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JCN Open Access ORIGINAL ARTICLEpISSN 1738-6586 / eISSN 2005-5013 / J Clin Neurol 2015;11(4):339-348 / hp://!"#!oi#or$/10#3988/%&n#2015#11#4#339
Prognostic Tools for Early Mortality in Hemorrhagictro!e" ystematic Re#ie$ an% Meta&Analysis
'hrin i*hen(
Chun Shin$ '+o,-
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In*iue o pplie! elh
S&ien&e* S&hool o e!i&ine ?
rading
Scale (>S) score appearing to be the most promising variant1 'ith a pooled &/C across
four studies of .7; (529 CI:.7*
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Copyright © 2015 Korean Neurological Association 339
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JCN re!i&in$ rl orli in eorrh$i& Sro,e JCNi*hen ' e l#larly pertinent given that the risk of a poor outcome is
high er for ICH than for the other stroke subtypes1* and
the use of a prognostic model has been found to confer
greater accura cy than merely relying on clinical
udgment.2 In the a bsence of 'ellestablished interventions
to reduce deaths from ICH1 accurate prognostic tools may
prove useful for infor med decisionmaking in the acute
phase of ICH1 including the options of transferring to
intensive care1 rehabilitation1 and palliation. In the
research setting1 prognostic scores may also prove useful
for the risk stratification of participants in clini cal trials
of interventions for ICH.
Eublished systematic revie's of prognostic models in
ICH date back at least + years1-1; and the only recent
systematic revie' that 'e are a'are of 'as reported in a
conference a b stract in +1 and has not been reported
else'here in mor e detail.7 & comprehensive update seems
timely given +) the recent publication of ne' studies that
have evaluated diff er ent prognostic scores and ) theabsence of a unified system that is accepted in routine
clinical practice.
Hence1 in the present study 'e aimed to synthesize the
r e cent evidence on prognostic tools in patients presenting
'ith ICH1 and to determine the comparative performances
of dif
ferent scor es.
bolysis) or those that specifically evaluated the prognosis
of a stroke affecting a particular brain area (e.g.1 basal
ganglia).
earch strategyWe searched !"#I$! and !%&S! (in &pril +*1
using the ?vidSE interface) using the search terms listed in
Su p plementary (in the onlineonly "ata Supplement)1
'ithout any language restriction. We also checked the
bi bliographies of the included studies for other potentially
suitable studies.
t+%y selection an% %ata
e*tractionStudy screening and data eJtraction 'ere performed by
pair s of revie'ers (selected from A..1 C.S.A.1 A.E.1 and
@.A.#.) 'ho independently scanned all titles and abstracts
for po tentially relevant articles1 'hose fullteJt versions
'ere r e trieved for further detailed evaluation. &nyuncer tainties and discrepancies 'ere resolved through
discussion and 'ith a third revie'er. We also contacted
authors if any aspects of their articles reBuired further
clar ification.
We used a standardized form for data collection that in
cluded details of the setting and date of the study1
geogr a phi cal location1 selection criteria1 and other
characteristics of the
participants1 and outcome
measur es.
Eligi,ility criteria
METHO'
Assessment of st+%y #ali%ity
Study validity 'as assessed by pairs of revie'ers
indepen dently checking 'hether there 'as clear
reporting of the
We selected studies that collected clinical variables (or
sets of these variables) used to calculate risk scores
pr edicting early mortality (,- months) in adult patients at
the time of presentation 'ith ICH. We stipulated that
studies had to have a sample size of K+ participants1
'ith the main f ocus being on those presenting 'ith
primary ICH. ?ur specific interest 'as the reporting of the
discrimination ability of the tool1 measured based on thearea under the receiver o perat ing characteristic curve
(&/C) or cstatistic. We aimed to base our systematic
revie' on moreuptodate evidence1 and as such
restricted our selection to the past decade3 that is1 studies
published from * to &pril +*.
