(Stroke. 1999;30:2025-2032.)
© 1999 American Heart Association, Inc.
Original Contributions |
Extravasation of Radiographic Contrast Is an Independent Predictor of Death in Primary Intracerebral Hemorrhage
From the Departments of Neurology(K.J.B., D.L.T.), Radiology (A.B.B., T.A., W.A.C.), and Neurological Surgery (K.J.B., A.B.B., H.M.B., W.A.C.), University of Washington School of Medicine, Harborview Medical Center, Seattle, Washington.
Correspondence to Kyra J Becker, MD, Box 359775, Harborview Medical Center, 325 Ninth Ave, Seattle, WA 98104-2499. E-mail kjb{at}u.washington.edu
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Abstract |
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Background and Purpose—Hematomas that enlarge following presentation with primary intracerebral hemorrhage (ICH) are associated with increased mortality, but the mechanisms of hematoma enlargement are poorly understood. We interpreted the presence of contrast extravasation into the hematoma after CT angiography (CTA) as evidence of ongoing hemorrhage and sought to identify the clinical significance of contrast extravasation as well as factors associated with the risk of extravasation.
Methods—We reviewed the clinical records and radiographic studies of all patients with intracranial hemorrhage undergoing CTA from 1994 to 1997. Only patients with primary ICH were included in this study. Univariate and multivariate logistic regression analyses were performed to determine the associations between clinical and radiological variables and the risk of hospital death or contrast extravasation.
Results—Data were available for 113 patients. Contrast
extravasation was seen in 46% of patients at the time of CTA, and the
presence of contrast extravasation was associated with increased
fatality: 63.5% versus 16.4% in patients without extravasation
(P=0.011). There was a trend toward a shorter time
(median±SD) from symptom onset to CTA in patients with extravasation
(4.6±19 hours) than in patients with no evidence of extravasation
(6.6±28 hours; P=0.065). Multivariate
analysis revealed that hematoma size (P=0.022),
Glasgow Coma Scale (GCS) score (P=0.016), extravasation
of contrast (P=0.006), infratentorial ICH
(P=0.014), and lack of surgery (P<0.001)
were independently associated with hospital death. Variables
independently associated with contrast extravasation were hematoma size
(P=0.024), MABP >120 mm Hg
(P=0.012), and GCS score of 
8
(P<0.005).
Conclusions—Contrast extravasation into the hematoma after ICH is associated with increased fatality. The risk of contrast extravasation is increased with extreme hypertension, depressed consciousness, and large hemorrhages. If contrast extravasation represents ongoing hemorrhage, the findings in this study may have implications for therapy of ICH, particularly with regard to blood pressure management.
Key Words: angiography • blood pressure • intracerebral hemorrhage • outcome
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Introduction |
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Mortality in primary intracerebral hemorrhage (ICH) is high, and the risk of death is increased in patients with large clots, low Glasgow Coma Scale (GCS) score, and intraventricular blood.1 2 3 4 Hematoma enlargement after admission is also associated with poor outcome.5 The incidence of hematoma enlargement, as assessed by CT, is approximately 14% to 20%.5 6 The mechanism by which hematomas enlarge is unclear, but growth is usually attributed to bleeding into the necrotic and edematous tissue surrounding the primary hemorrhage and not to continued bleeding from the initial vascular source.7 8 Factors associated with hematoma enlargement include a prior history of stroke, liver disease, hyperglycemia, and hypertension.6
Appropriate blood pressure management in patients with acute ICH is controversial. On the one hand, elevated blood pressure may promote recurrent hemorrhage and thus hematoma enlargement. On the other hand, overly aggressive treatment of hypertension may decrease cerebral blood flow (CBF) to areas of the brain where perfusion may already be compromised. An ischemic penumbra, or an area characterized by a relative decrease in CBF, surrounds the core of a focal ischemic infarct.9 10 Whether an ischemic penumbra exists in ICH, however, is debated. Mayer and colleagues8 showed, using single-photon emission tomography (SPECT), that blood flow in the areas surrounding the hematoma is markedly decreased, and the magnitude of this decrease is maximal within the first 24 hours after hemorrhage. Using positron emission tomography (PET), a more quantitative and reliable measure of CBF, however, regions of perfusion-dependent brain tissue around the hematoma could not be identified.11 Similar debates about the existence of a penumbra in ICH exist in animal models, and the disparities seem to depend on the techniques used to measure CBF. With hydrogen ion clearance, a relatively unreliable measure of CBF,12 13 evidence of penumbra around the site of ICH can be identified,14 but with radiolabeled microspheres, the gold standard for CBF measurement,15 16 no evidence for an ischemic penumbra in ICH can be found.17
In our institution, CT angiography is frequently performed in patients who present with ICH to screen for an underlying vascular abnormality. In most instances the CT angiogram (CTA) is performed at the time of ICH diagnosis. Review of these studies revealed frequent extravasation of radiographic contrast material into the hematoma. We interpreted extravasation as evidence of ongoing hemorrhage and sought to determine the clinical and radiographic characteristics of patients with contrast extravasation as well as the relationship between contrast extravasation and fatality.
