(Stroke. 1997;28:2370-2375.)
© 1997 American Heart Association, Inc.
Articles |
Predisposing Factors to Enlargement of Spontaneous Intracerebral Hematoma
From the Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, Osaka, Japan.
Correspondence to Seiji Kazui, MD, Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, 5–7-1 Fujishirodai, Suita, Osaka 565, Japan. E mail skazui@hsp.ncvc.go.jp
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose Enlargement of intracerebral hemorrhage is a major cause of clinical deterioration. Identification of factors that predispose to hematoma enlargement is important in managing patients.
Methods We selected 186 patients (71 women and 115 men; mean age, 64.8±12.5 years) with spontaneous intracerebral hemorrhage who had undergone an initial CT within 24 hours and a second scan within 120 hours of symptom onset. We compared patients with (n=41) and without (n=145) hematoma enlargement according to clinical characteristics and laboratory data.
Results By multiple logistic regression analysis (n=139),
interaction of long interval (>6 hours) from onset to first CT and
small hematoma (<25 cm3) strongly reduced risk of
enlargement. The analysis also demonstrated that the following
factors independently predisposed to enlargement: history of brain
infarction; liver disease; interaction of fasting plasma glucose 
141
mg/dL and systolic blood pressure on admission 200
mm Hg; and interaction of glycosylated hemoglobin A1c
5.1% and systolic blood pressure on admission 200
mm Hg.
Conclusions A patient examined >6 hours after ictus who has a
hematoma volume <25 cm3 is unlikely to experience further
hematoma growth. Prevention of brain infarction and premorbid
management of liver disease may serve to lower the risk of hematoma
enlargement. Although it remains controversial whether antihypertensive
drugs should be used in the acute phase of
intracerebral hemorrhage, poorly controlled
diabetics with high systolic blood pressure (200 mm
Hg) on admission also were at high risk of hematoma enlargement.
Key Words: hematoma • hypertension • intracerebral hemorrhage • diabetes mellitus
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Enlargement of ICH is a major cause of clinical deterioration.1 2 3 4 Identification of factors that predispose to enlargement is important in managing patients with acute ICH. We classified ICH patients into groups with and without radiographic evidence of enlargement.3 By univariate and multivariate statistical analyses of clinical parameters, we determined factors influencing hematoma expansion.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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We retrospectively reviewed the records of 264 consecutive patients with ICH admitted to our stroke care unit whose diagnosis was confirmed by CT within 24 hours of the ictus from January 1, 1985, to December 31, 1994. CT examinations were repeated routinely within a few days of admission. An additional CT scan was also performed when a clinical deterioration was noticed. Excluded were patients with hemorrhage due to aneurysmal rupture (n=1), arteriovenous malformations (4), moyamoya disease (3), and infective endocarditis (5), as well as those receiving anticoagulants (9) or antiplatelet agents (12). Patients undergoing a second CT >120 hours after the onset of ICH (25) were also excluded because the hematoma margin became ill defined. In addition, we excluded patients who died (14) or who underwent neurosurgery (5) before a second CT examination. The remaining patients (n=186, 71 women and 115 men; mean age, 64.8±12.5 years) served as subjects for the present study.
Risk factors examined included age, sex, smoking habit, alcohol
consumption, hypertension,
hypercholesterolemia, diabetes mellitus, brain
infarction, ischemic heart disease, and liver disease.
Specifically, subjects were classified as nonsmokers or current
smokers; nondrinkers or current drinkers; and consumers of 46 or <46
g ethanol per day. Hypertension was present given a history of
antihypertensive medication, a systolic blood pressure
>160 mm Hg, or a diastolic blood pressure
>90 mm Hg at least twice before onset of ICH.
