApril2008andJune2011,49patientswithasevereSAHweretreatedattheDepartmentofNeurosurgery,FukuokaUniversity,Japan;10ofthesepatientshadamassiveIVHwitharupturedaneurysm.All10patients(threemenandsevenwomen;meanage,63.1±8.5years)weretreatedwithcoilingandneuroendoscopicremovaloftheIVHwithin2daysofonset.Coilingwassuccessfullyperformedatameanvolumeembolizationratioof21.8±5.5%.NeuroendoscopicremovaloftheIVHreducedthemeanGraebscorefrom10.5±2.0to4.8±2.5(p=0.005).Allexternaldrainswereremovedonday3.Norebleedingoracutehydrocephaluswasnoted.TheGlasgowOutcomeScalescoresatdischargeindicatedtwopatientswithgoodrecovery,threewithmoderatedisability,fourinavegetativestate,andonedead.Agoodmodi?edRankinScale(mRS)score(0–2)atleast6monthslater(meanfollow-upperiod,15.4±9.2months)wasobservedfor?vepatients(50%),andapoormRSscore(3–6)wasobservedfortheremainingfourpatients.Neuroen-doscopicallyremovingtheIVHfromalloftheventriclesbetweenthelateralandthefourthventricleandcoilingtherupturedaneurysmisasafe,feasibleapproachfortreatingsevereSAHwithmassiveIVH.

Ó2013ElsevierLtd.Allrightsreserved.

Articlehistory:

Received2July2012

Accepted26September2012

Keywords:Coiling

IntraventricularhemorrhageModi?edRankinscaleNeuroendoscopy

Subarachnoidhemorrhage

1.Introduction

Patientswithasubarachnoidhemorrhage(SAH)accompaniedbyanintraventricularhemorrhage(IVH)havepooroutcomes.1–3TheirGlasgowComaScale(GCS)scoreandWorldFederationofNeurosurgicalSocieties(WFNS)gradeonadmissiontendtobepoor(GCS7–12,WFNSgradeIVorGCS3–6,WFNSgradeV).TheincreasedintracranialpressurecausedbytheIVHandtheriskofaneurysmre-rupturearetwoproblemsthatneedtobeurgentlyaddressedinthesepatients.

Tominimizesecondaryneuronaldamageandtheriskofaneu-rysmre-rupture,bilateralorunilateralventriculardrainagewithaneurysmclippingorcoilingcanbeusedtoreducetheintracranialpressureinpatientswithanIVHduetoarupturedaneurysm.4Re-cently,somestudieshavereportedthatslowremovaloftheIVHthroughcontinuousventriculardrainageseemstobeinsuf?-cient5–7andthatradicalremovaloftheIVHpromotesbetterout-comes.8–10Here,wereportonaseriesofpatientswithasevere

SAHaccompaniedbyamassiveIVHwhoweretreatedwithacom-binationofcoilingtherupturedaneurysmandneuroendoscopical-lyremovingthebloodfromallventriclesbetweenthelateralandthefourthventricle.Thisprocedureisminimallyinvasiveandal-lowsradicalclotremovalbecauseofgoodvisualizationintheoper-ative?eld.

2.Materialsandmethods2.1.Patientpopulation

Westudied49consecutivepatientswhopresentedwithase-vereSAH(WFNSgradeIVorV)totheDepartmentofNeurosurgery,FukuokaUniversity,betweenApril2008andJune2011.Onadmis-sion,allpatientswereclinicallyevaluatedbyGCSandCTscanswithin1hour.Three-dimensionalCTangiographywasalsocarriedoutonadmissionforallpatients.Ofthese49patients,10hadamassiveIVHfromananeurysmruptureandweretreatedwithcoil-ingandneuroendoscopicIVHremoval(Table1andFig.1).TheinclusioncriterionforouranalyseswasthepresenceofamassiveIVH(Graebscore<6,withcompleteocclusionofthethirdand

Correspondingauthor.Tel.:+81928011011;fax:+81928659901.

E-mailaddress:tueba@fukuoka-u.ac.jp(T.Ueba).

