From the Department of Neurology(M.N.D., D.F.E., A.R.Z.) and Program in
Occupational Therapy (M.N.D., D.F.E.), Neurology/Neurosurgery Intensive Care
Unit, Washington University School of Medicine, St Louis, Mo.
Methods—Patients with spontaneous
supratentorial ICH were identified in our
prospectively collected database to determine the following: age, sex,
race, past medical history; Glasgow Coma Scale (GCS) score and blood
pressure on admission; use of mechanical ventilation, mannitol, and
ventriculostomy; and medical complications. CT scans performed within
24 hours of hemorrhage were retrospectively analyzed to
determine lesion size and location, pineal shift, cisternal effacement,
intraventricular hemorrhage (IVH), and
hydrocephalus. Outcome was determined with use of hospital disposition
(dead, nursing home, rehabilitation, home) and functional outcome
(Functional Independence Measure [FIM]) at 3 months. Patients with
and without hydrocephalus were compared and univariate and
multivariate analyses performed to determine
whether hydrocephalus was an independent predictor of mortality. Data
are presented as mean±SD.
Results—Of the 81 patients studied, 40 had hydrocephalus. Those
with hydrocephalus were younger (57±15 versus 67±15 years), had lower
GCS scores (8.2±4.2 versus 11±2.9), were more likely to have
ganglionic or thalamic hemorrhages, and were intubated more
frequently (70% versus 27%). Hospital mortality was higher in
patients with hydrocephalus (51% versus 2%), and fewer patients went
home (21% versus 35%). Those who died had higher hydrocephalus scores
(9.67±7.1 versus 5.75±4.5). Outcome was no different if a
ventriculostomy was placed. The final logistic regression model
included hydrocephalus score, gender, GCS, and pineal shift, and it
correctly predicted 85% of patients as dead or alive.
Multivariate analyses indicated that
hydrocephalus is an independent predictor of mortality.
Conclusions—We conclude that hydrocephalus is an independent
predictor of mortality after ICH.
Therapeutic options for patients with ICH are limited; the efficacy of
surgical intervention has not been clearly established, and medical
management, including treatment of hypertension9
and use of osmotic agents, remains
controversial.10 11 In addition, despite its
frequent use, the role of ventriculostomy in the management of
hydrocephalus following ICH is not well defined.
Through the use of our prospectively collected clinical database, we
sought to investigate the relationship between hydrocephalus and
outcome in ICH. CT scans were retrospectively analyzed to
determine lesion size and location, degree of pineal shift, cisternal
effacement, IVH, and hydrocephalus. These variables were correlated
with clinical features, treatment and outcome with
univariate and multivariate
analyses.
Clinical Data
Clinical Management
Decision to withdraw therapy was always made after extensive
discussions with the patient's family. Such decisions were based on
the expressed wishes of the patient or a designated surrogate. The
discussions were always initiated in the setting of a very poor
neurological condition that was either not improving or deteriorating
despite aggressive therapy.
CT Analysis
Although several scoring systems exist for grading hydrocephalus, none
can be applied to situations in which a mass lesion distorts normal
brain anatomy.15 16 We therefore
developed a system that grades each of 8 portions of the
ventricular system independently. The hydrocephalus score
was determined by grading the frontal horn, atrium, and temporal horn
of each lateral ventricle and the third and fourth ventricles. Each
region was graded as mild or moderate or marked using the following
criteria: frontal horn, rounding with increased radius, decreased
ventricular angle, and sulcal effacement of the frontal
lobe; atria, rounding and enlargement with sulcal effacement of the
parieto-occipital lobe; temporal horns, increasing width; third
ventricle, increased width with ballooning of the anterior recess; and
fourth ventricle, ballooning. A score of 0 for no, 1 for mild, 2 for
moderate, and 3 for marked hydrocephalus was assigned to each region
and the scores summed. A total score of 0 indicates no hydrocephalus
and the maximum score of 24 indicates marked hydrocephalus of all
ventricles.
Statistical Analysis
In order to determine intrarater and interrater reliability of the
hydrocephalus score 14 CT scans were selected and scored independently
by two observers (M.N.D. and A.R.Z.) as well as on two separate
occasions by one observer (A.R.Z.). Intraclass correlation coefficients
for intrarater and interrater hydrocephalus scores were 0.83 and 0.92,
respectively.
