(Stroke. 1999;30:761-764.)
© 1999 American Heart Association, Inc.
Original Contributions |
Hemorrhage After an Acute Ischemic Stroke
From the Istituto di Clinica Neurologica, Università degli Studi di Milano, IRCCS Ospedale Maggiore Policlinico (C.M., A.C., E.A., A.P., L.C.) and the Servizio di Neuroradiologia, Ospedale "Niguarda-Cà Granda" (E.B., C. De G.) Milan, Italy.
Correspondence to Livia Candelise, MD, Istituto di Clinica Neurologica, Università degli Studi di Milano, Ospedale Maggiore Policlinico, IRCCS, Via F. Sforza 35, 20122 Milano, Italia. E-mail pitagora{at}imiucca.csi.unimi.it
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose—Hemorrhagic transformation is frequently seen on CT scans obtained in the subacute phase of ischemic stroke. Its prognostic value is controversial.
Methods—We analyzed 554 patients with acute ischemic stroke enrolled in the Multicenter Acute Stroke Trial–Italy (MAST-I) study in whom a second CT scan was performed on day 5. Presence of 1) intraparenchymal hemorrhages (hematoma or hemorrhagic infarction), 2) extraparenchymal bleeding (intraventricular or subarachnoid) and 3) cerebral edema (shift of midline structure, sulcal effacement or ventricular compression) alone or in association were evaluated. Death or disability at 6 months were considered as "unfavorable outcome."
Results—Patients who developed intraparenchymal
hemorrhages, extraparenchymal bleeding, or cerebral edema had
unfavorable outcome (83%, 100%, and 80%, respectively), but
multivariate analysis demonstrated that only
extraparenchymal bleeding (collinearity) and cerebral edema (OR=6.8;
95% CI, 4.5 to 10.4) were significant independent prognostic findings.
Unfavorable outcome correlated with size of intraparenchymal
hemorrhage (
2 for trend=30.5,
P<0.0001). Nevertheless, when a large hematoma was
present the negative effect was mostly due to concomitant
extraparenchymal bleeding (2=51.6,
P<0.0001), and when hemorrhagic infarction was detected
the negative effect was mostly explained by the association with
cerebral edema (2=36.6, P<0.0001).
Conclusions—Extraparenchymal bleeding and cerebral edema are the main prognostic CT scan findings in the subacute phase of ischemic stroke. Stroke patients with a high risk for developing these 2 types of brain damage should be identified. Measures to prevent and adequately treat their development should be implemented.
Key Words: hemorrhage • prognosis • stroke, acute • tomography, x-ray computed
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Clinicians are frequently worried when a patient with acute ischemic stroke develops a hemorrhagic transformation, even when it is only a CT scan event. The widespread use in clinical practice of antithrombotic and thrombolytic treatments, both carrying a high incidence of cerebral bleeding, heighten the need to understand whether hemorrhagic transformation is an indicator of bad outcome and whether a second CT scan in the subacute phase would help to improve acute stroke management.
Numerous studies have been conducted to identify predictors of a hemorrhagic transformation,1 2 3 4 5 6 7 8 9 with contradictory and uncertain results, due in part to the use of different and not comparable classifications.10 However, attempts to select patients at low risk for hemorrhagic transformation would be worthwhile only if it can be clearly demonstrated that the effect of hemorrhagic transformation is unfavorable. To date, few studies have addressed this issue.1 2 3 The evaluation of prognostic CT findings should include not only intraparenchymal hemorrhage but also the concomitant presence of extraparenchymal bleeding and signs of cerebral edema. These 2 CT findings are well known predictors of bad outcome, the former in patients with primary intracerebral hemorrhage11 12 13 14 15 and the latter in patients with cerebral infarct.
The aim of this study was to evaluate the long-term prognostic value of the development of parenchymal hemorrhages, extraparenchymal bleeding, and cerebral edema after an acute ischemic stroke.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The Multicenter Acute Stroke Trial–Italy (MAST-I), a randomized controlled clinical trial on streptokinase and/or aspirin, enrolled 622 patients with acute ischemic stroke.16 All patients had a basal CT scan performed within 6 hours of stroke onset and before randomization to exclude the presence of intracranial bleeding. A second CT scan was performed if possible on day 5 as part of a standardized clinical and instrumental evaluation. Sixty-eight patients did not undergo the second CT scan, in 50 cases because death intervened. Of the other 18, 7 had a favorable and 9 an unfavorable 6-month outcome. All CT scans were reviewed centrally by a neuroradiological committee blinded to treatment allocation and clinical course.