0967-5868/$-seefrontmatterÓ2013ElsevierLtd.Allrightsreserved.http://wendang.chazidian.com/10.1016/j.jocn.2012.09.042

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M.Iwaasaetal./JournalofClinicalNeuroscience20(2013)1264–1268

Table1

CharacteristicsofpatientswithseveresubarachnoidhemorrhageandmassiveintraventricularhemorrhageNumberAge(years)Male:FemaleWFNSgradeIVWFNSgradeV

Aneurysmsize(mm)VER(%)

Graebscore(preoperative)Graebscore(postoperative)GOSscoreatdischargeGRMDSDVSD

Followupperiod(months)mRSscoreatfollow-up0123456

10

63.1±8.53:719

9.3±2.921.8±5.510.5±2.0

4.8±2.5(P=0.005)a23041

15.4±9.24100311

1265

wasappliedtoevaluatethechangesintheGraebscore.Differencesofp<0.05wereconsideredstatisticallysigni?cant.AnalyseswereperformedwiththeStatisticalPackagefortheSocialSciences(SPSS,Chicago,IL,USA).2.3.Neuroendoscopicmaneuvers

FortheneuroendoscopicremovalofIVH,a?exibleendoscope(VISERA,OlympusMedicalSystems,Tokyo,Japan)wasusedinallpatients.Intubatedpatientswereplacedinasupineposition.Thesurgicalapproachwasthroughfrontalburrholes2cmanteriortothecoronalsutureand2cmlateraltothemidline.ToreachtheventriclesusingtheNeuroport(OlympusMedicalSystems),thetrajectorywasorientedtowardtheforamenofMonro(Fig.2).Aspirationmaneuversthroughtheworkingchannelwerealternatedwithrinsingwitharti?cialcerebrospinal?uid(ART-CEREB,OtsukaPharmaceutical,Tokyo,Japan)andwerecontinueduntiltherednessbeyondthescopebegantodisappearandtheventricularwallsbecamevisible.Theprocedurecanbelimitedtoonesideorextendedtotheothersidethroughtheseptumpelluci-dum,dependingonthevolumeofthedilatedventricles.Thoroughaspirationandirrigationwasusedtocompletelycleartheclotsinthelateralventricleandthentheclotsintheaqueductandfourthventricle.Duringthisprocedure,theirrigationwasisovolumetricbecausetheclotsoccludedtheoutlets,andtheaqueductwasen-D=dead,GOS=GlasgowOutcomeScale,GR=goodrecovery,MD=moderatelydisabled,mRS=modi?edRankinscale,SD=severelydisabled,VER=volume

1266M.Iwaasaetal./JournalofClinicalNeuroscience20(2013)1264–1268

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Aetro=,ertnuimmmCImtDlaaeeaoooPCCCmssiccc-PPoPodcl,inc--c-c...AtgsaraAolAAAVCC.C.AIIAIAVnnbpiileikthonrccaeae=RvfSC=doNeA,esFdy?VriciWargVVVVVed,tIVVVVVtdsroeiramlbextg=acensiaSMMFFFFFFFMiStdraaRhcyimlcn,el)udrascrmeelvineambaesige6153789084losi=cAy(6566556865cddrDnoySlai,rescetuitalhnraprtaedhaneb=op.

2rgeieotmmmesceilau0o=otrebmPn1234567891caeDdi.TDAMychoSvertebralartery–posteriorinferiorcerebellararteryaneurysminonepatient,andaposteriorcommunicatingarteryaneurysminthreepatients.TheneuroendoscopicremovaloftheIVHwasper-formedpriortocoilingin?veofthe10patients.Inthreeofthe10patients,externaldrainagewasperformed?rst,followedbycoilingandthenneuroendoscopicevacuationoftheIVH.Thisorderofprocedureswasrequiredinthesethreepatientsbecausetheneuroendoscopicteamwasunavailable.CoilingwasperformedpriortotheneuroendoscopicremovaloftheIVHintheremainingtwopatients.Themeananeurysmdiameterandmeanvolumeembolizationratio(VER)(excludingthepatientwiththevertebralarterydissectinganeurysm)were9.3±2.9mmand21.8±5.5%,respectively.Inthecaseofthepatientwiththevertebralarterydis-sectinganeurysm,theparentarterywasembolized.Thecoilingwassuccessfullyperformedwithoutintraproceduralruptureormajorvesselocclusioninallpatients(Table2).3.2.ReductionoftheGraebscore

