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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

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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). &lthough 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. &lthough 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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!lo"al "urden of stroe #$nternet%. >eneva0 World Health

?rganization3 * 8cited +* &pr 7=. &vailable from0 /D#0

'' ' .' h o .i n t c a r di o va sc u

larPdiseasesencvdPatlasP+2Pbur denPstr ok e.pdf .

. 4hrift &>1 "e'ey H1 acdonell D&1 c$eil FF1 "onnan >&.

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http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://dx.doi.org/10.3988/http://www.who.int/cardiovascu-http://dx.doi.org/10.3988/http://www.who.int/cardiovascu-


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