We eJcluded studies that 'ere aimed solely at
deter min ing correlations bet'een mortality and single
la borator y (e.g.1 albumin or troponin) or radiological
(e.g.1 lesion vol ume) variables. We did not include
studies of only f unction al outcomes. Since our main
focus 'as on stroke patients presenting to healthcare
facilities and 'e 'anted to maJi mize the generalizability
of the findings1 'e eJcluded studies involving narro'
subgroups of ICH patients 'ho had been deemed to
reBuire admission to intensive care. We also
eJ cluded studies that focused on mortality
in specific subsets of
patients (e.g.1 follo'ing certain interventions
such as thr om
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JCN re!i&in$ rl orli in eorrh$i& Sro,e JCNi*hen ' e l#of patient assessments1 missing or incomplete data1 use of
ardized treatment protocols1 and 'hether the study involved a
ation or validation cohor t.
analysis
Statistical analysis 'as conducted by an eJperienced meta analyst
A.#.) using Cochrane Collaboration Devan 2.6 soft'are ($ordic
Cochrane Centre1 Aobenhavn1 "enmar k). We chose to base our
sis on the &/C or cstatistic since these are eBuivalent measures
of the discr imination ability for binary outcomes.5 In the present
conteJt the dis crimination ability refers to ho' 'ell the model
parates patients 'ho subseBuently die from those 'ho are sur vi
vors. Lor studies that investigated both derivation and
vali dation components1 'e chose to analyze data relating
to the validation portion. If different mortality time
points 'er e used in a particular study1 'e used 6 days as
the first choice and inpatient mortality as the second
choice1 and 'here nei ther 'as available 'e accepted a
time point of ,- months f or analysis. If multiple &/C
values 'ere available for a par tic ular prognostic tool1 'e
calculated a 'eighted pooled aver age using a random
effects inversevariance metaanalysis.
If the &/Cs 'ere listed 'ithout standard errors1 'e
deter
340 J Clin Neurol 2015;11(4):339-348
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mined these values through HanleyMs method and the529
confidence intervals (CIs).+
We assessed heterogeneity using the I statistic and by
vi sual inspection of Lorest plots. 4he performance of the
pr og nostic score 'as udged according to the follo'ing
&/C thresholds that have been described by other
r esear cher s0 eJcellent (&/C ≥.5)1 good (&/C ≥.7
and ,.5)1 fair (&/C ≥.; and ,.7)1 and poor (&/C
,.;).++
RE(LT
We selected ++ relevant studies from 1-6 articles
identified by searching the electronic databases (the flo'
chart of study selection is sho'n in Lig. +).*121+ 4he
characteristics and results of the included studies are
reported in 4able +1 and our appraisal of study validity is presented in 4able . Nar i ables reBuired for the
calculation of each prognostic model are listed in 4able 6.
4he included studies involved *+1222 participants
(sample sizes ranged from +2* to 6;125 in the ++
studies) 'ith a mean age of -; years1 'hile 229 of them
'ere male. SiJ of the studies addressed the 6day
mortality1 three addr essed inpatient mortality1+61+51 and
t'o addressed mortality at 5 or + days.*12 Lour studies
recruited patients from t'o or more healthcare sites.*121+1+5
4he geographical locations 'er e diverse1 and included
$orth &merica1 !urope1 eJico1 and !ast &sia. "ata
from the study performed in 4ai'an 'er e reported in
t'o separate articles1 'ith HemphillICH scor es available
from one and ICH>rading Scale (>S) scores f r om the
other1 'ith substantial overlap in the included patients.+-1+
4itles and abstracts for screening from search0
1-6 after deduplication
!Jcluded articles that clearly did not
meet inclusion criteria (n:12-)
"etailed checking of fulltest versions
of potentially eligible articles (n:*+)
!Jcluded (n:6)0
ainly ischaemic stroke0 +7
"id not report &/C or outcome
of interest0 ++
Intensive care patients only0 +
4otal number of studies included in systematic
revie'0 ++
)ig- .- Llo' chart of study selection. &/C0 area under receiver oper ating characteristic curve.
