Surgical Neurology 63 (2005) 343 – 348

www.surgicalneurology-online.com

Factors influencing outcome in intracerebral hematoma: a simple, reliable,

and accurate method to grade intracerebral hemorrhage
Mark Shaya, MDa, Arvind Dubey, MDa, Caglar Berk, MDa, Eduardo Gonzalez-Toledo, MD, PhDb,
John Zhang, MD, PhDa, Gloria Caldito, PhDc, Anil Nanda, MD, FACSa,*
Departments of aNeurosurgery, bPathology, and cBiometrics, Louisiana State University Health Sciences Center in Shreveport,
Shreveport, LA 71130-3932, USA
Received 18 March 2004; accepted 3 June 2004

Abstract Background: Intracerebral hemorrhage (ICH) is a major public health problem. This subset of
stroke often coexists with other serious medical problems such as hypertension, diabetes, and
obesity. Management of hemorrhagic stroke is controversial and there is no standardized system for
assessing presentation and predicting outcome of this disease. We propose a new grading system
based on clinical and radiologic factors important in influencing outcome in ICH that can be used by
the entire health care team.
Methods: We conducted a retrospective study of the last 50 patients who presented with
hypertensive ICHs to Louisiana State University Health Sciences Center in Shreveport during 2001
to 2003. Significant predictors of outcome at 6 months as measured by the Glasgow outcome score
(GOS) were determined and a grading system based on clot volume, hydrocephalus on initial
computed tomographic scan, and focal neurologic deficit was formulated.
Results: Three factors observed to have significant association with GOS were presence of a focal
neurologic deficit on initial presentation ( P = .003), presence of hydrocephalus on initial computed
tomographic scan ( P b .0001), and clot volume ( P = .003). Patients were scored on these variables
as follows: absence of any focal neurologic deficit (1 point); neurologically intact (1 point); absence
of hydrocephalus (1 point); and clot volume b20 mL (3 points), 20 to 50 mL (2 points), and N50 mL
(1 point). The scores were summed to assign an ICH grade to each patient for predicting his GOS at
6 months. Given the nonsignificant difference between a patient’s grade and his actual observed
GOS (mean difference 0.04, P = .79), as well as their significant correlation (correlation coefficient =
0.76, P b .0001), we believe our grading system is useful for predicting a patient’s GOS.
Conclusion: An accurate and reliable grading scale for ICH is helpful in standardizing the
management of ICH, improving communication of patient presentation among health care workers,
and predicting outcomes.
D 2005 Elsevier Inc. All rights reserved.
Keywords: Intracerebral hemorrhage; Outcome; Glasgow outcome scale; Hypertension

