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Resuscitation

jo u r n al hom ep age:w w w . e l s e v i e r . c o m / l o c a t e / r e s u s c i t a t i o n

Clinical Paper

AWARE—AWAreness during REsuscitation—A prospective study

Sam Parnia

a,∗

, Ken Spearpoint

b

, Gabriele de Vos

c

, Peter Fenwick

d

, Diana Goldberg

a

, Jie Yang

a

, Jiawen Zhu

a

, Katie Baker

d

, Hayley Killingback

e

, Paula McLean

f

,

Melanie Wood

f

, A. Maziar Zafari

g

, Neal Dickert

g

, Roland Beisteiner

h

, Fritz Sterz

h

, Michael Berger

h

, Celia Warlow

i

, Siobhan Bullock

i

, Salli Lovett

j

,

Russell Metcalfe Smith McPara

k

, Sandra Marti-Navarette

l

, Pam Cushing

m

, Paul Wills

n

, Kayla Harris

d

, Jenny Sutton

o

, Anthony Walmsley

p

, Charles D. Deakin

d

, Paul Little

d

, Mark Farber

q

, Bruce Greyson

r

, Elinor R. Schoenfeld

a

aStonyBrookMedicalCenter,StateUniversityofNewYorkatStonyBrook,NY,USA

bHammersmithHospitalImperialCollege,UniversityofLondon,UK

cMontefioreMedicalCenter,NewYork,USA

dUniversityHospitalSouthampton,Southampton,UK

eRoyalBournemouthHospital,Bournemouth,UK

fStGeorgesHospital,UniversityofLondon,UK

gEmoryUniversitySchoolofMedicine&AtlantaVeteransAffairsMedicalCenter,Atlanta,USA

hMedicalUniversityofVienna,Austria

iNorthamptonGeneralHospital,Northampton,UK

jListerHospital,Stevenage,UK

kCedarSinai,USA

lCroydonUniversityHospital,UK

mJamesPagetHospital,UK

nAshford&StPetersNHSTrust,UK

oAddenbrookesHospital,UniversityofCambridge,UK

pEastSussexHospital,EastSussex,UK

qIndianaUniversity,WishardMemorialHospital,Indianapolis,USA

rUniversityofVirginia,Charlottesville,VA,USA

a r t i c l e i n f o

Articlehistory:

Received28June2014

Receivedinrevisedform2September2014 Accepted7September2014

Keywords:

Cardiacarrest Consciousness Awareness

Neardeathexperiences Outofbodyexperiences Posttraumaticstressdisorder Implicitmemory

Explicitmemory

a b s t r a c t

Background:Cardiacarrest(CA)survivorsexperiencecognitivedeficitsincludingpost-traumaticstress disorder(PTSD).Itisunclearwhetherthesearerelatedtocognitive/mentalexperiencesandawareness duringCPR.Despiteanecdotalreportsthebroadrangeofcognitive/mentalexperiencesandawareness associatedwithCPRhasnotbeensystematicallystudied.

Methods:Theincidenceandvalidityofawarenesstogetherwiththerange,characteristicsandthemes relatingtomemories/cognitiveprocessesduringCAwasinvestigatedthrougha4yearmulti-center observationalstudyusingathreestagequantitativeandqualitativeinterviewsystem.Thefeasibility ofobjectivelytestingtheaccuracyofclaimsofvisualandauditoryawarenesswasexaminedusingspe- cifictests.Theoutcomemeasureswere(1)awareness/memoriesduringCAand(2)objectiveverification ofclaimsofawarenessusingspecifictests.

Results:Among2060CAevents,140survivorscompletedstage1interviews,while101of140patients completedstage2interviews.46%hadmemorieswith7majorcognitivethemes:fear;animals/plants;

brightlight;violence/persecution;deja-vu;family;recallingeventspost-CAand9%hadNDEs,while2%

describedawarenesswithexplicitrecallof‘seeing’and‘hearing’actualeventsrelatedtotheirresusci- tation.Onehadaverifiableperiodofconsciousawarenessduringwhichtimecerebralfunctionwasnot expected.

ASpanishtranslatedversionofthesummaryofthisarticleappearsasAppendixinthefinalonlineversionathttp://dx.doi.org/10.1016/j.resuscitation.2014.09.004.

Correspondingauthorat:DepartmentofMedicine,StateUniversityofNewYorkatStonyBrook,StonyBrookMedicalCenter,T17-040HealthSciencesCenter,Stony Brook,NY11794-8172,USA.

E-mailaddress:sam.parnia@stonybrookmedicine.edu(S.Parnia).

http://dx.doi.org/10.1016/j.resuscitation.2014.09.004 0300-9572/©2014ElsevierIrelandLtd.Allrightsreserved.

