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REVISTA

BRASILEIRA

DE

ANESTESIOLOGIA

PublicaçãoOficialdaSociedadeBrasileiradeAnestesiologia

www.sba.com.br

SCIENTIFIC

ARTICLE

The

effect

of

sugammadex

on

postoperative

cognitive

function

and

recovery

Özcan

Pis

¸kin

a,

,

Gamze

Küc

¸ükosman

a

,

Deniz

Utku

Altun

b

,

Murat

C

¸imencan

a

,

Banu

Özen

c

,

Bengü

Gülhan

Aydın

a

,

Rahs

¸an

Dilek

Okyay

a

,

Hilal

Ayo˘

glu

a

,

Is

¸ıl

Özkoc

¸ak

Turan

d

aDepartmentofAnesthesiologyandReanimation,SchoolofMedicine,BulentEcevitUniversity,Zonguldak,Turkey bProvincialHealthDirectorateofSanliurfa,Sanliurfa,Turkey

cDepartmentofNeurology,SchoolofMedicine,BulentEcevitUniversity,Zonguldak,Turkey

dDepartmentofAnesthesiologyandReanimation,AnkaraNumunePracticeandResearchHospital,Ankara,Turkey

Received29May2014;accepted28October2014 Availableonline23May2015

KEYWORDS

Sugammadex; Neostigmine; Postoperative cognitive dysfunction; MMSE; MoCA

Abstract

Backgroundandobjective: Sugammadex is thefirst selective relaxant binding agent.When

comparedwithneostigmine,followingsugammadexadministrationpatientswakeearlierand

haveshorterrecoverytimes.Inthisstudy,wehypothesizedthatfastandclearawakeningin

patientsundergoinggeneralanesthesiahaspositiveeffectsoncognitivefunctionsintheearly

periodafteroperation.

Methods:Approved by the local ethical committee, 128 patients were enrolled in this

randomized,prospective,controlled,double-blindstudy.Patientswereallocatedtoeither

Sug-ammadexgroup(GroupS)ortheNeostigminegroup(GroupN).Theprimaryoutcomeofthestudy

wasearlypostoperativecognitiverecoveryasmeasuredbytheMontrealCognitiveAssessment

(MoCA)andMiniMentalStateExamination(MMSE).Afterbaselineassessment12---24hbefore

theoperation.Aftertheoperation,whentheModifiedAldreteRecoveryScorewas≥9theMMSE

and1hlatertheMoCAtestswererepeated.

Results:AlthoughtherewasareductioninMoCAandMMSEscoresinbothGroupSandGroupN

betweenpreoperativeandpostoperativescores,therewasnostatisticallysignificantdifference

intheslopes(p>0.05).ThetimetoreachTOF0.9was2.19mininGroupSand6.47mininGroup

N(p<0.0001).Recoverytimewas8.26mininGroupSand16.93mininGroupN(p<0.0001).

Conclusion:We showed that the surgical procedure and/or accompanying anesthetic

pro-cedure may cause atemporary orpermanent regression in cognitive function in theearly

Correspondingauthor.

E-mail:drozcanp@gmail.com(Ö.Pis¸kin). http://dx.doi.org/10.1016/j.bjane.2014.10.003

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postoperativeperiod.However,bettercognitiveperformancecouldnotbeprovedinthe

Sug-ammadexcomparedtotheNeostigmine.

©2015SociedadeBrasileiradeAnestesiologia.Publishedby ElsevierEditoraLtda.Thisisan

openaccessarticleundertheCCBY-NC-NDlicense(

http://creativecommons.org/licenses/by-nc-nd/4.0/).

PALAVRAS-CHAVE

Sugamadex; Neostigmina; Disfunc¸ãocognitiva nopós-operatório; MMSE;

MoCA

Oefeitodesugamadexsobreafunc¸ãocognitivaerecuperac¸ãonopós-operatório

Resumo

Justificativaeobjetivo: Sugamadexéoprimeiroagente deligac¸ãorelaxante seletivo.Após

aadministrac¸ãodesugamadex,ostemposdedespertarederecuperac¸ãodospacientessão

menores, emcomparac¸ãocomneostigmina. Nesteestudo,ahipótese foi queum despertar

maisrápidoeclarodospacientessubmetidosàanestesiageralpossuiefeitospositivossobreas

func¸õescognitivasnopós-operatórioimediato.