1. Introduction to an $8 billion cost to society to treat new cases of ICH

annually. Although ICH accounts for about 10% to 15% of
Intracerebral hemorrhage (ICH) is a major public health
all strokes, there is generally greater morbidity and mortality
problem in the United States. The estimated lifetime cost for
with hemorrhagic strokes than with other types of strokes.
a new case of hypertensive ICH is over $120 000 [16]. There
Predisposing factors for hemorrhagic stroke are uncon-
are about 70 000 new cases of ICH annually. This translates
trolled hypertension, diabetes, smoking, obesity, and use of
stimulant drugs. African Americans are more prone to this
* Corresponding author. Tel.: +1 318 675 7352; fax: +1 318 675 7111. type of stroke than are Caucasians (50 per 100 000 versus
E-mail address: ananca@lsuhsc.edu (A. Nanda). 28 per 100 000, respectively) [13]. Management of hemor-
0090-3019/$ – see front matter D 2005 Elsevier Inc. All rights reserved.
doi:10.1016/j.surneu.2004.06.019
344 M. Shaya et al. / Surgical Neurology 63 (2005) 343–348
rhagic stroke is also a controversial subject, with some
centers surgically evacuating clots and others using more
conservative management [1,9,12,20]. There is no clear
definition for the proper indications for surgery in this
condition.
Because ICH is a common disease in areas where
uncontrolled hypertension is prevalent, having a scale to
assess patients on initial presentation may help in assessing
severity of disease, dictating aggressiveness of intervention,
and predicting outcome. What is needed is a simple,
reproducible, and accurate grading system for ICH. Thus
far, some scoring models have been proposed that take into
account Glasgow coma score (GCS), age, and findings on
radiographs. We analyzed 50 consecutive patients who
presented with ICH and we were able to identify factors that
are significant in relation to outcome. Furthermore, we have
devised a useful and reliable predictive scoring system for
ICH, which is currently in use at our hospital and local
emergency rooms that regularly refer patients with hyper-
tensive bleeds. We will also present 10 consecutive patients
where our proposed grading system was used at initial
presentation and then followed up prospectively.
2. Subjects and methods
2.1. Patient selection
We performed a retrospective study of patients present-
ing with hypertensive bleeds. Charts of 50 patients with
nontraumatic, first-time ICH presenting initially to Louisi-
ana State University Health Sciences Center in Shreveport
(LSUHSC-S) were reviewed. None of our subjects had
prior ischemic or hemorrhagic strokes. Nine patients in our
original database search were transferred from outlying
clinics, as our hospital is the major referral center for the 3-
state area (Louisiana, eastern Texas, and southern Arkan-
sas). These patients were not included in our study because
they did not receive their initial treatment at LSUHSC-S.
Only medical record numbers were used to identify
patients and no reference was made to names anywhere
in our data retrieval and analysis. This study was
conducted according to the consent and confidentiality
guidelines of LSUHSC-S.
2.2. Data retrieval
Emergency room histories and intensive care unit flow
sheets were reviewed, and data on the following variables
were recorded for data analysis: age, race, presenting blood
pressure, mean arterial pressure after stabilization, comor-
bidities, compliance with medication, smoking history, use
of illicit drugs or stimulants, ICP range (if they required a
ventriculostomy), and GCS on discharge. None of the 50
patients had surgery for their hematomas, because medical
management is our principal method of treatment of deep
hypertensive bleeds. None of the hemorrhagic strokes
studied showed evidence of clot reaching the surface of
the cortex. Radiographs were reviewed by our neuroradiol-
ogist to determine the exact location of the hypertensive
bleed, presence and severity of hydrocephalus, degree of
midline shift, degree of ventricular extension, and volume of
the clot. Volume of clot was determined using the ABC/2
method of Kothari et al [10]. Patients were divided into 3
categories based on the volume of clot (b20, 20-50, and N50
mL). The notes from clinic visits were also reviewed to
determine the Glasgow outcome score (GOS) at 6 months. If
no clinic visit was located, a telephone interview was
arranged and the GOS was determined by speaking with the
referring doctor, patient, or family.
2.3. Statistical analysis
We tested for significant association of GOS at 6 months
with each of the above-mentioned clinical and radiologic
variables using logistic regression analysis for an ordered-
category outcome. Significant predictors of GOS were
determined using both simple and multivariable models.
We devised a scoring system for obtaining a predictive
index for GOS using variables found to be significantly
associated with it. We then compared and correlated our
resulting predictive index with the actual GOS values. We
tested our hypothesis of no significant difference between
the predicted and the actual GOS values using the Wilcoxon
signed rank test and determined significant correlation
between the two using the Spearman rank correlation
coefficient. SAS version 8.2 was used for statistical
computing and a 5% level of significance was used for all
statistical tests.
3. Results
Mean age at presentation was 55.6 years (range 21-92
years) and mean GCS on admission was 11.2 (range 3-15).
Fifty percent of our patients (n = 25) were male and 72% (n =
36) were African Americans. Fifty-two percent (n = 26) were
greater than one-pack-per-day smokers and 20% (n = 10) had
a history of taking an illicit drug within 1 week of
presentation. Among our 50 study subjects, initial mortality
(within 1 week) was 18% (n = 9). Mortality at 6 months was
