The Egyptian Journal of Radiology and Nuclear Medicine (2013) 44, 625634

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology and Nuclear Medicine

www.elsevier.com/locate/ejrnm
www.sciencedirect.com

ORIGINAL ARTICLE

MRI diusion-weighted imaging in intracranial

hemorrhage (ICH)
Sherif A. Khedr a,b,*, Hassan Mahmoud Kassem
Eman Awad c,3, Mohamed M. Fouad d,4

a,b,1

, Ahmed M. Hazzou

c,2

Radiology Department, Cairo University, Egypt

Radiology Department, Benh University, Egypt
c
Departement of Neurology and Psychatry, Ain Shams University, Egypt
d
Neurosurgery Department, Cairo University, Egypt
b

Received 16 March 2013; accepted 19 April 2013

Available online 5 June 2013

KEYWORDS
DWI;
ICH;
Hemorrhagic infarction

Abstract Purpose: To assess the role of MRI DWI in detection and characterization of ICH.
Patients and methods: 61 patients with intracranial hemorrhage who underwent MRI (including
DWI, ADC, and GRE) and CT were retrospectively included in this study. MRI DWIs were analyzed for age, type, (primary parenchymal hemorrhage or hemorrhagic lesion) and location of the
hemorrhage. The results were compared with conventional MRI sequences, GRE, and CT to assess
the diagnostic accuracy of DWI in assessment of patients with intracranial hematoma.
Results: We had 61 patients with intracranial hemorrhage, six cases were missed by DWI. MRI
DWI was accurate for the detection of hyperacute, medium, large sized acute, early and late sub
acute, subdural, hemorrhagic components of arterial and venous infarction, intraventricular hemorrhage. DWI showed low sensitivity in detection of subarachnoid and small intraparenchymal
hemorrhage The ADC measurements in hyperacute, acute, early and late subacute hematoma were
statistically equivalent and were signicantly less than the late subacute hematoma as well as the
contralateral white matter.

* Corresponding author at: Radiology Department, Cairo University,

Jeddah, Saudi Arabia. Tel.: +966 540953377.
E-mail addresses: sherifkheder@yahoo.com (S.A. Khedr), kassem_
hassan60@yahoo.com (H.M. Kassem), ahazzou@gmail.com (A.M.
Hazzou), Awademan541@gmail.com (E. Awad), mmfoad@hotmail.
com (M.M. Fouad).
1
Tel.: +966 54108516.
2
Tel.: +966 509706661.
3
Tel.: +966 56411026.
4
Tel.: +20 1005389192.
Peer review under responsibility of Egyptian Society of Radiology and
Nuclear Medicine.

Production and hosting by Elsevier

0378-603X 2013 Production and hosting by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear Medicine.
Open access under CC BY-NC-ND license. http://dx.doi.org/10.1016/j.ejrnm.2013.04.010

626

S.A. Khedr et al.

Conclusion: MRI DWI was accurate in detection, characterization and staging hyperacute, acute,
subacute hemorrhage as well as hemorrhagic components of arterial and venous infarctions and of
low diagnostic accuracy in subarachnoid and small parenchymal hemorrhage.
2013 Production and hosting by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear
Medicine. Open access under CC BY-NC-ND license.

1. Introduction
Non contrast computed tomography (CT) has been the standard imaging modality for the initial evaluation of patients
presenting with acute stroke symptoms (1,2). The primary
diagnostic advantage of CT in the hyperacute phase (06 h)
is its ability to rule out the presence of hemorrhage. Accurate
early detection of blood is crucial since a history of intracerebral hemorrhage is a contraindication to the use of thrombolytic agents. However, a major disadvantage of conventional
CT within the rst few hours of symptom onset is its limited
sensitivity for identifying early evidence of cerebral ischemia.
Conversely, multimodal magnetic resonance imaging (MRI),
including diffusion-weighted imaging (DWI), has excellent
capacity to delineate the presence, size, location, and extent
of hyperacute ischemia (3) but unproven reliability in identifying early parenchymal hemorrhage. The advent of thrombolytic therapy and other interventional therapies for acute
ischemic stroke has led to increasing interest in using MRI
to select and stratify candidates for treatments (4). Currently,
many stroke centers obtain both CT and MRI in the initial
evaluation of patients with stroke. The use of both modalities
is time consuming and expensive (4).
2. Purpose
To assess the role of MRI diffusion weighted imaging in detection and characterization of intracranial hemorrhage.

