a b s t r a c t

Imaging in acute stroke has traditionally focussed on the 4Ps-parenchyma, pipes, perfusion, and penumbra-and has increasingly relied upon advanced techniques including magnetic resonance imaging to evaluate such pa- tients. However, as per European Magnetic Resonance Forum estimates, the availability of magnetic resonance imaging scanners for the general population in India (0.5 per million inhabitants) is quite low as compared to Europe (11 per million) and United States (35 per million), with most of them only present in urban cities. On the other hand, computed tomography (CT) is more widely available and has reduced scanning duration. Com- puted tomography angiography of cervical and intracranial vessels is relatively simpler to perform with extended coverage and can provide all pertinent information required in such patients. This imaging review will discuss relevant imaging findings on CT angiography in patients with acute ischemic stroke through illustrated cases.

(C) 2015

1. Introduction

In India, 1.44 to 1.64 million cases of acute strokes occur every year resulting in 0.63 million deaths [1]. Estimates of the prevalence of stroke in India alone range from 44 to 843 per 100000 population [2]. Acute is- chemic stroke (AIS) accounts for 68% to 80% of strokes, with Large vessel occlusion being responsible for nearly 41% of these patients [3]. It is im- portant to identify large vessel occlusion as intravenous thrombolysis is less effective and associated with poor prognosis in such patients.

Imaging in AIS has always traditionally focused on the 4Ps- parenchyma, pipes, perfusion, and penumbra. Existing guidelines recom- mend only plain computed tomography (CT) before intravenous throm- bolysis. vascular imaging (CT/magnetic resonance angiography) is recommended only if intraarterial therapy is planned [4]. However, ad- vanced Imaging techniques such as CT/magnetic resonance angiography and perfusion are being widely used in AIS, to identify favorable penum- bral pattern and patient selection for endovascular intervention. Perfusion studies require higher slice CT scanners for whole brain coverage and technical expertise for postprocessing. As per European Magnetic Resonance Forum estimates available online, prevalence of magnetic resonance imaging per million populations is quite low in India (0.5) as compared to Europe (11) and United States (35). Computed tomography is more widely available and has shorter scanning duration which is of

? This research received no grant from any funding agency in the public, commercial, or not-for-profit sectors.

?? The author(s) declare(s) that there is no conflict of interest.

* Corresponding author.

E-mail address: [email protected] (S. Varadharajan).

importance in patients with stroke. Computed tomography angiography of cervical and intracranial vessels is relatively simpler to perform with extended coverage from aortic arch to the distal cortical vessels. It can yield useful information for the management of acute stroke patients and prognostication of those outside the therapeutic time window.

Following article will review imaging findings of patients with acute ischemic stroke on CTA through illustrative cases focusing on the 4Ps of stroke imaging.

Computed tomography angiography protocol

Patients presenting with acute ischemic stroke are initially imaged with plain CT of the head followed by CTA. Routinely, 50 to 70 mL of nonionic iodinated contrast media (containing 300 mg I/mL) is injected through pressure injector at rate of 4 to 5 mL/s followed by a saline chase of approximately the same amount. Scanning is initiated by bolus tracking method with minimum delay of 5 seconds, followed by acquisition from arch of aorta to vertex. Raw data acquired in axial plane are reconstructed into sagittal and coronal maximum intensity projection images.

1. Parenchyma
   1. Watershed infarcts

Location of cortical and deep water shed zones is well established, and patients presenting with infarcts in these regions need to be evaluated for abnormalities involving ipsilateral common or internal Carotid arteries. As

http://dx.doi.org/10.1016/j.ajem.2015.10.056

0735-6757/(C) 2015

Fig. 1. Middle-aged male patient presenting with symptoms of transient ischemic attack. Computed tomography angiography source images show presence of both cortical and deep wa- tershed infarcts (arrows).

shown in Fig. 1, deep watershed infarcts are often seen as multiple hypodense foci along watershed zone within centrum semiovale in linear fashion. Computed tomography angiography can demonstrate narrowing of ipsilateral carotid artery in such patients. Apart from carotid bifurca- tion, other sites such as supraclinoid portion can also be involved as illus- trated in Fig. 2, and care should be taken to assess the entire carotid circulation from its origin from aortic arch till Internal carotid artery (ICA) bifurcation. Atherosclerotic narrowing of carotid bifurcation is most commonly seen in such patients with deep watershed infarcts as illustrated in Fig. 3.

1. Pipes (cervical and intracranial vessels)

floating thrombus“>Computed tomography angiography can detect focal changes in caliber of vessels apart from occlusion. Both the wall and lumen of visualized vessels need to be assessed within abnormal segments.

Dissection

Computed tomography angiography in carotid dissections usually shows irregular luminal stenosis just beyond the carotid bulb,

progressing to occlusion in a few patients as demonstrated in Figs. 4 and 5. Other imaging findings of vessel dissection include mural hema- toma, the intimal flap, and a Dissecting aneurysm. Medical management (antiplatelets) is required in patients with stenosis, whereas surgical or endovascular management is needed in those with dissecting aneurysms [5]. Dissections can occur spontaneously or after trauma. Diagnosis of dissection is often missed in absence of intimal flap, and one needs to be aware of other indirect imaging findings in such pa- tients. Presence of intramural hematoma can be associated with subtle hyperattenuation on CT with associated narrowing on CTA as shown in Fig. 6. Diagnosis is such patients can also be established by demon- strating intramural hematoma by using magnetic resonance imaging (T1-weighted precontrast black blood imaging).