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Subjects and Methods |
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CT Angiography
Each patient was imaged according to the same protocol using a high-speed CT system (CTi or CT Advantage; General Electric. Axial non-enhanced, nonhelical 5-mm images were obtained at 7-mm intervals throughout the brain. After acquisition of the initial scan, 180 cc of nonionic iodinated contrast material (Optiray 300, Ioversol injection; Mallinkrodt Medical) was administered intravenously by power injector at 4 cc/sec. After a 20-second delay, during the arterial phase of contrast opacification, axial helical 1-mm images were obtained from the circle of Willis through the hematoma at 0.-mm intervals with a pitch of 1:1.4. Postinfusion, nonhelical, contiguous axial 5-mm images were obtained to evaluate contrast extravasation and change in clot size during the examination.
CT Review
All patients who had undergone CTA from 1994 to 1997 were
identified through a radiology database. Patients with history of
trauma or evidence of tumor, SAH, aneurysm, or other vascular
malformation on CT scan or follow-up studies were excluded from
analysis. CT scans were reviewed independently by 2
neuroradiologists (A.B.B., W.A.C.) who were blinded to the clinical
data. Hematoma volume was estimated before and after contrast injection
with the ABC÷2 method.18 The presence or absence of
contrast extravasation was determined by visualization of high-density
contrast within the clot or ventricular system.
Extravasation was considered minimal if visible on only 1 or 2
postcontrast CT sections and extensive if present on 3 or more
sections. Hematoma location (infratentorial versus
supratentorial) and the presence or absence of
intraventricular hemorrhage (IVH) were
recorded. The amount of intraventricular
hemorrhage was considered small if blood was visible in only 1
chamber and large if visible in >1 chamber. All discrepancies in
qualitative evaluations were adjudicated; hematoma size was calculated
as the average of both CT readers' values.
Chart Review
Clinical data were obtained through chart review by an
investigator (H.M.B.) blinded to the radiological data. The following
data were recorded: elapsed time from symptom onset to CTA;
systolic blood pressure (SBP), diastolic blood
pressure (DBP), and mean arterial blood pressure (MABP) at
the time of CTA; prothrombin time, expressed as the international
normalized ratio (INR), activated partial thromboplastin time
(aPTT) and platelet count at admission; use of antithrombotic drugs
(heparin, warfarin, aspirin, ticlopidine); initial GCS score;
therapeutic drug use (osmotic agents, diuretics,
antihypertensives) before CTA; initial partial pressure of carbon
dioxide (PCO2); and glucose levels.
When possible, the premorbid medical history was obtained, with special
reference to diabetes mellitus, hypertension, ethanol abuse, and
tobacco abuse. If an intraparenchymal intracranial pressure (ICP)
monitor was placed, initial ICP was recorded. Whether or not
patients underwent surgical intervention (ventriculostomy,
decompressive surgery) was noted.
Outcome Measures
Hospital fatality was the primary outcome measure. The presence
or absence of contrast extravasation was analyzed as a
secondary outcome measure.