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Conclusions:CAsurvivorscommonlyexperienceabroadrangeofcognitivethemes,with2%exhibitingfull awareness.Thissupportsotherrecentstudiesthathaveindicatedconsciousnessmaybepresentdespite clinicallyundetectableconsciousness.ThistogetherwithfearfulexperiencesmaycontributetoPTSDand othercognitivedeficitspostCA.

©2014ElsevierIrelandLtd.Allrightsreserved.

1. Introduction

Theobservationthatsuccessfulcardiacarrest(CA)resuscita- tionisassociatedwithanumberofpsychologicalandcognitive outcomesincludingpost-traumaticstressdisorder,depressionand memorylossaswellasspecificmentalprocessesthatmayshare somesimilaritieswithawarenessduringanaesthesia,1,2hasraised thepossibilitythatawarenessmayalsooccurduringresuscitation fromCA.3 Inadditiontoauditoryperceptions,whicharecharac- teristicof awareness during anesthesia, CAsurvivors have also reportedexperiencingvivid visualperceptions,characterizedby theperceivedabilitytoobserveandrecallactualeventsoccurring aroundthem.4Althoughawarenessduringanesthesiaisassociated withdreamlikestates,thespecificmentalexperiencedescribedin associationwithCAisunknown.CApatientshavereportedvisual perceptionstogetherwithcognitiveand mentalactivityinclud- ingthoughtprocesses,reasoningandmemoryformation.3Patients havealsobeenreportedtorecallspecificdetailsrelatingtoevents thatwereoccurringduringresuscitation.4

Althoughtherehavebeenmanyanecdotalreportsofthisphe- nomenon,onlyahandfulofstudieshaveusedrigorousresearch methodologytoexaminethementalstatethatisassociatedwith CAresuscitation.4–7Thesestudieshaveexaminedthescientifically impreciseyet commonlyused termof ‘near-death experiences’

(NDE).3WhileNDEhavebeenreportedby10%ofCAsurvivors,3 theoverallbroadercognitive/mentalexperiencesassociatedwith CA,aswellasawareness,andtheassociationbetweenactualCA eventsandauditory/visualrecollectionofeventshasnotbeenstud- ied.Theprimaryaimofthisstudywastoexaminetheincidence ofawarenessandthebroadrangeofmentalexperiencesduring resuscitation.Thesecondaryaimwastoinvestigatethefeasibility ofestablishinganovelmethodologytotesttheaccuracyofreports ofvisualandauditoryperceptionandawarenessduringCA.

2. Methods

In this multicenter observational study, methods were ini- tially pilot tested at 5 hospitals prior to study start-up (01/2007–06/2008)atwhichpointthestudyteamrecruited15US, UKandAustrianhospitals(outofanoriginalselectedgroupof25) toparticipateindatacollection.Between07/2008and12/2012the firstgroupofCApatientswereenrolledintheAWAREstudy.These patientswereidentifiedusingalocalpagingsystemthatalerted stafftoCAevents.CApatientswereeligibleforstudyparticipation iftheymetthefollowinginclusioncriteria:

•CA as defined by cessation of heartbeat and respiration (in- hospital or out-of-hospital with on-going cardiopulmonary resuscitation(CPR)onarrivalattheemergencydepartment(ED)).

•Age>18years.

•Survivingpatientsdeemedfitforinterviewbytheirphysicians andcaregivers.

•Survivingpatientsprovidinginformedconsenttoparticipation.

Whenpossible,interviewswerecompletedbyaresearchnurse or physician while the CA survivor was still an inpatient. The

interviewers all underwent dedicated training regarding the interviewmethodologybythestudychief/principleinvestigator.

Informedconsentwasobtainedwhenpatientsweredeemedmed- icallyfittocompleteanin-personinterviewpriortodischarge.For patientswhocouldnotbeinterviewedduringtheirhospitalstay,a telephoneinterviewprotocolwasestablishedtoconsentandinter- viewthesepatientsbytelephonetominimizelossestofollowup.

Giventheseverityofthecondition,thestudyprovidedforalarge proportionofpatientsbeingunabletoparticipateduetoillhealth inthesamplesizecalculations.