Intraluminal free-floating thrombus

Intraluminal free-floating component should be suspected when contrast is seen circumferentially around the thrombus as seen in Figs. 7 and 8. Identification of intraluminal free-floating thrombus (FFT) is important because there is higher risk of recurrent embolic events in such patients and management involves prompt anticoagulation for

Fig. 2. Computed tomography angiography axial and coronal images of patient in Fig. 1 showing nonvisualization of right supraclinoid ICA (arrow and star) suggestive of stenosis.

Fig. 3. Another patient with left parieto-occipital watershed infarct (star) showing ulcerated plaque at left carotid bifurcation (arrow).

clot lysis [6]. Computed tomography angiography, especially the axial source images, can identify such intraluminal FFT and guide manage- ment. The most important imaging differential to consider in patients with such FFT is complex ulcerated plaque [7].

1. Perfusion
   1. Collaterals

Collaterals in patients with acute stroke are an important prognostic factor, and presence of adequate collaterals often leads to reduced long term deficits. They are also associated with a reduced risk of bleeding postthrombolysis and thus influence prognosis. There are numerous

methods of grading collaterals on CTA [8]. Status of collaterals is better evaluated on sagittal and coronal reformatted images. Good collaterals can even compensate for complete occlusion of a major intracranial ves- sel as demonstrated in Fig. 10.

1. Penumbra/infarct core

Computed tomography angiography source images can sometimes represent cerebral blood volume and, therefore, better predictor of in- farct core as compared to CT (Fig. 9). However, it has also been shown that sometimes CTA abnormalities can reverse due to overestimation especially using faster acquisition protocol and can vary with collateral status [9]. Thus, it should be interpreted with caution and be used as

Fig. 4. Middle-aged female patient showing subtle watershed infarct within left centrum semiovale (arrow) and CTA sagittal image showing abrupt narrowing of left ICA just beyond the carotid bulb (arrow) suggestive of dissection.

Fig. 5. Young adult with history of trauma and cerebrovascular accident showing multiple craniofacial fractures on axial bone window images, right gangliocapsular infarct (not shown), and posttraumatic dissection of right ICA on sagittal CTA image.

rough estimate of infarct burden and thereby prognosis after evaluation of other factors such as collaterals.

1. Conclusions

diagnostic yield of CT angiography in patients with AIS is very high [10]. Apart from identifying obvious large vessel stenosis or occlusion, careful interpretation can help in diagnosis, guide management, prog- nosticate, and predict long-term outcome in such patients.

References

1. Murthy J. Thrombolysis for stroke in India: miles to go. Neurol India 2007;55(1):3-5.
2. Prasad K, Vibha D, Meenakshi. Cerebrovascular disease in South Asia-part I: a burn- ing problem. JRSM Cardiovasc Dis 2012;1 [pii: cvd.2012.012025].
3. Wasay M, Khatri IA, Kaul S. Stroke in South Asian countries. Nat Rev Neurol 2014;10:

135-43.

1. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/ American Stroke Association. Stroke 2013;44:870-947.
2. Rahme RJ, Aoun SG, McClendon Jr J, El Ahmadieh TY, Bendok BR. Spontaneous cervi- cal and cerebral arterial dissections: diagnosis and management. Neuroimaging Clin N Am 2013;23(4):661-71.
3. Mokin M, Kass-Hout T, Kass-Hout O, Radovic V, Siddiqui AH, Levy EI, et al. Intrave- nous heparin for the treatment of intraluminal thrombus in patients with acute ischemic stroke: a case series. J Neurointerv Surg 2013;5(2):144-50.
4. Jaberi A, Lum C, Stefanski P, Thornhill R, Iancu D, Petrcich W, et al. Computed tomogra- phy angiography intraluminal filling defect is predictive of internal carotid artery free- floating thrombus. Neuroradiology 2014;56(1):15-23.
5. Yeo LL, Paliwal P, Teoh HL, Seet RC, Chan BP, Ting E, et al. Assessment of intracranial collaterals on CT angiography in anterior circulation acute ischemic stroke. AJNR Am J Neuroradiol 2015;36(2):289-94.
6. Watanabe M, Qureshi AI. Are CT angiography source images accurate for evaluating infarct volume? J Neuroimaging 2013;23(2):163-4.
7. Deipolyi AR, Hamberg LM, Gonzalez RG, Hirsch JA, Hunter GJ. Diagnostic yield of emergency department arch-to-vertex CT angiography in patients with suspected acute stroke. AJNR Am J Neuroradiol 2015;36(2):265-8.

Fig. 6. Middle-aged patient with symptoms of posterior circulation stroke shows intramural hematoma and luminal narrowing (arrows) within distal right vertebral artery on axial plain and CTA images, respectively, suggestive of dissection.

Fig. 7. Patient presented with left-sided cerebrovascular accident and plain CT (not shown) showed infarcts within right Middle cerebral artery and watershed regions. Computed tomography angiography shows free-floating thrombus within left Common carotid artery (arrows).

Fig. 8. Middle-aged patient with posterior circulation stroke showing bilateral cerebellar infarcts and free-floating thrombus within left vertebral artery (arrow).

Fig. 9. Middle-aged patient with recurrent right-sided cerebrovascular accident. Computed tomography angiography source image shows multiple infarcts within left centrum semiovale closely matching diffusion weighted imaging infarct volume.

Fig. 10. Patient with recurrent TIAs showing left M1 occlusion (star) with good retrograde pial collaterals on sagittal and coronal reconstructed CTA images and no parenchymal infarcts.