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Topical Reviews

Section Editors: Larry Goldstein, MD, FAAN, FANA, FAHA, and Anne Abbott, PhD, MBBS, FRACP

Neuroimaging in Intracerebral Hemorrhage

Federica Macellari, MD; Maurizio Paciaroni, MD; Giancarlo Agnelli, MD; Valeria Caso, PhD, MD

I ntracerebral hemorrhage (ICH) is described as spontaneous

extravasation of blood into the brain parenchyma. This clinical
entity is present in 10% to 15% of all stroke cases1 in the Western
catheter angiogram and CT angiography (CTA) methods were
also analyzed and compared for their advantages in different
clinical situations. The purpose of our neuroimaging review
population, with reported incidence rates higher in Asia.24 It is of ICHs was to provide a framework for choosing a rational
also associated with a higher mortality rate compared with either diagnostic imaging plan, taking into account the clinical char-
ischemic stroke (IS) or subarachnoid hemorrhage.5 acteristics of the presenting patients. Because of the fact that
ICH is classified according to its primary (80% to 85%) a myriad of imaging modalities is available, it is important to
or secondary (15% to 20%) causes. More than 50% of pri- understand the indications and limitations of each technique
mary ICH events are directly correlated with hypertension in order to select the most appropriate study for each patient.
as a risk factor, whereas 30% are known to be associated
with cerebral amyloid angiopathy (CAA). The causes of Computed Tomography
secondary ICH include hemorrhage conversion of IS, amy- Contemporary CT, including noncontrast CT (NCCT), per-
loid angiopathy, stimulant drugs, vascular malformations fusion CT, and CTA, is generally used for hyperacute stroke
(aneurysms, arterovenous malformations, venous angioma, imaging. In fact, NCCT is commonly used in an emergency
cavernoma, dural arteriovenous fistula), coagulopathy (hered- room setting for acute stroke because of its convenience and its
itary, acquired, induced by anticoagulants or antiplatelets), high sensitivity for detecting ICH, which is a contraindication
neoplasms, trauma, vasculitis, Moyamoya disease, or sinus to thrombolytic therapy.10 Moreover, NCCT allows to quantify
venous thrombosis (Table1). hematoma volume and monitor hemorrhage evolution in ICH
Currently, ICH is classified as either primary or secondary accurately.11 That is, ICH volume can be calculated by using the
according to only causes. However, this classification does not ABC/2 method,12 derived from an approximation, according to
take into account the inherent differences of underlying vascu- the formula for ellipsoids, where A is the greatest hemorrhage
lar pathologies. Hence, a more systematic stratification based diameter; B, the diameter at 90 to A; and C, the approximate
on new criteria is currently being developed.1 Specifically, number of CT slices with hemorrhage multiplied by slice thick-
Meretoja etal6 have proposed the SMASH-U classification, nesses13 (Figure1). Nonetheless, some studies assessing the
based on the underlying diseases of ICH: Structural lesions reliability of the ABC/2 method have shown that it produces
(cavernomas and arterovenous malformations), Medication a larger percentage of error compared with other measure-
(anticoagulation), Amyloid angiopathy, Systemic diseases ment techniques, particularly for irregular-shaped objects.14
(liver cirrhosis, thrombocytopenia, and various rare conditions), In fact, comparing the ABC/2 method with the manual plani-
Hypertension, and Undetermined causes. This classification metric method, the former consistently overestimated infarct
has proven to be feasible and is also associated with survival volume by a median false increase of 7.33 cm3.15 Whereas,
prognosis.6 Another classification used in clinical practice dis- the Quantomo method for quantitative tomography has been
tinguishes between deep and lobar ICHs according to location. reported to more reliably detect smaller changes in ICH volume
Deep ICHs are located in the basal ganglia, thalamus, internal compared with the ABC/2 method. This is because Quantomo
capsule, cerebellum, or brain stem and are generally related to method measures the geometry of individual hematoma vol-
hypertension. Whereas, lobar ICHs usually require more exten- umes, whereas the ABC/2 method approximates all hema-
sive diagnostic testing because of their wider range of causes.7 toma volumes such as ellipsoid.16 To this regard, Huttner etal12
Regarding clinical outcome, ICH is commonly characterized reported an overestimation of 32.1% in hematoma volume cal-
by hematoma expansion and early neurological deterioration culations for irregular and dichotomized shapes of hematomas
within the first few hours of onset.8 Thus, rapid management among ICH patients with a history of warfarin use. Both initial
including diagnostic work-up needs to be performed. hematoma volume and hematoma growth are independent pre-
We reviewed the available neuroimaging tools for ICH, as dictors of clinical outcome and mortality.8,17 To date, though the
well as the changes in ICH in response to blood breakdown ABC/2 method is the most readily available assessment at bed-
products, seen on CT and MR at various stages (Table2).9 Both side, protocols for accurate assessment of hematoma volume

