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NEURAD-491; No. of Pages 10 ARTICLE IN PRESS


Journal of Neuroradiology (2014) xxx, xxx—xxx

Available online at

ScienceDirect
www.sciencedirect.com

REVIEW

Imaging of acute stroke: CT and/or MRI


Karl-Olof Lövblad a,∗,b, Stephen Altrichter a,b,
Vitor Mendes Pereira a,b, Maria Vargas a,b,
Ana Marcos Gonzalez a,b, Sven Haller a,b, Roman Sztajzel a,b

a
Service neuro-diagnostique et neuro-interventionnel, DISIM, 4, rue Gabrielle-Perret-Gentil, 1211 Genève,
Switzerland
b
Service de neurologie, Genève, Switzerland

KEYWORDS Summary Acute ischemic stroke is now clearly recognized as a medical emergency. As such
Stroke; diagnosis has to be done quickly and in a precise way during the therapeutic window. Both com-
Imaging; puted tomography and magnetic resonance imaging are tools that can adequately demonstrate
Magnetic resonance ischemia really very early on. MRI using diffusion techniques has a much higher sensitivity for
imaging; acute lesions but its implementation has not been unproblematic due to initial resistance and
Computed some technical problems. Thus, very often CT is still preferred with MR used for situations
tomography where the answer given is not sufficient as well as for follow-up of lesions. However, the par-
allel development of new therapeutic strategies have rendered the precision of the tools more
and more sophisticated and their combined use can help to improve patient outcomes in ways
never imagined previously. No matter which technique is used, be it alone or in combination,
the idea is to speed up and optimize management in order to provide early revascularization
and reperfusion.
© 2014 Published by Elsevier Masson SAS.

Introduction neuroprotective agents have unfortunately proven to be only


successful in the laboratory setting [4], thrombolysis and
Since cerebral ischemia has been declared to be at least par- thrombectomy have proven to have their benefits in patients
tially treatable within the therapeutic window, stroke has treated within a clearly defined therapeutic window [5]. Ini-
now become a clearly defined medical emergency [1—3]. tially, brain imaging has been done on an exclusion basis
Indeed, the trend started by the NINDS trials was followed only, meaning that unenhanced CT was used mainly to deter-
by an increasing interest in both pharmacological and inter- mine if there was hemorrhage or some other kind of easily
ventional therapies for acute ischemia. While almost all visible brain pathology (e.g. tumour) that caused the acute
neurological deficit [5—10]. While this was an initial success
and worked for the first trial it is also true that this did not
per se determine that all these patients really had ischemia;
∗ Corresponding author. indeed, the exclusion of hemorrhage is per se not equiva-
E-mail address: karl-olof.lovblad@hcuge.ch (K.-O. Lövblad). lent with the presence of a stroke; thus, most new imaging

http://dx.doi.org/10.1016/j.neurad.2014.10.005
0150-9861/© 2014 Published by Elsevier Masson SAS.

Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
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techniques also revolve around determining if there is some spin labeling or dual source CT that can be added to current
kind of stroke mimic. One major issue is that since there protocols.
is very little time available (4.5 hours currently for MCA
ischemia using rTPA), the patient needs to be acutely
treated within this therapeutic window. Since any given Computed tomography
stroke protocol is very complicated and imaging only rep-
resents a portion of any kind of acute management, it is Computed tomography has been the cornerstone of brain
imperative that imaging provides both a quick and precise imaging since its introduction in the early 1970s [11,12].
answer, thus not prolonging the time needed to make a Besides its use for the diagnosis of any brain pathology, in
decision on treatment. A majority of patients with acute stroke it was primarily used for lesion exclusion then became
stroke still arrive outside the therapeutic window but those a strong diagnostic tool once the NINDS studies proved that
who do still need a full work-up with a neurological exam- therapy was feasible. It was also the main neuroradiological
ination, full laboratory tests etc. Indeed, and much to the tool until the emergence of MR and it was marred by ques-
distress of many traditional neurologists and even neuro- tions of low resolution especially in the posterior fossa until
radiologists, imaging has become an inherent part of the recently. However, the technique that set things in motion
early work-up and as such represents a little part, but a was the development of spiral CT [13], then volumetric CT
part that is technology intensive and personnel intensive. and also of scanners with more and more rows of detectors.
The main aims of primary neuroimaging are manifold: first CT in our opinion has the easiest capacity to detect hemor-
of all the overall aim even before imaging is to exclude rhage, be it intraparenchymal or subarachnoid. It can also
another pathology: the main pathology to be excluded is in well-trained hands demonstrate rather well the presence
of course hemorrhage (since thrombolysis is the treatment of ischemic changes [14] (Figs. 1—3).
being proposed) but it also encompasses diseases such as The acute signs on CT [15,16], when read by experienced
multiple sclerosis, epilepsy, functional states. Thus, after readers are quite accurate: one can see the dense artery
having simply looked at the parenchyma it is necessary to which corresponds to the clot, as well as signs of early
look at some more parameters that can be obtained with swelling and edema: this will lead to smaller sulci on the
either CT or MRI. The next logical step is to see if there affected side; also as soon as there is slight water accumula-
really is cerebral ischemia: indeed, treatment should not be tion one will have a loss of the capacity of CT to differentiate
done only when nothing is seen but offered to patients who between white and grey matter. This is especially well seen
actually are harboring an acute cerebrovascular event: this in the basal ganglia and in the insula but can be seen every-
can be done by looking for further signs of ischemia on DWI where. Additionally, where CT has proven to be of prime
with MR or for the acute signs of ischemia on CT; then when importance is the capacity to demonstrate the presence of
that is done the level of occlusion can be looked for: here early hypo density: indeed, this was shown at least for tap to
CT can sometimes often demonstrate an acute hyperdense be an early sign of potential malignant hemorrhagic trans-
artery and T2* will show a thrombus as well. When this is formation, especially if the hypo density was more than 30%
done one will also look at the proximal vessels in order to of the affected territory. Where CT played an important role
provide almost a one stop shopping approach: one is also to was in showing that when one third or more of the affected
look at the level of the carotids and possibly of the aortic territory was hypo dense there is an acute danger of increas-
arch in order to see if there is any plaque or calcification that ing fatal hemorrhage by initiating treatment with rTPA [17].
may be the cause of embolism. Also, adding perfusion imag- This may create the need for other drugs or approaches such
ing will allow assessing the perfusion status of the tissue. as other thrombolytic or even other mechanical practices.
While this was only initially possible with nuclear medicine While very useful, the one-third approach has not been
techniques such as PET and SPECT, and PET with O still without limitations or criticisms. Thus, scoring systems have
remains the gold standard, techniques using CT and MRI have been developed that try to address this. One of the more
progressed greatly over the last decades. These techniques known ones is the ASPECTS score [18] where a number of
have allowed determining a model of the penumbra based points is allocated to the MCA territory and points subtracted
on either the diffusion-perfusion mismatch and on a match for each hypodense area. The aspects score is used more and
or mismatch of the perfusion maps. Imaging will also be used more and has even been applied to DWI [19—21].
to detect any kind of complication due directly or indirectly Brain hemodynamics are at the core of the cerebral
to the treatment or procedure: CT will demonstrate an early ischemic event: indeed, initially the drop in cerebral blood
bleeding well but may be more problematic when it comes flow (CBF) will be compensated by an increase in collateral
to demonstrating the presence of small ischemic changes. blood flow and in the local cerebral blood volume (CBV); this
Here, MRI with diffusion has a major role. Final outcome is will maintain some kind of penumbra or tissue at risk. While
of course based on measures such as clinical status and clini- the hemodynamic models do not reflect the electrophysi-
cal scores but also by imaging: here CT can demonstrate final ological model initially postulated in the penumbra, they
lesions but less well that T2 images done at 3 months. While have proven to be perfectly usable working models for daily
FLAIR after a few weeks will often provide a lesion defini- clinical practice. Then, when both CBF and SBV drop, tissue
tion that approximates the final size, imaging at 3 months will be considered lost. Thus, adding perfusion techniques
with T2 MRI is mandatory. MRI can also be done in order can help identify the hypoperfused territory (Fig. 4) as well
to assess the possibility and success of any preadaptation as an infarcted core (Fig. 5). This can be done by looking
measures. This review mainly aims to look at the differences for a match or a mismatch visually between the perfusion
between CT and MRI for the acute detection of ischemia maps of CBF and CBV; when both are decreased and there is
and looks at some current novel methods such as arterial a match, there will often be massive infarction whereas in

Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
http://dx.doi.org/10.1016/j.neurad.2014.10.005
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Imaging of acute stroke: CT and/or MRI 3

Figure 1 Patient with left-sided symptoms and right cerebral ischemia. Right hyperdense MCA (a), with occlusion seen on CTA
(b: arrow, c), there is loss of white grey differentiation: the right-sided striatum is no longer visible (d: arrow, e), as well as loss of
sulcal effacement (f, g).

Figure 2 Predictive effect of CT; this is the same case as figure


1. One can see that the area affected by the sulcal effacement
Figure 3 Predictive effect of CT: patient with infarction in
and slight hypodensity on the early CT (A) corresponds to the
the basal ganglia on the left: the area where there is acute loss
final infarction almost perfectly on follow-up CT (B).
of differentiation of white and grey matter with disappearance
of the striatum (A) becomes hypodense on the late CT (B).
a mismatch when only CBF is decreased, a lesser infarct is
to be expected (Figs. 4 and 5). been introduced in clinical practice to subtract calcifica-
However due to its very high increase in usage, CT has tions (Fig. 6) or provide more objective measures of insular
become an important factor in the irradiation of the popu- density. It has been used to differentiate hemorrhage from
lation so that care must be taken when using it in order not contrast extravasation inpatients after interventional stroke
to do unnecessary studies. therapy [22]. Indeed, very often after interventional thera-
Dual source CT is a technique that has been available pies, contrast extravasation has been problematic in that
for some time but which has known recent resurgence. Ini- it will either mimic blood or even obscure an underlying
tially used for bone density measurement, it has recently pathology such as an ischemic region.

Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
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Figure 4 Patient with a right hemispheric stroke and a mismatch on perfusion CT: there is a decrease in CBF (c) in the right MCA
territory but the CBV is normal (b). MTT is increased (d). The final CT on the right show very little lesion (e).

Figure 5 Patient with a left hemispheric stroke and matching hypoperfusion: there is a match in the surfaces of decreased CBV
(b) and CBF (c). MTT is increased (d). There is a large final lesion (e).

The combined use of techniques such as PET and CT or not significant may be found to be inflammatory and thus
PET and MRI has known a great increase over the last few the cause of embolism.
years but while not really usable in the emergency situation
we describe here, PET CT will be of use on the work-up of
patients with carotid disease. Indeed, it may well demon- Magnetic resonance imaging
strate the presence of activity in plaques that are sometimes
morphologically not suspicious and may thus help to provide Magnetic resonance imaging has proven itself to be a revolu-
treatment to some patients [23]. These techniques are gain- tionary and evolutionary tool, maybe even more so than CT.
ing in acceptance quickly since sometimes plaques that are While the advantages of its non-ionising nature are evident,

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Imaging of acute stroke: CT and/or MRI 5

