ORIGINAL RESEARCH

published: 12 March 2019

doi: 10.3389/fneur.2019.00217

Intraventricular Hemorrhage Severity

as a Predictor of Outcome in
Intracerebral Hemorrhage
Gabriela Trifan*, Baback Arshi and Fernando D. Testai

Department of Neurology and Rehabilitation, University of Illinois at Chicago College of Medicine, Chicago, IL, United States

Background/Objective: Intraventricular hemorrhage (IVH) extension after spontaneous

supratentorial intracerebral hemorrhage (sICH) is an independent predictor of worse
outcome. However, there is a paucity of data looking at the degree of IVH severity and
its impact on outcome. This study addresses the contribution of IVH severity to outcome
at time of hospital discharge after sICH.
Methods: Two hundred and ten patients were included in the study. Baseline
demographic and radiologic characteristics were abstracted. First available CT scans
were reviewed for hematoma volume and location, IVH extension and presence of
hydrocephalus (HCP). IVH severity was calculated using Graeb scale. Multivariate logistic
Edited by: regression models were developed to investigate the association of IVH severity with poor
Andreas Charidimou,
Massachusetts General Hospital and outcomes at hospital discharge, defined as modified Rankin scale score (mRS) >3.
Harvard Medical School,
Results: Fifty-three percent of patients had IVH extension while 18% had surgical
United States
procedures done. Poor outcome (mRS >3) was seen for 56% of patients. Median IVH
Reviewed by:
Joshua Goldstein, extension severity on the Graeb scale was two. Presence of IVH was associated with poor
Harvard Medical School, outcome in univariate and multivariate analysis (p < 0.005). Compared to patients with
United States
Marta Rubiera, no IVH, IVH severity influenced outcome only when Graeb scores were ≥5 (OR = 1.3,
Hospital Universitari Vall d’Hebron, 95% CI 0.49–3.23, p = 0.63, and OR = 2.9, 95% CI, 1.1–7.6, p = 0.03 for Graeb <5
Spain
and ≥5, respectively.
*Correspondence:
Gabriela Trifan Conclusions: Higher IVH severity (defined as Graeb score ≥5) is associated with worse
[email protected] outcome at time of hospital discharge, while lower IVH severity (Graeb scores 1–4) has
similar outcomes to patients without IVH. IVH severity should be used in favor of IVH
Specialty section:
This article was submitted to presence for prognostication purposes.
Stroke,
Keywords: IVH, Graeb score, outcome, spontaneous ICH, supratentorial hemorrhage
a section of the journal
Frontiers in Neurology

Received: 15 January 2019

Accepted: 20 February 2019
INTRODUCTION
Published: 12 March 2019
Spontaneous intracerebral hemorrhage (sICH) has an overall incidence of 24.6 per 100,000
Citation: patient-years and the incidence increases with age (1). sICH accounts for 10–15% of all strokes and
Trifan G, Arshi B and Testai FD (2019)
is characterized by a 30–50% 3-month mortality rate (2–4). Intraventricular hemorrhage (IVH)
Intraventricular Hemorrhage Severity
as a Predictor of Outcome in
extension can be seen in up to 54% of sICH and is an independent predictor of worse outcome
Intracerebral Hemorrhage. and neurological deterioration (4–13). IVH extension is included as a variable in the calculation
Front. Neurol. 10:217. of the ICH score. The ICH score is a prognostic tool commonly used in clinical practice. This
doi: 10.3389/fneur.2019.00217 includes age ≥80 years, Glasgow coma scale (GCS), infratentorial location, hematoma volume, and

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Trifan et al. IVH Severity and Outcome in ICH

presence of IVH. The ICH scores ranges from 0 to 6, with 30-

day mortality rates increasing from 0% for a score of 0 to 100%
for score of 5 or 6 (11). In the ICH score, IVH extension is
indicated as present or absent regardless of severity (8, 12). While
it is already established that IVH extension is independently
associated with high mortality and poor functional outcome,
the impact of the degree of IVH severity is not completely
understood. The objective of this study is to determine the
contribution of IVH severity to outcome after sICH.