18% (n = 9), because patients who survived the first week
were able to survive past 6 months. At 6 months, 44% (n =
22) had a GOS of 5 (neurologically intact, able to perform
usual daily activities).
The most common comorbidity in our patients was
hypertension followed by diabetes and obesity. Mean
systolic blood pressure on arrival was 192 (range 148-
280), and mean diastolic pressure on admission was 106
(range 84-148). Those patients with a history of stimulant
drug use presented with higher blood pressures (mean
systolic blood pressure 215 and mean diastolic pressure 118
in stimulant users) than patients with no history of drug use
(mean systolic blood pressure 190 and mean diastolic
pressure 100). Twenty-six percent of patients (n = 13) were
noncompliant with blood pressure medications, which were
 M. Shaya et al. / Surgical Neurology 63 (2005) 343–348
Table 1
Significant predictors for GOS among ICH patients using univariate analyses
Factor P Odds ratio
No focal neurologic deficit .003
Absence of hydrocephalus b .0001
No ventricular extension of clot .002
High GCS on admission b .0001
Low clot volume .003
Minimal midline shift b .0001
prescribed within the last 2 years. Location of hypertensive
bleeds occurred most commonly in basal ganglia (60%),
thalamus (11%), and caudate (9%). This study does not use
location as a factor for prognosis; however, some recent
studies support the use of location as a prognostic factor [7].
Because we did not study infratentorial hemorrhages,
location was not a crucial factor in studying these deep
supratentorial hemorrhages. Mean clot volume was 19.1 mL
(range 0.4-74.3 mL) and mean midline shift was 3.2 mm
(range 0-10.7 mm). Thirty-two percent of patients (n = 16)
showed hydrocephalus (presence of dilated ventricles and/or
prominent temporal horns) on initial computed tomographic
(CT) scan and 48% (n = 24) showed evidence of ventricular
extension of the clot.
Using simple logistic regression models (separate uni-
variate analyses), significant predictive factors of a good
GOS were the absence of any focal neurologic deficit,
absence of hydrocephalus on initial CT scan, high GCS on
admission, low clot volume, minimal midline shift, and no
ventricular extension of the clot. The resulting P values and
the corresponding odds ratios are shown in Table 1.
The patients in this study who were assigned a grade of
5 (meaning clot volume N50 mL, presence of hydroceph-
alus, and focal neurologic defect present) all died (n = 8).
All of those who were given a grade of 1 (small clot,
without hydrocephalus, and absence of a neurologic defect)
lived (n = 18). Of these 18 patients, 16 had a GOS of 5 and
only 2 had a GOS score of 4.
Age, sex, blood pressure, ICH location, and presence of
comorbidities were not associated with GOS. Predictors of
initial mortality (within 1 week) were GCS on admission,
ventricular extension, and volume of clot. Using a
multivariable logistic regression model and a stepwise
selection of variables among the above significant factors,
GCS on admission and clot volume were the only
Table 2
Grading ICH using points
Variable
Clot volume (mL) b 20
20 -50
N 50
Hydrocephalus Absent
Present
Focal neurologic deficit Absent
Present
345
95% Confidence interval for odds ratio
14.3 2.5-81.4
77.4 9.6-623.7
8.5 2.3-31.9
2.02 1.4 -2.8
0.95 0.91-0.98
0.63 0.5-0.8
independent significant predictors of GOS, suggesting that
an efficient ICH grading system can be formulated based on
these 2 factors. However, we did not use GCS on admission
to determine an ICH grade, as it does not take into account
radiologic and clinical factors, which may predict worse
outcome. For our ICH grading system, we incorporated
only patient information on focal neurologic deficit,
hydrocephalus, and clot volume, as these are important
clinical variables that the physician can readily measure at
the time of admission. We designed a succinct grading
system that can easily be communicated to health workers
and that can quickly be determined at time of admission.
Our scoring system for ICH using clot volume, hydroceph-
alus, and presence of focal neurologic deficit as applied to
our 50 patients is shown in Table 2. The ICH grade was
determined by adding up the points for a potential score of
1 to 5.
Using the calculated ICH grade of a patient to predict his
GOS, we compared and correlated the predicted (ICH
grade) and actual observed GOS scores. Mean difference
between the predicted and the actual GOS scores is 0.04
with an SE of 0.15 ( P = .79). The Spearman correlation
coefficient between the predicted and the observed values
was 0.76 ( P b .0001). Given the nonsignificant difference
between the predicted and the actual observed GOS and the
highly significant correlation between them, we can
conclude that our ICH grading system for predicting GOS
at 6 months is reliable.
4. Discussion
Grading systems for neurologic disease are important to
identify critical patients, communicate information about
patients, and give some idea of patient outcome [6,14,15].
The GCS is the most widely used scale in neurology and can
be used for both traumatic and nontraumatic disease. For
ICH, there is still no widely used, standardized scale for
assessing patients. An ideal scale would take into account
clinical and radiologic factors, which give an indication of
Points
disease severity at initial presentation and predict how the
1 disease will progress. Having a standardized grade would
2
3
allow for better administration of treatment and may help to
0 better classify patients participating in research protocols.
1 Many grading systems have been proposed thus far and
0 provide some information on patient prognosis [2,3,11,17-
1 19]. Grading systems described previously are limited in that
346 M. Shaya et al. / Surgical Neurology 63 (2005) 343–348