Statistics
Univariate analyses for associations with
hospital fatality or extravasation were performed with
2 test statistics for categorical and
dichotomous data and the Wilcoxon Rank Sum (WRS) test statistic
for continuous data. Independent associations with hospital fatality or
extravasation were determined using a stepwise logistic regression
model. Variables were retained in the model for P0.20
and excluded if their retention resulted in loss of 10 or more cases in
the final model. Continuous data are expressed as either the mean or
median±SD. Statistical analyses were performed with SPSS
version 7.0; significance was set at P<0.05.
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Results |
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Clinical and radiographic data were available for 113 patients. Extravasation of radiographic contrast in to the hematoma was observed in 52 (46%) of the studies. There was a trend toward a shorter median (range) time from symptom onset to CTA in patients with extravasation, 4.6±19 hours (1.4 to 120), than in patients with no evidence of extravasation, 6.6±28 hours (0.5 to 144); WRS P=0.065 (Figure 1
). There
was significant correlation (P=0.02, Spearman rank order)
between initial GCS score and time to CTA. Figures 2, 3, and 4 depict the
radiographic appearance of patients with no, minimal, or
extensive contrast extravasation. In most cases, the contrast
extravasated into the center of the hematoma, as seen in Figures 3 and 4.
Layering of contrast into a hematoma cavity was occasionally seen
(Figure 3), but contrast extravasation into the periphery of the
hematoma was almost never seen.
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The overall fatality was 38.1% (43 of 113). The hospital fatality rate
for patients with evidence of extravasation, 33 of 52 (63.5%), was
significantly higher than in patients without extravasation, 10 of 61
(16.4%) (OR 8.86; 95% CI 3.67 to 21.4; 2
P=0.011). The association of extravasation with fatality was
also seen when the analysis was limited to patients with
supratentorial ICH, 15 of 28 (53.6%) versus 5 of
41 (12.2%) (OR 12.7; 95% CI 4.39 to 36.8; 2
P<0.001).
By the time of evaluation in the emergency department, 18.5% of patients had received antihypertensive medications, 33.9% had received furosemide, and 26.4% had received mannitol; use of these medications was not associated with hospital fatality. Of the 113 patients, 64 (56.6%) had an ICP monitor placed at admission. Initial mean ICP was 17.5±16.5 mm Hg; ICP was higher among patients who died (27.1±25.2 mm Hg) than those that survived (14.6± 11.8 mm Hg), although the difference failed to reach statistical significance. Mean ICP did not differ among patients with and without extravasation. Ventriculostomies, or intraventricular catheters, were placed in 26.5% of patients, and decompressive surgery was performed on 29.2% of patients. Surgery was performed on 10 patients with infratentorial hemorrhage and 23 patients with supratentorial hemorrhage. The mean GCS score of patient undergoing decompressive surgery was 7.6±5.1, not statistically different from the mean GCS of those patients not undergoing decompression (8.4±5.0). The median age of the patients undergoing surgery was significantly less than that of those not receiving surgical intervention (55.0±13.5 years versus 64.0±15.0 years; WRS P=0.003).
Table 1 shows the results of the
univariate analyses for hospital fatality. In
brief, decreased level of consciousness (as measured by GCS), contrast
extravasation, increasing hematoma size,
intraventricular rupture of blood, increased
glucose, and increased pulse pressure were associated with the risk of
hospital death. Neither the systolic blood pressure (SBP) nor
the mean arterial blood pressure (MABP) was associated with
hospital fatality. The location of the ICH
(supratentorial versus infratentorial) did not
influence mortality in this univariate analysis.
Patients who underwent decompressive surgery were more likely to
survive.
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Univariate predictors of contrast extravasation include
decreasing GCS, increasing hematoma size,
intraventricular blood, increasing MABP, increasing
SBP, pulse pressure >60 mm Hg, glucose >8.3 mmol/L (150
mg/dL), decreasing PCO2, and
furosemide use prior to CTA. Use of antihypertensives before CTA was
associated with decreased frequency of extravasation (Table 2).
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Using a backward stepwise logistic regression, variables
independently associated with hospital fatality were lack of surgical
intervention, GCS 8, infratentorial location of ICH, extravasation of
contrast, and increasing hematoma size (Table 3). Other variables included in the
analysis were age, gender, pulse pressure >60 mm Hg,
systolic blood pressure >180 mm Hg, glucose, time to
CTA, and presence of IVH. Variables independently associated with
contrast extravasation were hematoma size, GCS 8, and MABP >120
mm Hg (Table 3). Other variables included in the
analysis were age, gender, use of furosemide before CTA, time
to CTA, glucose >8.3 mmol/L (150 mg/dL), hematoma location
(infratentorial versus supratentorial),
systolic blood pressure >180 mm Hg, and pulse pressure
>60 mm Hg.
