The Modified Graeb Score

An Enhanced Tool for Intraventricular Hemorrhage Measurement and

Prediction of Functional Outcome
Timothy C Morgan, MPH*; Jesse Dawson, MD*; Danielle Spengler; Kennedy R. Lees, MD;
Chanel Aldrich; Nishant K. Mishra, MBBS; Karen Lane, CCRP; Terence J. Quinn, MD;
Marie Diener-West, PhD; Christopher J. Weir, PhD; Peter Higgins, MRCP; Mark Rafferty, MBChB;
Katie Kinsley; Wendy Ziai, MD; Issam Awad, MD; Matthew R. Walters, MD‡;
Daniel Hanley, MD‡; and the CLEAR and VISTA Investigators

Background and Purpose—Simple and rapid measures of intraventricular hemorrhage (IVH) volume are lacking. We
developed and validated a modification of the original Graeb scale to facilitate rapid assessment of IVH over time.
Methods—We explored the relationship between the modified Graeb scale (mGS), original Graeb scale, measured IVH
volume, and outcome using data from the Clot Lysis: Evaluating Accelerated Resolution of Hemorrhage with rtPA B
(CLEAR B) study. We also explored its reliability. We then evaluated the relationship between mGS and outcome in a
large sample of participants with IVH using data contained within the Virtual International Stroke Trials Archive (VISTA).
We defined outcome using the modified Rankin scale (>3 signifying poor outcome).
Results—The CLEAR B study included 360 scans from 36 subjects. The mGS score and IVH volume were highly correlated
(R = 0.80, P<0.0001, R2 0.65). Baseline mGS was predictive of poor outcome (area under receiving operating characteristic
curve 0.74, 95% confidence interval, 0.57–0.91), whereas the original Graeb scale was not. The VISTA study included
399 participants. Each unit increase in the mGS led to a 12% increase in the odds of a poor outcome (odds ratio, 1.12;
95% confidence interval, 1.05–1.19). Measures of reliability (intra- and inter- reader) were good in both studies.
Conclusions—The mGS, a semiquantitative scale for IVH volume measurement, is a reliable measure with prognostic
validity suitable for rapid use in clinical practice and in research. (Stroke. 2013;44:635–641.)
Key Words: cerebral hemorrhage ■ interobserver variation ■ intraventricular pressure ■ outcomes assessment

I ntraventricular hemorrhage (IVH) secondary to spontane-

ous intracerebral hemorrhage (ICH) results in death in 32%
to 43% of cases1–8 and poor functional outcome in most sur-
vivors.5,7,9–15 In severe IVH with obstruction of the third or
fourth ventricle, the placement of an extraventricular drain
can help lower raised intracranial pressure.12 Meta-analysis
shows this reduces mortality, but poor outcomes remain com-
monplace.16 In addition to extraventricular drain placement,
the use of intraventricular thrombolytic therapy may improve
outcomes and is being evaluated in the Clot Lysis Evaluating
Accelerated Resolution of Intraventricular Hemorrhage trial
program.17 A pivotal phase III study (Clot Lysis: Evaluating
Accelerated Resolution of Hemorrhage with rtPA III [CLEAR
III]) of the effect of thrombolytic based removal of ventricular
blood on functional outcome is underway.18
The use of thrombolytic drugs in this setting is associated
with bleeding risk.19 To reduce this risk, the CLEAR study
criteria include ICH and IVH clot stability, defined by
consecutive computed tomography scans of brain (CT) no
less than 6 hours apart showing no increase in ICH and IVH
volume.20 Although rapid, reliable, and well validated means
of assessing ICH volume are available,21,22 IVH volume
assessment remains laborious, time consuming, and subject
to variability between readers.23 A reliable, simple, quick, and