which can result or contribute to a worse outcome than

Fig. 1. This patient initially presented with a GCS of 12; however, he also
had large clot volume and hydrocephalus and presented with a neurologic
deficit. This patient was assigned a grade 5 according to our grade. He
expired 1 day after presenting to the emergency room.
they often place emphasis on 1 radiologic or clinical factor
that predicts poor outcome (ie, ventricular extension of
blood, GCS on admission, and hydrocephalus). Other
grading systems are not easy to use and would not be
practical in an emergency situation. A grading system, which
takes into account certain radiologic features along with a
brief clinical assessment, would be useful in patient triage
and management. In addition, this grading system should be
easy to use by every member of the health care team, and no
special training should be required. Assessing a patient’s
ICH grade should be fast, and an assessment using our
grading system can be done in a few minutes.
The GCS is the most widely used neurologic grading
system. In fact, it is an accurate predictor of outcome at 6
months as was shown in many previous studies [2,8,11,18].
However, the GCS score does not take into account critical
radiologic factors (such as hydrocephalus and clot volume),
would have been predicted just with an initial GCS score.
For example, a patient with a clot of 55 mL and extensive
hydrocephalus may have had a reasonably good examina-
tion in the emergency room, only to be intubated and in
critical condition in the intensive care unit a few hours later
(Fig. 1). Our grading system takes into account radiologic
predictors of worse outcome so that a good GCS score with
a worrisome CT scan would be given a score appropriate for
the predicted outcome.
The grading system we are proposing is consistent in
predicting those patients who will survive and those who will
not survive a supratentorial hypertensive bleed. A grade 5
consistently predicts death and a score of 1 or 2 consistently
predicts survival. If one groups patients who were given a
grade of 3, 4, or 5 (n = 20), 16 were permanently disabled or
died by 6 months. If one groups those with a grade of 1 and 2
(n = 30), 29 had at least a GOS of 4. In the prospective arm of
this study, which is currently under way at LSUHSC-S, this
grading scheme is accurate and consistent in predicting
survival, disability, and death from hypertensive bleed. Our
proposed grading system was used prospectively in 10
consecutive patients, and initial ICH grade correlates well
with the GOS at 6 months (Table 3).
Our grading system assesses 1 clinical and 2 radiologic
factors. Neurologic deficit in our grading system takes into
account any major deficit that is evident on initial
presentation (arm weakness, hemiplegia, leg weakness,
facial droop, etc). Hydrocephalus is determined on CT scan
by the presence of dilated ventricles, prominent temporal
horns, or a dilated third ventricle. In certain situations,
intraventricular blood may be evident and an external
ventricular drain (EVD) is used for drainage of blood.
These situations would score 1 point for hydrocephalus,
because a drain has been used emergently and hydroceph-
alus would have been inevitable if no intervention were
done. Patients who required an EVD in our study (n = 8)
had a frontal burr hole placed in the emergency department
or the intensive care unit on the side opposite the ventricular
blood (Fig. 2). The EVD is weaned by raising the drain
about 5 cm H2O per day, provided their neurologic