Thestudyreceivedethicalapprovalateachparticipatingsite prior tothe start of data collection.Followingadvice fromthe ethicscommittee,a protocolwasimplementedtoavoid contac- tingindividualsnotinterviewedduringtheirhospitalstaywhodied afterhospitaldischarge.Deathregistriesandletterstothepatients’

doctorsrequestingpermissiontocontacttheirpatientswereimple- mented to identify patients who either died or should not be contacted.Ifnoobjectionsorconcernswereraisedandpatients werestillaliveafterdischarge,amemberoftheoriginalclinical teamsentanintroductorylettertogetherwithastampedaddressed enveloperequestingpermissiontocontactpatientsforthestudy whoweremissedwhileinhospital.Forthesepatientswhoagreed tobecontacted,amemberoftheresearchteam,obtainedinformed consent,andcompleteddatacollectionviathetelephone.However duetotheseverityofthemedicalcondition(andinparticularthe differinglevelsofphysicalimpairment)combinedwiththerequire- mentssetforth bytheethicscommitteefor contactingpatients (outlinedabove),thetimetotelephoneinterviewsfollowinghos- pitaldischargewasbetween3monthsand1year.Allin-hospital interviewswerecarriedoutpriortodischarge.Thesetookplace between3daysand4weeksaftercardiacarrestdependingonthe severityofthepatients’criticalillness.

Toassesstheaccuracyofclaimsofvisualawareness(VA)dur- ingCA,eachhospitalinstalledbetween50and100shelvesinareas whereCAresuscitationwasdeemedlikelytooccur(e.g.emergency department,acutemedicalwards).Eachshelfcontainedoneimage onlyvisiblefromabovetheshelf(theseweredifferentandincluded acombinationofnationalisticandreligioussymbols,people,ani- mals,andmajornewspaperheadlines).Theseimageswereinstalled topermitevaluation ofVA claimsdescribedin prior accounts.4 Theseincludetheperceptionofbeingabletoobservetheirown CAresuscitationfromavantagepointabove.Itwaspostulatedthat shouldalargeproportionofpatientsdescribeVAcombinedwith theperceptionofbeingabletoobserveeventsfromavantagepoint above,theshelves couldbeusedtopotentiallytestthevalidity ofsuchclaims(astheimageswereonlyvisibleiflookingdown fromtheceiling).1 Consideringtheseperceptionsmaybeoccur- ringafterbrainfunctionhasreturnedfollowingresuscitation,we

1Someresearchershaveproposedsuchrecollectionsandperceptionsarelikely illusory.Thismethodwasproposedasatooltotestthisparticularhypothesis.We consideredthistobeimportantasdespitewidespreadinterestnostudieshadobjec- tivelytestedthisclaim.Itwasconsideredthatshouldalargegroupofpatients withVAandtheabilitytoobserveeventsfromaboveconsistentlyfailtoidentify theimages,thiscouldsupportthehypothesisthattheexperienceshadoccurred throughadifferentmechanism(suchasillusions)tothatperceivedbythepatients themselves.

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alsoinstalledadifferentimage(triangle)ontheundersideofeach shelftotesttheaccuracyofVAbasedonthepossibilitythatpatients couldhavelookedupwardsafterCArecoveryorhadtheireyesopen duringCA.

Using a three stage interview process, patients were asked generalandfocusedquestionsabouttheirremembrancesduring cardiac arrest. Stage1 of the interviewsincluded demographic questionsaswellasgeneralquestionsontheperceptionofaware- nessandmemoriesduringCA.Stage2interviewsprobedfurther intothenatureoftheexperiencesusingscriptedopenendedques- tionsandthe16itemGreysonNDEscale.8ThisvalidatedNDEscale wasusedtodefineNDE’sinthisstudy.Foreachofthe16items intheNDEscale,responseswerescored0(notpresent),1(weakly present)or2(stronglypresent).Outofapossiblemaximumscoreof 32,aNDEwasconsideredpresentwithascoreof≥7,whileexpe- riences<7arenotcompatiblewithNDE.8 Patientswithdetailed auditoryandvisualrecollectionsrelating totheirperiodof car- diacarrestwereflaggedfor afurtherin-depthinterview (stage 3)toobtaindetailsoftheirexperience.Thislaterinterviewwas conductedbythestudyprincipalinvestigator(PI).

Using both the qualitative and quantitative data, patients’

memoriesandexperiences wereinitiallyclassifiedinto2broad categories:

(1)Noperceptionofawarenessand/ormemories.

(2)Perceptionofawarenessand/ormemories.

Based onpatient’sresponsestotheNDE scalethesecond categorywassubdividedintothreefurthercategories.

(3)Detailednon-NDEmemorieswithoutrecallandawarenessof CAevents.

(4)DetailedNDEmemorieswithoutrecall andawarenessofCA events.

(5)DetailedNDEmemorieswithdetailedauditoryand/orVAwith recallofCAevents.

