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ORIGINAL ARTICLE

MRI diffusion-weighted imaging in intracranial

hemorrhage (ICH)

Sherif A. Khedr   a,b,*, Hassan Mahmoud Kassem   a,b,1, Ahmed M. Hazzou   c,2,

Eman Awad   c,3, Mohamed M. Fouad   d,4

a Radiology Department, Cairo University, Egyptb Radiology Department, Benh University, Egyptc Departement of Neurology and Psychatry, Ain Shams University, Egyptd Neurosurgery Department, Cairo University, Egypt

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 ana-

lyzed 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 hem-

orrhage. 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 significantly 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:   [email protected]   (S.A. Khedr),   kassem_ [email protected]   (H.M. Kassem),   [email protected]   (A.M.

Hazzou),   [email protected]  (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

The Egyptian Journal of Radiology and Nuclear Medicine (2013)  44, 625–634

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology and Nuclear Medicine

www.elsevier.com/locate/ejrnmwww.sciencedirect.com

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

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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

1. Introduction

Non contrast computed tomography (CT) has been the stan-

dard 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 (0–6 h)

is its ability to rule out the presence of hemorrhage. Accurate

early detection of blood is crucial since a history of intracere-

bral hemorrhage is a contraindication to the use of thrombo-

lytic agents. However, a major disadvantage of conventional

CT within the first 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 extentof hyperacute ischemia (3)  but unproven reliability in identify-

ing early parenchymal hemorrhage. The advent of thrombo-

lytic 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 detec-

tion and characterization of intracranial hemorrhage.

3. Patients

Among all consecutive patients admitted to our institution be-

tween March 2008 and Feb. 2011, we retrospectively selected

those who fulfilled the following criteria: (1) Intracranial

hematoma unrelated to neoplasm; (2) patients performed

MRI (including DWI and GRE) and CT with time interval be-

tween the CT and MRI examinations 2–4 h.

61 patients (10 females and 51 males; mean age, 56 years;

range, 19–83) fulfilled 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 imag-

ing 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]). Theparameters of conventional MR imaging were a 256 192 ma-

trix, a 23-cm field of view, and a 5 mm/2 mm slice thickness/

intersection gap. Singleshot, spin-echo, echo-planar DWI se-

quences were obtained by applying diffusion gradients in three

orthogonal directions at each slice, with two diffusion weigh-

tings (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 param-

eters of 6500/96.8 (TR/TE), a 128 128 matrix, a 28-cm field 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 Light-

speed scanner (General Electric). Images were acquired follow-

ing the orbito-meatal plane with 3 mm thickness for the entire

examination.

5. Imaging analysis

All the MRI and CT examination were reviewed by experi-

enced neuroradiologist. Interpretations for each imaging

Table 1   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 3 Isointense Hyperintense Heterogeneous hyperintense Iso or hyperintense

Acute 11 Isointense Hypointense Hypo HypointenseSmall parenchymal hemorrhage 4 – Hypo or hyperintense Hypo or hyperintense Hypointense

Early subacute 7 Hyperintense Hypointense Hypointense Hypointense

Late subacute 9 Hyperintense Hyperintense Hyperintense Hyper or iso

Subdural 

Early 1 Hyperintense Hypointense Hypointense Hypointense

Late 4 Hyperintense Hyperintense Hypointense Iso or hypointense

Intraventricular 4 Hypointense Hypointense Hypointense Hypointense

Hemorrhagic arterial infarction 8 Heterogeneous hypo

and hyper

Heterogeneous hypo

and hyper

Heterogeneous hypo

and hyper

Heterogeneous hypo

and hyper

Hemorrhagic venous infarction 7 Heterogeneous hypo

and hyperintense

Heterogeneous hypo

and hyperintense

Heterogeneous hypo

and hyperintense

Heterogeneous hypo

and hyperintense

Subarachnoid hemorrhage 3 Hypo or hyperintense Hypointense Hypointense Hypointense

626 S.A. Khedr et al.

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

different days to avoid reader recognition or recall of findings

from the other modality. The order of presentation of the films

was randomized and differed for each modality.