Hypercholesterolemia was defined as total serum
cholesterol concentration >220 mg/dL. Diabetes mellitus
was diagnosed according to the definition cited by the National
Diabetes Data Group.5 We classified the infarctions
according to the system of the National Institute of Neurological
Disorders and Stroke.6 Clinically diagnosed liver diseases
included cirrhosis, chronic active hepatitis, alcoholic liver damage,
fatty liver, and others. Just before the first CT, the patient's
neurological state was evaluated by a neurologist, including level of
consciousness, aphasia, neglect or other discrete deficits in higher
cortical function, abnormalities in visual fields, eye position,
pupillary function, gaze, motor and sensory function, and plantar
responses. A GCS score7 was calculated from the written
description of the examination. Motor weakness was graded from 0
(complete plegia) to 5 (full strength). Systolic and
diastolic blood pressures were recorded when CT was
performed and at 10 AM on hospital days 2, 3, 4, 5, 6, 7,
and 30. Clinical outcome was assessed by the modified Rankin
Scale8 (grades 0 to 5) at 30 days or at discharge, if
sooner. Death represented a Rankin score of
6.9
The intervals from the onset of ICH to the first and second CT scans
(T1 and T2) were recorded in each patient. In cases of onset during
sleep, the recorded onset was on awaking. All CTs were retrieved
and evaluated by two of the authors (S.K. and H.Y.) and three of their
associates until a consensus was reached regarding hematoma location,
such as putaminal, thalamic, lobar, pontine, cerebellar, or others. If
the origin of a massive ICH could not be determined as either thalamic
or putaminal, the designation was mixed. ICH volume was determined in
the following manner.9 10 11 12 On the CT slice with the largest
area of ICH, the longest diameter (A) of the hematoma was measured from
the centimeter scale on the film. The largest possible diameter
perpendicular to the longest diameter represented the
second diameter (B). The height of the hematoma was calculated by
multiplying the number of slices involved by slice thickness, providing
the third diameter (C). Each diameter was determined to half a
centimeter.12 13 Hemorrhage within the
ventricular system was not measured. The three diameters
were multiplied and then divided by 2 (AxBxC/2) to obtain the volume
of ICH. Kothari and coauthors12 have found that this
formula AxBxC/2 correlates highly with volumes calculated by
planimetric methods and shows excellent interrater and intrarater
agreement. A cutpoint, V2-V1 12.5 cm3 or V2/V1 1.4
(where V1 is hematoma volume on the first CT and V2 is hematoma volume
on the second CT), which we have determined previously by receiver
characteristic curve analyses,3 defined hematoma
enlargement. We divided the 186 patients into enlargement and
nonenlargement groups.
The following laboratory tests for hematology and blood chemistry were
performed at admission: sodium, potassium, chloride, aspartate
aminotransferase, alanine aminotransferase, lactate dehydrogenase,
creatine kinase, urea nitrogen, creatinine, total protein,
total bilirubin, blood glucose, white cell count, red cell count,
hemoglobin, hematocrit, and platelet count. On the next weekday
morning, laboratory studies were performed as follows: total protein,
albumin, albumin-globulin ratio, gamma-glutamyl
transpeptidase, total cholesterol,
triglyceride, uric acid, FPG, HbA1c,
prothrombin time, activated partial thromboplastin time,
fibrinogen, and fibrin degradation products. Left
ventricular hypertrophy was diagnosed
electrocardiographically by Estes criteria (score
4).14 15
Statistical Analyses
We used the Base SAS and SAS/STAT, version 6 (SAS Institute Inc)
for statistical analysis. Univariate
analyses were performed based on the 
2 test for
categorical variables or Fisher's exact test for instances in
which the individual cells of a 2x2 table had counts less than five.
Continuous variables were assessed twice, as dichotomized
variables for the 2 test or Fisher's exact test and
as continuous measures for the t test (age, time interval
from onset to CT, hematoma volume, serum electrolytes, blood cell
counts, and values of blood pressure) or Wilcoxon rank sum test
(other laboratory tests). The Wilcoxon rank sum test was also
used in analyzing Estes score, GCS score, score of motor weakness, and
modified Rankin scale. Values of P<.05 were considered
statistically significant. We performed multivariate
analyses for the patients with full laboratory data using a
logistic regression model16 to identify factors predictive
of hematoma enlargement. We chose variables for entry on the basis
of clinical importance from among those with values of
P<.05 after univariate testing. Significant
interactions were assessed among the variables by the Breslow-Day
test with values of P<.15. We performed variable
selection using the stepwise procedure of forward selection with a test
for backward elimination with values of P>.15.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Hematoma location was as follows (Table 1
): putaminal in 64 patients (34%),
thalamic in 61 (33%), mixed in 5 (3%), lobar in 31 (17%), pontine in
10 (5%), cerebellar in 8 (4%), and other sites in 7 (4%). A history
of hypertension was documented in 154 patients (83%). The mean T1 was
6.5±6.2 hours, and T2 was 32.0±29.1 hours.
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Forty-one patients (22%) fulfilled the criteria for hematoma enlargement, and the remaining 145 patients (78%) represented the nonenlargement group.