/ali%ity assessmentost of the studies had a retrospective design1 or
per f or med posthoc analyses of prospectively collected
clinical data. We 'ere able to determine that the
prognostic variables 'er e collected early in the course of
the presentation in five stud ies.
21+-+5
4reatment path'ays'ere seldom reported1 'ith only one study eJplicitly
stating that all participants r eceived similar care.2 "etails
on losses to follo'up or missing data 'ere reported for
seven studies (4able ).*121+1+*1+21+;1+7 !ight studies aimed to
perform model validation1 t'o had a miJed derivation
validation design1+71 and one that had a pur ely derivation
design.+6 We considered the findings of these der i vation
studies to be less robust than those that had been su b
mitted for eJternal validation.
0+antitati#e comparison of
A(CWe 'ere able to evaluate the follo'ing prognostic models
in the comparative Buantitative analysis0 HemphillICH
(nine cohorts)*121+1+*+71 and ICH>S (four cohorts).*1+21+-1+7
4he &/Cs from individual studies and the pooled mean
&/Cs across studies are sho'n in Lig..
Hemphill&ICH score
4he predictive accuracy of the HemphillICH model f or
mortality has been evaluated in 5 cohorts comprising
617+5 participants 'orld'ide.*121+1+*+71 Eoint estimates of
the &/C ranged from .; to .771 'ith a 'eighted
pooled average of .7 (529 CI:.;;
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par tici pants in the /S1 Spain1 4ai'an1 and the /A. Eoint estimates of the &/C ranged from .;* to
.771 'ith a 'eighted pooled aver
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Ta,le .- Characteristicsof included studies
Mortality rate A(C an% A(C category 1e*cellent2goo%2fair2poor3
6 days0 *9 HemphillICH0 &/C:.77 (good)
HemphillICH0 &/C:.7+* (good) (S!:.6+)1 sens:--91 spec:7;93
4akahashiSingle hospital1 Detrospective1 derivation1
6 days0 669%roderick0 &/C:.;;6 (fair) (S!:.6-)1 sens:*291 spec:59
C&D40 &/C:.7- (good)3
-
Weimar
Fapan3 +557CS0 >lasgo' Coma Scale1
>4W>0 >et With 4he >uidelines1 $IHSS0 national Institutes of Health Stroke Scale1 S!0 standard error 1 sens0 sensitivity1 spec0 specificity.
t+%y I't+%y setting4
perio%
t+%y %esign4
name of score
Patients5
n
Age5
years
Males5
6
Clarke
*+4'o centers1 /S&3
+557
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JCNi*hen ' e l#JCN re!i&in$ rl orli in eorrh$i& Sro,eage of .7; (529 CI:.7*arr ett et al.1* 'ith a reported
difference of .+* in the &/C1 favor ing the ICH>S model.
In contrast1 the other three studies dem onstrated far
smaller absolute differences in &/C1 'ith an average
difference of .6 that 'as also in favor of the ICH >Smodel.
Get 7ith The G+i%elines 1G7TG3 mo%el $ith or
$itho+t
National Instit+tes of Health tro!e cale
1NIH3
?nly one study analyzed the performance of the >W4>
score for predicting inpatient mortality1+5 that study
enr olled
6;125 participants in /S and Canada. 4he >W4> alone
(based on age1 vascular risk factors1 comorbid conditions1
and mode of arrival at the hospital) does not reBuire a detailed clinical eJamination or neuroimaging1 but in that
study it demonstrated a relatively poor predictive
accuracy 'ith an &/C of .--. Ho'ever1 combining the
>W4> mod el 'ith the $IHSS (in +162 participants)
resulted in a mar k edly improved pooled &/C of .7.