MATERIALS AND METHODS

This study is a single-center retrospective analysis of patients
with sICH admitted to a tertiary care center from 2007 to
2015. This study was approved by the local Institutional Review
Board and follows the guidelines set forth by the Strengthening
the Reporting of Observational Studies in Epidemiology
(STROBE) statement. Electronic medical records were screened
for discharge diagnosis of ICH using ICD-9 and ICD-10 codes.
We included patients aged older than 18 with spontaneous sICH,
which was defined as parenchymal hemorrhage that was not
related to tumor, vascular malformations, or trauma. Exclusion
criteria were hemorrhagic infarction, anticoagulation associated
ICH, and intraventricular treatment with recombinant activated
tissue plasminogen activator (Figure 1). Early restriction of care
FIGURE 1 | Flow chart of inclusion and exclusion criteria.
in patients with anticipated poor outcome might lead to self-
fulfilling prophecy and introduce bias in predictive models (14).
Thus, we also excluded patients with withdrawal of support
within the 48 h of admission. Statistical Analysis
Descriptive variables are presented as percentages, mean ±
standard deviation (SD), or median and interquartile range
Clinical and Radiologic Information (IQR). Fisher Exact test and Mann Whitney test were used
Sociodemographic information, medical history, baseline GCS, to compare categorical and continuous variables, respectively.
surgical procedures, and outcome at hospital discharge were Logistic regression analysis was used to identify predictors
abstracted from the electronic medical records. Hematoma of poor outcome at hospital discharge. Variables included in
volume was determined using the ABC/2 formula (15). ICH the statistical analysis were chosen based on their known
score was calculated as previously described (11). The severity influence on outcome. ICH volume and Graeb score were
of IVH extension was calculated using the Graeb scale (16). initially analyzed as continuous variables. Logistic regression
The Graeb scale is a semiquantitative tool for IVH extension analyses were performed to determine the association of different
scoring, ranging from 0 to 12 points, with higher scores denoting variables of interest with outcome. Two different adjustment
increased IVH volumes; a maximum of four is given for each models were utilized. In model 1, the results were adjusted by
lateral ventricle if expanded and filled with blood and up to the components of the ICH score (age, GCS, and ICH volume).
2 for the third and fourth ventricle if filled with blood and In model 2, the results were adjusted by variable characteristics
expanded (16). Hydrocephalus (HCP) was assessed using the with p<0.05 in univariate analysis. Patients with IVH extension
score proposed by Diringer et al. (17). In this score, the frontal were then subcategorized based on the degree of IVH severity
horn, atrium, and temporal horn of each lateral ventricle as well using the Graeb scale. Outcomes at hospital discharge for each
as the third and fourth ventricles are individually assigned a 0, 1, Graeb score were compared to patients without IVH extension
2, or points for no, mild, moderate, or marked HCP, respectively. using logistic regression. The Graeb score cut point for poor
This score ranges from 0 to 24 with higher scores indicating outcome was identified and used to group patients based on IVH
worse HCP. severity. Multivariate logistic regression analyses for groups using
The radiologic variables were determined by research the Graeb score cut point were performed adjusting by the two
personnel blinded to the outcomes using the first available non- proposed models.
contrast computed tomography (CT) of the head. Functional Presence of multicollinearity among outcome and
outcome was assessed using modified Rankin scale (mRS) at time independent variables was assessed using weighted regression.
of hospital discharge. mRS was dichotomized into good outcome Multicollinearity was defined as variance inflation factor ≥5
(0–3 points) and poor outcome (4–6 points) (18). or tolerance of <0.20 (19). Statistical analyses were done using

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Trifan et al. IVH Severity and Outcome in ICH

SPSS version 24 (SPSS Inc., Chicago, Il) with p < 0.05 indicating effect of each degree of IVH extension severity on outcome
statistical significance. at time of hospital discharge, only Graeb scores ≥5 were
significantly associated with poor outcome (OR = 12, 95% CI,
1.4–102.3, p = 0.025) (Table 4). In multivariate analysis adjusted
RESULTS for model 1, subjects with Graeb score <5 had similar outcomes
to individuals with no IVH extension (OR = 1.5, 95% CI, 0.5–
A total of 511 cases were screened and 210 met the inclusion 4.0, p = 0.4), while patients with Graeb score ≥5, had a 4-
criteria (Figure 1). Baseline demographic, radiologic, and clinical fold increase risk for mRS>3, compared with no IVH extension
characteristics are shown in Table 1. The large majority of the patients (OR = 4.0, 95% CI, 1.6–10.1, p = 0.003) (Table 5).
patients (98%) had first ever sICH and 46% had documented Similar findings were seen after adjusting for variables in model 2:
history of hypertension. Hematoma affected the deep brain patients with IVH extension severity as measured on Graeb scale
structures in 64% of cases. History of antiplatelet medication use ≥5, were three times more likely to have poor outcome at time
was seen in 9% of cases. IVH extension was present in 53% of of hospital discharge compared with sICH patients without IVH
patients with sICH, and of these, the median Graeb score was extension (OR = 2.9, 95% CI, 1.11–7.59, p = 0.03) (Table 5).
2. Hydrocephalus was observed in 48% of patients and surgical The overall mortality rate was 13%. sICH patients
hematoma evacuation was performed in 20 cases (10%). All the with IVH extension had higher mortality rates (21%)
patients that required VP shunt placement (8%) were in the ICH compared with patients without IVH extension (4%),
with IVH extension group. Poor outcome (mRS >3) at hospital
discharge was seen in 56% of all patients.
Multicollinearity was not observed between the independent
variables studied and outcome. In univariate analysis, history TABLE 2 | Univariate analysis for predictors of poor outcome.