A series of analyses were performed to derive a model to
identify factors related to hospital mortality, which was compared to
the actual outcome. Continuous variables were converted to binary
variables using the following cut points: GCS score (
Univariate logistic regression equations were then computed
for each potential predictor variable. Variables were included
in the multivariate analysis if the
univariate P value was
The incidence of hydrocephalus was higher in patients with deep
hemorrhages (P<0.001; Table 2
As expected, patients with hydrocephalus were significantly more likely
to receive a ventriculostomy (P<0.001). Only 1 patient
without hydrocephalus in the retrospective CT scan analysis had
a ventriculostomy placed compared with 12 patients (30%) with
hydrocephalus. Those with hydrocephalus were more frequently intubated
(70% versus 27; P<0.0001), most likely a reflection of
their lower GCS scores. The incidence of congestive heart failure,
seizures, and pneumonia did not differ between those with and without
hydrocephalus.
Outcome differed considerably between the groups (Table 3
Outcome did not differ in those patients treated with a
ventriculostomy. Hematoma size tended to be smaller (19.8±22.1 versus
38.5±34.7 cc; P=0.09) and IVH score was higher (7.4±3.6
versus 3.9±2.6; P<0.004) in those treated with
ventriculostomy, whereas age and GCS score did not differ. Mortality,
hospital disposition, and FIM score at 3 months did not differ between
those patients treated with and without a ventriculostomy.
Univariate logistic regression analyses were
computed to determine the relationship between individual predictor
variables and mortality. The parameter estimates,
standard errors, ORs, and P values of each of these
variables are presented in Table 4
The final multivariate logistic regression model and
the variables not included in the final model are presented
in Table 4
Over the past 2 decades a large number of investigators have attempted
to define factors associated with outcome from ICH. Predictors of
outcome in early studies17 18 19 20 21 included age, ICH
location, electrocardiagraphic abnormalities, and history of
hypertension. More recent studies3 5 22 23 24 have
also identified lesion size, level of consciousness, midline shift,
blood pressure or pulse pressure, and IVH as factors related to
outcome.
Review of these studies reveals considerable variability in the factors
identified. Some of this variability results from the statistical
techniques used, because the univariate analyses
used in early studies determine only whether a single factor is related
to outcome. The more recent studies applied
multivariate regression analyses; these
determine which of several factors, when taken together, relate to
outcome. This technique has the advantage of being able to determine
whether 2 factors covary and only 1 independently predicts outcome.
Factors identified with multivariate techniques include
age, ICH size, level of consciousness, IVH, and pulse pressure.
Despite the frequency with which it occurs in ICH patients, none of
these studies included hydrocephalus in their analyses. The
reason for this omission is not clear, although it may reflect the fact
that a means of quantifying hydrocephalus in the setting of ICH did not
exist. Previously available methods for defining hydrocephalus all
relied on the relationship between ventricular size and
shape and the anatomy of the surrounding
tissues.15 16 In the presence of a mass lesion
that distorts the normal anatomy, these methods cannot be
applied. Additionally, the mass of the hematoma may compress sites of
communication within and between ventricles, leading to "trapped
ventricles." In an attempt to overcome these problems, we chose to
analyze separate regions of each lateral ventricle as well as
the third and fourth ventricles independently. The results of our
intrarater and interrater reliability testing indicate that the scale
can be applied in a consistent and reliable manner.
We used several approaches to determine whether hydrocephalus is an
independent predictor of mortality. The OR of 1.26 (95% confidence
limits, 1.13 to 1.42) in the univariate analysis
indicates that hydrocephalus is a predictor of mortality. The
present multivariate analysis included all
potentially confounding variables identified by our
univariate analyses and the literature. This model
yielded an OR of 1.63 (1.20 to 2.31) for hydrocephalus, which suggests
that it is an independent predictor of mortality. Surprisingly, the
addition of hydrocephalus to the model resulted in some previously
identified predictors of outcome (size, IVH) being forced out of the
model. This suggests that size and IVH may be surrogates of the more
direct predictor—hydrocephalus. Caution should be exercised in
interpreting this finding, however, since these results await
validation with an independent data set. This model correctly
classified as alive or dead 85% of the patients, a degree of accuracy
very similar to previously published models.