MRI (including DWI and GRE) and CT with time interval between the CT and MRI examinations 24 h.
61 patients (10 females and 51 males; mean age, 56 years;
range, 1983) fullled these criteria and constituted our study
group.
4. Imaging techniques
MR examination was done for all patients using Magnetom
symphony, syngo, 1.5 T machine. The conventional MR imaging protocol included (a) axial T1-weighted spin-echo (467/9
[repetition time (TR) msec/echo time (TE) msec]), (b) axial
T2-weighted fast spin-echo (3417/102 [effective echo time]),
and (c) axial FLAIR (10000/400/2200 [inversion time]). The
parameters of conventional MR imaging were a 256 192 matrix, a 23-cm eld of view, and a 5 mm/2 mm slice thickness/
intersection gap. Singleshot, spin-echo, echo-planar DWI sequences were obtained by applying diffusion gradients in three
orthogonal directions at each slice, with two diffusion weightings (b value = 0 and 900 or 1000 s/mm2). Isotropic DWI
was generated on-line by averaging three orthogonal-axis
images. The DWI examination acquired 20 slices with parameters of 6500/96.8 (TR/TE), a 128 128 matrix, a 28-cm eld of
view, and 5-mm slice thickness with a 2-mm intersection gap.
gradient-echo imaging (TR/TE = 450/20).
Computed tomographic scans were performed on Lightspeed scanner (General Electric). Images were acquired following the orbito-meatal plane with 3 mm thickness for the entire
examination.

3. Patients
Among all consecutive patients admitted to our institution between March 2008 and Feb. 2011, we retrospectively selected
those who fullled the following criteria: (1) Intracranial
hematoma unrelated to neoplasm; (2) patients performed
Table 1

5. Imaging analysis
All the MRI and CT examination were reviewed by experienced neuroradiologist. Interpretations for each imaging

Signal intensities of intracerebral hematoma-according to the various stages demonstrated on MR images.

Stage of hematoma No of patients

T1 WIs

T2 WIs

DWI

GRE

Hyper acute
Acute
Small parenchymal hemorrhage
Early subacute
Late subacute

3
11
4
7
9

Isointense
Isointense

Hyperintense
Hyperintense

Hyperintense
Hypointense
Hypo or hyperintense
Hypointense
Hyperintense

Heterogeneous hyperintense
Hypo
Hypo or hyperintense
Hypointense
Hyperintense

Iso or hyperintense
Hypointense
Hypointense
Hypointense
Hyper or iso

Subdural
Early
Late
Intraventricular
Hemorrhagic arterial infarction

1
4
4
8

Hemorrhagic venous infarction

Subarachnoid hemorrhage

Hyperintense
Hyperintense
Hypointense
Heterogeneous hypo
and hyper
Heterogeneous hypo
and hyperintense
Hypo or hyperintense

Hypointense
Hyperintense
Hypointense
Heterogeneous hypo
and hyper
Heterogeneous hypo
and hyperintense
Hypointense

Hypointense
Hypointense
Hypointense
Heterogeneous hypo
and hyper
Heterogeneous hypo
and hyperintense
Hypointense

Hypointense
Iso or hypointense
Hypointense
Heterogeneous hypo
and hyper
Heterogeneous hypo
and hyperintense
Hypointense

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH)

Table 2 Diagnostic accuracy of DWI, GRE and CT for
detection of small intraparenchymal hemorrhage.