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Discussion |
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Our study showed that nearly one half of all patients who underwent CTA had active extravasation of contrast at the time of presentation and that contrast extravasation was an independent predictor of hospital fatality. As in other studies, the GCS and hematoma size at presentation were also independent predictors of fatality.2 19 20 In addition, the initial GCS score and hematoma size were significantly associated with contrast extravasation. Presumably, contrast extravasation indicates ongoing hemorrhage and would therefore predispose to hematoma enlargement. Consistent with our findings, hematoma enlargement was previously observed to occur more frequently in patients with disturbed consciousness and in patients with large hematomas.5 6 Causality cannot be determined from observational studies such as this, but it is unlikely that a low GCS or a large hematoma would predispose to continued hemorrhage; it is more likely that continued hemorrhage produces larger hematomas that impair consciousness. Indeed, in a study in which patients underwent initial CT scan within 3 hours of symptom onset and follow-up scan 1 hour later, 26% had evidence of hematoma growth that was associated with clinical deterioration, as evidenced by a decrease in the GCS.21 In fact, any clinical deterioration that occurs within the first 12 hours after symptom onset is usually related to hematoma growth.22
Because hematoma enlargement occurs primarily in the initial hours after hemorrhage,5 6 one would expect that the risk of extravasation would be higher in patients undergoing early CTA. The median time to CTA in patients with extravasation was 4.6 hours in our study, compared with 6.6 hours in patients without extravasation, although the difference was not significant. Contrast extravasation was seen as late as 5 days after symptom onset in 1 patient.
We have no institutional guidelines for the management of hypertension in ICH, but in general, labetalol is used in an attempt to keep the MABP <120 mm Hg, and in this study contrast extravasation was independently associated with MABP >120 mm Hg. The association of contrast extravasation with hypertension is an important one and implies that elevation in blood pressure might contribute to the risk of continued hemorrhage. Elevated blood pressure at admission has been associated with increased mortality,20 23 increased hematoma size,23 and hematoma enlargement.5 6 The bulk of recent data show no evidence for an ischemic penumbra in acute ICH, either experimentally17 or clinically.11 Xenon blood flow studies even suggest that some patients have focal hyperperfusion in the acute stages of ICH.24 These data suggest that more aggressive blood pressure management in patients with ICH may be warranted,25 and a preliminary study11 shows that there is no compromise in CBF (as assessed by PET) in patients whom the MABP is lowered by 15%.
In our univariate analysis, hyperglycemia (glucose >8.3 mmol/L [150 mg/dL]) was associated with hematoma enlargement. The association between hyperglycemia and hematoma enlargement has been noted previously.6 Hyperglycemia also predisposes to hemorrhagic transformation of ischemic infarcts, both spontaneously26 27 and after tPA administration.28 Our univariate analysis also showed an association between increasing glucose and fatality. The association between hyperglycemia and increased morbidity and mortality following both ischemic29 30 31 and hemorrhagic stroke19 32 has been documented previously. The mechanism by which hyperglycemia contributes to worse outcome and predisposes to hemorrhage in stroke is unclear, but the association appears robust.
The observed mortality in our study was 38.1%, consistent with other studies that report mortality to be approximately 30% to 50%.33 34 35 36 It is important to appreciate that the primary outcome measure in our study was hospital fatality, whereas other studies use 30-day,20 33 34 90-day,5 36 or 180-day35 fatality rates. The fatality among our patients with contrast extravasation was 63.5%. Previous studies have also reported increased fatality in patients with hematomas that enlarge after admission.5 We also noted increased fatality in patients with infratentorial hemorrhage, an association that would be better understood if the proportions of patients with pure cerebellar hemorrhage and those with brain stem hemorrhage were known.