From the Division of Brain Injury Outcomes, The Johns Hopkins Medical Institutions, Baltimore, MD (T.C.M., K.L., K.W., W.Z., D.H.); the Institute
of Cardiovascular and Medical Sciences, College of Medical, Veterinary, Life Sciences, University of Glasgow, Glasgow, UK (J.D., K.R.L., N.K.M.,
T.J.Q., P.H., M.R., M.R.W.); Boston University School of Medicine, Boston, MA (D.S.); the Department of Mechanical Engineering, University of
Delaware, Newark, DE (C.A.); the Department of Biostatistics, Johns Hopkins School of Public Health, Baltimore, MD (M.D.-W.); the Robertson Centre
for Biostatistics, University of Glasgow, Glasgow, UK (C.J.W.); and the Section of Neurosurgery, University of Chicago Medicine and Biological Sciences,
Chicago, IL (I.A.).
*
Drs Morgan and Dawson joint first authors.
‡
These authors are co-senior authors.
Louis Caplan, MD, was guest editor for this article.
Correspondence to Jesse Dawson, MD, Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, Life Sciences, University of
Glasgow, Glasgow, UK. E-mail jesse.dawson@glasgow.ac.uk
© 2013 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.112.670653

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at University of Pittsburgh--HSLS on May 3, 2015
636  Stroke  March 2013
clinically meaningful approximation of IVH volume is needed
not only for clinical trials such as CLEAR, but also clinical
practice more widely. The Graeb score is a semiquantative
score ranging from 0 to 12, which could be used for this
purpose. However, it lacks the ability to differentiate specific
regions of the ventricular system, which may limit its
relationship with true IVH volume, its ability to detect IVH
growth or removal in subcompartments of the ventricular
system, and its ability to predict outcome.
We report a program of research in which trained asses-
sors evaluated and validated a modification of the original
Graeb score (oGS),24 called the modified Graeb Scale score
(mGS), which we designed to address the above issues. Also
described as the expanded Graeb scale, Hinson et al25 provide
an excellent description of the mGS. However, this study (to
our knowledge) is the first validation of this modified Graeb
scale. In Study One we explored the relationship between the
mGs, oGS, volumetrically measured IVH, and outcome using
data from the CLEAR B trial. We then explored in Study Two
the relationship between mGS and 90-day functional outcome
in a large sample of patients with IVH using data from the
Virtual International Stroke Trials Archive (VISTA).26
Methods
Development of the Modified Graeb Scale
The oGS was based on only the third, fourth, right and left lateral
ventricles.24 A maximum score of 4 is given for each lateral ventricle,
where it is expanded and filled with blood and a maximum score of 2
is given for the third and fourth ventricles if they are similarly filled.
The maximum possible score is therefore 12. For the mGS, we intro-
duced scores for separate ventricular compartments to better reflect
total IVH volume and selective regional accumulation or removal
of blood. The mGS is thus based on the fourth ventricle (maximum
score 4), third (maximum score 4), right and left lateral ventricles
(maximum score 4 for each), right and left occipital horns (maximum
score 2 for each), and the right and left temporal horns (maximum
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score 2 for each). An additional score of +1 is given to each compart-
ment if it is expanded beyond normal anatomic limits attributable to
clot. The boundaries between the lateral ventricle, the occipital horn,
and the temporal horn are composed of 3 planes that intersect in (and
project outwardly from) the trigone, or the central region where the
3 compartments converge. The maximum possible score is 32, in
which every compartment is filled with blood and expanded. A score
of 0 denotes no intraventricular blood. The scoring rubric is shown
in Figure 1.
Observer Training Before Review of CT Images
Observers (J.D., N.M., T.M., D.S.) were trained in application of the
mGS score using a set of training scans (n=80) before review of any
scans included in this study. Written guidance could be consulted27
and, after review, a telephone conference was convened in which
questions were addressed and scoring rules were clarified.
Study One – Relationship Between oGS, mGS,
IVH Volume, and Outcome in Patients Undergoing
Thrombolytic Therapy
Data from the CLEAR B trial (a multicenter trial coordinated by
Johns Hopkins University) were used. This was a dose-finding phase
II clinical trial to evaluate the efficacy of intraventricular administra-
tion of thrombolytic agent (recombinant tissue plasminogen activa-
tor [rt-PA]) for patients with severe IVH secondary to spontaneous
ICH.18 Inclusion criteria included complete obstruction of the third
or fourth ventricle(s) requiring the placement of an extraventricular
drain, small ICH (< 30 mL) at time of enrolment, IVH and ICH clot
stability at time of enrollment, and acquisition of the first CT scan
within 24 hours of symptom onset. Additional details regarding the
CLEAR eligibility specifications are available elsewhere.17
Each scan was scored using the both the oGS and mGS scor-
ing systems. Two independent assessors scored the data set using
the mGS to assess inter-reader variability. Additionally, 1 of the 2
readers rescored the data set 18 months later to assess intrareader
reliability. Two readers calculated the IVH volumes by a computed
free-hand tracing technique using medical imaging software (Alice,
Perceptive Informatics, Boston, MA), which is consistent with es-
tablished methods.23
Figure 1.   The modified Graeb
scale.
 Morgan et al   The Modified Graeb Score    637

