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Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
Resuscitation
xxx
(2014)
xxx–xxx
Contents
lists
available
at
ScienceDirect
Resuscitation
j
ourna
l
h
o
me
pa
g
e
:
www.elsevier.com/locate/resuscitation
Clinical
Paper
AWARE—AWAreness
during
REsuscitation—A
prospective
study夽
Sam
Parniaa,∗,
Ken
Spearpointb,
Gabriele
de
Vosc,
Peter
Fenwickd,
Diana
Goldberga,
Jie
Yanga,
Jiawen
Zhua,
Katie
Bakerd,
Hayley
Killingbacke,
Paula
McLeanf,
Melanie
Woodf,
A.
Maziar
Zafarig,
Neal
Dickertg,
Roland
Beisteinerh,
Fritz
Sterzh,
Michael
Bergerh,
Celia
Warlowi,
Siobhan
Bullocki,
Salli
Lovettj,
Russell
Metcalfe
Smith
McParak,
Sandra
Marti-Navarettel,
Pam
Cushingm,
Paul
Willsn,
Kayla
Harrisd,
Jenny
Suttono,
Anthony
Walmsleyp,
Charles
D.
Deakind,
Paul
Littled,
Mark
Farberq,
Bruce
Greysonr,
Elinor
R.
Schoenfelda
aStony
Brook
Medical
Center,
State
University
of
New
York
at
Stony
Brook,
NY,
USA
bHammersmith
Hospital
Imperial
College,
University
of
London,
UK
cMontefiore
Medical
Center,
New
York,
USA
dUniversity
Hospital
Southampton,
Southampton,
UK
eRoyal
Bournemouth
Hospital,
Bournemouth,
UK
fSt
Georges
Hospital,
University
of
London,
UK
gEmory
University
School
of
Medicine
&
Atlanta
Veterans
Affairs
Medical
Center,
Atlanta,
USA
hMedical
University
of
Vienna,
Austria
iNorthampton
General
Hospital,
Northampton,
UK
jLister
Hospital,
Stevenage,
UK
kCedar
Sinai,
USA
lCroydon
University
Hospital,
UK
mJames
Paget
Hospital,
UK
nAshford
&
St
Peters
NHS
Trust,
UK
oAddenbrookes
Hospital,
University
of
Cambridge,
UK
pEast
Sussex
Hospital,
East
Sussex,
UK
qIndiana
University,
Wishard
Memorial
Hospital,
Indianapolis,
USA
rUniversity
of
Virginia,
Charlottesville,
VA,
USA
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
28
June
2014
Received
in
revised
form
2
September
2014
Accepted
7
September
2014
Keywords:
Cardiac
arrest
Consciousness
Awareness
Near
death
experiences
Out
of
body
experiences
Post
traumatic
stress
disorder
Implicit
memory
Explicit
memory
a
b
s
t
r
a
c
t
Background:
Cardiac
arrest
(CA)
survivors
experience
cognitive
deficits
including
post-traumatic
stress
disorder
(PTSD).
It
is
unclear
whether
these
are
related
to
cognitive/mental
experiences
and
awareness
during
CPR.
Despite
anecdotal
reports
the
broad
range
of
cognitive/mental
experiences
and
awareness
associated
with
CPR
has
not
been
systematically
studied.
Methods:
The
incidence
and
validity
of
awareness
together
with
the
range,
characteristics
and
themes
relating
to
memories/cognitive
processes
during
CA
was
investigated
through
a
4
year
multi-center
observational
study
using
a
three
stage
quantitative
and
qualitative
interview
system.
The
feasibility
of
objectively
testing
the
accuracy
of
claims
of
visual
and
auditory
awareness
was
examined
using
spe-
cific
tests.
The
outcome
measures
were
(1)
awareness/memories
during
CA
and
(2)
objective
verification
of
claims
of
awareness
using
specific
tests.
Results:
Among
2060
CA
events,
140
survivors
completed
stage
1
interviews,
while
101
of
140
patients
completed
stage
2
interviews.
46%
had
memories
with
7
major
cognitive
themes:
fear;
animals/plants;
bright
light;
violence/persecution;
deja-vu;
family;
recalling
events
post-CA
and
9%
had
NDEs,
while
2%
described
awareness
with
explicit
recall
of
‘seeing’
and
‘hearing’
actual
events
related
to
their
resusci-
tation.
One
had
a
verifiable
period
of
conscious
awareness
during
which
time
cerebral
function
was
not
expected.
夽A
Spanish
translated
version
of
the
summary
of
this
article
appears
as
Appendix
in
the
final
online
version
at
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004.
∗Corresponding
author
at:
Department
of
Medicine,
State
University
of
New
York
at
Stony
Brook,
Stony
Brook
Medical
Center,
T17-040
Health
Sciences
Center,
Stony
Brook,
NY
11794-8172,
USA.
E-mail
address:
sam.parnia@stonybrookmedicine.edu
(S.
Parnia).
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
0300-9572/©
2014
Elsevier
Ireland
Ltd.
All
rights
reserved.
Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
2
S.
Parnia
et
al.
/
Resuscitation
xxx
(2014)
xxx–xxx
Conclusions:
CA
survivors
commonly
experience
a
broad
range
of
cognitive
themes,
with
2%
exhibiting
full
awareness.