AftertheneuroendoscopicremovaloftheIVH,areductioninhydrocephaluswasobservedinallpatients,andtheGraebscalescore(mean±standarddeviation)wasreducedfrom10.5±2.0to4.8±2.5(p=0.005)(Fig.1,Table1).Within3daysoftheoperation,alloftheexternaldrainswereremoved,andpatientsunderwentrehabilitation.Norebleedingordelayedhydrocephalusrequiringfurtherexternaldrainagewasobservedduringtheacutestage.However,ventriculoperitoneal(VP)shuntswererequiredtotreatnormalpressurehydrocephalus(NPH)insixpatientsaftertheyhadbeenreferredtorehabilitationhospitalsatleast1monthaftertheirinitialpresentation(Table2).3.3.Outcomes

TheGOSoutcomesatdischargewereasfollows:goodrecovery(twopatients),moderatedisability(threepatients),andvegetativestate(fourpatients).Onepatientdied6daysaftertheonsetoftheSAH.AgoodmRSscore(0–2)at6monthsorlater(meanfollow-upperiod,15.4±9.2months)wasobservedin?vepatients(50.0%),andapoormRSscore(3–6)wasobservedintheremaining?vepa-tients(Table2).NoneoftheeightpatientswhosemRSscoreat6monthsorlaterwas64hadocularmobilityabnormalitiesthatmighthavebeencausedbytheremovaloftheaqueductandfourthventricleclots.Twopatientscouldnotbeevaluatedat6monthsorlater:onewasdead,andtheotheronewasstillinavegetativestate.4.Discussion

Ourstudyshowsthatthecombinationofcoilingrupturedaneu-rysmsandneuroendoscopicallyremovinganIVHfromthelateraltothefourthventricleissafeandfeasibleinpatientswithasevereSAHaccompaniedbyamassiveIVH.

PatientswithanIVHduetoanSAHhavepoorWFNSgradesandpooroutcomes.1–3Adamsetal.12reportedthatpooroutcomeswerealmosttwiceasfrequentinsuchpatients.IVHinducestheacuteelevationofintracranialpressure,aswellasischemicencephalopathyandsecondaryhydrocephalus.13Moreover,bloodanditsderivativeshaveclearlybeenshowntobeproin?ammatoryagentsthatcausesecondaryneurologicaldamage.13,14Accordingly,theidenti?cationofadenseintraventricularclotonaCTscanhasanegativeprognosticvalueforpatientswithahigh-gradeSAH.3TheconventionalmanagementofIVHconsistsofexternalventriculardrainage,butcathetersinvariablybecomeoccludedbycoagulatedblood.Thisbloodmayremainintheventriclesforweeks,owingtothepoor?brinolyticactivityofcerebrospinal?uid,15thus

increasingtheriskofinfection.Althoughbothconventionaldrain-ageandneuroendoscopicremovaloftheIVHcouldcausereblee-dingofanuntreatedaneurysm,16–18thecombinationofcoilingandneuroendoscopicremovaloftheIVHwillminimizetheriskofrebleedingandcontroltheintracranialpressure,thusreducingdelayedischemicneurologicalde?cits.