Inordertoevaluateauditoryrecollectionsweproposedapro- tocoltointroduce “auditorystimuli”duringCAsimilartothose usedinstudiesofimplicitlearningduringanaesthesia.9Duringthe pilottestingphase,staffwereaskedtomentionthenamesofthree specificcitiesorcolorsandevaluatethesurvivors’abilitytorecall thesethroughexplicitorimplicitmemoryrecall,howeverunlike therelativelycontrolledenvironmentofanesthesia,stafffoundit impracticaltoadministerthesestimuliandthiswasthereforenot carriedforwardtothemainstudy.Patientswhoclaimedtohavehad visualandauditoryawareness(category5above)whetheridenti- fiedinhospitalorduringthetelephoneinterviewwereinvitedto completeanin-depthinterviewconductedbythestudyprincipal investigatortoobtainmoredetailsoftheirexperiences.

Both quantitative and qualitative data were analyzed in a descriptive manner. Potential confounders suchas age,gender andtimetointerviewwereevaluated.Summariesofthescripted interviews were reviewed and responses grouped based upon themesidentified.Potentialdifferencesindemographiccharacter- isticsbetweenreportinggroupswasevaluated.Agewascompared usingtwosamplet-testorWilcoxon’sranksumtestwhensample sizesweresmall.Genderwascomparedusingchi-squaretestor Fisher’sexacttestwhensamplesizesweresmall.Statisticalanal- ysiswascarriedoutusingStatXact-9(CytelInc.,Cambridge,MA) andSAS9.3(SASInstituteInc.,Cary,NC).

3. Results

A total of 2060 CA events were recorded with an average 16% (n=330) overall survival tohospital discharge. Of the 330 survivors, 140patients werefound eligible, provided informed

consent,andwereinterviewed.Fifty-twointerviewswerecom- pleted in-hospital and 90 afterdischarge.Two patientsrefused interview and theremaining 188 patientseither did not meet inclusioncriteria,diedafterhospitaldischarge,werenotdeemed suitableforfurtherfollowupbytheirphysicians,ordidnotrespond totheinvitationlettersforatelephonefollowup.Asummaryof studyparticipationandoutcomesisreportedinFig.1.Fromthe140 patientscompletingstage1oftheinterviewprocess,101patients (72%) went ontocomplete stage2 interviews.The39 patients unabletocompletebothstagesdidsopredominantlyduetofatigue.

Amongthoseinterviewed67%(n=95)weremen.Themeanage (±SD)was64±13years(range21–94).Afterstage1interview61%

(85/140)ofpatientsreportednoperceptionofawarenessormemo- ries(category1).Althoughnopatientdemonstratedclinicalsignsof consciousnessduringCPRasassessedbytheabsenceofeyeopening response,motorresponse,verbalresponsewhetherspontaneously orinresponsetopain(chestcompressions)witharesultantGlas- gowComaScaleScoreof3/15,nonetheless39%(55/140)(category 2)respondedpositivelytothequestion“Doyourememberany- thingfromthetimeduringyourunconsciousness”.Therewereno significantdifferenceswithrespecttoageorgenderbetweenthese twogroups.

Amongthe101patientswhocompletedstage2interviews,no differencesexistedbyageorgender.ResponsestotheNDEscaleare summarizedinTable1and46(46%)confirmedhavinghadnorecall, awarenessormemories. Theremaining55of101patientswith perceivedawarenessormemories(category2)weresubdivided further. Forty-sixdescribed memoriesincompatible withaNDE

Table1

ResponsestotheGreysonNDEScalea(numberandpercentrespondingpositively toeachofthe16scalequestionsb).

Question n %

(1)Didyouhavetheimpressionthat everythinghappenedfasterorslower thanusual?

27 27

(2)Wereyourthoughtsspeededup? 7 7

(3)Didscenesfromyourpastcomebackto you?

5 5

(4)Didyousuddenlyseemtounderstand everything?

6 6

(5)Didyouhaveafeelingofpeaceor pleasantness?

22 22

(6)Didyouhaveafeelingofjoy? 9 9

(7)Didyoufeelasenseofharmonyor unitywiththeuniverse?

5 5

(8)Didyousee,orfeelsurroundedby,a brilliantlight?

7 7

(9)Wereyoursensesmorevividthan usual?

13 13

(10)Didyouseemtobeawareofthings goingonthatnormallyshouldhavebeen outofsightfromyouractualpointof viewasifbyextrasensoryperception?

7 7

(11)Didscenesfromthefuturecometo you?

0 0

(12)Didyoufeelseparatedfromyour body?

13 13

(13)Didyouseemtoentersomeother, unearthlyworld?

7 7

(14)Didyouseemtoencounteramystical beingorpresence,orhearan

unidentifiablevoice?