Diffusion weighted imaging was analyzed for

- Type of hemorrhage; parenchymal, intraventricular, sub-

arachnoid, 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 latesubacute.

6. Quantitative analysis

It was used to determine the apparent diffusion coefficient

(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

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 hemor-

rhage. 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

- 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 five 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 suba-

cute hematoma were significantly 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

Table 2   Diagnostic accuracy of DWI, GRE and CT for

detection of small intraparenchymal hemorrhage.

Sensitivity

(%)

Specificity

(%)

PPV

(%)

NPV

(%)

Accuracy

(%)

DWI 25 100 100 95 95.1

GRE 50 100 100 96.6 96.6

CT 100 100 100 100 100

Table 3   Diagnostic accuracy of DWI, GRE and CT fordetection of late subacute hematoma.

Sensitivity

(%)

Specificity

(%)

PPV

(%)

NPV

(%)

Accuracy

(%)

DWI 100 100 100 100 100

CT 55.5 100 100 92.8 93.4

Table 4   Diagnostic accuracy of DWI, GRE and CT for

detection of hemorrhagic brain lesions.

Sensitivity

(%)

Specificity

(%)

PPV

(%)

NPV

(%)

Accuracy

(%)

DWI 93.3 100 100 97.8 98.3GRE 100 100 100 100 100

CT 60 100 100 88.4 90.1

Table 5   Diagnostic accuracy of DWI, GRE and CT for

detection of subarachnoid hemorrhage.

Sensitivity

(%)

Specificity

(%)

PPV

(%)

NPV

(%)

Accuracy

(%)

DWI 33.3 100 100 96.6 96.7

CT 100 100 100 100 100

Table 6   Mean ADC in intracranial hematomas.

Stage of hematoma Mean ADC value

(106 mm2/s)

SD

Hyperacute

(intracellular oxyhemoglobin)

365.21 311.26

Acute

(intracellular deoxyhemoglobin)

354.68 378.23

Early subacute

(intracellular methemoglobin)

398.89 176.87

Subacute-chronic

(extracellular methemoglobin)

1, 121.32 24.61

Normal white matter 780.87 94.33

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symptoms and clinical examinations may suggest the diagno-

sis, only brain imaging studies can confirm the diagnosis anddifferentiate hemorrhage from ischemia with high accuracy.

This differentiation is critical in making acute treatment deci-

sions, 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 hema-

toma (Fig. 1), were detected by DWI showing heteroge-

neous hyperintense core, hypointese rim surrounded by

perifocal brain edema. The central hyperintensity has been

attributed to intracellular oxyhemoglobin and the hypoin-

tense rim to early intracellular deoxyhemoglobin at the

periphery of a hematoma. This characteristic hypointenserim has been reported to occur within the first few hours

of hemorrhage and in patients with acute neurologic symp-

toms 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 findings of previous studies

(8). The MR features of hyperintensity at the core of a

hematoma and focal variable hypointensity were consis-

tently found in all patients with hyperacute ICH. Hypoin-

tensity within a hyperacute hematoma, revealed by DWI,

may be an important feature for differentiating hemorrhage

from infarction in the practical clinical setting of hyper-

acute 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 hyper-

acute hematoma, seen on DWI may be the early presence

of paramagnetic deoxyhemoglobin   (11,12). In all patients

with hyperacute hematoma in the current study, T1-

weighted 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 finding consistent

with edema in adjacent parenchyma. Compared with T2-

weighted images, conventional gradient-echo images

showed mixed iso- or hyperintensity at the center of the

hemorrhage and a more noticeable hypointense rim at itsperiphery.

In the current study, all the 11 cases of acute hematoma

(Figs. 2 and 7) and cases of early subacute hematoma were de-

tected by DWI showing markedly hypointense core at DWI,

T2-weighted images, FLAIR and GRE. This hypointensity

has been attributed to the magnetic field inhomogeneity caused

by paramagnetic intracellular deoxyhemoglobin in acute

hematoma (13) and paramagnetic intracellular methemoglobin

in early subacute hematoma (14). At both stages, DWI consis-

tently revealed that in all these patients, a thin, markedly

hyperintense rim, varying in thickness and completeness, was

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.