Métodos: Apósaaprovac¸ãodoComitêdeÉticalocal,128pacientesforamincluídosnesteestudo

prospectivo,randômico,controladoeduplo-cego.Ospacientesforamdesignadosparaogrupo

sugamadex(Grupo S)ougruponeostigmina(GrupoN). Odesfechoprimáriodoestudofoi a

recuperac¸ãocognitivanopós-operatórioimediato,deacordocomamensurac¸ãodaAvaliac¸ão

deMontrealdaFunc¸ãoCognitiva(MoCA)ecomoMiniExamedoEstadoMental(MMSE).Apósa

avaliac¸ãoinicial12---24hantesdaoperac¸ão.Apósaoperac¸ão,quandooescoredeRecuperac¸ão

deAldretemodificadoera≥9,otesteMMSEe,umahoradepois,otesteMoCAforamrepetidos.

Resultados: Emboratenhahavidoumareduc¸ãonosescoresdeMoCAeMMSEtanto noGrupo

Squanto noGrupo N,entreosescorespré-epós-operatório,não houvediferenc¸a

estatisti-camentesignificativanasreduc¸ões(p>0,05).OtempoparaatingirTOF0.9foide2,19minno

Grupo Sede6,47minnoGrupo N(p<0,0001).Otempode recuperac¸ãofoide 8,26min no

GrupoSede16,93minnoGrupoN(p<0,0001)

Conclusão:Mostramosqueoprocedimentocirúrgicoe/ouprocedimentoanestésicode

acom-panhamentopode causaruma regressãotemporária ou permanentedafunc¸ãocognitiva no

pós-operatórioimediato.Noentanto,umdesempenhocognitivomelhornãopodeserprovado

nogruposugamadexemcomparac¸ãocomogruponeostigmina.

©2015SociedadeBrasileiradeAnestesiologia.PublicadoporElsevierEditoraLtda.Este ´eum

artigo OpenAccess sobumalicenc¸aCCBY-NC-ND(

http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Patientswhoundergomajorsurgerywithgeneral anesthe-sia mayexperiencememoryimpairmentandregressionof high-executive functions such as ordering, planning, and organization after the operation.1 This intellectual and cognitiveworseningisknownaspostoperativecognitive dys-function (POCD).POCDoften creates temporary cognitive impairmentbut,especiallyinolderpatients,itmaytakethe formofpermanentdecline.1Todate,controlledstudiesand animal modelshave notestablisheddiagnosticcriteriafor POCD,anditsetiologyisnotfullyunderstood.2---4However, animal studies have provided strong evidence that expo-suretoanestheticagentsmaycausepermanentlearningand memoryimpairment.5---8

Sugammadex(Bridion®,MerckSharpandDohme (MSD),

Oss, The Netherlands) is a rapid andselectively effective aminosteroidagentthathasrecentlyentereduse.Through rocuroniumandvecuroniumencapsulation,itcauses rapid recovery independent of the time of administration.9---13 Comparedtopatientsgivenneostigminetorecover,patients givensugammadex have been observed torecoverwith a clearerlevelofconsciousness.

Inthisstudy,wehypothesizedthatfastandclear awak-eninginpatientsundergoinggeneralanesthesiahaspositive effects on cognitive functions in the early period after operation.Totest thishypothesis,postoperativecognitive functionsofpatientswereevaluated,comparingthosegiven neostigmineorsugammadexforrevivalaftergeneral anes-thesiawithrocuronium-basedneuromuscularblock.

Method

This randomized, prospective, controlled, double-blind study wasapproved by the BülentEcevit University Prac-ticeandResearchHospital EthicsCommittee(2012/07-7). Thestudyincludedpatientswithplannedoperationsunder general anesthesia (abdominal surgery; upper extremity orthopedicinterventions;gynecology;plasticsurgery; urol-ogy;ear, nose, and throat; and spinal surgery operations lastingatleast 60min) whocouldread andwriteTurkish, werebetween 18 and60 yearsof age, andhad American SocietyofAnesthesiologists(ASA)scoresofIorII.