Hemorrhagic transformation was defined as a parenchymal area of increased density within an area of low attenuation in a typical vascular distribution on noncontrasted CT scan and was subdivided into the following 4 categories on the basis of standardized definitions: (1) intracerebral hemorrhage (hematoma): homogeneous region of high attenuation exceeding the vascular territory of the presumed infarction, including extra-infarct hemorrhagic lesions; (2) large hemorrhagic infarction (type III): homogeneous region(s) of high attenuation of total presumed cerebral infarct area; (3) medium hemorrhagic infarction (type II): homogeneous or heterogeneous region(s) of high attenuation within an infarct area; and (4) petechial hemorrhagic infarction (type I): small petechial and linear high-attenuation region(s) within an infarct area.
Extraparenchymal bleeding (presence of intracranial blood around the brain in either intraventricular or subarachnoid spaces) was also evaluated.
Signs of cerebral edema were defined as either focal with sulcal effacement or ventricular compression, or severe with shift of midline structure.
All patients were assessed 6 months after randomization by telephone
interview. In surviving patients, disability was graded according to
the 5-item modified Rankin Scale. Death or survival with a Rankin Scale
score of 
3 was considered an "unfavorable outcome."
Statistical analysis was performed by SPSS statistical
analysis software (SPSS, Inc). The rate of association
between variables is presented in terms of OR, and the
relative 95% CIs were calculated by the Cornfield method. The
statistical significance of OR was tested by the
2 method, and P<0.05 was
considered statistically significant. 2 for
trend was used to test the risk in different categories. To evaluate
the predictor factors associated with unfavorable outcome, a logistic
regression was performed by STATA statistical analysis software
(Stata Corp).
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Results |
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Findings in the 554 patients with a second CT scan were as follows: intraparenchymal hemorrhagic transformation of any category in 109 scans; extraparenchymal bleeding in 21 scans, either intraventricular (n=17) or only in the subarachnoid space (n=4); signs of cerebral edema in 301 scans, either severe due to shift of midline structures (n=117) or focal due to sulcal effacement and/or ventricular compression (n=184).
The 3 CT scan findings evaluated were all important 6-month prognostic
predictors (Table 1
); in fact,
83% of patients with intraparenchymal hemorrhagic transformation,
100% with extraparenchymal bleeding, and 80% with signs of cerebral
edema were dead or disabled at follow-up. The results of
univariate analysis are presented in Table 2. In view of the concomitant presence of
>1 of the 3 findings in the same CT scan, we also performed a
multivariate analysis corrected by age which
demonstrated that intraparenchymal hemorrhage alone was not a
significant predictor of unfavorable outcome (OR=1.2; 95% CI, 0.7 to
2.2), whereas extraparenchymal bleeding always predicted it
(collinearity) and cerebral edema was significantly associated with it
(OR=6.8; 95% CI, 4.5 to 10.4) (Table 2). The same results were
obtained in the subgroup of 272 patients treated with streptokinase
(Table 2).