Received September 30, 2013; final revision received November 28, 2013; accepted December 3, 2013.
From the Stroke Unit and Division of Cardiovascular Medicine, University of Perugia, Perugia, Italy.
Correspondence to Valeria Caso, PhD, MD, Stroke Unit and Division of Cardiovascular Medicine, University of Perugia, Santa Maria della Misericordia
Hospital, Sant Andrea delle Fratte, 06126 Perugia, Italy. E-mail vcaso@hotmail.com
(Stroke. 2014;45:903-908.)
2014 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.113.003701

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904StrokeMarch 2014

Table 1. Intracerebral Hemorrhage (ICH) Classification the lesion area tends to shrink and become less intense, los-
According to Causes ing 1.5 Houndsfield units per day. The periphery of the lesion
tends to take on an uneven profile, which acquires a pseudoab-
Primary Causes Secondary Causes
scess (ring-like) appearance, as seen on contrast. Reductions in
Hypertension Hemorrhage conversion of ischemic stroke edema and mass effect can also occur up until the ninth week,
Cerebral amyloid angiopathy Stimulant drugs when only a confined region of modest hypodensity can be
Vascular malformation
observed on CT.23
Arteriovenous malformation Contrast-enhanced CTA is able to identify patients at high
Venous angioma risk of hemorrhage enlargement (HE), by revealing a spot
Cavernoma sign, which is a contrast medium extravasation within the
Dural arteriovenous fistula hematoma.24 Spot sign is highly predictive of HE and has been
reported to have a positive predictive value of 73%, a negative
predictive value of 84%, sensitivity of 63%, and specificity of
Iatrogenic (anticoagulants, antiplatelets) 90%.25 HE usually occurs in 30% of patients with ICH <3 hours
Neoplasms of symptom onset,26 and the frequency of spot sign is highest
Trauma in patients presenting <3 hours, but its accuracy in predicting
Vasculitis HE remains high, regardless of time from symptom onset.27
Moyamoya disease
Furthermore, spot sign is associated with poor prognosis, high
Sinus venous thrombosis
rates of early clinical deterioration, high mortality, more severe
clinical presentation, and decompression of the hemorrhage into
and its characteristics should be incorporated into the CT scan- the intraventricular space.25,2833 ICH volume 30 cm3 together
ner consoles, because this can allow the operator to obtain such with Glasgow Coma Scale score, presence of intraventricular
information accurately in a timely manner.14 CT scan is also blood, and age 80 years have been included as independent
able to determine the approximate age of hematomas, by eval- variables for 30-day mortality in the ICH score developed by
uating for the density of the lesions measured in Houndsfield Hemphill etal.34 The utility of detecting the spot sign on clinical
units, according to the value of x-ray attenuation corrected for decision making and outcome improvement remains question-
the attenuation coefficient of water. The Houndsfield units for able. So, patients with spot sign are amenable to other studies,35
water is equal to 0, blood is between 30 and 45, gray substance with the purpose of demonstrating the feasibility of CTA in
is between 37 and 45, white substance is between 20 and 30, the hyperacute phase and the reliability of spot sign in emer-
whereas bone is between 700 and 3000.18,19 At onset, hematoma gency setting for guiding the therapy with factor VII or other
is commonly seen as uniform and smooth hyperintense signals prothrombotic to avoid HE and, therefore, a worse outcome.36
on CT. Over the course of the first 48 hours, large hematomas CTAs performed <96 hours from symptom onset have a
tend to show fluid levels, indicating that they are not solidified high accuracy for predicting underlying vascular anoma-
yet.20 To this regard, fluid blood levels have been defined as a lies, with sensitivities 95% and specificities approaching
horizontal interface between hypodense bloody serum layered 100%. Positive and negative predictive values have also been
above hyperdense settled blood. Fluid blood levels in acute ICH reported to be in excess of 97%.37,38 Even so, CTA exposes
are moderately sensitive (59%) to the presence of coagulopa- patients to the risks of radiation, as well as risks associated
thy (ie, abnormal prothrombin time and partial thromboplas- with contrast-induced nephropathy (CIN) and allergic reac-
tin time) and highly specific (98%) for this condition.21 Blood/ tion, which can lead to death. Furthermore, the risk of contrast
fluid levels are also frequent in thrombolysis-related ICH and on bloodbrain barrier permeability has unknown effects on
associated with higher hemorrhage volumes.22 Over the first 72 bleeding risks and the worsening of vasogenic edema.3943
hours, a hypodense region can be detected around lesions, as a CIN is defined as a 25% elevation from baseline serum
result of the edema that surrounds the brain tissue; a noteworthy creatinine levels or an absolute increase of 0.5 mg/dL <48 to
mass effect can be detected as well. Three to 20 days after onset, 72 hours of contrast administration.44 CIN is associated with