Glasgo$ Coma cale 1GC3
We identified only one recent study that involved a
pr ognos tic validation of the >CS.+2 4hat study recruited
+16-* par tic ipants in the /A and found an &/C of .7;
(529 CI:.72 S models to the
same par tici pants.
)+nctional o+tcome ris! stratification scale 1)(NC3
>arrett et al.* validated the prognostic accuracy of the
L/ $C score in 6-- patients in the /S1 and found an
&/C of .7; (529 CI:.76
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JCNi*hen ' e l#JCN re!i&in$ rl orli in eorrh$i& Sro,e4he !ssenICH score 'as validated in + study involving
6;+
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6** J Clin Neurol 2015;11(4):339-348 ww w .thejcn.com 344
Ta,le :- Nariables reBuired for estimating the prognostic score
Pre%ictor Hemphill&ICH Essen&ICH ICH&G )(NC
,-:
&ge1 years
≥7:+
,7:
-erman patients.2 4he &/C of .76 (529 CI:.;7
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Study or Subgroup "iscriminant ability Weight
&/C
IN1 random1 529 CI
.-.-. Hemphill&ICH
Clarke *+ >ood ++.69 .77 (.761 .56)
>arrett +6* Lair ++.29 .;* (.;1 .;7)
atchett -+* >ood +.9 .7+ (.;-1 .77)
EarryFones +6+2 >ood +.59 .7- (.7*1 .77)
Eeng ++- and Chuang 5+ Lair ++.*9 .; (.-71 .;-)
Domano ;+; Lair 5.;9 .;* (.-71 .7)
DuizSandoval ;+7 >ood ++.*9 .76 (.;51 .77)
4akahashi - >ood +.9 .76 (.;;1 .75)
Weimar -2 >ood ++.69 .76 (.;71 .77)
+,total 1;= 1=-??5 =->arrett +6* >ood 7.+9 .77 (.721 .5)
EarryFones +6+2 >ood 67.*9 .7; (.72 .75)
Eeng ++- and Chuang 5+ Lair -.*9 .;* (.-21
.7*) DuizSandoval ;+7
>ood ;.+9 .77 (.721.5) +,total 1;? 1=->@5
=-;=3 Heterogeneity0 4au:.3 chi:;.*1 df:6 ( p,.-)3 I:76.59
4est for subgroup differences0 Chi:-.1 df:+ ( p:.+)1 I:76.59 .2 .; +
)ig- 9- etaanalysis of the areas under the receiver operating characteristic curve (&/C) for various prognostic models. CI0 confidence
interval1 ICH0 intracerebral hemorrhage.
tina1 4ai'an1 and the /A). <hough the HemphillICH
score 'as introduced more than + years ago1 it is not yet
'idely adopted in clinical practice. Instead1 'e found nu
merous instances 'here researchers have modified the
HemphillICH score to try and improve its predictive
accu racy1 'ith varying degrees of success. 4heavailability of sev eral versions of the ICH score can
seem be'ilder ing O an important finding of our
systematic revie' is that the ICH >S score seems the one
most likely to offer some consistent advantage over the
original HemphillICH score. 4he slightly improved
performance 'hen using the ICH>S score may stem from
the greater detail 'ith 'hich the site and size of the
hemorrhage are considered1 as 'ell as the inclusion of
additional age categories (4able 6). Ho'ever1 'e
r ecognize that these changes may make the ICH>S score
more com plicated to calculate in practice.
We also identified variations in the compleJity and in
the reBuirement for specialist kno'ledge 'hen using
some of the tools (e.g.1 reproducibility 'hen interpreting
hemorr hage volume on C4 scans and calculation of
subscores such as the $IHSS). 4he need for specialist
eJpertise may prove to be a barrier in emergency
departments 'here clinicians may pr e fer a tool that is
simply based on clinical variables1 such as the >CS and
the (as yet unvalidated) ICH IndeJ.+61+2 Indeed1 EarryFones
et al.+2 found that the &/C of the >CS score 'as as good
as that of the ICH score in a /A validation cohor t1
but 'e 'ere unable to identify other recent data sets for
con firming the generalizability of these findings. 4his is
an in teresting point1 since the >CS score can be rapidly
assessed at the initial presentation and does not reBuire
specialist neu rological imaging procedures or eJpertise.