The results of univariate analyses are shown in
Tables 2, 3 and 4. T1 and T2 were significantly shorter in patients
with hematoma enlargement (P=.0003 for both) (Table 2). These patients had a significantly
higher Estes score (P=.0013), lower GCS score
(P=.0246), greater degree of paresis (P=.0007 for
upper limb and P=.0009 for lower limb), and higher modified
Rankin scale score (P=.0001) than those in the
nonenlargement group (Table 3). Among
laboratory parameters, levels of urea nitrogen
(P=.0385), creatinine (P=.0202), and
FPG (P=.0015) were significantly higher in the enlarged
group than in the nonenlarged group (Table 3).
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After dichotomization, all aforementioned variables were also
significantly different between groups (Table 4). Additional factors with statistical
significance by the 2 test were as follows. A history of
brain infarction was found in 7 patients (5 lacunar and 2
atherothrombotic) in the enlargement group and in 9 patients (6 lacunar
and 3 atherothrombotic) in the other group. A history of brain
infarction was significantly more frequent in patients with hematoma
enlargement than in those with nonenlarged hematoma
(P=.028). The incidence of liver disease was significantly
higher in the enlargement group than in nonenlargement group
(P=.025). Larger V1 (25 cm3) was significantly
more frequent in the enlargement group than in the nonenlargement group
(P=.047). Incidence of abnormal eye position or muscle tonus
was significantly higher in the enlargement group (P=.025
and P=.021, respectively). Significantly larger numbers of
patients with hematoma growth had higher FPG (141 mg/dL;
P=.001), higher HbA1c (5.1%;
P=.049), and more prolonged prothrombin time (
78%;
P=.007) and activated partial thromboplastin time
(35 s; P=.011) (Table 4). Although differences in blood
pressures at the time of the first and second CTs did not reach the
statistically significant level by the t test (Table 2
), a
significantly larger number of patients with enlarged hematoma had
higher (200 mm Hg) systolic blood pressure at the
time of the first CT (SBP1) than those without enlargement (Table 4).
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For multivariate analyses (n=139), the
following nine variables were chosen from those with the values of
P<.05 after univariate testing to avoid effects
of overlapping of clinical importance of variables: history of
brain infarction, liver disease, high Estes score (4), delayed T1
(>6 hours), large V1 (25 cm3), high serum
creatinine level (1.5 mg/dL), high FPG level, (141
mg/dL), high HbA1c level (5.1%), and high SBP1
(200 mm Hg). The Breslow-Day test revealed significant
interactions as follows: T1 and V1; V1 and SBP1; serum
creatinine and FPG; FPG and SBP1; and HbA1c and
SBP1. After stratification five variables were obtained; T1>6
hours and V1<25 cm3; V1 25 cm3 and SBP1
200 mm Hg; serum creatinine 1.5 mg/dL and FPG
141 mg/dL; FPG 141 mg/dL and SBP1 200 mm Hg; and
HbA1c 5.1% and SBP1 200 mm Hg. A total of 14
variables (9 from univariate analyses and 5
from the Breslow-Day test) were considered for logistic regression
analyses. Table 5 summarizes the
results of multiple logistic regression with values of
P<.15. Five independent factors concerning hematoma
extension were yielded. History of brain infarction, liver disease,
interaction of FPG 141 mg/dL and SBP1 200 mm Hg, and
interaction of HbA1c 5.1% and SBP1 200 mm Hg
significantly enhanced the risk of hematoma enlargement, and
interaction of T1>6 hours and V1<25 cm3 significantly
reduced the risk of hematoma enlargement. This model was highly
significant with the likelihood test (P=.0001).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Univariate analyses in the present study revealed a number of factors that were significantly different between the patients with and without hematoma enlargement: history of brain infarction or liver disease, T1 and T2, V1
25 cm,3 Estes
score, GCS score, degree of paresis, modified Rankin scale, incidence
of abnormal eye position or muscle tonus, incidence of high SBP1
200 mm Hg, urea nitrogen, creatinine, FPG,
incidence of abnormal HbA1c, prothrombin time, and
activated partial thromboplastin time. These factors can be
summarized into five categories: (1) time intervals from stroke onset
to CT scan; (2) clinical features reflecting a large hematoma; (3)
underlying diseases aggravating atherosclerosis and
arteriolosclerosis; (4) liver disease; and (5) high systolic
blood pressure at the time of admission. A shorter interval from onset to CT was demonstrated in the enlargement group. Active bleeding in ICH is generally believed to cease within a few hours of onset.17 Therefore, there is a greater chance of detecting enlarging hematoma with early CT scanning.3 4
The incidence of V1 25 cm3 was higher in the enlargement
group, probably because more hematomas in this group were actively
growing at the time of the first CT scan. Large hematomas resulted in
severe neurological deficits such as profound consciousness
disturbance (low GCS score), dense hemiparesis, abnormal eye
position or muscle tonus, and poor outcome (high modified Rankin
score). Broderick and coauthors13 have demonstrated that
ICH volume was a powerful predictor of 30-day mortality and morbidity.