This
supports
other
recent
studies
that
have
indicated
consciousness
may
be
present
despite
clinically
undetectable
consciousness.
This
together
with
fearful
experiences
may
contribute
to
PTSD
and
other
cognitive
deficits
post
CA.
©
2014
Elsevier
Ireland
Ltd.
All
rights
reserved.
1.
Introduction
The
observation
that
successful
cardiac
arrest
(CA)
resuscita-
tion
is
associated
with
a
number
of
psychological
and
cognitive
outcomes
including
post-traumatic
stress
disorder,
depression
and
memory
loss
as
well
as
specific
mental
processes
that
may
share
some
similarities
with
awareness
during
anaesthesia,1,2 has
raised
the
possibility
that
awareness
may
also
occur
during
resuscitation
from
CA.3In
addition
to
auditory
perceptions,
which
are
charac-
teristic
of
awareness
during
anesthesia,
CA
survivors
have
also
reported
experiencing
vivid
visual
perceptions,
characterized
by
the
perceived
ability
to
observe
and
recall
actual
events
occurring
around
them.4Although
awareness
during
anesthesia
is
associated
with
dream
like
states,
the
specific
mental
experience
described
in
association
with
CA
is
unknown.
CA
patients
have
reported
visual
perceptions
together
with
cognitive
and
mental
activity
includ-
ing
thought
processes,
reasoning
and
memory
formation.3Patients
have
also
been
reported
to
recall
specific
details
relating
to
events
that
were
occurring
during
resuscitation.4
Although
there
have
been
many
anecdotal
reports
of
this
phe-
nomenon,
only
a
handful
of
studies
have
used
rigorous
research
methodology
to
examine
the
mental
state
that
is
associated
with
CA
resuscitation.4–7 These
studies
have
examined
the
scientifically
imprecise
yet
commonly
used
term
of
‘near-death
experiences’
(NDE).3While
NDE
have
been
reported
by
10%
of
CA
survivors,3
the
overall
broader
cognitive/mental
experiences
associated
with
CA,
as
well
as
awareness,
and
the
association
between
actual
CA
events
and
auditory/visual
recollection
of
events
has
not
been
stud-
ied.
The
primary
aim
of
this
study
was
to
examine
the
incidence
of
awareness
and
the
broad
range
of
mental
experiences
during
resuscitation.
The
secondary
aim
was
to
investigate
the
feasibility
of
establishing
a
novel
methodology
to
test
the
accuracy
of
reports
of
visual
and
auditory
perception
and
awareness
during
CA.
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)
at
which
point
the
study
team
recruited
15
US,
UK
and
Austrian
hospitals
(out
of
an
original
selected
group
of
25)
to
participate
in
data
collection.
Between
07/2008
and
12/2012
the
first
group
of
CA
patients
were
enrolled
in
the
AWARE
study.
These
patients
were
identified
using
a
local
paging
system
that
alerted
staff
to
CA
events.
CA
patients
were
eligible
for
study
participation
if
they
met
the
following
inclusion
criteria:
•CA
as
defined
by
cessation
of
heartbeat
and
respiration
(in-
hospital
or
out-of-hospital
with
on-going
cardiopulmonary
resuscitation
(CPR)
on
arrival
at
the
emergency
department
(ED)).
•Age
>
18
years.
•Surviving
patients
deemed
fit
for
interview
by
their
physicians
and
caregivers.
•Surviving
patients
providing
informed
consent
to
participation.
When
possible,
interviews
were
completed
by
a
research
nurse
or
physician
while
the
CA
survivor
was
still
an
inpatient.
The
interviewers
all
underwent
dedicated
training
regarding
the
interview
methodology
by
the
study
chief/principle
investigator.
Informed
consent
was
obtained
when
patients
were
deemed
med-
ically
fit
to
complete
an
in-person
interview
prior
to
discharge.
For
patients
who
could
not
be
interviewed
during
their
hospital
stay,
a
telephone
interview
protocol
was
established
to
consent
and
inter-
view
these
patients
by
telephone
to
minimize
losses
to
follow
up.
Given
the
severity
of
the
condition,
the
study
provided
for
a
large
proportion
of
patients
being
unable
to
participate
due
to
ill
health
in
the
sample
size
calculations.
The
study
received
ethical
approval
at
each
participating
site
prior
to
the
start
of
data
collection.
Following
advice
from
the
ethics
committee,
a
protocol
was
implemented
to
avoid
contac-
ting
individuals
not
interviewed
during
their
hospital
stay
who
died
after
hospital
discharge.
Death
registries
and
letters
to
the
patients’
doctors
requesting
permission
to
contact
their
patients
were
imple-
mented
to
identify
patients
who
either
died
or
should
not
be
contacted.
If
no
objections
or
concerns
were
raised
and
patients
were
still
alive
after
discharge,
a
member
of
the
original
clinical
team
sent
an
introductory
letter
together
with
a
stamped
addressed
envelope
requesting
permission
to
contact
patients
for
the
study
who
were
missed
while
in
hospital.
For
these
patients
who
agreed
to
be
contacted,
a
member
of
the
research
team,
obtained
informed
consent,
and
completed
data
collection
via
the
telephone.
However
due
to
the
severity
of
the
medical
condition
(and
in
particular
the
differing
levels
of
physical
impairment)
combined
with
the
require-
ments
set
forth
by
the
ethics
committee
for
contacting
patients
(outlined
above),
the
time
to
telephone
interviews
following
hos-
pital
discharge
was
between
3
months
and
1
year.