The incidence of contrast extravasation in our study is similar to that observed by others using different radiographic modalities. Yamaguchi et al37 found that 42% of patients with primary ICH had contrast extravasation during intra-arterial angiography when performed within 5 hours of symptom onset. Similar rates of gadolinium extravasation into cerebral hematomas have been observed during MR scanning.38 The literature also reports that approximately 20% of hematomas enlarge after presentation.5 6 This frequency is almost identical to the frequency of patients with extensive contrast extravasation (27/113=23.9%) in our study. Nearly half of our patients had at least some evidence of contrast extravasation, and it is probable that CTA is more sensitive at detecting small amounts of contrast extravasation than standard CT is for appreciating small changes in hematoma size. The fact that contrast extravasation tended to occur centrally within the hematoma suggests that it is extravasating from a vascular source and not from necrotic and edematous tissue surrounding the primary hemorrhage.7 8 To validate our findings and the presumption that extravasation is evidence of ongoing bleeding predisposing to hematoma enlargement, a prospective study with CTA at the time of presentation and comparison of initial hematoma size with that 24 hours later could be performed.
If hematoma enlargement were due to ongoing bleeding, it should be more frequent in patients with coagulopathy, alcohol abuse, and liver disease. There were no relationships between these variables and extravasation in our study, although relationships with coagulopathy and hematoma growth have been documented.5 6 Our ability to confirm these findings was likely limited by the small sample size and the lack of patients with documented coagulopathy, alcohol abuse, or liver disease in this series.
This study is limited by its retrospective nature. We have no clear protocol for when and on whom to perform CTA; in general, a CTA is obtained when the hemorrhage or the clinical situation seems atypical for primary hypertensive hemorrhage or when a surgical evacuation is planned. Thus, there is likely a bias toward the type of patient who undergoes CTA in this series, as suggested by the high proportion receiving surgical intervention (nearly 30%). In addition, the institutional criteria for surgical intervention in supratentorial hemorrhage are not explicit and are often dependent on the attending physician. Thus, the relationship between mortality and lack of surgical intervention must therefore be viewed cautiously, because patients who are likely to do well (ie, younger patients with a higher GCS) are more likely to receive aggressive therapy. Furthermore, it may be less likely for medical support to be withdrawn in patients who have undergone surgical intervention. Information about functional outcome would be important.
Conclusions
This is the first study to examine the role of CTA in primary
intracerebral hemorrhage. We found active
extravasation of contrast in 46% of our patients. Extravasation is
likely a surrogate for ongoing bleeding, and it is the most significant
radiological variable associated with fatality in the
multivariate model. The association between
extravasation and fatality was strong and independent of the previously
identified associations with admission GCS, admission hematoma size,
and fatality. The risk of extravasation is increased in patients with
elevated blood pressure, large hematomas, and depressed levels of
consciousness. It remains unclear whether aggressive antihypertensive
therapy in the acute phase of ICH would decrease the risk of
extravasation, and thus mortality, but this hypothesis could be tested
in a prospective randomized trial.
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Acknowledgments |
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Dr Tirschwell is funded by a PHS Individual NRSA, 1 F32 NS10445-01, from the National Institute of Neurological Disorders and Stroke and by the Genentech, Inc, Clinical Research Training Fellowship in Stroke from the American Academy of Neurology Education and Research Foundation.
Received June 11, 1999; revision received July 23, 1999; accepted July 23, 1999.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
- Tuhrim S, Horowitz DR, Sacher M, Godbold JH. Validation and comparison of models predicting survival following intracerebral hemorrhage. Crit Care Med. 1995;23:950–954.[Medline] [Order article via Infotrieve]
- Juvela S. Risk factors for impaired outcome after spontaneous intracerebral hemorrhage. Arch Neurol. 1995;52:1193–1200.[Abstract]
- Mase G, Zorzon M, Biasutti E, Tasca G, Vitrani B, Cazzato G. Immediate prognosis of primary intracerebral hemorrhage using an easy model for the prediction of survival. Acta Neurol Scand. 1995;91:306–309.[Medline] [Order article via Infotrieve]
- Portenoy RK, Lipton RB, Berger AR, Lesser ML, Lantos G. Intracerebral haemorrhage: a model for the prediction of outcome. J Neurol Neurosurg Psychiatry. 1987;50:976–979.[Abstract]
-
Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Tanaka R.