Table 2. Appearance of Intracerebral Hemorrhage on Noncontrast CT (NCCT) and MR by Stage9

Phase of Blood NCCT T1-Weighted MR T2-Weighted MR T2*-Weighted MR
Hyperacute Oxyhemoglobin Smooth, hyperdense Hypointense or isointense Hyperintense Marked hypointensity
Acute (1248 h) Deoxyhemoglobin Hyperdense with fluid levels Isointensity or slight hypointensity Hypointense with Marked hypointensity
with thin hyperintense rim in the hyperintense
periphery perilesional rim
Early subacute Methemoglobin Hypodense region of edema Hyperintensity Hypointensity Hypointensity
(72 h) intracellular with mass effect
Late subacute Methemoglobin Less intense with ring-like Hyperintensity Hyperintensity Hypointensity
(320 d) extracellular profile
Chronic (9 wk) Hemosiderin and Isodense or modest Hypointensity Hypointensity Hyperintense or isointense core
ferritin confined hypodensity surrounded by hypointense rim

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Macellari etal Neuroimaging in ICH 905

regions and evidence whether blood is within the larger isch-

emic infarct.59 A primary hematoma tends to be round and
have a larger surrounding edema than would be seen on IS.
Furthermore, hematomas do not necessarily respect vascular
territories.59 In case of hemorrhagic transformation of IS, MR
angiography can identify the location of vascular occlusion.
MR has a high diagnostic rate for detecting underlying
causes of secondary hemorrhages, including vascular mal-
formations, tumors, and cerebral vein thrombosis, as well as
a high diagnostic yield for young patients having lobar ICH
and no history of hypertension.60 Thus, MR is the most sen-
Figure 1. Intracerebral hemorrhage evidenced on CT (ABC/2 sitive tool for detecting cerebral venous thrombosis in the
formula by CT).
acute, subacute, and chronic phases.61 Contrast-enhanced MR
venography is able to show the thrombosed segment of the
5-fold higher risks of prolonged hospitalization and mortal- venous sinus and is generally well correlated with conven-
ity.4547 In an emergency setting, it is neither feasible to adopt tional angiographic findings.62 It also assists in distinguishing
preventive measures such as prehydration with the addition anatomic variants, such as a hypoplastic sinus, from cerebral
of acetylcysteine48nor possible to fully know patient history. venous thrombosis.63
However, the incidence of CIN, even in emergency settings, MR is the most sensitive and specific neuroradiologic
has been reported to be low (2%).49 modality for detecting cavernomas, the abnormal capillary-like
vessels with intermingled connective tissue whose rupture
Magnetic Resonance can lead to ICH.64 Cavernoma has a hyperintense popcorn
Stroke MR protocols should include T1, T2, T2* or gradient echo balllike appearance at T2-weighted imaging. The central
(GE), fluid-attenuated inversion recovery, contrast-enhanced, component, hyperintense, indicates subrecent bleeding; the
diffusion-weighted, and p erfusion-weighted images, as well hypointense halo consists of hemosiderin and is the outcome
as MR angiography.50 The appearance of ICH on MR is pri- of remote bleeding.
marily affected by the age of hematoma, as well as the type With MR, it is possible to detect previously existing and
of MR contrast used. The substrate responsible for early clinically silent cerebral MBs that are not detectable on CT.
hemorrhage identification on MR scan is deoxyhemoglobin, MBs provide a lifetime history of hemorrhage. MBs are small
a blood degradation product with paramagnetic properties, dot-like lesions having a hypointense appearance on GE
because of its unpaired electrons. On GE images, a few areas sequences and are usually smaller than 5 to 10 mm (Figure2).
of hyperintensity can be detected in the lesion core, and of Pathological studies have proven that MBs correspond to
these, most are usually surrounded by hypointense bound- hemosiderin-laden macrophages adjacent to small vessels,
aries. Hyperintense signals are commonly found bordering suggesting previous extravasations of blood. MBs can have
the central lesion on T2-weighted and GE images, whereas numerous types of mimics, such as the calcification of the
