chapter 2 use of i maging in er cebrovascular d …...cerebral venous thrombosis (cvt) is an...

16
CHAPTER 2 Use of imaging in cerebrovascular disease P. Irimia, 1 S. Asenbaum, 2 M. Brainin, 3 H. Chabriat, 4 E. Martínez-Vila, 1 K. Niederkorn, 5 P. D. Schellinger, 6 R. J. Seitz, 7 J. C. Masdeu 1 1 University of Navarra, Pamplona, Spain; 2 Medical University of Vienna, Austria; 3 Donauklinikum and Donau-Universität, Maria Gugging, Austria; 4 Lariboisiere Hospital, University of Paris, France; 5 Karl Franzens University, Graz, Austria; 6 University Clinic at Erlangen, Germany; 7 University Hospital Düsseldorf, Germany neuroimaging techniques available for the evaluation of stroke patients has increased the complexity of decision making for physicians. Neurologists, who have been educated to manage acute stroke patients, should be trained in the use of neuroimaging, which allows for the development of a pathophysiologically oriented treatment. Successful care of acute stroke patients requires a rapid and accurate diagnosis because the time window for treatment is narrow. In the case of intravenous throm- bolysis for ischaemic stroke, the treatment is safer and more effective the earlier it is given [3]. Current recom- mendations call for a 4.5-h time limit for intravenous thrombolysis [4] that can be extended to 6 h for intra- arterial thrombolysis [5]. Thus, the neuroimaging proto- col designed to determine the cause of stroke should delay treatment as little as possible. Neuroimaging can provide information about the presence of ischaemic but still viable and thus salvageable tissue (penumbra tissue) and vessel occlusion in the hyperacute phase of ischemic stroke. This information is critical for an improved selec- tion of patients who could be treated with intravenous thrombolysis up to the 4.5-h limit and beyond [5]. Thus, neuroimaging criteria have been used for patient selec- tion and outcome in different trials, using thrombolysis beyond 3 h after stroke onset [6, 7]. Determining stroke type using neuroimaging goes well beyond separating ischaemic from haemorrhagic stroke. For instance, the depiction of multiple cortical infarcts may lead to a fuller work-up for cardiogenic emboli [8, 9]. In arterial dissec- tion, the characteristic semilunar high-intensity signal in the vessel wall on high-resolution T1-weighted magnetic resonance imaging (MRI) alerts to the presence of this cause of stroke [10]. 19 Objectives The objective of the task force is to actualize the EFNS Guideline on the use of neuroimaging for the manage- ment of acute stroke published in 2006. The Guideline is based on published scientific evidence as well as the con- sensus of experts. The resulting report is intended to provide updated and evidence-based recommendations regarding the use of diagnostic neuroimaging techniques, including cerebrovascular ultrasonography (US), in patients with stroke and thus guide neurologists, other healthcare professionals, and healthcare providers in clinical decision making and in the elaboration of clinical protocols. It is not intended to have legally binding implications in individual situations. Background Stroke is the second most common cause of death world- wide, and one of the major determining factors of hos- pital admission and permanent disability in the developed countries [1]. The proportion of the population over the age of 65 years is growing and this trend is likely to increase stroke incidence in the next decades [2]. Major advances in the understanding of the mechanisms of stroke and its management have been made thanks to the substantial progress in neuroimaging techniques. However, the multiplicity and continuous advances of European Handbook of Neurological Management: Volume 1, 2nd Edition Edited by N. E. Gilhus, M. P. Barnes and M. Brainin © 2011 Blackwell Publishing Ltd. ISBN: 978-1-405-18533-2

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Page 1: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

CHAPTER 2

Use of i maging in c erebrovascular d isease P. Irimia, 1 S. Asenbaum, 2 M. Brainin, 3 H. Chabriat, 4 E. Mart í nez - Vila, 1 K. Niederkorn, 5 P. D. Schellinger, 6 R. J. Seitz, 7 J. C. Masdeu 1 1 University of Navarra, Pamplona, Spain ; 2 Medical University of Vienna, Austria ; 3 Donauklinikum and Donau - Universit ä t, Maria Gugging, Austria ; 4 Lariboisiere Hospital, University of Paris, France ; 5 Karl Franzens University, Graz, Austria ; 6 University Clinic at Erlangen, Germany ; 7 University Hospital D ü sseldorf, Germany

neuroimaging techniques available for the evaluation

of stroke patients has increased the complexity of

decision making for physicians. Neurologists, who have

been educated to manage acute stroke patients, should

be trained in the use of neuroimaging, which allows

for the development of a pathophysiologically oriented

treatment.