Table 1.  Baseline Characteristics in Studies One and Two These 1250 cases were reviewed, and those with IVH were in-
cluded in further analyses. The presence of IVH, mGS score, and
Variable Study One Study Two ICH volume and location were recorded independently by 2 blinded
Age, y 57.0 (10.2) 69.2 (10.9) observers (J.D. and N.M.). Where mGS scores differed between ob-
servers, the mean score was used unless there was disagreement con-
Male sex 25 (69.4%) 247 (61.9%) cerning the presence of IVH. In such cases, scans were rereviewed
Systolic BP, mm|Hg 192.7 (42.5) 176.1 (28.8) and disputes resolved by consensus. ICH volumes were calculated
Diastolic BP, mm|Hg 110 (24.9) 93.6 (17.6) by M.R. and N.M. Computer assisted volumetric analysis of ICH
volume was performed (using IMAGE J software [http://rsbweb.nih.
Serum creatinine, μmol/L* N/A 77.6 (27.4) gov/ij/]), except for 136 participants, for which only a hard copy of
Baseline NIHSS, median (IQR) 23.0 (1.0–37.0) 15.0 (11.0–19.0) the scan was available. For these scans the ABC/2 method21 was used,
with the aid of digital callipers.
Smoker N/A 57 (14.3%)
DM 10 (28.7%) 65 (16.3%) Statistical Analysis
AF 3 (8.3%) 36 (9.0%)
The primary end point was poor outcome, defined as day 90 mRS
score >3. Analyses were conducted using SPSS version 19 (SPSS Inc,
Hypertension 29 (80.6%) 293 (73.4%) Chicago, IL). Variables associated with poor outcome were identi-
MI 4 (11.1%) 17 (4.3%) fied (using a chi-squared test for dichotomized variables or regres-
sion analysis for continuous variables). These variables were then
Previous stroke 3 (8.3%) 90 (22.6%)
included in a binary multiple logistic regression models to evaluate
↑ cholesterol N/A 50 (12.5%) the relationship between mGS and outcome. Baseline Glasgow Coma
ICH location Scale score, baseline blood glucose level, and use of anticoagulant
drugs before ICH were not available for all participants. Analyses
Deep 33 (91.7%) 343 (86.0%) were repeated including only patients with these variables recorded
Lobar 2 (5.6%) 54 (13.5%) to explore sensitivity of our findings. The ICC was used to assess
Posterior Fossa 0 (0.0%) 1 (0.0%) interobserver agreement using the mGS.
Primary IVH 1 (2.8%) 1 (0.0%)
ICH Volume, cm3 3.7 (0.8–12.6) 16.4 (9.9–41.2)
Results
Graeb Score, median (IQR) 20 (16–32) 6 (3–11) Study One (CLEAR B Analysis)
For continuous variables, values are expressed as mean (standard deviation) The sample included 360 scans from 36 subjects. Mean age
unless stated. For dichotomous variables, values are n (%). AF indicates was 58 years, with a standard deviation of 10 years. Baseline
atrial fibrillation; BP, blood pressure; DM, diabetes mellitus; ICH, intracerebral characteristics are shown in Table 1. Most hemorrhages were
hemorrhage; IQR, interquartile range; IVH, intraventricular hemorrhage; MI, in a deep location (91.7%). All had IVH and median ICH vol-
previous myocardial infarction; and NIHSS, National Institutes of Health Stroke
ume was 3.7 mL (IQR 0.8–12.6).
Scale. N/A = not available in CLEAR B dataset. P values are for t test, Mann–
Whitney tests or χ2 comparison. Correlation Between oGS, mGS, and Measured IVH Volume
*Not available for 73 patients in VISTA analysis. The oGS and mGS were highly correlated with IVH volume
(Figure 2, R=0.77, P<0.0001, R2 0.60 for oGS and R=0.80,
Functional outcome was measured using the modified Rankin P<0.0001, R2 0.65 for mGS [n=318 scans with IVH included]).
scale score (mRS) at 180 days (the primary end point in the CLEAR
trial program). This difference was not statistically significant (z=0.37,
P=0.71). The correlation between mGS score and IVH volume
appears strongest in smaller IVH cases (< 40 mL; R = 0.90, ver-
Statistical Analyses
sus R = 0.71 in cases of IVH > 40 mL). The change in oGS and
Analyses were conducted using SPSS version 19 (SPSS Inc, Chicago,
IL). A correlation was assessed between the oGS/mGS score and IVH mGS were also correlated with change in IVH volume (R=0.46,
volumetric measurements using Pearson correlation coefficient. The P=0.005 and R=0.57, P<0.001 respectively, n=36). This dif-
significance of the difference between the 2 correlation coefficients ference was not statistically significant (z=0.63, P=0.52).
was assessed using the Fishers r to z transformation (2-tailed test). However, the relationship between change in oGS and IVH
The change in oGS and mGS between baseline and study end were
similarly correlated to change in IVH volumetric measurements. volume appeared more variable than that for change in mGS (r2
Receiver operating characteristic (ROC) analysis was used to estab- 0.21 for oGS compared with r2 0.33 for mGS).
lish whether baseline oGS and mGS were predictive of day-180 func-
tional outcome. The intraclass correlation coefficient (ICC), which is Prediction of Day-180 Outcome Using oGS and mGS
equivalent to quadratic weighted kappa statistics, was calculated to Baseline mGS and IVH volume were predictive of out-
evaluate inter- and intraobserver variability for the mGS, as well as come. The area under the curve (AUC) for the prediction of
the agreement for IVH volume measurement.
poor 180-day outcome was 0.74, 95% CI 0.58 to 0.91 for IVH
volume, 0.74 (95% CI 0.57–0.90) for the mGS and 0.63 (95%
Study Two - Relationship Between mGS and 90-Day CI 0.45–0.82) for the oGS (Figure 3).
Functional Outcome
Data from VISTA were used for this study as the large sample size Reliability and Reproducibility of the mGS
would permit more definitive evaluation of the relationship between The ICC between the 2 readers using the free-hand tracing
mGS and outcome. The study was performed in the Institute of technique to assess IVH volume was 0.98 (95% confidence
Cardiovascular and Medical Sciences at the University of Glasgow. interval [CI], 0.98–0.98). The consistency between readers
For all patients with ICH, a baseline CT brain scan and a 90-day
mRS score were included. VISTA has been described in detail else- for the mGS was also high (ICC > 0.94; 95% CI, 0.93–0.95).
where•• and currently holds data for 1829 patients with ICH and CT Intrareader reproducibility for the mGS score was also good
scans for 1250 of these.26 (ICC 0.90; 95% CI, 0.85–0.95).