a hypointense signal is commonly observed on T1-weighted basal ganglia, diffused axonal injury, metastatic melanoma,
images, thereby indicating perifocal vasogenic edema.50 cavernous malformation, and small perforating arteries.65
There is strong evidence supporting the diagnostic accuracy MBs are considered markers of vascular pathology, includ-
of MR in the hyperacute setting51,52 even after only 20 min- ing hypertensive vasculopathy and CAA, as identified from
utes of symptom onset.53 A randomized trial investigating the histopathologic analyses of the vessels surrounding MBs.
role of MR in detecting ICH54 has reported that hyperacute Furthermore, MBs have been reported to be predictors of
ICH is detectable with excellent accuracy even when the rat- ICH in prospective observational studies on both ICH66,67 and
ers had only limited experience. Moreover, GE is as sensitive IS.68,69 MBs can indicate bleeding-prone angiopathy and a high
as NCCT in the detection of acute ICH, whereas a complete rate of hemorrhagic transformation in patients on anticoagu-
MR in patients with acute stroke has higher sensitivities for IS lation, antithrombotic, or thrombolytic therapies.70 However,
(diffusion-weighted imaging sequences) and chronic hemor-
rhage.55,56 However, in the case of minor bleeding, GE MR
may not be sufficient to distinguish acute bleeding from
chronic bleeding (ie, microbleeds [MBs]), and for this, NCCT
should be performed.56 Furthermore, patient factors (ie, clini-
cal instability, presence of pacemaker, claustrophobia) and
hospital factors (availability of MR) may cause obtaining an
MR impossible or impractical in the acute setting, and there-
fore, NCCT remains the neuroimaging modality of choice for
the diagnosis of acute stroke.57,58
MR is also a neuroradiological tool for distinguishing
between hemorrhagic transformation and primary ICH.
In fact, most HTs are smaller than their fields of ischemic Figure 2. Intracerebral hemorrhage evidenced on gradient echo
infarct; thus, MR can provide information on nonhemorrhagic MR in patients with deep microbleeds (black arrows).

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906StrokeMarch 2014

MBs are thought to be more than markers for minor episodes MR angiogram/venogram along with CT angiogram/veno-
of cerebrovascular extravasation. In fact, a recent pathologi- gram are reliable tools for confirming secondary causes of
cal study by Janaway etal71 has reported that a large putamen hemorrhage. Thus, these are reliable substitutes for catheter
haemosiderin, correlated with more MBs, was significantly angiogram, which is an invasive procedure that is not always
associated with putaminal indices of small-vessel ischemia readily available. In fact, catheter angiogram is associated
(microinfarcts, arteriolosclerosis, perivascular attenuation), with the risks of transient and permanent neurological deficits,
as well as lacunes in each examined brain region but neither 0.9% and 0.5%, respectively.79 It is expensive and time- and
with large-vessel disease nor whole-brain neurodegenerative labor-intensive, as well as requires patient cooperation, a sta-
pathologies. These findings suggest that basal ganglia MR ble patient condition, and continuous monitoring. Radiation
MBs are a surrogate for ischemic small-vessel disease rather doses of catheter angiography (5 times higher than CTA)80 are
than exclusively a hemorrhagic diathesis. delivered to both patients and operators. For this reason, CTA
Lobar localization of MBs and their associations with lobar should be considered the better initial screening approach for
ICH, especially in the elderly patients, render MBs possible identifying secondary vascular lesions, compared with cathe-
indicators of CAA. To this regard, the Boston criteria for prob- ter angiogram.81 Nonetheless, catheter angiogram remains the
able CAA specify that this diagnosis should not be made when diagnostic tool of choice for the treatment of aneurysms and
MBs are located in the basal ganglia, thalamus, or brain stem, arteriovenous malformation (Figure3).
the regions atypical for CAA pathology.72