Lurther valida tion studies of the >CS score and ICHIndeJ 'ould be usef ul1 particularly in resourcepoor areas
or as initial triage tools in nonspecialized healthcare
facilities.
Several prognostic models are associated 'ith
additional compleJity due to them reBuiring a detailed
neur ological eJamination to estimate the $IHSS score.21+5
Lor instance1 the >W4> model eJhibited a poor &/C
score (,.;) 'hen it 'as applied alone1 but this improved
to a good &/C scor e 'hen it 'as combined 'ith the
$IHSS.+5 Having to use both >W4> and $IHSS scores
together may prove too la bor i ous for clinicians1
particularly given that dedicated online training is
reBuired for calculating the $IHSS score.6 4he !ssen
ICH score also reBuires calculation of the $IHSS score
and this might eBually limit its acceptability1 par ticu larly
given that a previous study found no marked impr ove
ment in &/C over that for the HemphillICH scor e.2
ost of the available studies have not addressed the ac
ceptability and uptake of current prognostic scores in the
daytoday management of stroke patients. While the
avail ability of a prediction rule 'ith good performance is
an im portant prereBuisite1 patients 'ill not benefit from
the pr o
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Study or subgroup Weight
&/C
IN1 random1 529 CI
.-:-. E+rope an% North America
Clarke *+ +-.59 .77 (.761 .56)
>arrett +6* +;.9 .;* (.;1 .;7)
atchett -+* +2.+9 .7+ (.;-1 .77)
EarryFones +6+2 +5.29 .7- (.7*1 .77)
Domano ;+; +*.*9 .;* (.-71 .7)
Weimar -2 +-.59 .76 (.;71 .77)
+,total 1;. 1=-??5 =->A3
Heterogeneity0 4au:.3 chi:6;.61 df:2 ( p,.+)3 I:7;9
.-:-9 Asia an% o+th America
Eeng ++- and Chuang 5+ 6*.9 .; (.-71
.;-) DuizSandoval ;+7 6*.69 .76 (.;51
.77) 4akahashi ; 6+.29 .76
(.;;1 .75) +,total 1;?3 Heterogeneity0 4au:.+3 chi:+2.;-1 df: ( p,.*)3
I:7;9
.-:-: ample siBe 9arrett +6* +-.;9 .;* (.;1
.;7) EarryFones +6+2 +7.-9 .7-
(.7*1 .77) Eeng ++- and Chuang 5+ +-.-9
.; (.-71 .;-) DuizSandoval ;+7 +-.;9
.76 (.;51 .77) 4akahashi - +2.9
.76 (.;;1 .75) Weimar -2 +-.29
.76 (.;71 .77) +,total 1;= 1=-?5 =->?3
Heterogeneity0 4au:.3 chi:+6.51 df:6 ( p,.6)3 I:;79
.-:-< Mean or me%ian age ?= years an% a,o#e
Clarke *+ .69 .77 (.761 .56)
atchett -+* +*.9 .7+ (.;-1
.77) EarryFones +6+2 -6.79 .7-
(.7*1 .77) +,total 1;
1=->:5 =->>3 Heterogeneity0 4au:.3 chi:.;1 df: ( p,.-)3 I:;9
.-:- Mean or me%ian age ,elo$ ?= years
>arrett +6* 2.9 .;* (.;1
.;7) Eeng ++- and Chuang 5+ 2.9 .;
(.-71 .;-) DuizSandoval ;+7 2.+9 .76
(.;51 .77) Weimar -2 *.79 .76
(.;71 .77) +,total 1;
1=-?95 =->@3 Heterogeneity0 4au:.3 chi:+.+1 df:6 ( p,.+)3
I:7-9
.2 .; +
)ig- :- Subgroup analyses of the Hemphillintracerebral hemorrhage model according to the study design and characteristics of participants. CI0
confidence interval.