The relationship between hydrocephalus and outcome may vary with
different hemorrhage locations. In hematomas that occur close
to the ventricles, IVH and thus hydrocephalus are
common.25 Small thalamic hemorrhages can
easily cause hydrocephalus by compressing the cerebral aqueduct,
whereas small ganglionic hemorrhages rarely have any impact on
ventricular size. The relationship between hydrocephalus
and hematoma location was explored using an interaction term; however,
despite the rate of hydrocephalus differing by location, the
interaction term did not improve the predictive power of the model.
The association we found between male gender and increased mortality
was unexpected. Although previous studies had not identified such a
relationship, few studies searched for it. Two studies report a trend
toward increased mortality in males that was not statistically
significant.4 26 We plan to assess the robustness
of this finding by validating the model with an independent data
set.
A considerable number of patients in this study (16 of 81; 20%) had
therapy withdrawn. All but 2 of these patients died, and the 2
survivors were left with significant functional impairment (FIM scores
of 41 and 65). The majority of those patients who had care withdrawn
were those with hydrocephalus. While this could potentially complicate
the interpretation of these data, it must be considered that decisions
to withdraw care were made on the basis of the individual patient's
condition, lack of improvement, and expressed wishes, independent of
whether or not the patient had hydrocephalus. The withdrawal of care
must be taken into account when predictive models are developed.
Ideally, to develop an accurate model, all patients should receive
maximal therapy. The current ethical and social climate makes this
impossible. Therefore, although not done in the vast majority of
published reports on outcome from ICH, it is important to report the
frequency of this occurrence to facilitate interpretation of the
data.
While this study clearly demonstrates the relationship between the
presence of hydrocephalus and poor outcome, the impact of treatment of
hydrocephalus with ventriculostomy is much less clear. Our previous
report27 indicated that placement of a
ventriculostomy rarely led to clinical and radiographic
improvement and was associated with a high mortality rate. That study,
however, included only patients treated with ventriculostomy. The
present study includes patients with hydrocephalus regardless of
whether a ventriculostomy was placed, and there was no difference in
outcome. It is important to note that patients were not randomized and
that decisions to place a ventriculostomy were clinically based; thus,
it is not possible to exclude the chance that those treated with a
ventriculostomy might have had a worse outcome had the procedure not
been performed. This question can be answered only by a prospective
randomized study. In addition, the lack of an apparent response to
ventriculostomy may have resulted from failure of the
ventricular catheter to adequately drain cerebrospinal
fluid because of obstruction by IVH. The use of
thrombolytics instilled into the catheter may be
helpful in this setting and should be investigated in a controlled
trial.
Received March 9, 1998;
revision received April 24, 1998;
accepted April 24, 1998.
© 1998 American Heart Association, Inc.
Original Contributions
Hydrocephalus: A Previously Unrecognized Predictor of Poor Outcome From Supratentorial Intracerebral Hemorrhage
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—Although
several factors have been identified that predict outcome after
intracerebral hemorrhage (ICH), no previous
study has investigated the impact of hydrocephalus. The purpose of this
study was to determine whether the presence of hydrocephalus after ICH
would predict mortality and functional outcome.
Key Words: hydrocephalus • intracerebral hemorrhage • intraventricular hemorrhage • stroke outcome
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
There has been
considerable interest in predicting outcome after ICH. A number of
studies have investigated the relationship among clinical and
radiographic factors and outcome.1 2 3 4 5 6 7 8
Several variables have been found that predict mortality, although
they are not consistently identified across studies. Clinical
factors recognized include level of consciousness measured by the GCS
score, age, blood pressure, and pulse pressure.
Radiographic features include hematoma size, midline shift,
and the presence of IVH. None of these studies have investigated the
influence of hydrocephalus or the use of ventriculostomy on
outcome.
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
We prospectively record information on all admissions to the
neurology/neurosurgery ICU of a tertiary care academic hospital using a
computerized database (QUiC, Space Labs Inc). Data collected include
demographics, past medical history, clinical presentation,
diagnoses, treatments, complications, and outcome. On a daily basis an
individual nurse collects and records data using strict guidelines.