Catheter Angiogram
Subarachnoid hemorrhage, atypical (noncircular) hematoma
configuration, edema out of proportion seen on CT at admis-
sion, unusual hemorrhage location, or the presence of other
abnormal structures in the brain, including masses, are all dis-
tinctive radiological features of secondary causes of ICH.10 In
these cases, a catheter angiogram is necessary to best reveal
underlying conditions, including arteriovenous malforma-
tions, Moyamoya disease, tumors, vasculitis, reversible cere-
bral vasoconstriction syndrome, and cerebral vein thromboses.
Angiography may also be indicated in patients with no
obvious cause of bleeding. The angiographic yield has shown
to be significantly high in young patients without pre-existing
hypertension.73 Young age followed by the absence of hyper-
tension and lobar hemorrhage have been proven to be the main
factors influencing diagnostic choices in clinical practice.74
The presence of intraventricular hemorrhage in patients with
acute spontaneous ICH is not associated with an increased risk
of an underlying vascular lesion and should not be used to
select patients for neurovascular evaluation.75 Timing of cere-
bral angiography should take into consideration the clinical
state of the patient and the neurosurgeons judgment regarding
urgency of surgery.76 There is a tendency to perform diagnos-
tic investigations <1 or 2 days in younger patients.74 Delayed
angiography can also show unexpected underlying structural
lesions in patients without radiological suspicion of second-
ary causes of ICH,77 and therefore, a follow-up angiography
should be considered for all patients with a first-negative
angiogram, in the absence of a specific cause of hemorrhage.78

Figure 3. Catheter angiogram: Left temporal arteriovenous mal- Figure 4. Diagnostic work-up flowchart of intracerebral
formation before and after treatment (black arrows). hemorrhage.

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Macellari etal Neuroimaging in ICH 907

Conclusions 14. Divani AA, Majidi S, Luo X, Souslian FG, Zhang J, Abosch A, etal.
The ABCs of accurate volumetric measurement of cerebral hematoma.
An optimal neuroradiological diagnosis and management Stroke. 2011;42:15691574.
of ICH requires more than defining the size, location, and 15. Pedraza S, Puig J, Blasco G, Daunis-I-Estadella J, Boada I, Bardera A,
presence of intraventricular blood. In fact, knowing the etal. Reliability of the ABC/2 method in determining acute infarct vol-
ume. JNeuroimaging. 2012;22:155159.
causes of ICH will allow us to better diagnose and treat ICH.
16. Kosior JC, Idris S, Dowlatshahi D, Alzawahmah M, Eesa M, Sharma
Specifically, the pathogenesis provides more accurate infor- P, etal; PREDICT/Sunnybrook CTA ICH Study Investigators.
mation on predictive factors that can influence the clinical out- Quantomo: validation of a computer-assisted methodology for the
come and mortality: risk of hematoma expansion, presence of volumetric analysis of intracerebral haemorrhage. IntJ Stroke. 2011;
underlying diseases, and previous lesions such as MBs. 17. Broderick JP, Brott TG, Duldner JE, Tomsick T, Huster G. Volume of
Here, we propose a diagnostic flowchart that incorporates intracerebral hemorrhage. A powerful and easy-to-use predictor of
size, location, clinical risk factors, and pathogenesis that, when 30-day mortality. Stroke. 1993;24:987993.
considered together, can lead to a more accurate diagnosis 18. Feeman TG. TheMathematics of Medical Imaging: A Beginners Guide.
New York: Springer; 2010.
and, thus, a better management of ICH (Figure4). Regarding 19. Mosby. Mosbys Medical Dictionary. 9th ed. Elsevier; 2009.
those who may do without further imaging w ork-up, this deci- 20. Zilkha A. Intraparenchymal fluid-blood level: a CT sign of recent intra-
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Disclosures analysis of 244 cases from the GUSTO-1 trial with clinical correlation.
Dr Caso received honoraria as a member of the speaker bureau and Global Utilization of Streptokinase and Tissue Plasminogen Activator
advisory board of Boehringer Ingelheim. The other authors have no for Occluded Coronary Arteries. Stroke. 1998;29:563569.
conflicts to report. 23. Herold S, von Kummer R, Jaeger C. Follow-up of spontaneous
intracerebral haemorrhage by computed tomography. JNeurol.
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Neuroimaging in Intracerebral Hemorrhage
Federica Macellari, Maurizio Paciaroni, Giancarlo Agnelli and Valeria Caso

Stroke. 2014;45:903-908; originally published online January 14, 2014;

doi: 10.1161/STROKEAHA.113.003701
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