8 8

(15)Didyouseedeceasedorreligious spirits?

3 3

(16)Didyoucometoaborderorpointof noreturn?

8 8

n=101.MeanGreysonscore±SD=2.02±3.71.Scorerange=0–22.

aThetotalisbaseduponindividualscompletingtheinstrument(101/142,72%).

bApositiveresponsewasdefinedasresponsesofeitherweaklyorstrongly presentforeachitem.

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Fig.1. Summaryofstudyenrollmentandoutcomes.

andwithoutrecallofCAevents(medianNDEscore=2)(IQR=3) (category3).Theremaining9of101patients(9%)hadexperiences compatiblewithNDE’s.Seven(7%)hadnoauditoryorvisualrecall ofCAevents(medianNDEscalescore=10(IQR=4),highestNDE score22)(category4).ThedetailedNDEaccountfromonepatient inthisgroupissummarizedinTable2.Theothertwopatients(2%) experiencedspecificauditory/visualawareness(category5).Both patients had suffered ventricular fibrillation (VF) in non-acute areaswhereshelveshadnotbeenplaced.Theirdescriptionsare summarizedinTable2.Bothwerecontactedforfurtherin-depth interviews to verify their experiences against documented CA events.Onewasunabletofollowupduetoillhealth.Theother,a 57yearoldmandescribedtheperceptionofobservingeventsfrom thetopcorneroftheroomandcontinuedtoexperienceasensa- tionoflookingdownfromabove.Heaccuratelydescribedpeople, sounds, and activities from his resuscitation (Table 2 provides quotesfromthisinterview).Hismedicalrecordscorroboratedhis accountsandspecificallysupportedhisdescriptionsandtheuseof anautomatedexternaldefibrillator(AED).BasedoncurrentAED algorithms,thislikelycorrespondedwithupto3minofconscious awarenessduringCAandCPR.2AsbothCAeventshadoccurredin non-acuteareaswithoutshelvesfurtheranalysisoftheaccuracyof VAbasedontheabilitytovisualizetheimagesaboveorbelowthe shelfwasnotpossible.Despitetheinstallationofapproximately

2 Aftertherecognitionofafirstshockablerhythm,thebuiltinAEDalgorithms requireatleast2minofCPRbeforeafurtherrhythmcheckisfollowedbyasec- onddefibrillationattemptifadvised.Addingintimeforanalysisoftherhythmand defibrillationitislikelytheperiodofCAwouldhavebeenatleast3min.

1000shelves across the participatinghospitalsonly 22% of CA eventsactuallytookplaceinthecriticalandacutemedicalwards wheretheshelveshadbeeninstalledandconsequentlyover78%

ofCAeventstookplaceinroomswithoutashelf.

While NDE’s provided a quantifiable measure of a patients’

cognitiverecollections in relationto CA,using ourCA survivor interviewtranscriptsaspartofstage2interviews,weevaluated thenarrativesofpatients’memory’swithoutNDE’s(NDEscale<7).

Althoughpriorstudieshadbyenlargefocusedontheoccurrence ofNDE’sinCAonly,howeverourobservationthatothercognitive themesasidefromNDE’salsoexistinCAledtoanevaluationofthe narrativesforotherspecificthemes.Narrativeswerecategorized into7themes:(1)fear;(2)animalsandplants;(3)abrightlight;(4) violenceorafeelingofbeingpersecuted;(5)dejavuexperiences;

(6) seeingfamily;(7)recalling eventsthat likelyoccurredafter recoveryfromCA.NarrativesarepresentedinTable3bytheme.

4. Discussion

OurdatasuggestthatCApatientsmayexperiencearangeofcog- nitiveprocessesthatrelatebothtotheCAandpost-resuscitation periods.Although,therelativelyhighproportionofpatientswho perceivedhavingmemoriesandawarenesswasunexpectedand shouldbe confirmedthrough future research,the fact thatthe observedfrequencyofNDE(9%)inourstudywasconsistentwith reportsfromprior studies(approximately 10%),4–7 mayprovide somemeasureofinternalvalidityforthisobservation.

Thefindingthatconsciousawarenessmaybepresentduring CAisintriguingandsupportsotherrecentstudiesthathaveindi- catedconsciousnessmaybepresentinpatientsdespiteclinically

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Table2

Categories4and5recollectionsfromstructuredinterviews.