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diabetes mellitus (DM), neuropsychiatric disease, chronic alcoholor drugaddiction,GlasgowComa Scale (GCS)<15, historyofcardiopulmonaryarrestorstrokeintheprevious 12months,historyofpreviousoperationundergeneral anes-thesia, emergencysurgery, andpostoperative Mini-Mental StateExamination14 (MMSE)score<23andMontreal Cogni-tiveAssessment15(MoCA)score<21.

After receiving informed patient consent, the sugam-madex(Group S) and neostigmine(Group N)groups were createdusingtheclosed-envelopemethod.Toevaluate cog-nitive functions, the MMSE and MoCA tests were carried outbythesameneurologyexpert blindedtothepatient’s groupassignment.Allpatientswerevisited12---24hbefore theoperation.Thepatients’educationallevel, accompany-ingdiseases,anddemographicinformationwererecorded. Beforetheoperationthepatients’memory,attentive exec-utive functions, andmotor skills wereevaluatedwiththe MMSE and MoCA tests as a control cognitive evaluation (T0).Aftertheoperation,in thePACU,whenthe Modified

AldreteRecovery Score16 (MAS)was 9 theMMSE and 1h later the MoCA tests were repeated (T1). Neither group

wasgivenpremedication.Duringtheoperationmean arte-rial pressure (MAP), heart rate (HR), peripheral oxygen saturation(SpO2),bispectralindex(BIS),andadductor

mus-cleand nasopharyngeal temperature were monitored and recorded.Forneuromusculartransmissionmonitoringa TOF-WATCH® SX(OrganonTeknikaBV,Netherlands)devicewas

used.The temperature of the operatingroom was set to 21---25◦C.Thepatientswerecovered,andtheskin temper-atureofthe thenarregionwasmonitoredtoensureitdid not fall below 32◦C. All patients were given intravenous (IV)fentanyl(1␮g/kg)andpropofol(2mg/kg)foranesthesia induction. When BIS values were 40---60, TOF device cali-brationwascompletedandthreeconsecutivesingletwitch controlvalueswere recorded.Then, IV0.5mg/kg rocuro-nium wasadministered and the interval until TOF values reached0(TOF0)wasrecorded.WhenTOF0wasreachedthe

patientswereintubated.Tomaintainanesthesiaallpatients were given 50:50 O2/N2O and 2% sevoflurane titrated to

maintainBIS valuesbetween 40 and 60. Duringthe oper-ation,when TOF values were 25% (TOF25), a dose of one

quarteroftheinitialdoseofrocuroniumwasadministered. Attheendoftheoperation,whenTOF25wasreached,Group

SwasgivenIV2mg/kgsugammadexandGroupNwasgiven IV0.03mg/kg neostigmine+0.01mg/kg atropine. Patients wereextubatedwhentheirTOFvaluesreached90%(TOF90).

TheintervalbetweenTOF25 andTOF90wasrecordedin

sec-onds(TOF25---90).Duringtheoperation,amountsofadditional

medicationandtotalrocuroniumwererecorded.Afterskin suturingwasfinished,anestheticgaseswerestoppedinboth groups. This timewasrecorded astheend of anesthesia. The time fromwhen anesthetic gases were stoppeduntil MAS≥9wasrecordedastherecoveryperiod.Afterthe oper-ation,patientsweretransferred tothePACU.Allpatients weregivenIV1mg/kgtramadolaftertheskinincisionwas finishedfor postoperative pain relief. At 20, 40, 60, and 120min post-operation, visual analog scores17 (VAS) were recorded. When VAS>4 a non-steroidal anti-inflammatory analgesicagentwasadministeredandrecorded.

The primary outcome of the study was early postop-erativecognitive recovery as measured by the MoCA and MMSE.The secondary outcomewastimefromthe startof

thereversaladministrationtotherecoveryofaratioof0.9 in patients receiving rocuronium as NMBA during general anesthesiaforasurgicalprocedure.