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638  Stroke  March 2013
Study Two (VISTA Analysis)
Of the 1250 patients reviewed, 31.9% (399) had IVH and were
included in subsequent analyses. Baseline characteristics are
shown in Table 1. Briefly, the majority of hemorrhages were
in a deep location (86.0%), median ICH volume was 16.4 cm3
(IQR 9.9–41.2 cm3), and median mGS was 6, IQR 3 to 11.
Poor outcome occurred in 272 (69.2%), and 117 (29.3%) died.
In 6 cases (1.5%), a primary outcome could not be assigned
because the participants were known to be alive but had no
recorded mRS score. Sensitivity analysis, where the missing
outcomes of these cases were assumed to all be poor versus
assumed to all be good, did not change results given below
(data not shown).
mGS and 90-Day Outcome
On univariate analysis, greater age, increasing baseline
National Institutes of Health Stroke Scale score, ICH volume,
lobar hemorrhage location, and mGS score were predictive of
poor outcome. When these variables were included in a mul-
tivariable model, the mGS remained predictive of poor out-
come. Each unit increase in score led to a 12% increase in
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Figure 2.  Scatter plot of measured intraventricular
hemorrhage volume in milliliters vs the original and
modified Graeb scores.
the odds of a poor outcome (OR, 1.12; 95% CI, 1.05–1.19;
Table 3). When previous antithrombotic drug use (n=336) and
Glasgow Coma Scale (GCS; n=185) were added to the model,
the mGS remained similarly predictive of outcome. GCS was
not independently predictive. When blood glucose level was
added to the model (n=169), the 95% CI for the mGS crossed
unity (95% CI for OR 0.99–1.14). Neither lobar hemorrhage
or blood glucose predicted of outcome in this analysis.
Reliability of the mGS Score
The agreement rate between the 2 observers (n=1250 scans)
was 73.7% (95% CI, 71.0–76.2) with corresponding intraclass
correlation coefficient of 0.94 (95% CI, 0.93–0.95).
Discussion
Our studies show that the mGS, a simple semiquantitative
score that takes only a few minutes to administer, is a valid
and reproducible measure of IVH volume. In our CLEAR B
investigation, we have shown that the mGS has good inter-
and intrareader reliability, is closely related to IVH volume
and is similarly predictive of outcome to actual IVH volume.