Category4recollections

“Ihavecomebackfromtheothersideoflife...Godsent(me)back,itwas not(my)time—(I)hadmanythingstodo...(Itraveled)throughatunnel towardaverystronglight,whichdidn’tdazzleorhurt(my)eyes...there wereotherpeopleinthetunnelwhom(I)didnotrecognize.When(I) emerged(I)describedaverybeautifulcrystalcity...therewasariver thatranthroughthemiddleofthecity(with)themostcrystalclear waters.Thereweremanypeople,withoutfaces,whowerewashingin thewaters...thepeoplewereverybeautiful...therewasthemost beautifulsinging...(andIwas)movedtotears.(My)nextrecollection waslookingupatadoctordoingchestcompressions”.

Category5recollections Recollection#1

(Beforethecardiacarrest)“Iwasanswering(thenurse),butIcouldalso feelarealhardpressureonmygroin.Icouldfeelthepressure,couldn’t feelthepainoranythinglikethat,justrealhardpressure,likesomeone wasreallypushingdownonme.AndIwasstilltalkingto(thenurse)and thenallofasudden,Iwasn’t.Imusthave(blankedout)....butthenIcan remembervividlyanautomatedvoicesaying,“shockthepatient,shock thepatient,”andwiththat,upin(the)corneroftheroomtherewasa (woman)beckoningme...Icanrememberthinkingtomyself,“Ican’tget upthere”...shebeckonedme...Ifeltthatsheknewme,IfeltthatI couldtrusther,andIfeltshewasthereforareasonandIdidn’tknow whatthatwas...andthenextsecond,Iwasupthere,lookingdownat me,thenurse,andanothermanwhohadabaldhead...Icouldn’tseehis facebutIcouldseethebackofhisbody.Hewasquiteachunkyfella... Hehadbluescrubson,andhehadabluehat,butIcouldtellhedidn’t haveanyhair,becauseofwherethehatwas.

ThenextthingIrememberiswakingupon(the)bed.And(thenurse)said tome:“Ohyounoddedoff...youarebackwithusnow.”Whethershe saidthosewords,whetherthatautomatedvoicereallyhappened,Idon’t know....Icanrememberfeelingquiteeuphoric...

Iknowwho(themanwiththebluehadwas)...I(didn’t)knowhisfull name,but...hewasthemanthat...(Isaw)thenextday...Isawthis man[cometovisitme]andIknewwhoIhadseenthedaybefore.”

Post-scriptMedicalrecordreviewconfirmedtheuseoftheAED,the medicalteampresentduringthecardiacarrestandtherolethe identified“man”playedinrespondingtothecardiacarrest.

Recollection#2

“Atthebeginning,Ithink,Iheardthenursesay‘dial444cardiacarrest’.I feltscared.Iwasontheceilinglookingdown.IsawanursethatIdidnot knowbeforehandwhoIsawaftertheevent.Icouldseemybodyand saweverythingatonce.Isawmybloodpressurebeingtakenwhilstthe doctorwasputtingsomethingdownmythroat.Isawanursepumping onmychest...Isawbloodgasesandbloodsugarlevelsbeingtaken.”

undetectable consciousness.9–15 For instance, implicit learning with the absence of explicit recall has been demonstrated in patientswithundetectableconsciousness,9–13whileothershave demonstratedconscious awarenessduringpersistent vegetative states (PVS).14,15 Asthe relative contribution of implicit learn- ingand memoryin CAisunknownit remains unclearwhether therecalled experiences reflect thetotality of patients’ experi- ences orsimply thetip ofa deepericebergof experiences not recalled through explicit memory. It is intriguing to consider whetherpatientsmayhavegreaterconsciousactivityduringCA (andwhetherthisandfearfulexperiencesmayimpacttheoccur- renceofPTSD)thanisevidentthroughexplicitrecall,perhapsdue totheimpactofpost-resuscitationglobalcerebralinflammation and/orsedativesonmemoryconsolidation andrecall.However, theresultsofthisandotherstudies(outlinedabove)raisethepos- sibilitythatadditionalassessmentsmaybeneededtocomplement currentlyusedclinicaltestsofconsciousnessandawareness.

AlthoughtheetiologyofawarenessduringCAisunknown,the resultsofourstudyandinparticularourverifiedcaseofVAsug- gestitmaybedissimilartoawarenessduringanesthesia.While someinvestigatorshavehypothesizedtheremaybeabriefsurgeof electricalactivityaftercardiacstandstill,16incontrasttoanesthe- siatypicallythereisnomeasurablebrainfunctionwithinseconds aftercardiacstandstill.17–21This‘flatlined’isoelectricbrainstate

Table3

Majornon-NDEcognitivethemesrecalledbypatientsfollowingcardiacarrest.

Fear

“Iwasterrified.IwastoldIwasgoingtodieandthequickestwaywasto saythelastshortwordIcouldremember”

“BeingdraggedthroughdeepwaterwithabigringandIhate swimming—itwashorrid”.