Poweranalysis

To test the significance of differences between repeated measuresindependentgroupstheconventionaleffectsize requiredforthettestisassumedtobemedium(d=0.50), sofor thestudytohave80%power itwascalculatedthat bothgroupsneededaminimumsamplesizeof128(n=64).18

Statisticalanalysis

Statistical analyses for this study were completed using the SPSS for Windows 15.0 softwarepackage. Descriptive statistics were used (mean, median, standard deviation, minimumandmaximumvalues)toevaluatedata. Measure-ment values aregiven asmeans and standard deviations. Categoricalvariables(numbervalues)aregivenasnumbers and percentages. The chi-square test was used to com-pare categorical variables.The Levene’s test wasusedto evaluatethehomogeneitywithingroupsforparametric con-ditions.Iftheresultsofthehomogeneitytestsshowedthat parametric conditions were met, mixed ANOVA was used for comparisons between groups; ifparametric conditions were notmet,the Wilcoxon signed-ranktest wasusedto compare measurement values before and after, and the Mann---WhitneyUtestwasusedforcomparisonsof indepen-dentgroups.Significancewasacceptedatp<0.05.

Results

This study was conducted from September 2012 to July 2013with128patients.Thirty-eightpatientswereexcluded becausetheirMMSEandMoCAtargetscoreswerelow,and threewereexcludedbecausetheycouldnotbeextubated attheendoftheoperation.Ofthe87patientsincludedin thestudy,48.2%(n=42)wereinGroupSand51.8%(n=45) wereinGroupN.

Thedemographiccharacteristicsofthepatientsare pre-sentedinTable1.Thetotalamountofrocuroniumconsumed was 67.02±15.85mg in Group S and 62.44±11.65mg in Group N (Table 1). There was a statistically significant difference in average age between the groups (p<0.05). Therewerenosignificantdifferencesbetweenthegroupsin weight,BMI,durationofoperation,durationofanesthesia, andtotalamountofrocuroniumconsumed(p>0.05).

ThetimetoreachTOF0.9was2.19min inGroup Sand 6.47mininGroupN(p<0.0001).Recoverytimewas8.26min inGroupSand16.93mininGroupN(p<0.0001)(Table2).

TheMMSET0andT1scoresinGroupSwere26.98±1.957

and26.90±1.936,andinGroupNwere27.00±2.286and 25.82±2.724, respectively. The MoCAT0 andT1 scores in

GroupSwere23.26±1.988and23.17±2.294andinGroupN were23.56±2.482and23.04±2.868,respectively.Inboth tests the T1 mean was lower than the T0 mean.

Depen-dent groupswerecomparedwiththet-test,andrepeated measurementvalueswerecompared.Todeterminethe dif-ference between the MMSE and MoCA at T0 and T1, the

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Table1 Distributionofsociodemograficfactorsandoperativedetailsviagroups.

GroupS(±SD)

(n=42)

GroupN(±SD)

(n=45)

pa

Meanage,years 32.07±11.50 37.38±11.95 <0.05

Gender(F/M) 12/30 22/23 >0.05

Educationyears(<9years/9---12years/>12years) 12/18/12 17/18/10 >0.05 Weight,kg 74.83±14.93 75.33±13.92 >0.05 BMI,kg/cm2 25.25±4.08 26.70±4.63 >0.05

ASAclass(I/II) 17/25 18/27 >0.05

Durationoftheoperation,min 118.86±42.94 115.49±46.51 >0.05 Durationoftheanesthesiology,min 125.21±38.91 124.18±48.39 >0.05 Rocuronium,mg 67.02±15.85 62.44±11.65 >0.05 Tramadol,mg 74.83±14.93 75.33±13.92 >0.05

F,Female;M,Male;BMI,bodymassindex;ASA,AmericanSocietyofAnesthesiologistscore.

a Chi-squaretest(2×n)andIndependentsamplettest.

Table2 TimetorecoveryofTOFratioto0.9(min)andtımetorecoveryofAldrete≥9(min).

GroupS(±SD) GroupN(±SD) pa

TimetorecoveryofTOFratioto0.9 2.19±1.47 6.47±1.92 <0.0001 TimetorecoveryofAldrete≥9 8.26±5.02 16.93±8.00 <0.0001

TOF,trainoffour.

a Independentttestforgroups.