Further, it gives greater flexibility in terms of its ability to
detect IVH in differing ventricular compartments and gives a
more accurate measure of change in IVH volume over time.
We then explored the predictive ability of mGS in a wider
population of IVH patients using VISTA dataset, the largest
dataset of its kind, with a sufficient sample size for adjusted
analyses to be performed. Here we found a 12% increased
odds of poor outcome for each incremental increase in mGS
independent of other measures such as ICH volume and
baseline stroke severity. Our data come from 2 separate stud-
ies, conducted in different institutions by similarly trained
but different observers and in different populations of IVH
patients. Not only do our data show that the mGS is a useful
means of quantifying IVH extent, it highlights the crucial
importance of quantifying IVH in both clinical research and
clinical practice.
There are other methods available for the semiquantitative
assessment of IVH volume.28 This IVH score is a quick and
easy assessment tool in which the user assesses the scan, and
then uses a simple exponential equation to approximate the
IVH volume in mL. It correlates well with measured IVH
volume (R = 0.8),28 but has not been validated using multiple
longitudinal assessments nor has it been reduced to a form
Table 2.  Multivariable Logistic Regression Analysis in
Study Two
Variable OR 95% CI for OR P Value
Age, y 1.10 1.06–1.13 <0.0001
Baseline NIHSS 1.20 1.12–1.27 <0.0001
ICH volume, cm3 1.04 1.02–1.06 <0.0001
Lobar hemorrhage 2.42 0.83–7.00 0.104
mGS 1.12 1.05–1.19 <0.0001
CI indicates confidence interval; ICH, intracerebral hemorrhage; mGS,
modified Graeb score; NIHSS, National Institutes of Health Stroke Scale; and OR,
odds ratio for poor outcome (mRS>3) and refers to change in odds ratio per unit
increase in variable for continuous variables.
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Morgan et al   The Modified Graeb Score    639
Figure 3.  Receiver operating characteristics
curves for baseline intraventricular hemor-
rhage (IVH), original Graeb score (oGS), and
modified Graeb score (mGS) for prediction of
poor day-180 outcome. Area under the curve
for baseline IVH 0.74 (95% CI, 0.58–0.91).
AUC for mGS 0.74 (95% CI, 0.57–0.90). AUC
for oGS 0.63 (95% CI, 0.45–0.82).
that is used in prospective clinical trials. Another assessment
method, semiautomatic image segmentation, has been
proposed for IVH measurement. This technique uses minimal
user input to identify IVH, and can give a very accurate
measure of the total volume of the segmented structure.29
However, this method requires sophisticated software that
is not validated, nor is it readily available in most clinical
settings. Using our proposed methods, the CT scan is all that
is required to assign the mGS. Furthermore, the ease of use
and excellent reproducibility means that the mGS can be used
by highly trained neuroradiologists and less sophisticated CT
readers alike.
It is already known that presence of IVH and IVH vol-
ume are strong predictors of mortality and outcome.5,30 We
found that mGS score adds to the predictive information
provided by other key variables such as baseline National
Institutes of Health Stroke Scale (NIHSS) score and ICH
volume in our VISTA analysis. We were unable to adjust
for potentially important variables such as blood glu-
cose level, GCS, score and previous antithrombotic drug
use as they were measured in only a small number of the
eligible participants (n=169, 185, and 336, respectively).
However we explored sensitivity of our results to this in
these smaller sample sizes and results were broadly similar.
It is important to note that patients with suppressed GCS
were typically excluded from clinical trials contained in
the VISTA archive meaning this analysis cannot confirm
utility of the mGS with regard to outcome prediction in