of hypertension (HTN), history of diabetes (DM), GCS score, Univariate

hematoma volume, Graeb score, hydrocephalus score on
admission, and clot evacuation, were all associated with poor Variable OR (95% CI) P-value

outcome (p < 0.05) (Table 2). In model 1, age, hematoma

Age 1.01 (1.00–1.03) 0.1
volume, GCS score, and Graeb score were independently Male gender 1 (0.58–1.74) 1
associated with poor outcome; in model 2, only GCS score, History of HTN 0.6 (0.31–0.97) 0.04
hematoma volume and Graeb score remained significantly History of DM 2.7 (1.19–6.02) 0.02
associated with poor outcome (Table 3). When analyzing the Antithrombotic use 1.6 (0.58–4.40) 0.37
GCS score 0.70 (0.59–0.76) <0.0001
sICH volume 1.06 (1.04–1.08) <0.0001
TABLE 1 | Characteristics. *IVH extension 1.38 (1.25–1.53) <0.0001
Hydrocephalus score 1.14 (1.07–1.20) <0.0001
Variables Participants (N = 210)
Hematoma location 0.8 (0.44–1.36) 0.38
VP shunt placement 3.4 (0.99–13.03) 0.051
Age mean ± SD 56 ± 13
Clot evacuation 0.3 (0.95–0.92) 0.035
Male gender, n (%) 120 (57%)
GCS score at baseline (median, IQR) 14 (9–15)
HTN, Hypertension; DM, Diabetes Mellitus; GCS, Glasgow coma scale; sICH,
ICH volume, mL (median, IQR) 20 (6–38) spontaneous intracerebral hemorrhage. *As measured by Graeb scale.
IVH extension, n (%) 112 (53)
Graeb score (median, IQR) 2 (0–7) TABLE 3 | Multivariate analysis for predictors of poor outcome (mRS >3).
Hydrocephalus score (median, IQR) 0 (0–8)
Hematoma location, n (%) Variable Model 1 Model 2

Deep 134 (64) OR (95% CI) P value OR (95% CI) P value

Lobar 76 (36)
Antiplatelet use at baseline n (%) 18 (9) Age 1.03 (1.00–1.06) 0.03 1.03 (1.01–1.06) 0.02

Past medical history n (%) GCS score 0.76 (0.65–0.88) < 0.0001 0.76 (0.66–0.88) < 0.0001
sICH vol 1.05 (1.03–1.07) < 0.0001 1.05 (1.02–1.07) < 0.0001
Diabetes 36 (17)
*IVH extension 1.21 (1.07–1.36) 0.002 1.16 (1.02–1.31) 0.02
Hypertension 134 (64)
Hydrocephalus score 1.05 (0.98–1.14) 0.12 1.05 (0.97–1.31) 0.20
Previous ICH 4 (2)
Clot evacuation 0.98 (0.12–4.92) 0.98 0.80 (0.16–3.91) 0.79
Ischemic stroke 22 (10)
History of HTN 0.61 (0.28–1.32) 0.21 0.77 (0.35–1.69) 0.52
Surgical procedure type, n (%)
History of DM 1.46 (0.48–4.43) 0.51 1.38 (0.46–4.02) 0.57
VP shunt placement 17 (8)
Clot evacuation 20 (10) HTN, Hypertension; DM, Diabetes Mellitus; GCS, Glasgow coma scale; sICH,
mRS score at discharge median (IQR) 4 (2–5) spontaneous intracerebral hemorrhage. *As measured by Graeb scale. In model 1
outcomes were adjusted by the ICH score variables (age, GCS, hematoma volume, and
sICH, spontaneous intracerebral hemorrhage; IVH, intraventricular hemorrhage; VP shunt, IVH extension). In model 2 outcomes were adjusted by variables that had p ≤ 0.05 in the
Ventriculoperitoneal shunt; mRS, Modified Rankin Scale score. univariate analysis.