“Ifeltscared”

Animalsandplants

“Allplants,noflowers”.

“Sawlionsandtigers”.

Brightlight

“Thesunwasshining”

“Recalledseeingagoldenflashoflight”

Family

“Familytalking10orso.Notbeingabletotalktothem”

“Myfamily(son,daughter,son-in-lawandwife)came”

Beingpersecutedorexperiencingviolence

“Beingdraggedthroughdeepwater”

“ThiswholeeventseemedfullofviolenceandIamnotaviolentman,it wasoutofcharacter”.

“Ihadtogothroughaceremonyand...theceremonywastoget burned.Therewere4menwithme,whicheverliedwoulddie....Isaw menincoffinsbeingburiedupright.

Dejavuexperiences

“...experiencedasenseofDe-javuandfeltlikeknewwhatpeoplewere goingtodobeforetheydiditafterthearrest.Thislastedabout3days”

Eventsoccurringafterinitialrecoveryfromcardiacarrest

Experienced...“atoothcomingoutwhentubewasremovedfrommy mouth”

which occurs with CAonset usually continues throughout CPR sinceinsufficientcerebralbloodflow(CBF)isachieved22tomeet cerebral metabolic requirements during conventional CPR.23–25 Howeveritwasestimatedourpatientmaintainedawarenessfor a number of minutes into CA.While certain deep coma states maylead toa selectiveabsence ofcorticalelectrical activityin thepresenceofdeeperbrainactivity,26thisseemsunlikelyduring CAasthis conditionisassociated withglobalratherthanselec- tivecorticalhypoperfusionasevidencedbythelossofbrainstem function.Thus,withinamodelthatassumesacausativerelation- shipbetweencorticalactivityandconsciousnesstheoccurrence ofmentalprocessesandtheabilitytoaccuratelydescribeevents during CA as occurred in our verified case of VA when cere- bralfunctionisordinarilyabsentoratbestseverelyimpairedis perplexing.27 This is particularlythe case as reductions in CBF typicallyleadtodeliriumfollowedbycoma,ratherthananaccurate andlucidmentalstate.28

Despitemanyanecdotalreportsandrecentstudiessupporting theoccurrenceofNDE’sandpossibleVAduringCA,thiswasthe firstlarge-scalestudytoinvestigatethefrequencyofawareness, whileattemptingtocorrelatepatients’claimsofVAwithevents thatoccurredduringcardiacarrest.Whilethelowincidence(2%)of explicitrecallofVAimpairedourabilitytouseimagestoobjectively examinethevalidityofspecificclaimsassociatedwithVA,nonethe- lessourverifiedcaseofVAsuggestsconsciousawarenessmayoccur beyondthefirst20–30safterCA(whensomeresidualbrainelec- tricalactivitymayoccur)16 while providing a quantifiabletime periodofawarenessafterthebrainordinarilyreachesanisolectric state.17–21Thecaseindicatestheexperiencelikelyoccurredduring CAratherthanafterrecoveryfromCAorbeforeCA.NoCBFwould beexpectedsinceunlikeventriculartachycardia,VFisincompatible withcardiaccontractilityparticularlyafterCPRhasstoppedduring arhythmcheck.29Although,similarexperienceshavebeencatego- rizedusingthescientificallyundefinedandimprecisetermofout ofbodyexperiences(OBE’s),andfurthercategorizedasautoscopy andopticalillusions,30–32ourstudysuggeststhatVAandveridical

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perceptionduringCAaredissimilartoautoscopysincepatientsdid notdescribeseeingtheirowndouble.4–7Furthermoreashalluci- nationsrefertoexperiencesthatdonotcorrespondwithobjective reality,ourfindingsdonotsuggestthatVAinCAislikelytobe hallucinatoryorillusorysincetherecollectionscorrespondedwith actualverifiedevents.Ourresultsalsohighlightlimitationswiththe categorizationofexperiencesinrelationtoCAashallucinatory,33 particularlyastherealityofhumanexperienceisnotdetermined neurologically.34,35Althoughalterationsinspecificneuromodu- latorsinvolvedwitheveryday“real”experiencescanalsoleadto illusionsorhallucinations,howeverthisdoesnotproveordisprove therealityofanyspecificexperiencewhetheritbelove,NDE’sor otherwise.34,35Infacttherealityofanyexperienceandthemeaning associatedwithitis determinedsocially(ratherthan neurolog- ically)throughasocialprocesswherebyhumansdetermineand ascribemeaningtophenomenonandexperiencewithinanygiven cultureorsociety(includingscientificgroupsandsocieties).34–35