Successful care of acute stroke patients requires a rapid

and accurate diagnosis because the time window for

treatment is narrow. In the case of intravenous throm-

bolysis for ischaemic stroke, the treatment is safer and

more effective the earlier it is given [3] . Current recom-

mendations call for a 4.5 - h time limit for intravenous

thrombolysis [4] that can be extended to 6 h for intra -

arterial thrombolysis [5] . Thus, the neuroimaging proto-

col designed to determine the cause of stroke should

delay treatment as little as possible. Neuroimaging can

provide information about the presence of ischaemic but

still viable and thus salvageable tissue (penumbra tissue)

and vessel occlusion in the hyperacute phase of ischemic

stroke. This information is critical for an improved selec-

tion of patients who could be treated with intravenous

thrombolysis up to the 4.5 - h limit and beyond [5] . Thus,

neuroimaging criteria have been used for patient selec-

tion and outcome in different trials, using thrombolysis

beyond 3 h after stroke onset [6, 7] . Determining stroke

type using neuroimaging goes well beyond separating

ischaemic from haemorrhagic stroke. For instance, the

depiction of multiple cortical infarcts may lead to a fuller

work - up for cardiogenic emboli [8, 9] . In arterial dissec-

tion, the characteristic semilunar high - intensity signal in

the vessel wall on high - resolution T1 - weighted magnetic

resonance imaging (MRI) alerts to the presence of this

cause of stroke [10] .

19

Objectives

The objective of the task force is to actualize the EFNS

Guideline on the use of neuroimaging for the manage-

ment of acute stroke published in 2006. The Guideline is

based on published scientifi c evidence as well as the con-

sensus of experts. The resulting report is intended to

provide updated and evidence - based recommendations

regarding the use of diagnostic neuroimaging techniques,

including cerebrovascular ultrasonography (US), in

patients with stroke and thus guide neurologists, other

healthcare professionals, and healthcare providers in

clinical decision making and in the elaboration of clinical

protocols. It is not intended to have legally binding

implications in individual situations.

Background

Stroke is the second most common cause of death world-

wide, and one of the major determining factors of hos-

pital admission and permanent disability in the developed

countries [1] . The proportion of the population over the

age of 65 years is growing and this trend is likely to

increase stroke incidence in the next decades [2] . Major

advances in the understanding of the mechanisms of

stroke and its management have been made thanks to

the substantial progress in neuroimaging techniques.

However, the multiplicity and continuous advances of

European Handbook of Neurological Management: Volume 1, 2nd Edition

Edited by N. E. Gilhus, M. P. Barnes and M. Brainin

© 2011 Blackwell Publishing Ltd. ISBN: 978-1-405-18533-2

Page 2: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

20 SECTION 1 Investigations

Search s trategy

The Cochrane Library was consulted and no studies were

found regarding the use of neuroimaging techniques in

stroke. A comprehensive literature review using the

MEDLINE database has been conducted by searching for

the period 1965 – 2009. Relevant literature in English,

including existing guidelines, meta - analyses, systematic

reviews, randomized controlled trials, and observational

studies have been critically assessed. Selected articles have

been rated based on the quality of study design, and clini-

cal practice recommendations have been developed and

stratifi ed to refl ect the quality and the content of the

evidence according to EFNS criteria [11] .

Method for r eaching c onsensus

The author panel critically assessed the topic through

analysis of the medical literature. A draft guideline with

specifi c recommendations was circulated to all panel

members. Each panellist studied and commented in

writing on this draft, which was revised to progressively

accommodate the panel consensus. After the approval of

the panellists, two independent experts gave their opinion

on the fi nal version.

Results

Imaging of the b rain The primary objectives of brain imaging in acute stroke

are to exclude a non - vascular lesion as the cause of the

symptoms and to determine whether the stroke is caused

by an ischaemic infarction or a haemorrhage. It is not

possible to exclude stroke mimics, such as a neoplasm,

and distinguish between ischaemic and haemorrhagic

stroke based exclusively on the history and physical

examination [12] . Determining the nature of the lesion

by brain imaging is necessary before starting any treat-

ment, particularly thrombolysis and antithrombotic

drugs (Class I, Level A).

Secondary objectives of brain imaging are to facilitate

the identifi cation of stroke mechanisms, to detect sal-

vageable tissue, and to improve the selection of patients

who could be candidates for reperfusion therapies.