Thetest resultsareillustrated inFig.1,whichshows that althoughtheT0andT1MMSEvaluesinGroupSwerereduced,

theslopeofthereductiondidnotshowastatistically signif-icantdifference(p>0.05).InGroup N,althoughtherewas astatisticallysignificant fallinMMSEvaluesfromT0 toT1

(p<0.05) there was no statistically significant difference between the slope values. Fig. 2 indicates that although therewasareductioninMoCAvaluesinbothGroupsSand

27

26.8

26.6

26.4

26.2

26

25.8

Groups

Estimated marginal means

Group S Group N

T0 T1

Figure1 MMSEscoreslopesofthegroupsfromT0toT1.

NfromT0toT1,therewasnostatisticallysignificant

differ-enceintheslopes(p>0.05)(Table3;Fig.3).

Discussion

In this study, the effects of sugammadex on recovery and cognitive functions were compared with those of

23 23.1 23.2 23.3 23.4 23.5 23.6

Groups

Estimated marginal means

Group S Group N

T0 T1

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Table3 MMSEandMoCAscoresatpreoperativeand

post-operativeperiod.

T0(±SD) T1(±SD) pa

GroupS

MMSE 26.98±1.957 26.90±1.936 >0.05 MoCA 23.26±1.988 23.17±2.294 >0.05

GroupN

MMSE 27.00±2.286 25.82±2.724 <0.05 MoCA 23.56±2.482 23.04±2.868 >0.05

T0,preoperative;T1,postoperative. aPairedsamplettest.

neostigmine.AlthoughthesugammadexgroupreachedTOF 0.9 earlier than the neostigmine group and had shorter recovery times, no significant improvement in cognitive recoverywasidentified.

Surgical procedures and accompanying anesthetic pro-ceduresmaycausetemporaryor permanentpostoperative regression in cognitive functions; this situation is known as POCD.4 However, whether the surgical procedure or anesthesia administration causes POCD is not fully understood.2,3,19,20Manyrandomizedcontrolledstudieshave shown that the incidence of POCD increases in patients whoare older or undergoing cardiopulmonary bypassand lowerextremityorthopedicoperations.20 Todeterminethe effectof sugammadexandneostigmineoncognitive func-tion,thisstudyexcludedpatientsabovetheageof60years andthoseundergoingcardiac, cranial,and lower extrem-ity operations. Independent risk factors for development ofPOCD wereeliminated.In addition,therewasa signif-icant difference in average age between the two groups (GroupS:32.07±11.50andGroupN:37.38±11.95). John-sonetal.21foundthattheincidenceofPOCDwasverylow inmiddle-agedindividualsand determinedthattherewas nosignificantdifferenceinPOCDbetweenpatientswhohad undergoneanoperationintheprevious3monthsandhealthy volunteers. Therefore, we believe that the difference in

0 10 20 30 40 50 60 70 80 90

100 Group S

BIS

Baseline TOF0 60min. after

induction

BIS TOF25 MAS 9

0 10 20 30 40 50 60 70 80 90

100 Group N

BIS

Figure3 B˙IS valuesin group N and group S patients. B˙IS, Bispectral ˙Index.

agebetween thetwogroups didnotnegativelyaffect the cognitivetestscores.

There is no international consensus on how cognitive function shouldbeevaluatedafteran operation.22 To this end,almost30testshavebeendescribed,buttheir advan-tages have not been demonstrated. The MMSE test is frequentlyusedtoevaluatecognitivefunction after anes-thesiabecauseittakesashortertimetoadminister,andhas been found tobemoreuseful by patientsand physicians. TheMoCAtesthasbecomepopularrecentlyandisused fre-quentlyasitisnotdependentondemographicvariablessuch asageandeducation.23BoththeMMSEandMoCAtestshave high validityand reliability,withTurkish validityand reli-abilitystudies havingbeencompleted.23,24 Basedonthese factors, the MMSE andMoCA tests were usedto evaluate cognitivefunctioninthisstudy.

Thereare somereservations about whenand how fre-quently cognitive evaluation tests should be performed after operations.2,3,20 Factors that may negatively affect the cognitive evaluation scores are painafter the opera-tion,disruptedsleep,andlearning/memorizingofthetests duetotheirfrequentrepetition.1Inthisstudy,toprevent the effects of these factors all patients had a VAS score <4 and MAS score ≥9 before postoperative evaluation. In addition,topreventmemorizingandlearningof the eval-uationtests,thetestswereonlyconductedonceafterthe operation.