Figure 8 Patient with acute posterior fossa infarction: on the


acute CT (A) there is no visible lesion while on the DWI one has
clearly a lesion of the left pons (B).
Figure 6 Dual source energy CT of a patient after intra-
arterial thrombolysis for a left MCA stroke: on the left one
can see some blood (A) but on the right there is more contrast scanners that this technique could translate from the lab
extravasation visible (B) thus allowing differentiation between to the clinical site. Once it was clinically applied to patients
acute blood and contrast on the same examination. with acute stroke, it showed itself to have a high sensitiv-
ity and specificity [31—34]. As in animal models the capacity
for detection of acute ischemic changes starts minutes after
the examinations were initially extremely time consuming stroke onset only [35]. Comparison studies have shown DWI
and ill suited to acutely ill patients. It would be the advent to be far superior to CT [36—42] (Figs. 7 and 8). Of interest
of echo-planar imaging that was the revolution not just for also is the capacity of DWI volumes to correlate with clinical
stroke but for many areas that required an increase in imag- status and outcome [43]; this implies that at least for stud-
ing speed and a reduction in overall acquisition time [24,25]. ies implicating drugs it can be used as a surrogate marker of
Indeed, echo-planar meant that diffusion and perfusion MRI ischemia. It is also known that diffusion lesions tend to grow
would be finally clinically feasible [26]. Conventional MR with time and this can be used more when using the so-called
has been in use from the start but more to demonstrate diffusion-perfusion mismatch [44]. The diffusion-perfusion
the presence of established ischemic lesions that will be mismatch is a rather simplistic model but which clinically
hypo-intense on T1 and hyper on T2 due to water accumu- works at times: one supposes that at an early time point
lation these conventional techniques are still used for the the diffusion lesion is the core and around that the hypop-
follow-up of patients where they remain the standard. erfused area represents the penumbra [45]. The problem is
Diffusion techniques are MR techniques that image water that from a historical perspective at least the penumbra is
movement [27—30]. These techniques are now more than 20 a physiological definition of an area between thresholds of
years old. Le Bihan et al. developed them; his team made a dysfunction and definitive damage, Thresholds of ischemia
Stejskal-Tanner modification of a spin echo technique. Thus, are also present in the diffusion image and most certainly on
the protons were given an impulsion and if they moved more the ADC maps: while this has not been as well reproduced
or less would transmit more or less signal back. The tech- in humans as in the animal models it seems that there is a
nique was initially very sensitive to motion and it was only definable threshold [46,47]. Also, another area where diffu-
with the development of clinically available echo-planar sion imaging has helped to do a lot of progress is its capacity

Figure 7 Acute CT in a patient with a right hemisyndrome and aphasia: slight hypodensity in left hemisphere visible on CT (A),
but there is a large DWI lesion (B) on the MRI performed afterwards on the same day.

Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
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contrast that is due to the induction of local changes in mag-


netic susceptibility: this will allow to calculate maps of mean
transit time as well as of relative cerebral blood flow and
volume [52]. Additionally, T1-weighted techniques can be
used but are far less common but could be advantageous.
Another technique that has been available for a number of
years but has been underutilized is the so-called arterial
spin labeling technique [53—60]; this relies on the tagging
of blood flow at the cervical level with creation of maps of
cerebral blood flow at the distal cerebral level. This allows
obtaining perfusion maps without any contrast agent, which
could cause toxic allergic or nephrologic problems. Also with
advances in MR technology, it has been possible to obtain
multi-slice data sets covering the whole brain. The disad-
Figure 9 Patient with proximal origin of embolic lesions vantage is fewer signals but there are many advantages of
of cardiac origin: there are bilateral lesions on the diffusion ASL besides the non-utilization of contrast such the possible
images. demonstration of collaterals and selective demonstration of
vascular territories. Thus, contradictory series have shown
to locate more precisely the lesions: this can even allow dif- data that is slightly contradictory with either concurrence
ferentiating between lesions that are due to a more distal or overestimation of hypoperfusion; this may be due in part
(Fig. 9) or a more proximal (Figs. 10 and 11) cause [48]. to the lower signal but also due to a lack in consensus on the
Those that have a more proximal origin will be more dis- use of technical parameters used for ASL in clinical practice
tributed widely with at times a starry sky appearance of the across vendor platforms [61—67].
emboli on the DWI images (Fig. 9). For patients who some- While conventional T2* imaging has been playing a major
times wake-up with a stroke, a mismatch between FLAIR role in imaging of hemorrhage and calcifications, the advent
and diffusion can be sought: if the lesions are of same size, of so-called susceptibility-weighted imaging has changed
it is highly probably that the lesion is more than the allowed this even further: indeed, these SWI images now allow to
therapeutic window (Fig. 12). obtain high-resolution images of e.g. the brain. While good
Perfusion techniques have been available for a long time for the detection of hemorrhage these sequences could also
using MR scanners [49—51]. These techniques can be per- improve our knowledge about the presence of trans cerebral
formed in a multitude of ways. The most frequent way is veins in acute stroke [68,69].
to use T2* imaging techniques: images are repeated quickly MR Angiography techniques: these techniques have
using echo-planar technology and images covering the whole evolved greatly over the last decade. At first images based
brain are done: a gadolinium based chelate is then injected on either time-of-flight or phase contrast techniques were
and when this enters into the blood there is a decrease in used. These did not involve any contrast agent but used