Computed t omography ( CT ) Conventional CT of the head is the examination most

frequently used for the emergent evaluation of patients

with acute stroke because of its wide availability and use-

fulness (Class II, Level B). It has been utilized as a screen-

ing tool in most of the major therapeutic trials conducted

to date [3] . It is useful to distinguish between ischaemic

stroke and intracerebral or subarachnoid haemorrhage

(SAH), and can also rule out other conditions that could

mimic stroke, such as brain tumours. Signs of early isch-

emia may be identifi ed as early as 2 hrs from stroke onset,

although they may appear much later [13] . Early infarct

signs include the hyperdense middle cerebral artery

(MCA) sign [14, 15] (indicative of a thrombus or embolus

in the M1 segment of the vessel), the MCA dot sign [16,

17] (indicating thrombosis of M2 or M3 MCA branches),

the loss of grey - white differentiation in the cortical

ribbon [18] or the lentiform nucleus [19] , and sulcal

effacement [20] . The presence of some of these signs has

been associated with poor outcome [20 – 22] . In the Euro-

pean Cooperative Acute Stroke Study (ECASS) I trial

those patients with signs of early infarction involving

more than one - third of the territory of the MCA had an

increased risk of haemorrhagic transformation following

treatment with thrombolysis [23] . A secondary analysis

of other thrombolytic trials with a 6 - h time window

(ECASS II and Multicentre Acute Stroke Trial – Europe

(MAST - E)) demonstrated that the presence of early CT

changes was a risk factor for intracerebral haemorrhage

(ICH) [24, 25] , and similar results have been observed in

larger series of patients [26] . However, in the National

Institute of Neurological Disease and Stroke (NINDS)

trial and the Australian Streptokinase Trial there was no

relation between intracranial haemorrhage and early CT

changes [27, 28] , and it has been argued that the poorer

outcome in patients with CT changes may have more to

do with delayed treatment than with the changes them-

selves, with additional damage of the potentially salvage-

able tissue in the larger, CT - visible infarcts [29] . Because

ischaemic changes are diffi cult to detect for clinicians

without an adequate training in reading CT [30, 31] ,

scoring systems have been developed to quantify early CT

changes, such as the Alberta Stroke Programme Early CT

Score (ASPECTS). More extensive early changes using

ASPECTS correlate with high rates of intracranial haem-

orrhage and poor outcome at long term. Therefore, its

use could improve the identifi cation of ischaemic stroke

Page 3: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

CHAPTER 2 Imaging in cerebrovascular disease 21

patients who would particularly benefi t from thromboly-

sis and those at risk of symptomatic haemorrhage [32,

33] . However, given the confl icting evidence, the pres-

ence of decreased attenuation on early CT, even affecting

more than one - third of the MCA territory, cannot be

construed as an absolute contraindication for the use of

thrombolytic therapy in the fi rst 3 h after stroke (Class

IV, Good Clinical Practice Point (GCPP)).

Conventional CT contrast enhancement is not indi-

cated for the acute diagnosis of stroke, and seldom may

be helpful to show the infarcted area in the subacute stage

(2 – 3 weeks after stroke onset) when there may be obscu-

ration of the infarction by the ‘ fogging effect ’ [34, 35]

(Class IV, Level C).

Computed tomography shows acute ICHs larger than

5 mm in diameter as areas of increased attenuation. Not

depicted by CT are petechial haemorrhages and bleedings

in patients with very low haemoglobin levels [36] ,

because the high density of blood on CT is a function of

haemoglobin concentration. CT demonstrates the size

and topography of the haemorrhage and gives informa-

tion about the presence of mass effect, hydrocephalus,

and intraventricular extension of the bleeding. In addi-

tion, it may identify (although not as well as MRI) pos-

sible structural abnormalities (aneurysms, arteriovenous

malformations, or tumours) that caused the haemor-

rhage. The characteristic hyperdensity of ICH on CT

disappears with time, becoming hypodense after approx-

imately 8 – 10 days [37, 38] . For this reason, CT is not a

useful technique to distinguish between old haemorrhage

and infarction. With newer CT helical units, SAH can be

detected in 98 – 100% of patients in the fi rst 12 h from the

onset of symptoms [39, 40] and in 93% of patients

studied within the fi rst 24 h [41, 42] .

CT is the imaging procedure of choice to diagnose

SAH (Class I, Level A). Some experts recommend per-

forming the study with thin cuts (3 mm in thickness)

through the base of the brain, because small collections

of blood may be missed with thicker cuts [39, 43] (Class

IV, GCPP). CT cannot identify SAH in patients with low

haemoglobin levels, because blood may appear isodense,

and in those scanned after 3 weeks of the bleeding, when

blood has usually been metabolized [44] . Lumbar punc-

ture with CSF analysis should be performed when CT

scan is negative or doubtful [45] .

Cerebral venous thrombosis (CVT) is an uncommon

cause of stroke [46, 47] . CT can show direct signs of

venous thrombosis and other indirect non - specifi c signs,

but in about one - third of cases CT is normal [48, 49] .

Direct signs on unenhanced CT are the cord sign, cor-

responding to thrombosed cortical veins, and the dense

triangle sign, corresponding to a thrombus in the supe-

rior sagittal sinus, and, on enhanced CT of the sagittal

sinus, the delta sign [50] . Indirect signs such as local

hypodensities caused by oedema or infarction, hyperden-

sities secondary to haemorrhagic infarction, or brain

swelling and small ventricles suggest the diagnosis of

CVT. CT venography has emerged as a good procedure

to detect CVT [51 – 53] (Class III, Level C).