Therefore, more severe neurological deficits were considered
consequences of larger hematomas and thus were judged not to be
independent predisposing factors for hematoma enlargement.
The enlargement group had higher incidence of history of brain infarction; left ventricular hypertrophy on ECG (higher Estes score); higher levels of urea nitrogen, creatinine, and FPG; and higher incidence of abnormal HbA1c, all related to hypertension or diabetes mellitus. The clinical categories of brain infarction in our study were atherothrombotic or lacunar. Atherothrombotic infarction occurs in patients with atherosclerosis,5 and lacunar infarcts most often result from the occlusion of small arteries by hypertensive arteriopathy.18 Left ventricular hypertrophy represents a systemic complication of hypertension.14 Although high levels of FPG might represent stress hyperglycemia19 caused by large hematomas or dense neurological deficits, HbA1c provides an estimate of control of diabetes mellitus or blood glucose level for the preceding 3-month period.20 High levels of urea nitrogen and creatinine as well as abnormal HbA1c suggest uncontrolled hypertension or diabetes mellitus. In addition to aggravating atherosclerosis and arteriolosclerosis, hyperglycemia may precipitate hemorrhage by the analogy with hemorrhagic infarction, which has been indicated to be frequent and massive in hyperglycemic humans21 22 and cats.23
The incidence of liver disease and abnormal prothrombin time or activated partial thromboplastin time was significantly higher in patients with hematoma enlargement. Liver dysfunction, together with increased consumption of alcohol or thrombocytopenia, sometimes explains progression of ICH.24 25 Our data also supported this observation, although there were no differences in alcohol consumption, transaminase levels, or platelet count between the two groups. Decreased levels of coagulant factors caused by liver diseases easily resulted in prolonged bleeding.
The incidence of SBP1 200 mm Hg differed significantly
between the two groups. However, there were no other significant
differences related to blood pressure.
Previous studies have suggested various factors favoring growth of ICH.
Broderick and associates2 reported that a systolic
blood pressure 195 mm Hg was recorded during the first
6 hours in 5 of 6 patients who had shown neurological deterioration
with a >40% increase in hematoma volume. Marked hypertension was
observed in patients with active bleeding.26 27 Fujii and
coauthors25 demonstrated that the incidence of enlargement
significantly decreased with time and increased with severity of liver
dysfunction. They also demonstrated that patients with irregularly
shaped hematomas and those with coagulation abnormalities such as low
platelet counts had a higher risk of hematoma growth. Fehr and
Anderson28 pointed to alcohol abuse as a precipitating
factor. All these studies represented case reports or
univariate analyses. Recently Brott and
associates4 performed a prospective study of 103 patients
with ICH and found no significant predictor of hemorrhage
growth. The present study is the first that identifies independent
factors for ICH enlargement.
Multiple logistic regression analysis revealed that interaction
of T1>6 hours and V1 <25 cm3 powerfully reduced the risk
of hematoma enlargement. A patient examined >6 hours after ictus who
has a hematoma volume <25 cm3 is unlikely to experience
further hematoma growth. Short T1 (6 hours) or large V1(25
cm3) did not independently result in hematoma enlargement.
Most interestingly, multiple logistic regression demonstrated four
independent predisposing factors for hematoma enlargement: history of
brain infarction, liver disease, interaction of FPG 141 mg/dL and
SBP1 200 mm Hg, and interaction of HbA1c
5.1% and SBP1 200 mm Hg. Patients with a history of
brain infarction (atherothrombotic or lacunar) had high risk of
hematoma growth. Prevention of brain infarction may serve to lower the
risk of hematoma enlargement. Liver disease was an independent factor
in growth of hematomas. Prevention and premorbid management of
resulting coagulopathy should help to prevent hematoma enlargement.