All
in-hospital
interviews
were
carried
out
prior
to
discharge.
These
took
place
between
3
days
and
4
weeks
after
cardiac
arrest
depending
on
the
severity
of
the
patients’
critical
illness.
To
assess
the
accuracy
of
claims
of
visual
awareness
(VA)
dur-
ing
CA,
each
hospital
installed
between
50
and
100
shelves
in
areas
where
CA
resuscitation
was
deemed
likely
to
occur
(e.g.
emergency
department,
acute
medical
wards).
Each
shelf
contained
one
image
only
visible
from
above
the
shelf
(these
were
different
and
included
a
combination
of
nationalistic
and
religious
symbols,
people,
ani-
mals,
and
major
newspaper
headlines).
These
images
were
installed
to
permit
evaluation
of
VA
claims
described
in
prior
accounts.4
These
include
the
perception
of
being
able
to
observe
their
own
CA
resuscitation
from
a
vantage
point
above.
It
was
postulated
that
should
a
large
proportion
of
patients
describe
VA
combined
with
the
perception
of
being
able
to
observe
events
from
a
vantage
point
above,
the
shelves
could
be
used
to
potentially
test
the
validity
of
such
claims
(as
the
images
were
only
visible
if
looking
down
from
the
ceiling).1Considering
these
perceptions
may
be
occur-
ring
after
brain
function
has
returned
following
resuscitation,
we
1Some
researchers
have
proposed
such
recollections
and
perceptions
are
likely
illusory.
This
method
was
proposed
as
a
tool
to
test
this
particular
hypothesis.
We
considered
this
to
be
important
as
despite
widespread
interest
no
studies
had
objec-
tively
tested
this
claim.
It
was
considered
that
should
a
large
group
of
patients
with
VA
and
the
ability
to
observe
events
from
above
consistently
fail
to
identify
the
images,
this
could
support
the
hypothesis
that
the
experiences
had
occurred
through
a
different
mechanism
(such
as
illusions)
to
that
perceived
by
the
patients
themselves.
Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
S.
Parnia
et
al.
/
Resuscitation
xxx
(2014)
xxx–xxx
3
also
installed
a
different
image
(triangle)
on
the
underside
of
each
shelf
to
test
the
accuracy
of
VA
based
on
the
possibility
that
patients
could
have
looked
upwards
after
CA
recovery
or
had
their
eyes
open
during
CA.
Using
a
three
stage
interview
process,
patients
were
asked
general
and
focused
questions
about
their
remembrances
during
cardiac
arrest.
Stage
1
of
the
interviews
included
demographic
questions
as
well
as
general
questions
on
the
perception
of
aware-
ness
and
memories
during
CA.
Stage
2
interviews
probed
further
into
the
nature
of
the
experiences
using
scripted
open
ended
ques-
tions
and
the
16
item
Greyson
NDE
scale.8This
validated
NDE
scale
was
used
to
define
NDE’s
in
this
study.
For
each
of
the
16
items
in
the
NDE
scale,
responses
were
scored
0
(not
present),
1
(weakly
present)
or
2
(strongly
present).
Out
of
a
possible
maximum
score
of
32,
a
NDE
was
considered
present
with
a
score
of
≥7,
while
expe-
riences
<7
are
not
compatible
with
NDE.8Patients
with
detailed
auditory
and
visual
recollections
relating
to
their
period
of
car-
diac
arrest
were
flagged
for
a
further
in-depth
interview
(stage
3)
to
obtain
details
of
their
experience.
This
later
interview
was
conducted
by
the
study
principal
investigator
(PI).
Using
both
the
qualitative
and
quantitative
data,
patients’
memories
and
experiences
were
initially
classified
into
2
broad
categories:
(1)
No
perception
of
awareness
and/or
memories.
(2)
Perception
of
awareness
and/or
memories.
Based
on
patient’s
responses
to
the
NDE
scale
the
second
category
was
subdivided
into
three
further
categories.
(3)
Detailed
non-NDE
memories
without
recall
and
awareness
of
CA
events.
(4)
Detailed
NDE
memories
without
recall
and
awareness
of
CA
events.
(5)
Detailed
NDE
memories
with
detailed
auditory
and/or
VA
with
recall
of
CA
events.
In
order
to
evaluate
auditory
recollections
we
proposed
a
pro-
tocol
to
introduce
“auditory
stimuli”
during
CA
similar
to
those
used
in
studies
of
implicit
learning
during
anaesthesia.9During
the
pilot
testing
phase,
staff
were
asked
to
mention
the
names
of
three
specific
cities
or
colors
and
evaluate
the
survivors’
ability
to
recall
these
through
explicit
or
implicit
memory
recall,
however
unlike
the
relatively
controlled
environment
of
anesthesia,
staff
found
it
impractical
to
administer
these
stimuli
and
this
was
therefore
not
carried
forward
to
the
main
study.
Patients
who
claimed
to
have
had
visual
and
auditory
awareness
(category
5
above)
whether
identi-
fied
in
hospital
or
during
the
telephone
interview
were
invited
to
complete
an
in-depth
interview
conducted
by
the
study
principal
investigator
to
obtain
more
details
of
their
experiences.
Both
quantitative
and
qualitative
data
were
analyzed
in
a
descriptive
manner.