DWI
GRE
CT

Sensitivity
(%)

Specicity
(%)

PPV
(%)

NPV
(%)

Accuracy
(%)

25
50
100

100
100
100

100
100
100

95
96.6
100

95.1
96.6
100

modality (CT and MRI) for a single patient were performed on

different days to avoid reader recognition or recall of ndings
from the other modality. The order of presentation of the lms
was randomized and differed for each modality.
Diffusion weighted imaging was analyzed for
- Type of hemorrhage; parenchymal, intraventricular, subarachnoid, subdural, and epidural.
- Location of the hemorrhage; cortical, subcortical or basal
ganglia.
- Age of the hemorrhage. According to the time interval
between symptom onset and initial MRI, four stages were
categorized: hyperacute, acute, early subacute and late
subacute.

It was used to determine the apparent diffusion coefcient

(ADC) of each ICH (hyper acute, acute, early subacute and
late subacute) at its center, as seen at DWI. A region of interest
(ROI) was carefully placed within the hematoma and also in
contralateral normal white matter. The ROI was drawn as

Table 3 Diagnostic accuracy of DWI, GRE and CT for

detection of late subacute hematoma.
Sensitivity
(%)

Specicity
(%)

PPV
(%)

NPV
(%)

Accuracy
(%)

100
55.5

100
100

100
100

100
92.8

100
93.4

Table 4 Diagnostic accuracy of DWI, GRE and CT for

detection of hemorrhagic brain lesions.

DWI
GRE
CT

Sensitivity
(%)

Specicity
(%)

PPV
(%)

NPV
(%)

Accuracy
(%)

93.3
100
60

100
100
100

100
100
100

97.8
100
88.4

98.3
100
90.1

Table 5 Diagnostic accuracy of DWI, GRE and CT for

detection of subarachnoid hemorrhage.

DWI
CT

Table 6

Mean ADC in intracranial hematomas.

Stage of hematoma

Mean ADC value

(10 6 mm2/s)

SD

Hyperacute
(intracellular oxyhemoglobin)
Acute
(intracellular deoxyhemoglobin)
Early subacute
(intracellular methemoglobin)
Subacute-chronic
(extracellular methemoglobin)
Normal white matter

365.21

311.26

354.68

378.23

398.89

176.87

1, 121.32

24.61

780.87

94.33

large as possible while using a circular or rectangular ROI

on the workstation, and its area ranged from 14 to 302 mm2.
ADC calculation could not be done in small areas of hemorrhage. In each case, the radiologist measured the ROI and
the ADC values were calculated. All data concerning ADC
values are presented as means 1 standard deviation.
7. Statistical analysis
The presence of intracerebral hematomas was proved by CT,
GRE and conventional MRI sequences
8. Results

6. Quantitative analysis

DWI
CT

627

Sensitivity
(%)

Specicity
(%)

PPV
(%)

NPV
(%)

Accuracy
(%)

33.3
100

100
100

100
100

96.6
100

96.7
100

- Table 1 showed the signal intensities of the different types

of brain hemorrhage
- Hyperacute blood was found in three cases, all were
detected by diffusion weighted imaging,
- Acute intracerebral hematoma was found in 11 cases, all
were detected by diffusion weighted imaging
- Small parenchymal hemorrhage (post traumatic) was found
in four cases, three of them were missed by DWI (Table 2).
- Early subacute hematoma was found in seven cases, all
were detected by diffusion weighted imaging.
- Late subacute hematoma was found in nine cases, all were
detected by diffusion weighted imaging (Table 3).
- Subdural hematoma was found in ve cases (1 early and 4
late subacute), all were detected by diffusion weighted
imaging.
- Intraventricular hematoma was found in four cases, all
were equally detected by diffusion weighted imaging.
- Hemorrhagic arterial infarction was found in eight cases,
all were detected by DWI.
- Hemorrhagic venous infarction was found seven cases, one
case was missed by DWI (Table 4).
- Subarachnoid hemorrhage was found in three cases, two of
them were missed by DWI (Table 5).
The ADC measurements in hyperacute, acute, early and
late subacute hematoma were statistically equivalent. The
ADC measurements in hyperacute, acute, early and late subacute hematoma were signicantly less than the late subacute
hematoma as well as the contralateral white matter (Table 6).
9. Discussion
Neuroimaging plays a crucial role in the evaluation of patients
presenting with acute stroke symptoms. While patient

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S.A. Khedr et al.