Perfusion - CT (PCT) techniques, despite being less

sensitive than diffusion - weighted (DWI) MRI can show

the area of ischaemia [54, 55] . Also, may it help distin-

guish between reversible (ischaemic penumbra) and irre-

versible (infarction) areas of ischaemia with standardized

methodology [56 – 58] . Different preliminary studies

comparing PCT with MRI have shown comparable

results to depict penumbra tissue [59 – 62] . There is only

one study to date (in which the primary end point was

negative) demonstrating that perfusion CT may be used

for the selection of candidates to thrombolytic therapy

beyond the 3 - h window [63] . Pregnancy, diabetes, renal

failure, and allergy to contrast material are relative con-

traindications to performing a perfusion brain CT. Per-

fusion CT may be useful to characterize the presence of

marginally perfused tissue (Class II, Level B).

Magnetic r esonance i maging ( MRI ) Magnetic resonance imaging has a higher sensitivity than

conventional CT and results in lower inter - rater vari-

ability in the diagnosis of ischaemic stroke within the fi rst

hours of stroke onset [64 – 69] (Class I, Level A). MRI is

particularly useful to show lesions in the brain stem or

cerebellum, identify lacunar infarcts, and document

vessel occlusion and brain oedema [65, 66, 68] (Class I,

Level A).

In addition, MRI techniques can provide information

about tissue viability. DWI and perfusion (PI) MRI

studies may inform about the presence of reversibly

and irreversibly damaged ischaemic tissues in the hyper-

acute phase of stroke [70 – 78] (Class II, Level B). DWI

may demonstrate deeply ischaemic or infarcted brain

tissue within minutes of symptom onset [77] . However,

areas of abnormal DWI signal are not always infarcted

and the fi nding may disappear spontaneously or after

Page 4: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

22 SECTION 1 Investigations

thrombolysis [79 – 81] . PI requires the intravenous

administration of gadolinium and provides information

about brain tissue perfusion at a given time. Different

perfusion parameters give different perfusion lesion

volumes in the same patient [82, 83] . The absolute

volume difference or ratio of the PI area and the DWI

area (diffusion – perfusion mismatch) is a useful method

to estimate the presence of ischaemic penumbra tissue

[84] . Not only the volume of abnormally perfused tissue

but also the degree of perfusion drop predict the extent

of ischaemic brain damage [85] . PI/DWI mismatch has

been evaluated in several studies as a selection tool for

thrombolytic therapy beyond 3 h [86 – 89] and in a phase

II trial it was used as a selection tool and surrogate

parameter for thrombolysis within 3 – 9 h [63] . A proposal

for the standardization of perfusion and penumbral

imaging techniques has been published [56]

Some neuroimaging fi ndings on MRI, such as the

presence of leukoaraiosis [90] and large DWI lesions

[91] , are associated with an increased risk for symptom-

atic intracerebral haemorrhage associated with thrombo-

lytic treatment.

MRI may be useful to predict which patients will

develop massive swelling with an MCA infarct. The mea-

surement of infarct volume on DWI allows the predic-

tion of malignant infarction [92, 93] , and may be helpful

for early management of these patients [94, 95] .

MRI can help identify occluded intracranial arteries

by the loss of the normal intravascular fl ow voids [65] .

Some sequences, such as T2 * - weighted MRI or fl uid -

attenuated inversion recovery (FLAIR; hyperintense

artery sign), may demonstrate acute MCA thromboem-

bolism with a higher sensitivity than CT, but the type of

arterial change on MRI does not predict recanalization,

clinical outcome, or ICH after intravenous thrombolysis

[96, 97] .

Intracranial haemorrhage is easily detectable on MRI

using T2 * - weighted images [98 – 100] . MRI can identify

intraparenchymal haemorrhage within the fi rst 6 h after

symptom onset as accurately as CT [100, 101] (Class I,

Level A). Susceptibility - weighted T2 * sequences (gradi-

ent echo) can also detect clinically silent parenchymal

microbleeds, not visible on CT, which may leave enough

local haemosiderin to remain detectable for months or

years after the bleeding. Microbleeds are associated with

a history of ICH and prospectively have been shown to

pose a 3% risk of ICH [102] . Although some retrospec-

tive studies reported an increased risk of symptomatic

haemorrhage after thrombolysis [103, 104] , this risk was

not found in more recent studies [82, 105, 106] . The risk

of bleeding after thrombolysis in patients with micro-

bleeds is small [106] and their presence is not a contra-

indication to the use of thrombolytic therapy in the fi rst

3 h after stroke (Class III, Level C).

MRI is also useful to date the haemorrhagic event

accurately and to detect lesions (as tumours, vascular

malformations, or aneurysms) that may underlie the

ICH [107] . To detect these lesions, repeated studies may

be needed after some of the swelling and vasospasm have

subsided.