Ourresultsprovidefurtherunderstandingofthebroadmental experiencethatlikelyaccompaniesdeathaftercirculatorystand- still.Asmostpatients’experienceswereincompatiblewithaNDE, thetermNDEwhilecommonlyusedmaybeinsufficienttodescribe theexperiencethatisassociatedwiththebiologicalprocessesof deathaftercirculatorystandstill.Futureresearchshouldfocuson thementalstateofCAanditsimpactonthelivesofsurvivorsas wellasitsrelationshipwithcognitivedeficitsincludingPTSD.Our dataalsosuggest,theexperienceofCAmaybedistinguishedfrom thetermNDE,whichhasmanyscientificlimitationsincludinga lackofauniversallyacceptedphysiologicaldefinitionofbeing‘near death’.34–36Thisimprecisionmaycontributetoongoingconflicting viewswithinthescientificcommunityregardingthesubject.36–39

Ourstudyhadanumberoflimitationsincludingthefactthatwe wereunabletoascertainwhetherpatients’responsetotheques- tionofhavingmemoriesduringCA(incategory1)trulyreflecteda perceptionofhavingmemoriesorpossiblydifficultieswithunder- standingthequestion.Anadditionallimitation wasthelimited numberofpatientswithexplicitrecallofCAeventswhosemem- oriescouldhavebeenfurtheranalyzed.Furthermoreowingtothe acuityandseverityofthecriticalillnessassociatedwithCA,the timetointerviewforpatientswasinvariablynotexactlythesame foreverypatient,whichmayhaveintroducedbiases(suchasrecall biasandconfabulation)intherecollections.Whilepre-placement ofvisualtargetsinresuscitationareasaimedattestingVAwasfea- siblefromapracticalviewpoint(therewerenoreportedadverse incidents),theobservationthat78%ofCAeventstookplaceinareas withoutshelvesillustratesthechallengeinobjectivelytestingthe claimsofVAinCAusingourproposedmethodology.Italsosuggests thatadifferentandmorerefinedmethodologymaybeneededto provideanobjectivevisualtargettoexaminethemechanismofVA andtheperceivedabilitytoobserveeventsduringCA.Although inthisstudythepotentialroleofcofounderssuchasage,gender andtimetointerviewwereevaluated,ourresultsindicatedawide variationin thesevariables. Consequently alargerstudy would bewarrantedtofurtherexplore therelationshipbetweenthese variableswithVA.Suchastudyshouldalsoexploretheimpactof variablesthatmayimpactthequalityofcerebralbloodflowand cerebralrecoverysuchasthedurationofCA,qualityofCPRduring CA,locationofCA(in-hospitalversusout-ofhospital),underlying rhythm,useofhypothermiaduringCAandafterROSC.

5. Conclusions

CAsurvivorsexperienceabroadrangeofmemoriesfollowing CPRincludingfearfulandpersecutoryexperiencesaswellasaware- ness.WhileexplicitrecallofVAisrare,itisunclearwhetherthese experiencescontributetolaterPTSD.Studiesarealsoneededto

delineatetheroleofexplicitandimplicit memoryfollowingCA andtheimpactofthisphenomenonontheoccurrenceofPTSDand otherlifeadjustmentsamongCAsurvivors.

Conflictofintereststatement

Noneoftheauthorshaveanyconflictsofinteresttodeclare.

Financialsupport

ResuscitationCouncil(UK),NourFoundation,BialFoundation.

Researchersworkedindependentofthefundingbodiesandthe studysponsor.Furthermore,thestudysponsordidnotparticipate instudydesign,analysisandinterpretationofresultsorthewriting ofthemanuscript.

Ethicalapproval

Thisstudyobtainedethicsapprovalsfromeach participating centerpriortothestartofrecruitmentanddatacollection.Each survivingpatientgaveinformedconsentpriortotheirbeinginter- viewed.

Datasharing

Allauthorseitherhadaccesstoallthedataortheopportunity toreviewalldata.

Transparencydeclaration

ISamParniaasleadauthoraffirmthatthemanuscriptisanhon- est,accurate,andtransparentaccountofthestudybeingreported and that noimportantaspects of thestudyhave been omitted andthatanydiscrepanciesfromthestudyasplannedhavebeen explained.

Acknowledgements

We acknowledgetheBiostatistical Consultation and support fromtheBiostatisticalConsultingCoreattheSchoolofMedicine, StonyBrookUniversityaswellasthehelpofDr’sRamkrishnaRam- nauth,VikasKaura,MarkandPatel,JasperBondad,MarkandPatel, GeorginaSpencer,Jade Tomlin,RavKaurShah,RebeccaGarrett, LauraWilson,IsmaaKhan,andJadeTomlinwiththestudy.

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