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Trifan et al. IVH Severity and Outcome in ICH

p < 0.0001. Among patients with IVH extension, DISCUSSION

the mortality rates increased from 3% in patients
with Graeb scores <5, to 28% for those with scores The results of our study show that Graeb score ≥5 after
≥5, p < 0.0001 (Figure 2). sICH is an independent predictor of poor outcome at time of
hospital discharge. In contrast, patients with sICH and Graeb
scores <5 had similar outcomes to the sICH patients without
TABLE 4 | Odds for poor outcome (modified Rankin Scale>3) based on Graeb
IVH extension.
scores. To date, the presence of IVH extension after supratentorial
sICH is a known independent predictor of poor outcome (10, 12,
Graeb score N OR (95% CI) P-value
20–23). However, the contribution of IVH severity to outcome
0 98 Reference –
has not been thoroughly investigated. Tuhrim et al. was the
1 5 0.5 (0.1–4.6) 0.534
first to demonstrate that IVH volume is associated with higher
2 10 1.2 (0.5–7.2) 0.310
30-day mortality rates (10). Young et al. identified a threshold
volume of 20 mL as being predictive of poor outcome (20).
3 7 4.9 (0.9–26.8) 0.065
However, IVH extension volumes as low as 6 mL have been
4 8 1.2 (0.5–8.3) 0.359
shown to increase the likelihood of poor functional outcome
5 7 12 (1.4–102.3) 0.025
after sICH (24). Performing volumetric analysis requires imaging
6 21 6.3 (2.1–18.7) 0.001
reprocessing software that is not typically available in clinical
7 12 21.7 (2.7–175.1) 0.004
practice. This drawback has been circumvented by the use of
8 8 13.8 (1.6–116.8) 0.016
semiquantitative IVH extension severity scales which estimate
9 7 11.8 (1.4–102.3) 0.025
IVH extension volume by using visual grading systems.
10 12 21.6 (2.7–175.1) 0.004
Two independent groups showed that IVH extension severity,
11 10 17.7 (2.2–145.9) 0.008
measured as a continuous variable by the modified Graeb scale,
12∧ 5 – –
is associated with poor outcome in sICH (6, 25). These studies
∧ Unable to calculate due to no patients with good outcome. demonstrated that IVH extension severity scales can refine the

TABLE 5 | Odds for poor outcome (modified Rankin Scale>3) based on grouped Graeb scores.

Graeb score n Unadjusted Model 1 Model 2

OR (95% CI) P-value OR (95% CI) P-value OR (95% CI) P-value

1–4 30 1.9 (0.86–4.51) 0.1 1.5 (0.57–4.01) 0.410 1.3 (0.49–3.23) 0.63
5–12 82 12.7 (5.94–27.20) <0.0001 4.0 (1.59–10.15) 0.003 2.9 (1.11–7.59) 0.03

FIGURE 2 | Outcome at hospital discharge after intracerebral hemorrhage (ICH) with and without intraventricular hemorrhage (IVH).

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Trifan et al. IVH Severity and Outcome in ICH

TABLE 6 | Overview of selected studies in spontaneous intracerebral hemorrhage with intraventricular hemorrhage.

Study Type of study N Outcome scale Follow-up Results Notes

(% IVH) (months)

ICH WITH/WITHOUT IVH (NO SEVERITY GRADING)

Tuhrim et al. Prospective Mortality rates 1 42.5 vs. 8.5% No cutoff identified
(10) 129 (36%)
Steiner et al. Prospective Poor functional outcome 3 56.7 vs. 24.5% No cutoff identified
(21) 374 (45%) (mRS ≥4)
Bhattathiri et al. Prospective Favorable functional 6 31vs. 15% (p < 0.00001), when IVH No cutoff identified
(22) 902 (42%) outcome (GOS ≥4) absent vs. present
Hallevi et al. Retrospective Poor functional outcome 3 OR = 3.4, 95% CI = 2.21–5.09 No cutoff identified
(7) 406 (45%) (mRS ≥4) (p < 0.0001)
Bhatia et al. Prospective Mortality predictor Hospital OR = 2.66, 95% CI = 1.31–5.41 No cutoff identified
(12) 214 (48%) discharge (p = 0.007)
Mustanoja et al. Prospective Mortality rates 3 54 vs. 18% (p < 0.001) No cutoff identified
(13) 967 (41%)
ICH WITH/WITHOUT IVH (GRADED BASED ON SEVERITY)
Morgan et al. Databank Poor functional outcome 3 Increasing modified Graeb scores Modified Graeb Score used
(25) 1,250 (32%) (mRS ≥3) correlate with poor outcome. as a continuous variable
OR = 1.12, 95% CI = 1.05–1.16 No cutoff identified
(p < 0.0001)
ICH WITH/WITHOUT IVH (GRADED BASED ON DEFINED SEVERITY CUTOFFS)
Godoy et al. Prospective Rate of favorable functional 6 36.4 vs. 14.7% vs. 16.7% for Graeb Graeb score 1–4 vs. 5–8
(23) 153 (48%) outcome (GOS ≥4) scores of 1–4, 5–8, and 9–12, vs. 9–12
respectively (p = 0.20) Included patients with
infratentorial
and supratentorial location
Nishikawa et al. Retrospective Functional outcome hospital OR = 3.96, 95% CI = 0.90–17.38; Graeb score ≤5 vs. >5
(9) 100 (35%) (KPS 50–100) discharge (p = 0.068)
Hansen et al. Prospective Survival and poor functional 1 and 3 Increasing modified Graeb scores Survival was analyzed by
(6) 198 (43%) outcome correlate with 30 days survival, OR = 1.16; modified Graeb scores divided
(mRS ≥4) 95% CI = 1.06–1.27 (p = 0.002) and poor into quartiles: the third and fourth
outcome OR = 1.11, 95% CI = 1.02–1.20 quartiles had worse survival vs.
(p = 0.011) first and second quartiles