Subarachnoid haemorrhage (SAH) can be detected

using T2 * [108] and FLAIR [109, 110] MR sequences, but

at present CT remains the imaging method of choice for

this diagnosis (Class I, Level A).

Arterial dissection is a leading cause of stroke in young

persons [47] . MRI is the initial procedure of choice [66,

68, 111, 112] , replacing conventional angiography as the

gold standard (Class II, Level B), because MRI can show

the mural haematoma of the dissected vessel on the axial

images [112] (high signal in the wall). Visualization of

these changes in the vertebral artery is more diffi cult than

for the larger carotid artery, making diagnosis of verte-

bral dissection less reliable. The study can be completed

with magnetic resonance angiography (MRA) to visual-

ize occlusion of the artery, pseudoaneurysms, or a long

stenotic segment with tapered ends [113, 114] . Other

techniques, including US [115 – 117] or CT angiography

[113, 114, 118, 119] , may be useful for the non - invasive

diagnosis of arterial dissection.

MRI combined with MRA is the method of choice for

the diagnosis and follow - up of CVT [49, 120 – 123] . MRI

is more sensitive than CT to show parechymal abnor-

malities and the presence of thrombosed veins.

In summary, MRI is very helpful in the clinical setting

for the management of acute stroke and to guide deci-

sions regarding thrombolysis (Class I, Level A). It is par-

ticularly helpful for the study of stroke patients for whom

perfusion CT may be dangerous, such as those with renal

failure or diabetes. However, MRI in the acute phase of

stroke is not widely available at European hospitals [124] .

Other limitations and contraindications for the use of

MRI are: claustrophobia, agitation, morbid obesity, the

presence of intracranial ferromagnetic elements, an

aneurysm recently clipped or coiled, otic or cochlear

Page 5: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

CHAPTER 2 Imaging in cerebrovascular disease 23

implants, some old prosthetic heart valves, pacemakers,

and some, not all, neurostimulators.

SPECT and PET Single photon emission computed tomography (SPECT)

and positron emission tomography (PET) are functional

neuroimaging techniques based on the principles of

tracer technology using radiolabelled substances as sys-

temically administered tracers. In the setting of stroke,

SPECT has been used for the evaluation of cerebral perfu-

sion. Earlier perfusion SPECT studies failed to show any

advantage of SPECT over the structured clinical evalua-

tion (NIH, Canadian, Scandinavian stroke scales) in the

prediction of the evolution of acute stroke [125] .

However, using ethyl cysteinate dimer (ECD) SPECT in

the fi rst 6 h after stroke, Barthel et al. [126] were able to

determine which patients would develop massive MCA -

territory necrosis, with hemispheric herniation. These

patients have a high risk of haemorrhage following

thrombolysis and could potentially be helped by early

decompressive hemicraniectomy [127] . Complete MCA

infarctions were predicted with signifi cantly higher accu-

racy with early SPECT compared with early CT and clini-

cal parameters. The predictive value increased when the

fi ndings on CT, clinical examination, and SPECT were

considered [126] . Other studies have found SPECT to

add predictive value to the clinical score on admission

[128 – 130] . Those studies suggest that a patient with a

normal SPECT study performed within 3 h of stroke

onset will most likely recover spontaneously and there-

fore may not benefi t from thrombolysis. A patient with

a dense defi cit in the entire MCA distribution has a high

risk of haemorrhage with thrombolysis, and, depending

on age and other factors, should be considered for

decompressive hemicraniectomy. The patients most

likely to benefi t from thrombolysis are the ones with less

massive lesions [126, 128] . Thus, SPECT is helpful in the

evaluation of acute stroke (Class III, Level C). Unfortu-

nately, the need to perform either CT or MRI in acute

stroke renders the performance of SPECT diffi cult within

the time frame allotted for the evaluation of these patients.

SPECT is also helpful in the evaluation of cerebral perfu-

sion in non - acute cerebrovascular disease, for instance in

the days after a SAH [131] (Class III, Level C).

PET can be used to evaluate a large variety of physio-

logical variables including cerebral blood fl ow, cerebral

blood volume, and cerebral glucose metabolism, as well

as the density of neurotransmitters and neuroreceptors,

such as benzodiazepine receptors with fl umazenil, an

accurate marker of neuronal loss [132] . As PET has been

considered the gold standard for these kinds of measure-

ments in humans, it is also extremely well suited to help

identify the degree of ischaemic damage in the brain.

Heiss et al. compared 15 O - water PET and MRI in patients

with acute ischaemic stroke. They observed that DW/

PW – MRI mismatch overestimates the penumbra defi ned

by PET [133] . Although PET is the reference method for

quantitative perfusion imaging, it does not allow for the

reliable identifi cation of lesions in the vessels or non -

vascular lesions giving rise to the stroke syndrome. This,

coupled with the cost and current lack of availability of

this technique, renders it less useful than MRI and CT for

most practising neurologists.