Potential
confounders
such
as
age,
gender
and
time
to
interview
were
evaluated.
Summaries
of
the
scripted
interviews
were
reviewed
and
responses
grouped
based
upon
themes
identified.
Potential
differences
in
demographic
character-
istics
between
reporting
groups
was
evaluated.
Age
was
compared
using
two
sample
t-test
or
Wilcoxon’s
rank
sum
test
when
sample
sizes
were
small.
Gender
was
compared
using
chi-square
test
or
Fisher’s
exact
test
when
sample
sizes
were
small.
Statistical
anal-
ysis
was
carried
out
using
StatXact-9
(Cytel
Inc.,
Cambridge,
MA)
and
SAS
9.3
(SAS
Institute
Inc.,
Cary,
NC).
3.
Results
A
total
of
2060
CA
events
were
recorded
with
an
average
16%
(n
=
330)
overall
survival
to
hospital
discharge.
Of
the
330
survivors,
140
patients
were
found
eligible,
provided
informed
consent,
and
were
interviewed.
Fifty-two
interviews
were
com-
pleted
in-hospital
and
90
after
discharge.
Two
patients
refused
interview
and
the
remaining
188
patients
either
did
not
meet
inclusion
criteria,
died
after
hospital
discharge,
were
not
deemed
suitable
for
further
follow
up
by
their
physicians,
or
did
not
respond
to
the
invitation
letters
for
a
telephone
follow
up.
A
summary
of
study
participation
and
outcomes
is
reported
in
Fig.
1.
From
the
140
patients
completing
stage
1
of
the
interview
process,
101
patients
(72%)
went
on
to
complete
stage
2
interviews.
The
39
patients
unable
to
complete
both
stages
did
so
predominantly
due
to
fatigue.
Among
those
interviewed
67%
(n
=
95)
were
men.
The
mean
age
(±SD)
was
64
±
13
years
(range
21–94).
After
stage
1
interview
61%
(85/140)
of
patients
reported
no
perception
of
awareness
or
memo-
ries
(category
1).
Although
no
patient
demonstrated
clinical
signs
of
consciousness
during
CPR
as
assessed
by
the
absence
of
eye
opening
response,
motor
response,
verbal
response
whether
spontaneously
or
in
response
to
pain
(chest
compressions)
with
a
resultant
Glas-
gow
Coma
Scale
Score
of
3/15,
nonetheless
39%
(55/140)
(category
2)
responded
positively
to
the
question
“Do
you
remember
any-
thing
from
the
time
during
your
unconsciousness”.
There
were
no
significant
differences
with
respect
to
age
or
gender
between
these
two
groups.
Among
the
101
patients
who
completed
stage
2
interviews,
no
differences
existed
by
age
or
gender.
Responses
to
the
NDE
scale
are
summarized
in
Table
1
and
46
(46%)
confirmed
having
had
no
recall,
awareness
or
memories.
The
remaining
55
of
101
patients
with
perceived
awareness
or
memories
(category
2)
were
subdivided
further.
Forty-six
described
memories
incompatible
with
a
NDE
Table
1
Responses
to
the
Greyson
NDE
Scalea(number
and
percent
responding
positively
to
each
of
the
16
scale
questionsb).
Question
n
%
(1)
Did
you
have
the
impression
that
everything
happened
faster
or
slower
than
usual?
27
27
(2)
Were
your
thoughts
speeded
up? 7
7
(3)
Did
scenes
from
your
past
come
back
to
you?
5
5
(4)
Did
you
suddenly
seem
to
understand
everything?
6
6
(5)
Did
you
have
a
feeling
of
peace
or
pleasantness?
22
22
(6)
Did
you
have
a
feeling
of
joy?
9
9
(7)
Did
you
feel
a
sense
of
harmony
or
unity
with
the
universe?
5
5
(8)
Did
you
see,
or
feel
surrounded
by,
a
brilliant
light?
7
7
(9)
Were
your
senses
more
vivid
than
usual?
13
13
(10)
Did
you
seem
to
be
aware
of
things
going
on
that
normally
should
have
been
out
of
sight
from
your
actual
point
of
view
as
if
by
extrasensory
perception?
7
7
(11)
Did
scenes
from
the
future
come
to
you?
0
0
(12)
Did
you
feel
separated
from
your
body?
13
13
(13)
Did
you
seem
to
enter
some
other,
unearthly
world?
7
7
(14)
Did
you
seem
to
encounter
a
mystical
being
or
presence,
or
hear
an
unidentifiable
voice?
8
8
(15)
Did
you
see
deceased
or
religious
spirits?
3
3
(16)
Did
you
come
to
a
border
or
point
of
no
return?
8
8
n
=
101.
Mean
Greyson
score
±
SD
=
2.02
±
3.71.
Score
range
=
0–22.
aThe
total
is
based
upon
individuals
completing
the
instrument
(101/142,
72%).
bA
positive
response
was
defined
as
responses
of
either
weakly
or
strongly
present
for
each
item.
Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
4
S.
Parnia
et
al.
/
Resuscitation
xxx
(2014)
xxx–xxx
Fig.
1.
Summary
of
study
enrollment
and
outcomes.
and
without
recall
of
CA
events
(median
NDE
score
=
2)
(IQR
=
3)
(category
3).
