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

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology andNuclearMedicine

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

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

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KEYWORDS

DWI;

ICH;

Hemorrhagic infarction

Corresponding author at: Ra

ddah, Saudi Arabia. Tel.: +

mail addresses: sherifkheder

ssan60@yahoo.com (H.M.

azzou), Awademan541@gma

m (M.M. Fouad).

Tel.: +966 54108516.

Tel.: +966 509706661.

Tel.: +966 56411026.

Tel.: +20 1005389192.

er review under responsibility

uclear Medicine.

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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.

epartment, Cairo University,

53377.

.com (S.A. Khedr), kassem_

, ahazzou@gmail.com (A.M.

. Awad), mmfoad@hotmail.

tian Society of Radiology and

g by Elsevier

ing by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear Medicine.

4.010

Table 1 Signal intensities of intrac

Stage of hematoma No of patients

Hyper acute

Acute

Small parenchymal hemorrhage

Early subacute

Late subacute

Subdural

Early

Late

Intraventricular

Hemorrhagic arterial infarction

Hemorrhagic venous infarction

Subarachnoid hemorrhage

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.

1. Introduction

Non contrast computed tomography (CT) has been the stan-dard imaging modality for the initial evaluation of patientspresenting with acute stroke symptoms (1,2). The primarydiagnostic advantage of CT in the hyperacute phase (0–6 h)

is its ability to rule out the presence of hemorrhage. Accurateearly 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 conventionalCT within the first few hours of symptom onset is its limitedsensitivity for identifying early evidence of cerebral ischemia.

Conversely, multimodal magnetic resonance imaging (MRI),including diffusion-weighted imaging (DWI), has excellentcapacity 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 acuteischemic 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 initialevaluation 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) Intracranialhematoma unrelated to neoplasm; (2) patients performed

erebral hematoma-according to

T1 WIs T2 WI

3 Isointense Hyper

11 Isointense Hypoi

4 – Hypo

7 Hyperintense Hypoi

9 Hyperintense Hyper

1 Hyperintense Hypoi

4 Hyperintense Hyper

4 Hypointense Hypoi

8 Heterogeneous hypo

and hyper

Hetero

and hy

7 Heterogeneous hypo

and hyperintense

Hetero

and hy

3 Hypo or hyperintense Hypoi

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 studygroup.

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 threeorthogonal directions at each slice, with two diffusion weigh-

tings (b value = 0 and 900 or 1000 s/mm2). Isotropic DWIwas generated on-line by averaging three orthogonal-axisimages. The DWI examination acquired 20 slices with param-

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

5. Imaging analysis

All the MRI and CT examination were reviewed by experi-

enced neuroradiologist. Interpretations for each imaging

the various stages demonstrated on MR images.

s DWI GRE

intense Heterogeneous hyperintense Iso or hyperintense

ntense Hypo Hypointense

or hyperintense Hypo or hyperintense Hypointense

ntense Hypointense Hypointense

intense Hyperintense Hyper or iso

ntense Hypointense Hypointense

intense Hypointense Iso or hypointense

ntense Hypointense Hypointense

geneous hypo

per

Heterogeneous hypo

and hyper

Heterogeneous hypo

and hyper

geneous hypo

perintense

Heterogeneous hypo

and hyperintense

Heterogeneous hypo

and hyperintense

ntense Hypointense Hypointense

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 6 Mean ADC in intracranial hematomas.

Stage of hematoma Mean ADC value

(10�6 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

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH) 627

modality (CT and MRI) for a single patient were performed ondifferent days to avoid reader recognition or recall of findings

from the other modality. The order of presentation of the filmswas 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 basalganglia.

- Age of the hemorrhage. According to the time intervalbetween 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 andlate 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

(%)

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 98.3

GRE 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

large as possible while using a circular or rectangular ROIon 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 andthe 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 typesof brain hemorrhage

- Hyperacute blood was found in three cases, all weredetected by diffusion weighted imaging,

- Acute intracerebral hematoma was found in 11 cases, allwere 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, allwere detected by diffusion weighted imaging.

- Late subacute hematoma was found in nine cases, all weredetected by diffusion weighted imaging (Table 3).

- Subdural hematoma was found in five cases (1 early and 4

late subacute), all were detected by diffusion weightedimaging.