The database was searched to identify all patients admitted with a
primary diagnosis of supratentorial ICH over a
20-month period. Patients were excluded if the hemorrhage was
associated with trauma or subarachnoid hemorrhage or if
a CT scan performed within 24 hours of the hemorrhage was not
available. The study was approved by the institution's Human Studies
Committee.
The following historical data were included in the
analysis: age, sex, race, history of hypertension, atrial
fibrillation, and prior stroke. Data collected on
presentation included interval from ictus to admission, GCS
score, and blood pressure. The use of mechanical ventilation, mannitol,
and ventriculostomy were noted, as was the presence of medical
complications, including congestive heart failure, significant
arrhythmias, pneumonia, and sepsis. Outcome was determined by
hospital disposition (dead, nursing home, inpatient rehabilitation,
home) and 3-month functional outcome as assessed by use of the
telephone version of the FIM.12
All patients were admitted to the neurology/neurosurgery ICU and
managed concurrently by the ICU team and either the neurology or
neurosurgery service. Management followed a standardized
approach.13 Airway protection with endotracheal
intubation was performed for patients with a GCS score of 
8 or as
needed. Mean arterial pressure was treated with labetalol,
hydralazine, or intravenous
nicardipine when it exceeded 135 to 150 mm Hg or if
signs of end-organ dysfunction (cardiac ischemia, heart
failure, renal failure) developed. Osmotic therapy with mannitol was
administered to patients if there was concern for or evidence of
increased intracranial pressure. Hyperventilation and barbiturates were
not used. General criteria for surgical intervention included
moderate-sized cortical hemorrhage or deterioration due to
hematoma extension. The decision to insert a ventriculostomy was based
on clinical rather than radiographic criteria. If
hydrocephalus was thought to have contributed to deteriorating or poor
clinical status a ventriculostomy catheter (Codman External Drainage
System II, Codman & Shurtleff, Inc) was placed.
Cranial CT scans performed within 24 hours of hemorrhage
were retrospectively reviewed by investigators blinded to clinical
data. ICH was classified as deep (arising in the thalamus or basal
ganglia) or lobar. ICH volume was calculated using the formula
AxBxC/2, where A, B, and C represent the clot diameters in 3
dimensions at right angles to each other, as described by Broderick et
al.14 Degree of IVH was recorded using the
methods of Ruscalleda and Peiro,6 in which the
amount of blood visualized on CT is determined for the third, fourth,
and each lateral ventricle, and the four scores are summed. The left
and right ambient cisterns were scored as normal, effaced, or
obliterated and given a score of 0, 1, or 2, respectively. The scores
for the 2 cisterns were summed and then the total score was divided
into 3 groups based on total scores of 0, 1 to 2, and 3 to 4. Pineal
shift was measured (in millimeters) and corrected for
magnification.
Patients were divided into 2 groups: those with hydrocephalus
(score of 
1) and those without hydrocephalus. Comparisons between
groups were performed with use of independent sample t tests
and Fisher exact tests, as appropriate. All analyses were
computed with the SAS System for Windows, version 6.12 (SAS Inc). 8 versus
>8), hematoma size (27 versus >27 cc), pulse pressure
(85 versus >85), age (65 versus >65), cistern score (0 versus
1), and deep (thalamic and basal ganglia) versus lobar location. 0.25. The first
multivariate regression included non-CT variables
(age, gender, race, GCS score, and pulse pressure) to allow us to
explore the impact of the CT variables on the model. A backward
selection procedure was used to select the subset of predictors from
this group of variables. The second model was fit using the
variables remaining from the first analysis and adding CT
variables one at a time. A P value of <0.10 was used as
the criterion for retention of each new variable in the model. The
likelihood ratio was used to evaluate whether there was a significant
improvement in the model as each new variable was added. The final
multivariate model was fit using location and the
interaction of hydrocephalus and location. Predicted probabilities of
death were computed for each observation. A probability cut point of
0.50 was used to classify observations as events or nonevents. The
overall accuracy of the models was determined by comparing the
predicted values with the actual events.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Of the 81 patients enrolled in the study, 40 had some degree of
hydrocephalus. The interval from hemorrhage to admission to the
ICU was 12.8±10.5 hours and did not differ between patients with and
those without hydrocephalus. Those with hydrocephalus were, on average,
10 years younger than those without hydrocephalus (Table 1
). The patients with hydrocephalus were
more likely to have lower GCS scores and narrower pulse pressures on
admission (P<0.005 and P<0.05,
respectively).