Fig. 1 A 53-year-old man with hyperacute intracerebral hematoma with images obtained 2 h after the onset of symptoms. Left
frontotemporal hyperacute intracerebral hematoma with intraventricular extension appearing hyperdense in CT (a), isointense in T1WIs
(b), heterogeneous hyperintense in T2WIs (c), heterogeneous hyperintense in DWI with peripheral hypointense rim (arrow in d),
heterogeneous hypointense in ADC (e) and heterogeneous hyperintense in GRE (f). The peripheral hypointense rim is more obvious in
GRE.

symptoms and clinical examinations may suggest the diagnosis, only brain imaging studies can conrm the diagnosis and
differentiate hemorrhage from ischemia with high accuracy.
This differentiation is critical in making acute treatment decisions, including patient eligibility for thrombolytic therapy
(5,6).
In the current study we had 61 patients with intracranial
hemorrhage, six cases were missed by DWI.
- In the current study all the three cases of hyperacute hematoma (Fig. 1), were detected by DWI showing heterogeneous hyperintense core, hypointese rim surrounded by
perifocal brain edema. The central hyperintensity has been
attributed to intracellular oxyhemoglobin and the hypointense rim to early intracellular deoxyhemoglobin at the
periphery of a hematoma. This characteristic hypointense
rim has been reported to occur within the rst few hours
of hemorrhage and in patients with acute neurologic symptoms is valuable for differentiating between acute ischemic
stroke and hemorrhage (6,7). This hypointense rim was
more obvious in GRE than in DWI in the current study
(Fig. 1). The signal intensity of hyperacute ICH observed
at DWI was consistent with the ndings of previous studies
(8). The MR features of hyperintensity at the core of a
hematoma and focal variable hypointensity were consistently found in all patients with hyperacute ICH. Hypointensity within a hyperacute hematoma, revealed by DWI,
may be an important feature for differentiating hemorrhage

from infarction in the practical clinical setting of hyperacute stroke. The focal hypointensity seen at DWI within
a hyperacute hematoma may be caused by unclotted liquid
separated from a retracted clot (9,10). Previous studies have
suggested that the cause of hypointensity within a hyperacute hematoma, seen on DWI may be the early presence
of paramagnetic deoxyhemoglobin (11,12). In all patients
with hyperacute hematoma in the current study, T1weighted imaging revealed a thin, slight hypointense rim.
On T2-weighted images, this was iso- or hypointense and
was located at the periphery of the hematoma, inside the
region of perilesional hyperintensity, a nding consistent
with edema in adjacent parenchyma. Compared with T2weighted images, conventional gradient-echo images
showed mixed iso- or hyperintensity at the center of the
hemorrhage and a more noticeable hypointense rim at its
periphery.
In the current study, all the 11 cases of acute hematoma
(Figs. 2 and 7) and cases of early subacute hematoma were detected by DWI showing markedly hypointense core at DWI,
T2-weighted images, FLAIR and GRE. This hypointensity
has been attributed to the magnetic eld inhomogeneity caused
by paramagnetic intracellular deoxyhemoglobin in acute
hematoma (13) and paramagnetic intracellular methemoglobin
in early subacute hematoma (14). At both stages, DWI consistently revealed that in all these patients, a thin, markedly
hyperintense rim, varying in thickness and completeness, was

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH)

629

Fig. 2 A 49-year-old man with acute intracerebral hematoma with images obtained 2 days after the onset of symptoms. Acute right
frontal hematoma appearing hyperdense in CT (a), isointense in T1Wis with small hyperintense areas within (b), hypointense in T2WIs (c),
FLAIR (d), GRE (e), DWI (f), and ADC (g). It is surrounded by perifocal brain edema.

present at the periphery of the hematoma. The bright rims corresponded to the areas of hyperintensity seen on T2-weighted
images. In Echo-planar gradient-echo images the signal intensities observed were markedly hypointense, though the hyperintense rim seen at DWI was not demonstrated. T1-weighted
images showed the hematoma as heterogeneously isointense
at the acute stage and markedly hyperintense at the early subacute stage.

well as the distinction of hemorrhage versus nonhemorrhage

more difcult (15,16).
Late subacute hematoma was found in 9 cases in the current study, all of these cases showed marked hyper intense core
with hypo-intense rim (Fig. 4). All the cases also showed
marked hyper intensity at T1- and T2-weighted, and FLAIR
images while GRE demonstrated heterogeneous hyperintensity
(16,17).