Multivariate analysis of predictors of hematoma
enlargement in spontaneous intracerebral
hemorrhage. Stroke. 1998;29:1160–1166.
[Abstract/Free Full Text] -
Kazui S, Minematsu K, Yamamoto H, Sawada T, Yamaguchi
T. Predisposing factors to enlargement of spontaneous
intracerebral hematoma. Stroke. 1997;28:2370–2375.
[Abstract/Free Full Text] - Fisher C. Pathological observations in hypertensive hemorrhage. J Neuropathol Exp Neurol. 1971;30:536–550.[Medline] [Order article via Infotrieve]
-
Mayer SA, Lignelli A, Fink ME, Kessler DB, Thomas
CE, Swarup R, van Heertum RL. Perilesional blood flow and edema
formation in acute intracerebral hemorrhage: a
SPECT study. Stroke. 1998;29:1791–1798.
[Abstract/Free Full Text] - Hossmann KA. Viability thresholds and the penumbra of focal ischemia. Ann Neurol. 1994;36:557–565.[Medline] [Order article via Infotrieve]
-
Astrup J, Siesjö BK, Symon L. Thresholds in
cerebral ischemia: the ischemic penumbra.
Stroke. 1981;12:723–725.
[Free Full Text] - Powers WJ, Adams RE, Yundt KD, Manno EM, Diebert E, Zazulia A, Videen TO, Diringer MN. Acute pharmacological hypotension after intracerebral hemorrhage does not change cerebral blood flow. Stroke. 1999;30:242. Abstract 264.
- Tomida S, Wagner HG, Klatzo I, Nowak TS Jr. Effect of acute electrode placement on regional CBF in the gerbil: a comparison of blood flow measured by hydrogen clearance, [3H]nicotine, and [14C]iodoantipyrine techniques. J Cereb Blood Flow Metab. 1989;9:79–86.[Medline] [Order article via Infotrieve]
- von Kummer R, von Kries F, Herold S. Hydrogen clearance method for determining local cerebral blood flow, II: effect of heterogeneity in cerebral blood flow. J Cereb Blood Flow Metab. 1986;6:492–498.[Medline] [Order article via Infotrieve]
- Bullock R, Brock-Utne J, van Dellen J, Blake G. Intracerebral hemorrhage in a primate model: effect on regional cerebral blood flow. Surg Neurol. 1988;29:101–107.[Medline] [Order article via Infotrieve]
-
Heiss WD, Traupe H. Comparison between hydrogen
clearance and microsphere technique for rCBF measurement.
Stroke. 1981;12:161–167.
[Abstract/Free Full Text] -
Sakurada O, Kennedy C, Jehle J, Brown JD, Carbin GL
Sokoloff L. Measurement of local cerebral blood flow with iodo
[14C] antipyrine. Am J Physiol. 1978;234:H59–H66.
[Abstract/Free Full Text] -
Qureshi AI, Wilson DA, Hanley DF, Traystman RJ. No
evidence for an ischemic penumbra in massive experimental
intracerebral hemorrhage. Neurology. 1999;52:266–272.
[Abstract/Free Full Text] -
Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck
LR, Zuccarello M, Khoury J. The ABCs of measuring
intracerebral hemorrhage volumes.
Stroke. 1996;27:1304–1305.
[Abstract/Free Full Text] -
Fogelholm R, Avikainen S, Murros K. Prognostic value
and determinants of first-day mean arterial pressure in
spontaneous supratentorial
intracerebral hemorrhage. Stroke. 1997;28:1396–1400.
[Abstract/Free Full Text] - Tuhrim S, Dambrosia JM, Price TR, Mohr JP, Wolf PA, Heyman A, Kase CS. Prediction of intracerebral hemorrhage survival. Ann Neurol. 1988;24:258–263.[Medline] [Order article via Infotrieve]
-
Brott T, Broderick J, Kothari R, Barsan W, Tomsick T,
Sauerbeck L, Spilker J, Duldner J, Khoury J. Early hemorrhage
growth in patients with intracerebral
hemorrhage. Stroke. 1997;28:1–5.