View this table:
[in a new window]
Table 1. Clinical Characteristics ). Lesion size did not differ in those
with and without hydrocephalus. The IVH score and degree of cisternal
effacement were greater in the hydrocephalus group (P<0.004
and P<0.002, respectively); however, pineal shift was
greater in those patients without hydrocephalus
(P<0.003).
View this table:
[in a new window]
Table 2. CT Characteristics ). Over half of the patients with
hydrocephalus died compared with only 2% of those without
hydrocephalus. Similarly, fewer patients with hydrocephalus were
discharged to home or a rehabilitation facility. Among the survivors,
3-month FIM scores were not different in those with and without
hydrocephalus. A box plot of the hydrocephalus scores in those who
survived and those who died is presented in the
Figure.
View this table:
[in a new window]
Table 3. Outcome
View larger version (18K):
[in a new window]
Figure 1. Box plot showing the distribution of hydrocephalus scores in
patients who survived versus those who died. The dotted line indicates
the mean score, the solid line within the box indicates the median, the
box depicts the 25th and 75th percentiles, and the bars indicate the
10th and 90th percentiles. . Any variable in which the 95%
confidence limits of the OR does not include 1 conveys significantly
increased or decreased risk of mortality. The variables that
emerged from the analysis as significant univariate
predictors of mortality were deep hemorrhage location
(P<0.04), cisternal effacement
(P<0.003), pineal shift (P<0.001),
IVH score (P<0.0001), GCS score (P<0.0001), and
hydrocephalus (P<0.0001).
View this table:
[in a new window]
Table 4. Comparison of ORs From Univariate and
Multivariate Logistic Regression Models 
. GCS scores less than 8, male gender, pineal shift, and
hydrocephalus are independent predictors of mortality. The odds of
dying were 6.78 times greater for patients with admission GCS scores of
8. Each 1-point increase in the hydrocephalus score was associated
with a 1.64-fold increased risk of mortality. Each millimeter of pineal
shift was associated with a 1.27-fold increased risk of dying.
Comparison of the likelihood statistics for each model (45.54 versus
47.76) suggests that the addition of location and the interaction of
location with hydrocephalus did not significantly improve the fit of
the model. Thus, after accounting for the contributions of all other
variables in the model, hydrocephalus was an independent predictor
of mortality. The model correctly classified 85% of the patients
included in the analysis as alive or dead. Ninety percent of
the patients who survived were correctly classified, and 79% of the
patients who died were correctly classified.
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
This study demonstrates for the first time the impact of
hydrocephalus on outcome from ICH. Hydrocephalus was associated with a
considerably higher mortality and fewer patients being discharged to
home. Univariate and multivariate
analyses indicate that hydrocephalus is an independent
predictor of outcome. This finding, however, awaits validation with an
independent data set. Outcome was no different in patients treated with
a ventriculostomy.
Selected Abbreviations and Acronyms
FIM
=
Functional Independence Measure
GCS
=
Glasgow Coma Scale
ICH
=
intracerebral hemorrhage
ICU
=
intensive care unit
IVH
=
intraventricular hemorrhage
OR
=
odds ratio
Acknowledgments
The authors wish to acknowledge the support of the Neuroclinical
Service Line of Barnes-Jewish Hospital and the statistical advice
provided by Jack Batey of the Division of Biostatistics, Washington
University, St Louis, Mo.
Footnotes
Reprints requests to Michael Diringer, MD, Department of Neurology, Box 8111, Washington University School of Medicine, 660 S Euclid Ave, St Louis, MO 63110.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
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D. F. Edwards, H. Hollingsworth, A. R. Zazulia, and M. N. Diringer Artificial neural networks improve the prediction of mortality in intracerebral hemorrhage Neurology, July 1, 1999; 53(2): 351 - 351. [Abstract] [Full Text] [PDF]
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W. E. Stehbens, M. N. Diringer, D. F. Edwards, and A. R. Zazulia Hemocephalus and Not Hydrocephalus as a Predictor of Poor Outcome From Supratentorial Intracerebral Hemorrhage • Response Stroke, December 1, 1998; 29(12): 2668 - 2668. [Full Text] [PDF]
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