- Small post traumatic parenchymal hemorrhage was found

in four cases in our study, three cases of them were missed
by DWI. DWI showed in the fourth case small areas of
high signal. All these cases were detected by CT showing
small hyperdensity. These focal areas were hypointense by
GRE (we could not conrm if these areas were acute or
chronic hematoma) and missed by T1 and T2WIs. In addition, the four post traumatic patients in the current study,
showing small areas of restriction on DWI seen in the splenium of corpus callosum not seen by CT and GRE (Fig. 3).

- We had ve cases of Subdural hematoma (1 early subacute

and 4 late subacute), all showing heterogeneous signal at
DWI. This may be explained by the fact that the subdural
hematoma is almost always mixed (acute, early and late
subacute), and the hypointensity is caused by paramagnetic
intracellular deoxyhemoglobin and paramagnetic intracellular methemoglobin (17) (Fig. 5).
- We had 4 cases of intraventricular hematoma (Fig. 1), all
showing low signal at DWI.
- We had 8 cases of hemorrhagic arterial and 7 cases of hemorrhagic venous infarction (Figs. 6 and 7) all showing low
signal areas at DWI within the bright infarction.
- In our study all the eight cases of hemorrhagic arterial and
seven cases of hemorrhagic venous infarction (Figs. 6 and
8) appeared heteogenous on DWI showing areas of low signal intensity within areas of restricted diffusion. These ndings were in agreement with previous studies (18,19) and
was explained by the presence of prominent vasogenic
edema associated with mild cytotoxic edema (20). The hemorrhagic areas in hemorrhagic arterial and venous infarctions gave the signal intensity of early subacute
hematoma on DWI, T1WIs, and T2WIs.

Physicians should be aware that in cases of small hemorrhages, it may be difcult to make an exact distinction between acute and chronic hemorrhage based on GRE images
alone. A noncontrast CT may be necessary in these cases
to determine hemorrhage age. With acute medium-large hemorrhages, the characteristic appearance of mixed signal intensity and the surrounding hyperintensity due to edema is very
specic and will make the age of the hemorrhage apparent.
However, small hemorrhages may have similar characteristics
to calcications and intravascular thrombus and have minimal edema making the determination of hemorrhage age as

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S.A. Khedr et al.

Fig. 3 A 35-year-old man with post traumatic intracerebral hematoma with images obtained after 6 h. Left frontal small areas of
hemorrhage appearing hyperdense in CT (b) (straight arrow) hyperintense in FLAIR (d), not seen in T1 and T2WIs, appearing
hyperintense in DWI (j), hypointense in ADC (l) and GRE (n) interpreted as old hematoma. There is an area of diffusion restriction
(contusion) in the splenium of corpus callosum only seen in DWI (i), ADC (k) (curved arrow) and FLAIR (c).

The implication of this nding for the neuroimaging evaluation of acute stroke patients who are candidates for thrombolytic therapy is unclear. In the National Institute of
Neurological Disorders and Stroke (NINDS) trial, intravenous
tPA was shown to be effective based on CT enrollment criteria
(19). While it may be hypothesized that patients with MRI evidence of hemorrhagic transformation are at higher risk of
developing symptomatic hemorrhage if treated with thrombo-

lytics, it is also possible that overall this group of patients may

receive net benet from therapy (19,21,22).
- We had three cases of subarachnoid hemorrhage in our
study, only one case seen on DWI showed area of low signal intensity at the left temporal sulci surrounded by brain
edema (Fig. 8). These ndings were in agreement with previous studies (23,24,25).

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH)

631

Fig. 4 A 62-year-old man with late subacute intracerebral hematoma with images obtained 9 days after the onset of symptoms .The
hematoma in the right cerebellar hemisphere appearing hypodense in CT (a), hyperintense in T1WIs (b), T2WIs (c), FlAIR (d), DWI (e),
hypointense in ADC (f) and heterogeneous hyperintense in GRE (g).