[Abstract/Free Full Text] -
Flemming KD, Wijdicks EFM, Louis EK, Li H. Predicting
deterioration in patients with lobar haemorrhages. J
Neurol Neurosurg Psychiatry. 1999;66:600–605.
[Abstract/Free Full Text] -
Terayama Y, Tanahashi N, Fukuuchi Y, Gotoh F.
Prognostic value of admission blood pressure in patients with
intracerebral hemorrhage: Keio Cooperative
Stroke Study. Stroke. 1997;28:1185–1188.
[Abstract/Free Full Text] - Miyazawa N, Mitsuka S, Asahara T, Uchida M, Fukamachi A, Fukasawa I, Sasaki H, Nukui H. Clinical features of relative focal hyperfusion in patients with intracerebral hemorrhage detected by contrast-enhanced xenon CT. AJNR Am J Neuroradiol. 1998;19:1741–1746.[Abstract]
-
Broderick JP, Adams HP, Jr, Barsan W, Feinberg W,
Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski
JM, Zuccarello M. Guidelines for the management of spontaneous
intracerebral hemorrhage: a statement for
healthcare professionals from a Special Writing Group of the Stroke
Council, American Heart Association. Stroke. 1999;30:905–915.
[Free Full Text] - de Courten-Myers GM, Kleinholz M, Holm P, DeVoe G, Schmitt G, Wagner KR, Myers RE. Hemorrhagic infarct conversion in experimental stroke. Ann Emerg Med. 1992;21:120–126.[Medline] [Order article via Infotrieve]
-
Broderick JP, Hagen T, Brott T, Tomsick T.
Hyperglycemia and hemorrhagic transformation of cerebral infarcts.
Stroke. 1995;26:484–487.
[Abstract/Free Full Text] -
Demchuk AM, Morgenstern LB, Krieger DW, Linda Chi T, Hu
W, Wein TH, Hardy RJ, Grotta JC, Buchan AM. Serum glucose level and
diabetes predict tissue plasminogen activator-
related intracerebral hemorrhage in acute
ischemic stroke. Stroke. 1999;30:34–39.
[Abstract/Free Full Text] -
Bruno A, Biller J, Adams HP Jr, Clarke WR, Woolson RF,
Williams LS, Hansen MD. Acute blood glucose level and outcome from
ischemic stroke: Trial of ORG 10172 in Acute Stroke Treatment
(TOAST) Investigators. Neurology. 1999;52:280–284.
[Abstract/Free Full Text] -
Weir CJ, Murray GD, Dyker AG, Lees KR. Is
hyperglycaemia an independent predictor of poor outcome after acute
stroke? Results of a long-term follow up study. BMJ. 1997;314:1303–1306.
[Abstract/Free Full Text] -
Woo E, Chan YW, Yu YL, Huang CY. Admission glucose
level in relation to mortality and morbidity outcome in 252 stroke
patients. Stroke. 1988;19:185–191.
[Abstract/Free Full Text] - Franke CL, van Swieten JC, Algra A, van Gijn J. Prognostic factors in patients with intracerebral haematoma. J Neurol Neurosurg Psychiatry. 1992;55:653–657.[Abstract]
-
Fieschi C, Carolei A, Fiorelli M, Argentino C, Bozzao
L, Fazio C, Salvetti M, Bastianello S. Changing prognosis of primary
intracerebral hemorrhage: results of a clinical
and computed tomographic follow-up study of 104 patients.
Stroke. 1988;19:192–195.
[Abstract/Free Full Text] -
Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster
G. Volume of intracerebral hemorrhage: a
powerful and easy-to-use predictor of 30-day mortality.
Stroke. 1993;24:987–993.
[Abstract/Free Full Text] -
Daverat P, Castel JP, Dartigues JF, Orgogozo JM. Death
and functional outcome after spontaneous intracerebral
hemorrhage: a prospective study of 166 cases using
multivariate analysis. Stroke. 1991;22:1–6.