- Intraventricular hematoma was found in four cases, allwere 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 ofthem were missed by DWI (Table 5).

The ADC measurements in hyperacute, acute, early andlate subacute hematoma were statistically equivalent. TheADC measurements in hyperacute, acute, early and late suba-

cute hematoma were significantly less than the late subacutehematoma as well as the contralateral white matter (Table 6).

9. Discussion

Neuroimaging plays a crucial role in the evaluation of patientspresenting with acute stroke symptoms. While patient

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.

628 S.A. Khedr et al.

symptoms and clinical examinations may suggest the diagno-sis, only brain imaging studies can confirm the diagnosis and

differentiate 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 intracranialhemorrhage, 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 beenattributed 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 hoursof hemorrhage and in patients with acute neurologic symp-toms is valuable for differentiating between acute ischemic

stroke and hemorrhage (6,7). This hypointense rim wasmore 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 ahematoma 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 withina hyperacute hematoma may be caused by unclotted liquidseparated 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 presenceof 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 andwas located at the periphery of the hematoma, inside the

region of perilesional hyperintensity, a finding consistentwith edema in adjacent parenchyma. Compared with T2-weighted images, conventional gradient-echo images

showed mixed iso- or hyperintensity at the center of thehemorrhage 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 hypointensityhas been attributed to the magnetic field inhomogeneity causedby paramagnetic intracellular deoxyhemoglobin in acute

hematoma (13) and paramagnetic intracellular methemoglobinin 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. 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

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

responded to the areas of hyperintensity seen on T2-weightedimages. 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 isointenseat the acute stage and markedly hyperintense at the early sub-acute stage.

- Small post traumatic parenchymal hemorrhage was foundin four cases in our study, three cases of them were missed

by DWI. DWI showed in the fourth case small areas ofhigh signal. All these cases were detected by CT showingsmall hyperdensity. These focal areas were hypointense by

GRE (we could not confirm if these areas were acute orchronic 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 imagesalone. 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 characteristicsto 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 FLAIRimages while GRE demonstrated heterogeneous hyperintensity(16,17).

- We had five cases of Subdural hematoma (1 early subacuteand 4 late subacute), all showing heterogeneous signal at

DWI. This may be explained by the fact that the subduralhematoma is almost always mixed (acute, early and latesubacute), 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), allshowing 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 lowsignal areas at DWI within the bright infarction.

- In our study all the eight cases of hemorrhagic arterial andseven cases of hemorrhagic venous infarction (Figs. 6 and8) 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) andwas 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 subacutehematoma on DWI, T1WIs, and T2WIs.

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).

630 S.A. Khedr et al.

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, intravenoustPA 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 ofdeveloping symptomatic hemorrhage if treated with thrombo-

lytics, it is also possible that overall this group of patients mayreceive net benefit from therapy (19,21,22).

- We had three cases of subarachnoid hemorrhage in ourstudy, 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. 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

The ADCmeasurements in hyperacute, acute, early and latesubacute hematoma were statistically equivalent. The ADC

measurements in hyperacute, acute, early and late subacutehematoma 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 restrictionof diffusion in early stages of intracranial hematomas is uncer-

tain. Potential causes include, but are not limited to: (1) a shrink-age of extracellular space with clot retraction; (2) a change in theosmotic environment once blood becomes extravascular, which

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 (c–f). Left middle cerebral artery occlusion in MRA (g).

632 S.A. Khedr et al.

alters the shape of theRBC, a phenomenon related to the forma-

tion of the fibrin network associated with clot; (3) a conforma-tional change of the hemoglobin macromolecule within theRBC; 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, mediumand 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 onDWI 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, smallareas 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 regionsof hemorrhagic arterial and venous infarction not evident onCT. Our findings suggest that DWI was nearly as accurateas 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 andthe small number of cases. Although a complete understandingof the underlying biophysical basis may require further studies

with a large population, our data suggest that the appearanceof intracerebral hematomas on diffusion-weighted images isinfluenced 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. 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 (a–f). It appears

hyperintense in T1WIS, hypointense in T2WIs, FLAIR, DWI, ADC and GRE surrounded by brain edema.

MRI diffusion-weighted imaging in intracranial hemorrhage (ICH) 633

low diagnostic accuracy in subarachnoid and small parenchy-

mal hemorrhage.

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