Fig. 5 A 56-year-old man with subacute subdural hematoma with images obtained 5 days after the onset of symptoms. The hematoma
appears heterogeneously hypodense in CT (a), hyperintense in T1 and T2WIs (b and c), hypointense in DWI (d), hyperintense in ADC (e),
and heterogeneous hyperintense in GRE (f).

The ADC measurements in hyperacute, acute, early and late

subacute hematoma were statistically equivalent. The ADC
measurements in hyperacute, acute, early and late subacute
hematoma were signicantly less than the late subacute hematoma as well as the contralateral white matter (p value <.001).

The precise biophysical explanation for the observed restriction

of diffusion in early stages of intracranial hematomas is uncertain. Potential causes include, but are not limited to: (1) a shrinkage of extracellular space with clot retraction; (2) a change in the
osmotic environment once blood becomes extravascular, which

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S.A. Khedr et al.

Fig. 6 A 47 year old male with left frontotemporal hemorrhagic arterial infarct with images taken 3 days after symptoms .It appears
hypodense in CT (a). The hemorrhagic area is seen in the lentiform nucleus appearing slightly hyperintense in T1WIs (b), hypointense in
T2WIs, GRE, DWI and ADC (cf). Left middle cerebral artery occlusion in MRA (g).

alters the shape of the RBC, a phenomenon related to the formation of the brin network associated with clot; (3) a conformational change of the hemoglobin macromolecule within the
RBC; and the less likely possibility of (4) contraction of intact
RBCs (thereby decreasing intracellular space) (24,25).
Our study may have implications for the imaging evaluation of patients with acute stroke symptoms. Our ndings support prior studies suggesting that MRI DWI is accurate in
detection characterization and staging of hyperacute, medium
and large sized acute, and early sub acute hemorrhage. One
important caveat is that with small hemorrhages, blood that
appears as acute on CT may appear as ischemic foci on
DWI and as chronic hemorrhage on GRE MRI. A noncontrast CT may be required to conrm the diagnosis in these
cases. However in cases of post traumatic axonal injury, small
areas of contusion were detected by DWI in the corpus callosum in our study not detected by CT or GRE. Our study suggests that DWI and GRE MRI may be able to detect regions
of hemorrhagic arterial and venous infarction not evident on
CT. Our ndings suggest that DWI was nearly as accurate
as CT for the detection of early subacute hemorrhage and subdural hematoma. Our study conrms the superiority of DWI

for detection of late subacute subdural. DWI was not accurate

in detection of subarachnoid hemorrhage.
10. The limitations of this study
They include the lack of histopathological conrmation and
the small number of cases. Although a complete understanding
of the underlying biophysical basis may require further studies
with a large population, our data suggest that the appearance
of intracerebral hematomas on diffusion-weighted images is
inuenced not only by ADC values but also by magnetic susceptibility and T2 shine-through effects. In addition, our study
corroborates the key features of evolving intracerebral hematomas, as depicted by conventional MR imaging.
11. Conclusion
Due to its advantages in delineating ischemic pathophysiology,
MRI DWI was accurate in detection, characterization and
staging hyperacute, subacute hemorrhage as well as hemorrhagic components of arterial and venous infarctions and of

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH)

633

Fig. 7 A 58 year old female with right occipital hemorrhagic venous infarct appearing hypodense in CT (a). The hemorrhagic area
appears hyperintense in T1WIs (b), hypointense in T2 WIs (c), FLAIR (d), DWI (e), ADC (f), and GRE (g). There was marked
attenuation of the superior saggital sin in MRV (h).

Fig. 8 A 55 year old man with left sided subarachnoid hemorrhage seen by T1, FLAIR, T2WIs, DWI, ADC and GRE (af). It appears
hyperintense in T1WIS, hypointense in T2WIs, FLAIR, DWI, ADC and GRE surrounded by brain edema.

low diagnostic accuracy in subarachnoid and small parenchymal hemorrhage.

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