GOS, Glasgow Outcome Score; KPS, Karnofsky Performance Status Scale; IVH, intraventricular hemorrhage; mRS, modified Rankin Scale.

accuracy of our prediction models but did not identify a severity IVH extension as a dichotomized variable decreases the accuracy
threshold that could be used for prognostication purposes. of the prognostication tools commonly used in clinical practice.
Three studies investigating the association of pre-specified Our study has some limitations, including the relatively small
cut-off values with outcome showed mixed results for IVH sample size of patients with IVH extension. However, the sample
extension severity. In one of these studies, Graeb score size of our study is larger compared with previously reported
≥5 was associated with increased functional impairment at studies that looked at IVH extension severity and outcome.
hospital discharge (9). In another study, increasing IVH severity Second, functional outcome using mRS was determined at time
estimated using the Graeb scale with patients divided into of hospital discharge. Although 3- and 6-month outcomes are
quartiles correlated with decreased survival and functional preferable to report functional outcome, these data were not
independence (6). In contrast, another study of 153 patients with readily available for our cohort. Third, our study included only
sICH showed that increasing IVH extension severity measured patients with supratentorial sICH. Thus, these results cannot be
using Graeb score divided into tertiles was not significantly extrapolated to infratentorial ICH or ICH resulting from vascular
associated with 30-day mortality or disability at 6-months (23). malformations, tumor, or trauma. Fourth, in this study we used
These studies are summarized in Table 6. A direct comparison the Graeb score and did not look into the predictive value of
of our study with those presented in Table 6 is prevented by the other semiquantitative tools such as the modified Graeb score,
exclusion of sICH cases with infratentorial location in this series, IVH score, or LeRoux score. Increased IVH extension severity,
variations in the outcome measures, differences in follow-up, measured by any of these scores correlates with poor outcome
and other methodological details. However, all studies, including (24, 25). However, additional studies are necessary to determine
ours, confirm that IVH extension volume is a key contributor the severity cut-off points for these scoring systems.
to patient outcomes just like hematoma volume. In particular In conclusion, we showed that increased IVH extension
our study provides a unique perspective by showing outcomes severity, defined by a Graeb score ≥5, is an independent predictor
data for each degree of IVH extension severity and identifies an of poor outcome at hospital discharge after sICH. When using
IVH extension severity cutoff of Graeb ≥5 as a predictor of poor risk stratification tools for clinical severity grading after sICH,
neurologic outcome. Our study also highlights that the use of IVH extension should be given different weights based on the

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Trifan et al. IVH Severity and Outcome in ICH

amount of IVH extension present, rather than being used as a AUTHOR CONTRIBUTIONS
dichotomized variable.
FT and GT contributed conception and design of the study. GT
DATA AVAILABILITY organized the database and wrote the first draft of the manuscript.
GT and FT performed the statistical analysis. GT, FT, and BA
The datasets generated for this study are available on request to wrote sections of the manuscript. All authors contributed to
the corresponding author. manuscript revision, read, and approved the submitted version.

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of outcomes in intracerebral hemorrhage: data from the Helsinki ICH Study. under the terms of the Creative Commons Attribution License (CC BY). The
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DW, et al. Withdrawal of support in intracerebral hemorrhage publication in this journal is cited, in accordance with accepted academic practice.
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Frontiers in Neurology | www.frontiersin.org 6 March 2019 | Volume 10 | Article 217