Poorly controlled diabetics with high systolic blood pressure
(200 mm Hg) on admission also had high risk of hematoma
enlargement. It remains controversial whether antihypertensive drugs
should be used in the acute phase of ICH. High blood pressure may be an
adaptation to increased intracranial pressure (Cushing's phenomenon).
High blood pressure may increase intracranial pressure by increasing
cerebral perfusion pressure and promoting brain edema.29
Blood pressure reduction of 20% has been suggested on the basis of
cerebral blood flow studies.30 Kase and
Crowell29 have empirically adopted a policy of active blood
pressure control in patients with blood pressure 180/100 mm
Hg. Unfortunately, precise guidelines for blood pressure control are
not available. Our data may recommend that clinicians should lower
systolic blood pressure to <200 mm Hg at admission
for diabetics with ICH. Because the present study was
retrospective, prospective randomized trials are needed to determine
whether enlargement of ICH can be treated.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The authors thank H. Oe, MD, W. Kakuda, MD, and R. Ohtani, MD, for their evaluation of CT images. We are also indebted to H. Naritomi, MD, and H. Kinugawa, MD, for their helpful advice.
Received July 25, 1997; revision received September 5, 1997; accepted September 5, 1997.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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 E. M. Manno, J. L. D. Atkinson, J. R. Fulgham, and E. F. M. Wijdicks Emerging Medical and Surgical Management Strategies in the Evaluation and Treatment of Intracerebral Hemorrhage Mayo Clin. Proc., March 1, 2005; 80(3): 420 - 433. [Abstract] [PDF]
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NINDS ICH Workshop Participants Priorities for Clinical Research in Intracerebral Hemorrhage: Report From a National Institute of Neurological Disorders and Stroke Workshop Stroke, March 1, 2005; 36(3): e23 - e41. [Abstract] [Full Text] [PDF]
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R. Leira, A. Davalos, Y. Silva, A. Gil-Peralta, J. Tejada, M. Garcia, and J. Castillo Early neurologic deterioration in intracerebral hemorrhage: Predictors and associated factors Neurology, August 10, 2004; 63(3): 461 - 467. [Abstract] [Full Text] [PDF]
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K. S. Butcher, T. Baird, L. MacGregor, P. Desmond, B. Tress, and S. Davis Perihematomal Edema in Primary Intracerebral Hemorrhage Is Plasma Derived Stroke, August 1, 2004; 35(8): 1879 - 1885. [Abstract] [Full Text] [PDF]
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K. Ohwaki, E. Yano, H. Nagashima, M. Hirata, T. Nakagomi, and A. Tamura Blood Pressure Management in Acute Intracerebral Hemorrhage: Relationship Between Elevated Blood Pressure and Hematoma Enlargement Stroke, June 1, 2004; 35(6): 1364 - 1367. [Abstract] [Full Text] [PDF]
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 M. Willmot, J. Leonardi-Bee, and P. M.W. Bath High Blood Pressure in Acute Stroke and Subsequent Outcome: A Systematic Review Hypertension, January 1, 2004; 43(1): 18 - 24. [Abstract] [Full Text] [PDF]
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K. Minematsu Evacuation of Intracerebral Hematoma Is Likely to Be Beneficial Stroke, June 1, 2003; 34(6): 1567 - 1568. [Full Text] [PDF]
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S. A. Mayer Ultra-Early Hemostatic Therapy for Intracerebral Hemorrhage Stroke, January 1, 2003; 34(1): 224 - 229. [Abstract] [Full Text] [PDF]
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 A. I. Qureshi, S. Tuhrim, J. P. Broderick, H. H. Batjer, H. Hondo, and D. F. Hanley Spontaneous Intracerebral Hemorrhage N. Engl. J. Med., May 10, 2001; 344(19): 1450 - 1460. [Full Text] [PDF]
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T. G. Phan, M. Koh, R. A. Vierkant, and E. F.M. Wijdicks Hydrocephalus Is a Determinant of Early Mortality in Putaminal Hemorrhage Stroke, September 1, 2000; 31(9): 2157 - 2162. [Abstract] [Full Text] [PDF]
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K. J. Becker, A. B. Baxter, H. M. Bybee, D. L. Tirschwell, T. Abouelsaad, and W. A. Cohen Extravasation of Radiographic Contrast Is an Independent Predictor of Death in Primary Intracerebral Hemorrhage Stroke, October 1, 1999; 30(10): 2025 - 2032. [Abstract] [Full Text] [PDF]
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