Imaging of the e xtracranial v essels Imaging of the extracranial and intracranial vessels will

help identify the underlying mechanism of the stroke

(atherothrombotic, embolic, dissection, or other). Non -

invasive imaging methods are increasingly accepted as

replacements of digital substraction angiography (DSA)

in the evaluation of carotid stenosis prior to endarterec-

tomy [134] (Class IV, GCPP). US, comprising Doppler

sonography and colour - coded duplex sonography, is

probably the most common non - invasive imaging

examination performed to aid in the diagnosis of carotid

disease. The peak systolic velocity and the presence of

plaque on greyscale and/or colour Doppler/Duplex US

images are the main parameters that should be used

when diagnosing and grading internal carotid artery

(ICA) stenosis [135] . The examination may be limited

by the presence of extensive plaque calcifi cations, vessel

tortuosity and in patients with tandem lesions. In addi-

tion, Doppler US is both technician - and equipment -

dependent and all sonographers should be able to

demonstrate that they have validated their testing

procedures. Meta - analyses of published criteria for

US have demonstrated sensitivities of 98% and specifi ci-

ties of 88% for detecting > 50% ICA stenosis; and

94% and 90% respectively for detecting > 70% ICA

stenosis [136] .

Magnetic resonance angiography using time - of -

fl ight angiography (TOF) and contrast - enhanced MRA

(CEMRA) are powerful means to assess vascular pathol-

ogy. Either technique provides specifi c information:

Page 6: CHAPTER 2 Use of i maging in er cebrovascular d …...Cerebral venous thrombosis (CVT) is an uncommon cause of stroke [46, 47] . CT can show direct signs of venous thrombosis and other

24 SECTION 1 Investigations

while TOF visualizes changes of fl ow in the arteries or

veins depending on imaging parameters, CEMRA visual-

izes the vascular lumen. MRA and US have yielded com-

parable fi ndings. Two meta - analyses [137, 138] and

several reviews [139, 140] have compared the diagnostic

value of Doppler US, MRA, and conventional DSA for

the diagnosis of carotid artery stenosis. The meta - analysis

published by Blakeley et al. [137] in 1995 concluded

that Doppler US and MRA had similar diagnostic per-

formance in predicting carotid artery occlusion and

> 70% stenosis. In the systematic review performed by

Nederkoorn et al. [139] for the diagnosis of 70 – 99%

stenosis, MRA had a pooled sensitivity of 95% and a

pooled specifi city of 90%, and US 86% and 87% respec-

tively. For recognising occlusion, MRA had a sensitivity

of 98% and a specifi city of 100%, and DUS had a sensitiv-

ity of 96% and a specifi city of 100%. A meta - analysis

comparing the accuracy of TOF or CEMRA for the detec-

tion of ICA disease against intra - arterial angiography

showed that CEMRA is slightly more precise than TOF

for the detection of ICA high - grade ( ≥ 70 to 99%) stenosis

and occlusion, and appears to achieve a higher sensitivity

for the detection of moderate (50 – 69%) stenosis [141] .

Computed tomography angiography, a contrast - depen-

dent technique, has been compared with DSA for the

detection and quantifi cation of carotid stenosis and

occlusions [142 – 147] . A systematic review concludes that

this technique has demonstrated a good sensitivity and

specifi city for occlusion (97%), but the pooled sensitivity

and specifi city for detection of a 70 – 99% stenosis by CTA

were 85% and 93% respectively [146] (Class II, Level B).

In a systematic review, CEMRA is more accurate than

CTA to adequately evaluate 70 – 99% carotid stenosis

[148] , especially when there is an excess of calcium in the

plaque [149] . The difference among these modalities is

small, and other factors, such as availability and quality

of US performance, may render one procedure more

useful than the other (Class II, Level B).

Similarly to carotid stenosis, CEMRA and CTA may be

more sensitive in diagnosing vertebral artery stenosis

than DUS [150] .

Digital substraction angiography is the reference

method to determine the degree of carotid and vertebral

artery stenosis. Endarterectomy trials for symptomatic

[151 – 153] and asymptomatic [154] patients were per-

formed using this method. However, angiography carries

the risk of stroke and death [134, 155] , and many centres

are not using DSA prior to carotid endarterectomy

[135, 156 – 159] , particularly when non - invasive methods

are concordant (Class IV, GCPP). When non - invasive

methods are inconclusive or there is a discrepancy

between them, DSA is necessary.