[Abstract/Free Full Text] - Kreel L, Kay R, Woo J, Wong HY, Nicholls MG. The radiological (CT) and clinical sequelae of primary intracerebral haemorrhage. Br J Radiol. 1991;64:1096–1100.[Abstract]
- Yamaguchi K, Uemura K, Takahashi H, Kowada M, Kutsuzawa T. Intracerebral leakage of contrast medium in apoplexy. Br J Radiol. 1971;44:689–691.[Medline] [Order article via Infotrieve]
- Murai Y, Ikeda Y, Teramoto A, Tsuji Y. Magnetic resonance imaging-documented extravasation as an indicator of acute hypertensive intracerebral hemorrhage. J Neurosurg. 1998;88:650–655.[Medline] [Order article via Infotrieve]
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 J. Kim, A. Smith, J.C. Hemphill III, W.S. Smith, Y. Lu, W.P. Dillon, and M. Wintermark Contrast Extravasation on CT Predicts Mortality in Primary Intracerebral Hemorrhage AJNR Am. J. Neuroradiol., March 1, 2008; 29(3): 520 - 525. [Abstract] [Full Text] [PDF]
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R. Wada, R. I. Aviv, A. J. Fox, D. J. Sahlas, D. J. Gladstone, G. Tomlinson, and S. P. Symons CT Angiography "Spot Sign" Predicts Hematoma Expansion in Acute Intracerebral Hemorrhage Stroke, April 1, 2007; 38(4): 1257 - 1262. [Abstract] [Full Text] [PDF]
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 J. N. Goldstein, L. E. Fazen, R. Snider, K. Schwab, S. M. Greenberg, E. E. Smith, M. H. Lev, and J. Rosand Contrast extravasation on CT angiography predicts hematoma expansion in intracerebral hemorrhage Neurology, March 20, 2007; 68(12): 889 - 894. [Abstract] [Full Text] [PDF]
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 O. Takahashi, E.F. Cook, T. Nakamura, J. Saito, F. Ikawa, and T. Fukui Risk stratification for in-hospital mortality in spontaneous intracerebral haemorrhage: A Classification and Regression Tree Analysis QJM, November 1, 2006; 99(11): 743 - 750. [Abstract] [Full Text] [PDF]
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S. M. Davis, J. Broderick, M. Hennerici, N. C. Brun, M. N. Diringer, S. A. Mayer, K. Begtrup, T. Steiner, and for the Recombinant Activated Factor VII Intracere Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage Neurology, April 25, 2006; 66(8): 1175 - 1181. [Abstract] [Full Text] [PDF]
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P. Saloheimo, M. Ahonen, S. Juvela, J. Pyhtinen, E.-R. Savolainen, and M. Hillbom Regular Aspirin-Use Preceding the Onset of Primary Intracerebral Hemorrhage is an Independent Predictor for Death Stroke, January 1, 2006; 37(1): 129 - 133. [Abstract] [Full Text] [PDF]
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T. Steiner, J. Rosand, and M. Diringer Intracerebral Hemorrhage Associated With Oral Anticoagulant Therapy: Current Practices and Unresolved Questions Stroke, January 1, 2006; 37(1): 256 - 262. [Abstract] [Full Text] [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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 D. L. Brown and L. B. Morgenstern Stopping the Bleeding in Intracerebral Hemorrhage N. Engl. J. Med., February 24, 2005; 352(8): 828 - 830. [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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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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J. M. Gebel Jr, E. C. Jauch, T. G. Brott, J. Khoury, L. Sauerbeck, S. Salisbury, J. Spilker, T. A. Tomsick, J. Duldner, and J. P. Broderick Relative Edema Volume Is a Predictor of Outcome in Patients With Hyperacute Spontaneous Intracerebral Hemorrhage Stroke, November 1, 2002; 33(11): 2636 - 2641. [Abstract] [Full Text] [PDF]
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L.B. Morgenstern, A.M. Demchuk, D.H. Kim, R.F. Frankowski, and J.C. Grotta Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage Neurology, May 22, 2001; 56(10): 1294 - 1299. [Abstract] [Full Text] [PDF]
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K.J. Becker, A.B. Baxter, W.A. Cohen, H.M. Bybee, D.L. Tirschwell, D.W. Newell, H.R. Winn, and W.T. Longstreth Jr. Withdrawal of support in intracerebral hemorrhage may lead to self-fulfilling prophecies Neurology, March 27, 2001; 56(6): 766 - 772. [Abstract] [Full Text] [PDF]
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