The
remaining
9
of
101
patients
(9%)
had
experiences
compatible
with
NDE’s.
Seven
(7%)
had
no
auditory
or
visual
recall
of
CA
events
(median
NDE
scale
score
=
10
(IQR
=
4),
highest
NDE
score
22)
(category
4).
The
detailed
NDE
account
from
one
patient
in
this
group
is
summarized
in
Table
2.
The
other
two
patients
(2%)
experienced
specific
auditory/visual
awareness
(category
5).
Both
patients
had
suffered
ventricular
fibrillation
(VF)
in
non-acute
areas
where
shelves
had
not
been
placed.
Their
descriptions
are
summarized
in
Table
2.
Both
were
contacted
for
further
in-depth
interviews
to
verify
their
experiences
against
documented
CA
events.
One
was
unable
to
follow
up
due
to
ill
health.
The
other,
a
57
year
old
man
described
the
perception
of
observing
events
from
the
top
corner
of
the
room
and
continued
to
experience
a
sensa-
tion
of
looking
down
from
above.
He
accurately
described
people,
sounds,
and
activities
from
his
resuscitation
(Table
2
provides
quotes
from
this
interview).
His
medical
records
corroborated
his
accounts
and
specifically
supported
his
descriptions
and
the
use
of
an
automated
external
defibrillator
(AED).
Based
on
current
AED
algorithms,
this
likely
corresponded
with
up
to
3
min
of
conscious
awareness
during
CA
and
CPR.2As
both
CA
events
had
occurred
in
non-acute
areas
without
shelves
further
analysis
of
the
accuracy
of
VA
based
on
the
ability
to
visualize
the
images
above
or
below
the
shelf
was
not
possible.
Despite
the
installation
of
approximately
2After
the
recognition
of
a
first
shockable
rhythm,
the
built
in
AED
algorithms
require
at
least
2
min
of
CPR
before
a
further
rhythm
check
is
followed
by
a
sec-
ond
defibrillation
attempt
if
advised.
Adding
in
time
for
analysis
of
the
rhythm
and
defibrillation
it
is
likely
the
period
of
CA
would
have
been
at
least
3
min.
1000
shelves
across
the
participating
hospitals
only
22%
of
CA
events
actually
took
place
in
the
critical
and
acute
medical
wards
where
the
shelves
had
been
installed
and
consequently
over
78%
of
CA
events
took
place
in
rooms
without
a
shelf.
While
NDE’s
provided
a
quantifiable
measure
of
a
patients’
cognitive
recollections
in
relation
to
CA,
using
our
CA
survivor
interview
transcripts
as
part
of
stage
2
interviews,
we
evaluated
the
narratives
of
patients’
memory’s
without
NDE’s
(NDE
scale
<
7).
Although
prior
studies
had
by
enlarge
focused
on
the
occurrence
of
NDE’s
in
CA
only,
however
our
observation
that
other
cognitive
themes
aside
from
NDE’s
also
exist
in
CA
led
to
an
evaluation
of
the
narratives
for
other
specific
themes.
Narratives
were
categorized
into
7
themes:
(1)
fear;
(2)
animals
and
plants;
(3)
a
bright
light;
(4)
violence
or
a
feeling
of
being
persecuted;
(5)
deja
vu
experiences;
(6)
seeing
family;
(7)
recalling
events
that
likely
occurred
after
recovery
from
CA.
Narratives
are
presented
in
Table
3
by
theme.
4.
Discussion
Our
data
suggest
that
CA
patients
may
experience
a
range
of
cog-
nitive
processes
that
relate
both
to
the
CA
and
post-resuscitation
periods.
Although,
the
relatively
high
proportion
of
patients
who
perceived
having
memories
and
awareness
was
unexpected
and
should
be
confirmed
through
future
research,
the
fact
that
the
observed
frequency
of
NDE
(9%)
in
our
study
was
consistent
with
reports
from
prior
studies
(approximately
10%),4–7 may
provide
some
measure
of
internal
validity
for
this
observation.
The
finding
that
conscious
awareness
may
be
present
during
CA
is
intriguing
and
supports
other
recent
studies
that
have
indi-
cated
consciousness
may
be
present
in
patients
despite
clinically
Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
S.
Parnia
et
al.
/
Resuscitation
xxx
(2014)
xxx–xxx
5
Table
2
Categories
4
and
5
recollections
from
structured
interviews.
Category
4
recollections
“I
have
come
back
from
the
other
side
of
life.
.
.God
sent
(me)
back,
it
was
not
(my)
time—(I)
had
many
things
to
do.
.
.(I
traveled)
through
a
tunnel
toward
a
very
strong
light,
which
didn’t
dazzle
or
hurt
(my)
eyes.
.
.there
were
other
people
in
the
tunnel
whom
(I)
did
not
recognize.
When
(I)
emerged
(I)
described
a
very
beautiful
crystal
city.
.
.
there
was
a
river
that
ran
through
the
middle
of
the
city
(with)
the
most
crystal
clear
waters.
There
were
many
people,
without
faces,
who
were
washing
in
the
waters.
.
.the
people
were
very
beautiful.
.
.
there
was
the
most
beautiful
singing.
.
.(and
I
was)
moved
to
tears.
(My)
next
recollection
was
looking
up
at
a
doctor
doing
chest
compressions”.