Imaging of the i ntracranial v essels Transcranial Doppler (TCD) and transcranial colour -

coded duplex (TCCD) are non - invasive ultrasonographic

procedures that measure local blood fl ow velocity and

direction but also permit visualization of blood vessels

(TCCD) in the proximal portions of large intracranial

arteries [160, 161] . These methods are useful for the

screening of intracranial stenosis [162 – 164] and occlu-

sion [165, 166] in patients with cerebrovascular disease

(Class II, Level B). In children with sickle cell disease,

detection of asymptomatic intracerebral stenoses using

TCD allows selection of a group at high risk of future

stroke, who benefi t from exchange transfusion [167]

(Class II, Level B). It is also useful for the detection and

monitoring of intracranial artery vasospasm after SAH,

particularly in the MCA [168] (Class I, Level A). TCD

can be used to monitor recanalization during thromboly-

sis in acute MCA occlusions [169] (Class II, Level B).

There is increasing interest in its therapeutic use. In vitro

studies demonstrate it has an additive effect on clot lysis

when used with recombinant tissue plasminogen activa-

tor (rtPA), and clinical studies have suggested that con-

tinuous TCD monitoring in patients with acute MCA

occlusion treated with intravenous thrombolysis may

improve both early recanalization and clinical outcome

[170] . TCD allows for the documentation of a right - to -

left shunt in patients with ischaemic stroke (Class II,

Level A). TCD discloses a shower of air bubbles in the

MCA after the intravenous injection of saline mixed with

air bubbles [171 – 173] .

TCD is the only imaging technique that allows detec-

tion of circulating emboli, even in asymptomatic patients

(Class II, Level A). Emboli cause short - duration, high -

intensity signals, because they refl ect and backscatter

more ultrasound than the surrounding red blood cells.

Studies have shown that asymptomatic embolization is

common in acute stroke, particularly in patients with

carotid artery disease [174, 175] . In this group the pres-

ence of embolic signals has been shown to predict the risk

of stroke and transient ischaemic attack (TIA) [176 – 178]

(Class II, Level A). Embolic signals have also been used

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CHAPTER 2 Imaging in cerebrovascular disease 25

as surrogate markers to evaluate antiplatelet agents in

both single - centre studies [179] and in the multicentre

international Clopidogrel and Aspirin for Reduction of

Emboli in Symptomatic Carotid Stenosis trial [180] .

Embolic signal monitoring is used to monitor emboliza-

tion following carotid endarterectomy; the presence of

frequent embolic signals in this setting predicts early

postoperative stroke [181] and can be reduced by more

aggressive antiplatelet treatment, including dextran [182]

and clopidogrel [183] . TCD can also be used to evaluate

cerebrovascular reserve by determining the extent to

which MCA fl ow velocity can increase in response to

the vasodilator carbon dioxide or acetazolamide. Reserve

is reduced in a proportion of patients with carotid

occlusion and tight stenosis, and impaired reserve

predicts recurrent TIA and stroke risk, particularly in

the group with carotid occlusion [184, 185] (Class III,

Level B).

Transcranial Doppler examination cannot be per-

formed in about 10 – 15% of patients, particularly older

women, because they lack a transtemporal window

due to the thickness of the skull [186] . The use of intra-

venous echo contrast agents may improve detection of

fl ow velocities in patients with limited transtemporal

window [187] . TCD velocities may be altered in patients

with cardiac pump failure (low velocities) or anaemia

(increased velocities).

Magnetic resonance angiography (MRA) can identify

intracranial steno - occlusive lesions mainly in the proxi-

mal segments. Both TCD ultrasound and MRA non -

invasively identify 50 – 99% of intracranial large vessel

stenoses with substantial negative predictive value (86%

and 91% respectively) [188] . Compared with DSA, MRA

has a higher sensitivity and specifi city (superior to 80%)

for the identifi cation of proximal intracranial arterial ste-

nosis [189, 190] (Class II, Level B).

CT angiography is another useful technique with high

sensitivity and specifi city (superior to 90%) for the diag-

nosis of occlusion and intracranial stenosis [191, 192] ,

with the exception of stenosis in the cavernous portion

of the internal carotid or in arteries with circumferential

wall calcifi cation [189, 193] (Class II, Level B).

Magnetic resonance and CT angiography can be used to

show large aneurysms (Class II, Level B), but these tech-

niques fail to identify aneurysm of less than 5 mm in diam-

eter, those located in the intracranial carotid artery, and

cannot clearly establish the critical relationship of the neck

of the aneurysm(s) with arterial branches [194 – 197] .

Therefore non – invasive techniques have not replaced

DSA for aneurysm identifi cation and localization. The

sensitivity of 3 - dimensional time - of - fl ight MRA for cere-

bral aneurysms ≥ 5 mm after SAH is between 85% and

100% [198 – 200] , with lower percentages for aneurysms

< 5 mm [45, 198, 200] . CT angiography has a sensitivity

for aneurysms ≥ 5 mm between 95% and 100% and a

specifi city between 79% and 100% [45, 201 – 203] . Some

authors suggest that CT angiography can be used as a reli-

able alternative to DSA after SAH, particularly in cases in

which the risk of delaying surgery does not justify the per-

formance of a catheter study [45, 204] (Class II, Level B).

