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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 夽
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
aaStonyBrookMedicalCenter,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.
夽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.
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.
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.
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
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-script–MedicalrecordreviewconfirmedtheuseoftheAED,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
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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