Category
5
recollections
Recollection
#
1
(Before
the
cardiac
arrest)
“I
was
answering
(the
nurse),
but
I
could
also
feel
a
real
hard
pressure
on
my
groin.
I
could
feel
the
pressure,
couldn’t
feel
the
pain
or
anything
like
that,
just
real
hard
pressure,
like
someone
was
really
pushing
down
on
me.
And
I
was
still
talking
to
(the
nurse)
and
then
all
of
a
sudden,
I
wasn’t.
I
must
have
(blanked
out).
.
..but
then
I
can
remember
vividly
an
automated
voice
saying,
“shock
the
patient,
shock
the
patient,”
and
with
that,
up
in
(the)
corner
of
the
room
there
was
a
(woman)
beckoning
me.
.
.I
can
remember
thinking
to
myself,
“I
can’t
get
up
there”.
.
.she
beckoned
me.
.
.
I
felt
that
she
knew
me,
I
felt
that
I
could
trust
her,
and
I
felt
she
was
there
for
a
reason
and
I
didn’t
know
what
that
was.
.
.and
the
next
second,
I
was
up
there,
looking
down
at
me,
the
nurse,
and
another
man
who
had
a
bald
head.
.
.I
couldn’t
see
his
face
but
I
could
see
the
back
of
his
body.
He
was
quite
a
chunky
fella.
.
.
He
had
blue
scrubs
on,
and
he
had
a
blue
hat,
but
I
could
tell
he
didn’t
have
any
hair,
because
of
where
the
hat
was.
The
next
thing
I
remember
is
waking
up
on
(the)
bed.
And
(the
nurse)
said
to
me:
“Oh
you
nodded
off.
.
.you
are
back
with
us
now.”
Whether
she
said
those
words,
whether
that
automated
voice
really
happened,
I
don’t
know.
.
..
I
can
remember
feeling
quite
euphoric.
.
.
I
know
who
(the
man
with
the
blue
had
was).
.
.I
(didn’t)
know
his
full
name,
but.
.
.he
was
the
man
that.
.
.(I
saw)
the
next
day.
.
.I
saw
this
man
[come
to
visit
me]
and
I
knew
who
I
had
seen
the
day
before.”
Post-script
–
Medical
record
review
confirmed
the
use
of
the
AED,
the
medical
team
present
during
the
cardiac
arrest
and
the
role
the
identified
“man”
played
in
responding
to
the
cardiac
arrest.
Recollection
#
2
“At
the
beginning,
I
think,
I
heard
the
nurse
say
‘dial
444
cardiac
arrest’.
I
felt
scared.
I
was
on
the
ceiling
looking
down.
I
saw
a
nurse
that
I
did
not
know
beforehand
who
I
saw
after
the
event.
I
could
see
my
body
and
saw
everything
at
once.
I
saw
my
blood
pressure
being
taken
whilst
the
doctor
was
putting
something
down
my
throat.
I
saw
a
nurse
pumping
on
my
chest.
.
.I
saw
blood
gases
and
blood
sugar
levels
being
taken.”
undetectable
consciousness.9–15 For
instance,
implicit
learning
with
the
absence
of
explicit
recall
has
been
demonstrated
in
patients
with
undetectable
consciousness,9–13 while
others
have
demonstrated
conscious
awareness
during
persistent
vegetative
states
(PVS).14,15 As
the
relative
contribution
of
implicit
learn-
ing
and
memory
in
CA
is
unknown
it
remains
unclear
whether
the
recalled
experiences
reflect
the
totality
of
patients’
experi-
ences
or
simply
the
tip
of
a
deeper
iceberg
of
experiences
not
recalled
through
explicit
memory.
It
is
intriguing
to
consider
whether
patients
may
have
greater
conscious
activity
during
CA
(and
whether
this
and
fearful
experiences
may
impact
the
occur-
rence
of
PTSD)
than
is
evident
through
explicit
recall,
perhaps
due
to
the
impact
of
post-resuscitation
global
cerebral
inflammation
and/or
sedatives
on
memory
consolidation
and
recall.
However,
the
results
of
this
and
other
studies
(outlined
above)
raise
the
pos-
sibility
that
additional
assessments
may
be
needed
to
complement
currently
used
clinical
tests
of
consciousness
and
awareness.
Although
the
etiology
of
awareness
during
CA
is
unknown,
the
results
of
our
study
and
in
particular
our
verified
case
of
VA
sug-
gest
it
may
be
dissimilar
to
awareness
during
anesthesia.
While
some
investigators
have
hypothesized
there
may
be
a
brief
surge
of
electrical
activity
after
cardiac
standstill,16 in
contrast
to
anesthe-
sia
typically
there
is
no
measurable
brain
function
within
seconds
after
cardiac
standstill.17–21 This
‘flatlined’
isoelectric
brain
state
Table
3
Major
non-NDE
cognitive
themes
recalled
by
patients
following
cardiac
arrest.
Fear
“I
was
terrified.
I
was
told
I
was
going
to
die
and
the
quickest
way
was
to
say
the
last
short
word
I
could
remember”
“Being
dragged
through
deep
water
with
a
big
ring
and
I
hate
swimming—it
was
horrid”.
“I
felt
scared”
Animals
and
plants
“All
plants,
no
flowers”.
“Saw
lions
and
tigers”.
Bright
light
“The
sun
was
shining”
“Recalled
seeing
a
golden
flash
of
light”
Family
“Family
talking
10
or
so.