It is not known exactly when brain function returns after general anesthesia. Studies have shown that cogni-tivefunctionsareaffectedbyseveralfactorsaftersurgical procedures with anesthesia.1---3,19 As rapid and short-term effective anesthetic agents are metabolized less by the body, theymaycauseless cognitivedysfunction.Matthew et al.,8 in astudy of 921 patients undergoing major non-cardiac surgery, administered to one group a standard anesthetic protocol while theother group receiveda BIS-guided titrated anestheticprotocol. The BIS-guided group wasexposedlesstoanestheticagentsandwasdetermined tohavelessPOCDinthe3monthsaftersurgery.Thisstudy usedBISinboth groupstoreduceexposure toanesthetics andformonitoring.

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TOF1.0in8.5min.Inourstudy,thetimetoreachTOF0.9 forpatientsgivensugammadexwas2.19min,andthe recov-erytimewas8.26min,whileforpatientsgivenneostigmine thesetimeswere6.47and16.93min.Thepatientsgiven sug-ammadexwokeandrecoveredearlierthandidthosegiven neostigmine.

Manystudiesoftheeffectsoffastemergenceand recov-ery from anesthesia on postoperative cognitive function havebeenconducted.Broncoetal.27comparedtheeffects ofarapid-startandrecoveryinhalationagent,xenon,with another inhalation agent, sevoflurane, in terms of post-operative recoveryand cognitivefunction.Patientsin the xenongrouphadanearlieremergencetimeandbetter cog-nitive recovery. Coburn et al.28 compared the effects of xenonwithdesfluraneonpostoperativecognitive function in elderly patients; the eye-opening and extubation peri-odswereshorterinthexenongroup;however,theauthors stated that the effects on cognitive function were simi-lar to those of desflurane. Similarly, Rasmussen et al.29 determined that the effects on cognitive function of the fast-acting inhalation agent xenon and fast-acting intra-venous propofol were similar in elderly patients. In our study, to evaluate the cognitive function in both groups, MMSE and MoCA tests were administered at T0 and T1.

AlthoughtherewasanumericalreductioninMMSEandMoCA scoresatT1comparedtoT0,therewasnostatistically

sig-nificant difference in the reduction slopes. Studies have shown that the surgical procedure and/or accompanying anestheticproceduremaycauseatemporaryorpermanent regressionin cognitivefunctionin theearly postoperative period. However,better cognitive performance could not be proved in the sugammadex patients compared to the neostigminepatients.Nopriorstudiescomparingthe cogni-tiveperformanceofsugammadexandneostigminepatients werefound.

Calculatingthesamplesizeforan80%strengthrequired eachgrouptoinclude64patients,foratotalof128; how-ever,exclusioncriteriameantthatthestudywascompleted with87patients.Limitationsintermsoftheprojectduration meantthatbackupgroupswerenotincluded.Thiswasthe most important limitation of thestudy. In addition, post-operative cognitiveevaluation wascompleted only during theearlyperiod.Asaresult,theeffectsofsugammadexon cognitivefunctionwerecomparedonlyintheearlyperiod. Anotherlimitationof thestudy wasthatlowdosesof sug-ammadex (2mg/kg) were used.As a result,the effectof high-dose(16mg/kg)sugammadexonPOCDdevelopmentis unknown.

In conclusion, evaluating cognitive function after an operation is complicated; the many independent risk factorsandmultitude ofevaluation testsaddtothe diffi-culty.

Sugammadexis a verynewagent.Further studies that includemoredetailedstatisticalanalysis,differentdosesof sugammadex, andlarger sample sizes areneeded tofully understandtheeffectsofthisagentoncognitivefunctionin thelatepostoperativeperiod.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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Table 1 Distribution of sociodemografic factors and operative details via groups. Group S ( ± SD) (n = 42) Group N ( ± SD)(n=45) p a
Figure 3 B˙IS values in group N and group S patients. B˙IS, Bispectral ˙Index.

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