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present at the periphery of the hematoma. The bright rims cor-

responded to the areas of hyperintensity seen on T2-weighted

images. In Echo-planar gradient-echo images the signal inten-

sities observed were markedly hypointense, though the hyper-

intense rim seen at DWI was not demonstrated. T1-weightedimages showed the hematoma as heterogeneously isointense

at the acute stage and markedly hyperintense at the early sub-

acute stage.

- 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 confirm if these areas were acute or

chronic hematoma) and missed by T1 and T2WIs. In addi-

tion, the four post traumatic patients in the current study,

showing small areas of restriction on DWI seen in the sple-

nium of corpus callosum not seen by CT and GRE (Fig. 3).

Physicians should be aware that in cases of small hemor-

rhages, it may be difficult to make an exact distinction be-

tween 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 hem-

orrhages, the characteristic appearance of mixed signal inten-

sity and the surrounding hyperintensity due to edema is very

specific and will make the age of the hemorrhage apparent.

However, small hemorrhages may have similar characteristics

to calcifications and intravascular thrombus and have mini-

mal edema making the determination of hemorrhage age as

well as the distinction of hemorrhage versus nonhemorrhage

more difficult   (15,16).

Late subacute hematoma was found in 9 cases in the cur-

rent study, all of these cases showed marked hyper intense core

with hypo-intense rim (Fig. 4). All the cases also showedmarked hyper intensity at T1- and T2-weighted, and FLAIR

images while GRE demonstrated heterogeneous hyperintensity

(16,17).

- We had five 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 intracel-

lular 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 hem-orrhagic 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 sig-

nal intensity within areas of restricted diffusion. These find-

ings 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 hem-

orrhagic areas in hemorrhagic arterial and venous infarc-

tions gave the signal intensity of early subacute

hematoma on DWI, T1WIs, and T2WIs.

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.

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH) 629

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The implication of this finding for the neuroimaging evalu-

ation of acute stroke patients who are candidates for thrombo-

lytic 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 evi-

dence 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 benefit 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 sig-

nal intensity at the left temporal sulci surrounded by brain

edema (Fig. 8). These findings were in agreement with pre-

vious studies (23,24,25).

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).

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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 significantly less than the late subacute hema-

toma 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 uncer-

tain. Potential causesinclude,but arenot limited to:(1) a shrink-

age of extracellular space with clot retraction; (2) a change in the

osmotic environment once blood becomes extravascular, which

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).

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH) 631

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altersthe shape of theRBC, a phenomenon related to theforma-

tion of the fibrin network associated with clot; (3) a conforma-

tional 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 evalua-

tion of patients with acute stroke symptoms. Our findings sup-

port 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. Oneimportant 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 noncon-

trast CT may be required to confirm the diagnosis in these

cases. However in cases of post traumatic axonal injury, small

areas of contusion were detected by DWI in the corpus callo-

sum in our study not detected by CT or GRE. Our study sug-

gests that DWI and GRE MRI may be able to detect regions

of hemorrhagic arterial and venous infarction not evident on

CT. Our findings suggest that DWI was nearly as accurate

as CT for the detection of early subacute hemorrhage and sub-

dural hematoma. Our study confirms 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 confirmation 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

influenced not only by ADC values but also by magnetic sus-

ceptibility and T2 shine-through effects. In addition, our study

corroborates the key features of evolving intracerebral hema-

tomas, 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 hemor-

rhagic components of arterial and venous infarctions and of 

Fig. 6   A 47 year old male with left frontotemporal hemorrhagic arterial infarct with images taken 3 days after symptoms .It appearshypodense 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 (c–f). Left middle cerebral artery occlusion in MRA (g).

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low diagnostic accuracy in subarachnoid and small parenchy-

mal hemorrhage.

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