MR and CT angiography have been used for screening

individuals with a history of intracranial aneurysm or

SAH in fi rst - degree relatives [205, 206] (Class II, Level

B). Overall reported sensitivity for both techniques was

76 – 98% and specifi city was 85 – 100% [207] .

DSA is needed to demonstrate small aneurysms and

before surgery or endovascular treatment (Class I,

Level A).

Recommendations

Imaging of the b rain • Either non - contrast computed tomography (CT) or magnetic

resonance imaging (MRI) should be used for the defi nition of stroke type and treatment of stroke (Class I, Level A).

• The presence of early CT infarct signs cannot be construed as an absolute contraindication to thrombolysis in the fi rst 3 h after stroke (Class IV, GCPP).

• MRI has a higher sensitivity than conventional CT for the documentation of infarction within the fi rst hours of stroke onset, lesions in the posterior fossa, identifi cation of small

lesions, and documentation of vessel occlusion and brain oedema (Class I, Level A).

• In conjunction with MRI and magnetic resonance angiography (MRA), perfusion and diffusion MR are very helpful for the evaluation of patients with acute ischaemic stroke (Class I, Level A).

• Single photon emission computed tomography (SPECT) is helpful to predict the malignant course of brain swelling with large hemispheric infarctions (Class III, Level C). SPECT is also helpful in the evaluation of cerebral perfusion in

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26 SECTION 1 Investigations

non - acute cerebrovascular disease, for instance in the days after a subarachnoid haemorrhage (SAH) (Class III, Level C).

Detection of h aemorrhagic s troke • MRI can detect acute and chronic intracerebral haemorrhage

(Class I, Level A).

• Although the detection of SAH is possible with MRI, currently CT scan is the diagnostic procedure of choice (Class I, Level A). In case of doubt or negative CT scan, lumbar puncture and cerebrospinal fl uid (CSF) analysis is recommended (Class I, Level B)

Imaging of e xtracranial v essels • Although MRA has slightly higher sensitivity and specifi city

than ultrasonography (US) to determine carotid stenosis and occlusion, the usefulness of either procedure may be determined by other factors, such as availability (Class II, Level B).

• Computed tomography angiography (CTA) has a sensitivity and specifi city similar to MR for carotid occlusion and similar to US for the detection of severe stenosis (Class II, Level B).

• Digital substraction angiography (DSA) is generally recommended for grading carotid stenosis prior to endarterectomy (Class I, Level A), but when there is concordance of non - invasive methods cerebral arteriography may not be necessary (Class IV, GCPP).

Imaging of i ntracraneal v essels • Transcranial Doppler (TCD) is very useful for assessing

stroke risk of children aged 2 – 16 years with sickle cell

disease (Class II, Level B), detection and monitoring of vasospasm after SAH (Class I, Level A), diagnosis of intracranial steno - occlusive disease (Class II, Level B), diagnosis of right - to - left shunts (Class II, Level A), and for monitoring arterial recanalization after thrombolysis of acute middle cerebral artery (MCA) occlusions (Class II, Level B).

• TCD can detect cerebral emboli and impaired cerebral haemodynamics. The presence of embolic signals with carotid stenosis predicts early recurrent stroke risk (Class II, Level A). The detection of impaired cerebral haemodynamics in carotid occlusion may identify a group at high risk of recurrent stroke (Class III, Level B).

• MRA and CTA are very useful for the diagnosis of intracranial stenosis and cerebral aneurysms > 5 mm (Class II, Level B). MRA and CTA are the recommended techniques for screening cerebral aneurysms in individuals with a history of aneurysms or SAH in a fi rst - degree relative (Class II, Level B).

• DSA is the recommended technique for the diagnosis of cerebral aneurysm as the cause of SAH (Class I, Level A). CTA can be used as a reliable alternative to DSA in patients with SAH, particularly in cases in which the risk of delaying surgery for a catheter study is not justifi ed (Class II, Level B).

• MRI with MRA is recommended for the diagnosis and follow - up of cerebral venous thrombosis (Class II, Level B). Alternatively, CT venography is accurate and can be used for the same purpose (Class III, Level C).

Confl icts of i nterest J. Masdeu received an honorarium as Editor - in - Chief of

the Journal of Neuroimaging . With regard to this manu-

script there is no confl ict of interest.

P. D. Schellinger has received travel stipends, advisory

board and speakers honoraria from Boehringer Ingel-

heim, the manufacturers of Alteplase.

The rest of authors have reported no confl icts of inter-

est relevant to this manuscript.

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CHAPTER 2 Imaging in cerebrovascular disease 29

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