Figure 10 Patient a left-sided carotid stenosis on contrast-enhanced MRA (A) embolic lesions are only present in the ipsilateral
left hemisphere (B).

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Imaging of acute stroke: CT and/or MRI 7

Figure 11 Patient with carotid occlusion and stroke: there is a typical flame-like tapering of the carotid (A), compatible with a
dissection and there are internal watershed lesions due to occlusion (B).

Figure 12 Patient presenting in the morning with a wake-up stroke: there is a match in the size between the diffusion (A) and
the FLAIR image (B). Thus this patient is not eligible for thrombolysis.

inherent movement of intravascular fluids. One may also unenhanced CT alone. This was in a way sufficient to exclude
look for a matching between the occlusion seen as with the a hematoma or a mass as well as to demonstrate early severe
diffusion lesion: this is called the MRA-diffusion mismatch ischemia but was unfortunately insufficient for a more accu-
[70,71]. rate work-up. Nuclear medicine tools such as PET and SPECT
while they were able to demonstrate hypoperfusion and
even the penumbra were not usable due to the difficulty
Discussion of use in the clinical setting. PET and SPECT had initially
been used to establish the clinical data we have about brain
Since therapeutic options have emerged for acute ischemic perfusion and has established the baseline blood flow and
stroke there has been an increased pressure to develop tools volume values that we use today but the techniques, while
for an early diagnosis. Indeed, the era when stroke was syn- very precise were difficult to implement clinically and they
onymous with death or lengthy stays in recovery are now far have been partially abandoned; this is unfortunate because
gone. The main diagnostic tool over the first decades when as validation tools especially using PET with oxygen, they are
treatment was initiated was computed tomography. Indeed, still irreplaceable and could be used to validate new tech-
the early thrombolysis trials were done base don the use of niques more seriously. Also, the use of MRI was restricted in

Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
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the early phase due to the fact that it could only detect T2 a more powerful tool especially when looking for smaller
changes in the late phase and also due to the fact that early lesions that may not even be seen on CT.
scanners were closed and that patients could not take the
long examination times. Thus, there was a first technological Disclosure of interest
revolution when MR saw the development of early clinical
echo-planar scanners; this allowed implementing sequences
The authors declare that they have no conflicts of interest
such as diffusion and perfusion that allowed modeling the
concerning this article.
first human penumbra. Indeed, these techniques, which had
been in development for a while had been almost impos-
sible to use clinically due to time constraints and duet o References
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Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
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Please cite this article in press as: Lövblad K-O, et al. Imaging of acute stroke: CT and/or MRI. J Neuroradiol (2014),
http://dx.doi.org/10.1016/j.neurad.2014.10.005