those with profoundly suppressed consciousness on admis-
sion. However, mGS is related to outcome independent
of NIHSS score (which was more strongly predictive of
outcome than GCS in our analysis) and many participants
in CLEAR B had suppressed consciousness meaning it is
likely similarly predictive in this setting. Our data reaffirm
the need for clinical trials of strategies designed to limit the
extent of or remove IVH, and also raises the importance
of real time measuring IVH presence and extent in clinical
640  Stroke  March 2013
trials of ICH. Imbalances in baseline IVH rates and size
may have confounded results of other recent and important
trials.31 We believe randomization strategies should ensure
that presence of IVH is balanced between treatment arms
in clinical trials for ICH, or that mGS could be adjusted for
in statistical analysis.
The strengths of our program include the longitudinal aspect
of the CLEAR analysis, the large sample size in the VISTA
analysis, and the use of a simple tool and its training program
already used in clinical trials. This is combined with the fact
that our methods were validated using 2 datasets in differing
environments. Data from the VISTA archive come from rigor-
ously conducted and monitored clinical trials; we were unable
to assign end point status in only 6 cases (0.5%). We could
adjust for ICH volume, location, and baseline NIHSS but were
unable to include all cases of ICH contained within VISTA
since CT scans were not available for review for all clinical
trials. As mentioned, a further potential weakness is selection
bias in medical trials of ICH where patients with significantly
reduced conscious level have often been excluded. This may
explain why in the CLEAR B study the proportion with deep
ICH was higher and case fatality lower than that seen in previ-
ous population cohorts.32
In conclusion, we have shown that the mGS is a suitable
tool to assess the extent of IVH. It is reliable and valid, and
more closely related to change in IVH volume and outcome
than the oGS. The mGS could readily be used to assess out-
comes in clinical trials of ICH and IVH and to monitor prog-
ress of thrombolytic therapy for IVH.
Acknowledgments
VISTA-Acute members: K.R. Lees (Chair), A. Alexandrov, P.M.
Bath, E. Bluhmki, L. Claesson, S.M Davis, G. Donnan, H. C.
Diener, M. Fisher, B. Gregson, J. Grotta, W. Hacke, M.G. Hennerici,
M. Hommel, M. Kaste, P. Lyden, J. Marler, K. Muir, R. Sacco,
A. Shuaib, P. Teal, N.G. Wahlgren, S. Warach, and C. Weimar.
CLEAR Executive Committee: D. F. Hanley (Chair), I.A. Awad
(Co-Chair), M. Diener-West, M.E. Griswold, P. Keyl, K.R. Lees, A.
Marmarou, B. Gregson, J. Mighty, D.H. Rhoney, K. Dickersin, C.
Kase, and I. Barofsky.
Sources of Funding
The CLEAR B study was funded by the Food and Drug
Administration, Division of Orphan Products, and National Institutes
of Health (ClinicalTrials.gov Identifier: NCT00650858). The VISTA
study was funded by the Stroke Association (grant 2007/08) and ap-
proved by the VISTA steering committee. N.K.M. was supported by
an Overseas Research Student Award from the University of Glasgow.
D.H. is funded by CLEAR III 5U01-NS062851-03 and MISTIE II
5R01-NS046309-07.
Disclosures
None.
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 The Modified Graeb Score: An Enhanced Tool for Intraventricular Hemorrhage
Measurement and Prediction of Functional Outcome
Timothy C. Morgan, Jesse Dawson, Danielle Spengler, Kennedy R. Lees, Chanel Aldrich,
Nishant K. Mishra, Karen Lane, Terence J. Quinn, Marie Diener-West, Christopher J. Weir,
Peter Higgins, Mark Rafferty, Katie Kinsley, Wendy Ziai, Issam Awad, Matthew R. Walters and
Daniel Hanley
the CLEAR and VISTA Investigators

Stroke. 2013;44:635-641; originally published online January 31, 2013;

doi: 10.1161/STROKEAHA.112.670653
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