Not
being
able
to
talk
to
them”
“My
family
(son,
daughter,
son-in-law
and
wife)
came”
Being
persecuted
or
experiencing
violence
“Being
dragged
through
deep
water”
“This
whole
event
seemed
full
of
violence
and
I
am
not
a
violent
man,
it
was
out
of
character”.
“I
had
to
go
through
a
ceremony
and
.
.
.
the
ceremony
was
to
get
burned.
There
were
4
men
with
me,
whichever
lied
would
die.
.
..
I
saw
men
in
coffins
being
buried
upright.
Deja
vu
experiences
“.
.
.experienced
a
sense
of
De-ja
vu
and
felt
like
knew
what
people
were
going
to
do
before
they
did
it
after
the
arrest.
This
lasted
about
3
days”
Events
occurring
after
initial
recovery
from
cardiac
arrest
Experienced
.
.
.“a
tooth
coming
out
when
tube
was
removed
from
my
mouth”
which
occurs
with
CA
onset
usually
continues
throughout
CPR
since
insufficient
cerebral
blood
flow
(CBF)
is
achieved22 to
meet
cerebral
metabolic
requirements
during
conventional
CPR.23–25
However
it
was
estimated
our
patient
maintained
awareness
for
a
number
of
minutes
into
CA.
While
certain
deep
coma
states
may
lead
to
a
selective
absence
of
cortical
electrical
activity
in
the
presence
of
deeper
brain
activity,26 this
seems
unlikely
during
CA
as
this
condition
is
associated
with
global
rather
than
selec-
tive
cortical
hypoperfusion
as
evidenced
by
the
loss
of
brain
stem
function.
Thus,
within
a
model
that
assumes
a
causative
relation-
ship
between
cortical
activity
and
consciousness
the
occurrence
of
mental
processes
and
the
ability
to
accurately
describe
events
during
CA
as
occurred
in
our
verified
case
of
VA
when
cere-
bral
function
is
ordinarily
absent
or
at
best
severely
impaired
is
perplexing.27 This
is
particularly
the
case
as
reductions
in
CBF
typically
lead
to
delirium
followed
by
coma,
rather
than
an
accurate
and
lucid
mental
state.28
Despite
many
anecdotal
reports
and
recent
studies
supporting
the
occurrence
of
NDE’s
and
possible
VA
during
CA,
this
was
the
first
large-scale
study
to
investigate
the
frequency
of
awareness,
while
attempting
to
correlate
patients’
claims
of
VA
with
events
that
occurred
during
cardiac
arrest.
While
the
low
incidence
(2%)
of
explicit
recall
of
VA
impaired
our
ability
to
use
images
to
objectively
examine
the
validity
of
specific
claims
associated
with
VA,
nonethe-
less
our
verified
case
of
VA
suggests
conscious
awareness
may
occur
beyond
the
first
20–30
s
after
CA
(when
some
residual
brain
elec-
trical
activity
may
occur)16 while
providing
a
quantifiable
time
period
of
awareness
after
the
brain
ordinarily
reaches
an
isolectric
state.17–21 The
case
indicates
the
experience
likely
occurred
during
CA
rather
than
after
recovery
from
CA
or
before
CA.
No
CBF
would
be
expected
since
unlike
ventricular
tachycardia,
VF
is
incompatible
with
cardiac
contractility
particularly
after
CPR
has
stopped
during
a
rhythm
check.29 Although,
similar
experiences
have
been
catego-
rized
using
the
scientifically
undefined
and
imprecise
term
of
out
of
body
experiences
(OBE’s),
and
further
categorized
as
autoscopy
and
optical
illusions,30–32 our
study
suggests
that
VA
and
veridical
Please
cite
this
article
in
press
as:
Parnia
S,
et
al.
AWARE—AWAreness
during
REsuscitation—A
prospective
study.
Resuscitation
(2014),
http://dx.doi.org/10.1016/j.resuscitation.2014.09.004
ARTICLE IN PRESS
G Model
RESUS-6129;
No.
of
Pages
7
6
S.
Parnia
et
al.
/
Resuscitation
xxx
(2014)
xxx–xxx
perception
during
CA
are
dissimilar
to
autoscopy
since
patients
did
not
describe
seeing
their
own
double.4–7 Furthermore
as
halluci-
nations
refer
to
experiences
that
do
not
correspond
with
objective
reality,
our
findings
do
not
suggest
that
VA
in
CA
is
likely
to
be
hallucinatory
or
illusory
since
the
recollections
corresponded
with
actual
verified
events.
Our
results
also
highlight
limitations
with
the
categorization
of
experiences
in
relation
to
CA
as
hallucinatory,33
particularly
as
the
reality
of
human
experience
is
not
determined
neurologically.34,35 Although
alterations
in
specific
neuro
modu-
lators
involved
with
every
day
“real”
experiences
can
also
lead
to
illusions
or
hallucinations,
however
this
does
not
prove
or
disprove
the
reality
of
any
specific
experience
whether
it
be
love,
NDE’s
or
otherwise.34,35 In
fact
the
reality
of
any
experience
and
the
meaning
associated
with
it
is
determined
socially
(rather
than
neurolog-
ically)
through
a
social
process
whereby
humans
determine
and
ascribe
meaning
to
phenomenon
and
experience
within
any
given
culture
or
society
(including
scientific
groups
and
societies).34–35
Our
results
provide
further
understanding
of
the
broad
mental
experience
that
likely
accompanies
death
after
circulatory
stand-
still.