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liferation of prognostic scoring models if their uptake
and implementation is patchy. It is important to
determine 'hat clinicians 'ant or eJpect from a score and
'hat factors 'ould facilitate their use of it. Lurthermore1
the eJpectations of pa tients and their relatives also need
to be considered1 such as by determining 'hether
prognostic scoring is acceptable and useful to interactions
(as compared to relying on clinical udgment). Shared
decisionmaking is pivotal in moder n medicine1 but our
systematic revie' sho's that none of the current
prognostic models are able to achieve eJcellent per
formance1 and thus the acceptability of imperfect r esults
needs to be assessed. We note that a survey found that
5-9 of emergency physicians 'ere prepared to use a
pr ognostic tool for stroke or death in patients 'ith
transient ischemic attacks1 but only if the tool achieved a
sensitivity of K5;9.*
?ur systematic revie' has limitations. We focusedonly on larger studies (K+ participants) published
during the last + years1 and emphasized overall mortality
Obecause of the high rate of early mortality in ICHO
rather than the functional outcome. ost of the included
studies had a r et rospective design or 'ere posthoc
analyses of pr os pectively collected clinical data1 and 'e
did not categorize the studies into high and lo'Buality
subgroups. We selected pu blished studies that used the
&/C or cstatistic as their pr imar y measure1 and it is
possible that studies that found poor per formance have
not been reported on.
4he strengths of our systematic revie' are that 'e con
ducted an eJhaustive and uptodate search of the curr ent
evidence1 accompanied by critical appraisal and
Buantitative data analysis. 4o the best of our kno'ledge1
none of the pr e vious systematic revie's have performed
a metaanalysis of discrimination ability. We have
summarized the evidence f or the relative performances
from comprehensive data sets to help guide stroke
researchers and clinicians as to 'hich scor e to use1 further
develop1 or test.
& key Buestion to consider is 'hether 'e genuinely
need further research that might involve only minor modifications to the HemphillICH model1 and 'hich
may not pr ovide more than minor incremental benefits to
the clinical accura cy. 4he proliferation of variants of the
HemphillICH model may simply cause greater confusion
amongst clinicians and thereby have a detrimental effect
on clinical implementation. Luture studies should focus on
the factors that influence the acceptability and adoption of
scoring systems1 and 'hether their implementation leads
to consistent improvements in patient care relative to
simply using subective clinical udg ment.
In conclusions1 'e have highlighted several pr ognostic score
eJhibit good performance in ICH1 the front r un ners being
HemphillICH score and the ICH>S var i
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ant1 'hich 'e believe can usefully guide
clinicians in mak ing betterinformed
treatment decisions. <hough further
validation studies are needed1 the >CS and
ICH IndeJ may also be reasonable options in
situations 'here simple and rapid clinical
assessment is needed before neuroimaging
r e sults become available1 such as during
triage 'hen a patient initially presents to a
healthcare facility.
+pplementa
ry Materials
4he onlineonly "ata Supplement is
available 'ith this ar ti cle at
htt p0dJ.d oi.org+.6577 cn.+2.++.*.665.
Con:li&* o: Iner e*
4he authors have no financialconflicts of inter est.
/&,no+le!$e0en*
A..1 C.S.A.1 @.A.#.1 and E.A.. conceptualized the
revie' and devel oped the protocols. A..1 C.S.A.1
@.A.#.1 A.E.1 and #.&. selected studies and abstracted
the data. A.. and @.A.#. carried out the synthesis of
the
data and 'rote the manuscript 'hile receiving criticalinput from all au
thors. @.A.#. acts as
guarantor for the pa per .
R!R"C#
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