Holtzmanetal.8proposedcraniotomywithcorpuscallosotomyandfenestrationoftheseptumpellucidumasatreatmentforIVH,andtheyobtainedgoodoutcomes.Longattietal.10treated10pa-tientswithSAHaccompaniedbyIVH(WFNSgradeIVorV)usingsimultaneouscoilingandendoscopicclotremoval,andtheyalsoreportedgoodoutcomes.AsimilarstudybyNishikawaetal.19alsoreportedgoodoutcomes.Arecentreportonintraventricularinfu-sionoftissueplasminogenactivator(tPA)afteraneurysmcoilinginpatientswithIVHindicatedthatthisprocedurecouldbeaprom-isingalternative.20,21Thesedatadonotnecessarilymeanthatinva-sivetreatmentisalwaysneeded.Inaddition,thismaneuvercouldhaverisks,includingre-ruptureofthecoiledaneurysmsandparenchymalhemorrhage.22NeuroendoscopicremovalofanIVHmightbesaferthanintraventricularinfusionoftPA,especiallyinpatientswithcoilingatalowVER.4.1.Normalpressurehydrocephalus

ApreviouslypublishedseriesofpatientstreatedwithcoilingandendoscopicremovalofIVHindicatedthatVPshuntswerenotrequiredforhydrocephalus.10Inourseries,sixofthe10pa-tientshadNPHandrequiredaVPshunttoimprovetheircon-sciousnlevel.Inthepreviousstudy,theGraebscorewasreducedfrom11.5±0.7to4.7±2.2whena?exibleendoscopewasusedwithoutendoscopicthirdventriculostomy(ETV).InourstudytheGraebscorewassigni?cantlyreducedfrom10.5±2.0to4.8±2.5

(p=0.005)anda?exibleendoscopewasalsousedwithoutETV.ThereasonwhyoursixpatientshadNPHmightbeexplainedbythevolumeoftheSAH.Furtherstudyshouldbeconducted.

4.2.Limitationsandrelevanceofourreport

Arecentstudyshowedthatcoilingproducedfavorableout-comesinpatientswithanSAHofWFNSgradeIVorV.23Theques-tionariseswhetherourobservedoutcomeswerecausedsolelybytheeffectofcoilingorbytheadditiveeffectoftheneuroendoscopicremovaloftheIVH.Krameretal.24reportedthattheIVHvolumeisstronglyassociatedwithpoorneurologicaloutcomesfollowinganeurysmalIVH.Therearenodatacomparingtheoutcomesofpa-tientswithanSAHaccompaniedbyamassiveIVHwhoweretrea-tedbycoilingwithorwithoutremovaloftheIVH.Someauthorssuggestthatthepooroutcomesofthesepatientsarecausedbytheclotsinthethirdandfourthventriclesdirectlycompressingvi-talcentersinthethalamus,hypothalamus,andbrainstem.25–28Shapiroetal.29reportedmedullopontinesofteningongrossexam-inationandmultiplepontinemicroinfarctsonhistologicalanalysisafterautopsiesofsuchpatients.Forneuroendoscopicremovaltobefeasible,theIVHneedstoberemovedassoonaspossible.

FlexibleendoscopyhasrecentlybecomepopularasaminimallyinvasivebutradicalapproachinthemanagementofIVH.30–34A?exibleendoscopecaneasilyprovideaccesstothehematomaoveralargeventriculararea.Thisinstrumentrequiresskilledmanipula-tion,withoutwhichitisdif?culttoremovetheclotsbecausetheworkingchannelistoonarrowtosuctionorretrievethem.FurtherstudiesshouldbeconductedtoinvestigatewhetherinterventionsaimedatclearingventricularbloodintheacutestageofSAHwithIVH,suchascombinedtreatmentwithcoilingand

neuroendoscopy

1268M.Iwaasaetal./JournalofClinicalNeuroscience20(2013)1264–1268

orwithcoilingandtPAadministration,canimprovepatientoutcomes.5.Conclusion

ThecombinationofneuroendoscopicremovaloftheIVHfromalloftheventriclesbetweenthelateralandthefourthventricleandcoilingoftherupturedaneurysmisasafeandfeasibleap-proachfortreatingpatientswithasevereSAHaccompaniedbyamassiveIVH.

Con?ictsofinterest/disclosures

Theauthorsdeclarethattheyhaveno?nancialorothercon-?ictsofinterestinrelationtothisresearchanditspublication.References

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