Table 3
Summary of data for 10 patients with ICH where our proposed grading system was used and followed up prospectively
Patient no. Age (y)/sex Location Volume (mL) Hydrocephalus Focal neurologic deficit Grade GOS at 6 mo
1 89/F L thalamus 55 Present Present 5 1
2 40/M R basal ganglia 16 Absent Present 2 4
3 48/M L basal ganglia 37 Present Present 4 3
4 64/F L basal ganglia 70 Present Present 5 1
5 45/F R thalamus 13 Absent Absent 1 5
6 61/M L basal ganglia 6 Absent Absent 1 5
7 54/M R basal ganglia 22 Absent Present 3 3
8 60/M R basal ganglia 16 Present Absent 2 4
9 61/M L thalamus 65 Present Present 5 1
10 45/F L basal ganglia 58 Present Present 5 1
 M. Shaya et al. / Surgical Neurology 63 (2005) 343–348
Fig. 2. Extensive right frontal bleed with left frontal external ventricular
catheter. This patient was assigned a grade 3 and is currently in a
rehabilitation facility.
examination remains stable. Patients who fail EVD weaning
require shunt placement.
Patient age was shown not to be associated with outcome
in our study as has been shown by others [2,8,11,18].
Hemphill et al [5], however, did find that age was an
independent predictor of ICH outcome; therefore, age was
used in their method of determining an bICH scoreQ [5]. In
our study, our 2 oldest patients (a 93-year-old woman and an
89-year-old man) had a GOS of 5 and 4, respectively. Older
patients have more brain atrophy than younger patients, and
this may afford the older patient more space for brain
swelling and allow parenchyma to move more freely than in
a younger brain.
Regarding clot volume, we divided our patients into 3
groups based on clot size: small, medium, and large.
Whereas others have made the cutoff points at 30 and 60
mL for these divisions, we decreased these numbers to 20
and 50 mL. A small clot in our study was b20 mL, a
medium clot was 20 to 50 mL, and a large clot was N50 mL.
The reason for this is that, in our experience, we encountered
many clots that were b30 mL but, because they were located
medially (ie, thalamus), they were able to cause significant
neurologic deficit and cause intraventricular blood and
hydrocephalus (Fig. 3). Larger bleeds situated more laterally
may not be as dangerous as smaller bleeds that penetrate the
ventricular areas.
None of the patients in our study had surgery for their
hematomas. The Surgical Treatment for Intracerebral
Hemorrhage trial is a large, multicenter, randomized
controlled trial involving over 60 countries, 1300 accumu-
347
lated patients, and a 10-year time span. The Surgical
Treatment for Intracerebral Hemorrhage trial has shown
that urgent surgery does not appear to make much difference
in outcome [4]. We reserve surgery only for special cases
where the hematoma comes to the surface of the cortex and
there is significant benefit from performing an emergent
decompression.
Control of hypertension is the primary preventive
measure for ICH. Compliance with blood pressure medica-
tion has proven to be an important factor in our study,
because about 80% of our patients were noncompliant with
their blood pressure medications. Once an ICH occurred,
however, patients fared no better if they had been on blood
pressure control previously. Most of the patients in our study
who did not take their blood pressure medications did not
attend clinics regularly for blood pressure control and did not
fill prescriptions regularly. Due to the high numbers of
noncompliant patients in our study, we feel that prevention of
ICH through blood pressure control may be the most
practical approach in dealing with this disease at the present
time. Seventy-two percent of our patients were African
Americans. This stresses the fact that minorities may be
disproportionately affected by ICH, especially in areas where
comorbidities such as obesity, hypertension, and diabetes are
common. Minority awareness of ICH and community
programs that address blood pressure control and diabetic
teaching should be supported and encouraged. Programs that
teach about the dangers of obesity and drug use should be
started at an early age, especially in communities where
hypertension is common. As prevention may be the best way
to treat ICH, this fact cannot be stressed enough.
Fig. 3. A 62-year-old hypertensive patient who was noncompliant with her
blood pressure medication presented with right hemiparesis. CT scan shows
a small clot (18 mL) in the left thalamus causing significant intraventricular
blood and hydrocephalus due to its medial location. This patient was
assigned a grade 3. She required a tracheostomy and is undergoing
rehabilitation.
348 M. Shaya et al. / Surgical Neurology 63 (2005) 343–348
5. Conclusion
Our results show that using a grading system for ICH is a
fast, reliable, and reproducible method to assess the patient
and predict outcome from supratentorial hypertensive
intracranial hemorrhage. If neurologic examination dis-
closes any neurologic deficit and if CT scan shows a large
clot with hydrocephalus, these patients consistently do
poorly. Comorbidities of ICH such as hypertension, obesity,
and diabetes should also be identified, and prevention
should be a priority in areas where hypertension is common.
Our proposed grading system is currently in use at
LSUHSC-S and is useful in predicting patient outcome
and communication of severity of disease among health care
workers.
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Commentary
The article by Shaya et al describes a grading scale for
ICH in patients based on clinical and radiologic observa-
tions in the emergency room. They have done a retrospec-
tive study and a prospective study, testing their rating scale.
It appears to be a practical scoring system that could be
useful for clinicians who see these patients emergently.
The patient population described involved mostly deep
ICHs. Hence, their philosophy in nonoperation seems
appropriate. Surprisingly though, relatively few were
superficial, pointing on the surface and lobar in location.
Furthermore, the location of the hematoma as a clinical
factor was not important in their study, which is surprising,
because many other authors in the past have found large
hematomas in the frontal or temporal region that are
dynamic and do change the clinical course significantly
during the first 24 hours post ictus.
The article has value for clinicians because it approaches
a controversial subject with a grading scale that appears to
be useful. A prospective study currently under way at
LSUHSC-S will be interesting to follow, particularly if it
validates their method and if the spectrum of hematomas is
more consistent with that seen around the globe.
Julian T. Hoff, MD
Department of Neurosurgery
University of Michigan Medical Center
Ann Arbor, MI 48109-0338, USA