As
most
patients’
experiences
were
incompatible
with
a
NDE,
the
term
NDE
while
commonly
used
may
be
insufficient
to
describe
the
experience
that
is
associated
with
the
biological
processes
of
death
after
circulatory
standstill.
Future
research
should
focus
on
the
mental
state
of
CA
and
its
impact
on
the
lives
of
survivors
as
well
as
its
relationship
with
cognitive
deficits
including
PTSD.
Our
data
also
suggest,
the
experience
of
CA
may
be
distinguished
from
the
term
NDE,
which
has
many
scientific
limitations
including
a
lack
of
a
universally
accepted
physiological
definition
of
being
‘near
death’.34–36 This
imprecision
may
contribute
to
ongoing
conflicting
views
within
the
scientific
community
regarding
the
subject.36–39
Our
study
had
a
number
of
limitations
including
the
fact
that
we
were
unable
to
ascertain
whether
patients’
response
to
the
ques-
tion
of
having
memories
during
CA
(in
category
1)
truly
reflected
a
perception
of
having
memories
or
possibly
difficulties
with
under-
standing
the
question.
An
additional
limitation
was
the
limited
number
of
patients
with
explicit
recall
of
CA
events
whose
mem-
ories
could
have
been
further
analyzed.
Furthermore
owing
to
the
acuity
and
severity
of
the
critical
illness
associated
with
CA,
the
time
to
interview
for
patients
was
invariably
not
exactly
the
same
for
every
patient,
which
may
have
introduced
biases
(such
as
recall
bias
and
confabulation)
in
the
recollections.
While
pre-placement
of
visual
targets
in
resuscitation
areas
aimed
at
testing
VA
was
fea-
sible
from
a
practical
viewpoint
(there
were
no
reported
adverse
incidents),
the
observation
that
78%
of
CA
events
took
place
in
areas
without
shelves
illustrates
the
challenge
in
objectively
testing
the
claims
of
VA
in
CA
using
our
proposed
methodology.
It
also
suggests
that
a
different
and
more
refined
methodology
may
be
needed
to
provide
an
objective
visual
target
to
examine
the
mechanism
of
VA
and
the
perceived
ability
to
observe
events
during
CA.
Although
in
this
study
the
potential
role
of
cofounders
such
as
age,
gender
and
time
to
interview
were
evaluated,
our
results
indicated
a
wide
variation
in
these
variables.
Consequently
a
larger
study
would
be
warranted
to
further
explore
the
relationship
between
these
variables
with
VA.
Such
a
study
should
also
explore
the
impact
of
variables
that
may
impact
the
quality
of
cerebral
blood
flow
and
cerebral
recovery
such
as
the
duration
of
CA,
quality
of
CPR
during
CA,
location
of
CA
(in-hospital
versus
out-of
hospital),
underlying
rhythm,
use
of
hypothermia
during
CA
and
after
ROSC.
5.
Conclusions
CA
survivors
experience
a
broad
range
of
memories
following
CPR
including
fearful
and
persecutory
experiences
as
well
as
aware-
ness.
While
explicit
recall
of
VA
is
rare,
it
is
unclear
whether
these
experiences
contribute
to
later
PTSD.
Studies
are
also
needed
to
delineate
the
role
of
explicit
and
implicit
memory
following
CA
and
the
impact
of
this
phenomenon
on
the
occurrence
of
PTSD
and
other
life
adjustments
among
CA
survivors.
Conflict
of
interest
statement
None
of
the
authors
have
any
conflicts
of
interest
to
declare.
Financial
support
Resuscitation
Council
(UK),
Nour
Foundation,
Bial
Foundation.
Researchers
worked
independent
of
the
funding
bodies
and
the
study
sponsor.
Furthermore,
the
study
sponsor
did
not
participate
in
study
design,
analysis
and
interpretation
of
results
or
the
writing
of
the
manuscript.
Ethical
approval
This
study
obtained
ethics
approvals
from
each
participating
center
prior
to
the
start
of
recruitment
and
data
collection.
Each
surviving
patient
gave
informed
consent
prior
to
their
being
inter-
viewed.
Data
sharing
All
authors
either
had
access
to
all
the
data
or
the
opportunity
to
review
all
data.
Transparency
declaration
I
Sam
Parnia
as
lead
author
affirm
that
the
manuscript
is
an
hon-
est,
accurate,
and
transparent
account
of
the
study
being
reported
and
that
no
important
aspects
of
the
study
have
been
omitted
and
that
any
discrepancies
from
the
study
as
planned
have
been
explained.
Acknowledgements
We
acknowledge
the
Biostatistical
Consultation
and
support
from
the
Biostatistical
Consulting
Core
at
the
School
of
Medicine,
Stony
Brook
University
as
well
as
the
help
of
Dr’s
Ramkrishna
Ram-
nauth,
Vikas
Kaura,
Markand
Patel,
Jasper
Bondad,
Markand
Patel,
Georgina
Spencer,
Jade
Tomlin,
Rav
Kaur
Shah,
Rebecca
Garrett,
Laura
Wilson,
Ismaa
Khan,
and
Jade
Tomlin
with
the
study.
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