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The predictive prognostic value of each type of intraparenchymal
hemorrhagic transformation was also analyzed. We observed 23
hematomas (21%) and 86 hemorrhagic infarctions (79%), including 12
large, 42 medium, and 32 petechial. A linear correlation was found
between the severity of intraparenchymal hemorrhage and
prognosis: the outcome was unfavorable in 96% of the patients with
hematoma and in 92% with large, 81% with medium, and 72% with
petechial hemorrhagic infarction (2 for
trend=30.5, P<0.0001). The same correlation was observed in
the subgroup of patients given streptokinase
(2 for trend=4.56, P=0.03
Figure). Multivariate
analysis corrected by age of the independent prognostic value
of intraparenchymal hemorrhage categories together with the
other CT scan prognostic findings demonstrated that extraparenchymal
bleeding perfectly predicted (collinearity) and cerebral edema was
significantly associated with unfavorable outcome (OR=7.2, 95% CI, 4.7
to 11.1), whereas any category of intraparenchymal hemorrhages
alone was not a significant independent predictor of unfavorable
outcome (OR for hematoma=6.0, 95% CI, 0.6 to 56.7; OR for large
hemorrhagic infarction=2.6; 95% CI, 0.3 to 21.1; OR for medium
hemorrhagic infarction=1.1, 95% CI 0.5 to 2.6; OR for petechial
hemorrhagic infarction=0.8, 95% CI 0.3 to 1.8). The association
between the intraparenchymal hemorrhage categories and the
other 2 CT scan findings could explain this result. In fact, hematoma
was significantly associated with extraparenchymal bleeding (74%)
(2=51.6, P<0.0001), whereas most
hemorrhagic infarctions had associated signs of cerebral edema (96%)
(2 =36.6, P<0.0001). The same was
true for the streptokinase treated patients (Table 3).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The prognostic value of a second CT scan performed in the subacute phase of ischemic stroke is confirmed by the present study. Other studies have demonstrated that hemorrhagic transformation type could influence outcome. In particular, there is general agreement that hemorrhagic infarction has less effect than a clear hematoma2 3 4 17 and that larger lesions were associated with a more severe prognosis.3 4 5 18 19 However, ours is the first study to address this issue with use of a hemorrhagic classification whose reproducibility had been tested previously.10
The present results also provide some insights on reasons for
unfavorable outcome in patients developing a hemorrhagic
transformation. Intraparenchymal hematoma and hemorrhagic infarctions
might occur with 2 different mechanisms. Our findings indicate that the
unfavorable outcome of patients with hematoma results from the
concomitant presence of blood in the extraparenchymal space; 17 of 21
patients with this complication died within 10 days. This observation
is in agreement with studies on the prognosis of primary
intracerebral hemorrhage, which showed that the
presence of blood in extraparenchymal spaces significantly increases
the case fatality.11 12 13 14 15 Daverat et al14
found that intraventricular spread of
hemorrhage was the only independent predictor of 30-day
mortality, and other authors12 maintain that the absence
of intraventricular hemorrhage is the key
to survival. It is worth underlining that extraparenchymal bleeding,
although a more rare event than hemorrhagic transformation in general,
seems to be entirely caused by streptokinase treatment. Moreover, we
demonstrated that detection of this CT scan finding is more
reproducible (
=0.76; 0.69 to 0.97) than that of parenchymal
hemorrhage (=0.37; 0.21 to 0.53).10 Thus it is
a stronger and a more reliable indicator of
thrombolytic risk than hemorrhagic transformation in
general. On the other hand, only a few of our patients with hemorrhagic
infarction had associated extraparenchymal bleeding. Severe cerebral
edema could be the cause of unfavorable outcome in these patients. A
strong association between cerebral edema and hemorrhagic infarction
has already been reported.4 6 7 Lodder6 not
only indicated that midline shift and hemorrhages were closely
associated and carried a bad prognosis but also observed that this
association was more prevalent in patients with initial large infarct.
In this condition, edema and intraparenchymal hemorrhagic
transformation could both be caused by the same mechanism. Enhanced
blood-brain barrier permeability resulting from severe
ischemia20 or reperfusion damage21 22
could be hypothesized. Our results show that hemorrhagic infarction is
associated with signs of cerebral edema also in patients treated with
streptokinase. It is therefore likely that brain edema and bleeding
itself are probably due to reperfusion damage in streptokinase treated
patients. A SPECT study demonstrated that thrombolysis
may increase the luxury reperfusion and exacerbate ischemic
injury by augmenting metabolic derangements. Moreover, this
luxury perfusion was also associated with hemorrhagic
transformation.22 These results are consistent
with the recent observation that thrombolytic risk is
higher when early ischemic changes, expression of severe
infarction, are present on the basal CT scan.8
In conclusion, physicians who decide to use thrombolysis in acute stroke should be prepared to deal with 2 types of adverse events: extraparenchymal bleeding and cerebral edema. The first event is mostly related to local or systemic fibrinolysis activation and the second to the initial severity of the ischemic lesion. General fears concerning an undefined intraparenchymal hemorrhagic transformation could be dispelled while efforts should be made to tailor therapy on the basis of specific CT scan findings.
Received September 15, 1998; revision received November 26, 1998; accepted November 26, 1998.
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