Vessel Wall Magnetic Resonance Imaging for Evaluating Stroke
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REVIEW ARTICLE Ann Clin Neurophysiol 2021;23(1):17-28 https://doi.org/10.14253/acn.2021.23.1.17 ANNALS OF CLINICAL NEUROPHYSIOLOGY Targeting the culprit: vessel wall magnetic resonance imaging for evaluating stroke Seung Min Kim1, Sang Hee Ha2, Hanim Kwon2, Yeon Jung Kim2, Sung Ho Ahn3, Bum Joon Kim2 1Department of Neurology, Veterans Health Service Medical Center, Seoul, Korea 2Department of Neurology, Asan Medical Center, Seoul, Korea 3Department of Neurology, Pusan National University Yangsan Hospital, Yangsan, Korea Received: February 2, 2021 Revised: February 21, 2021 The pathogenesis of many strokes originates in the vessel wall. Despite this, most traditional Accepted: February 24, 2021 imaging focuses on the vascular lumen. Vessel-wall magnetic resonance imaging (VWMRI) is useful for establishing the etiology of intracranial stenosis. It also provides information regard- ing atherosclerotic plaque composition and thus plaque vulnerability, which is an indication of its potential to cause a stroke. In this review we focus on the characteristics of VWMRI findings in various arteriopathies related to intracranial artery stenosis, and discuss the clinical implica- Correspondence to tions of these findings. Bum Joon Kim Department of Neurology, Asan Medical Key words: Vessel-wall magnetic resonance imaging; Ischemic stroke; Intracranial athero- Center, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea sclerosis; Dissection; Moyamoya disease Tel: +82-2-3010-3981 Fax: +82-2-474-4691 E-mail: [email protected] INTRODUCTION ORCID Seung Min Kim Ischemic stroke is a cerebrovascular event caused by occlusion or stenosis of the cerebral https://orcid.org/0000-0001-5228-6512 arteries that supply blood flow to the brain parenchyma. Sudden interruption of this blood Sang Hee Ha flow causes ischemia and subsequent permanent damage to the involved brain tissue, https://orcid.org/0000-0002-2926-2368 Hanim Kwon resulting in a focal neurological deficit. More than 40% of arterial occlusions are attribut- https://orcid.org/0000-0003-1340-9529 able to arterial pathology, and predominantly atherosclerosis.1 Various etiologies of arterial Yeon Jung Kim stenosis, and stenosis of the intracranial arteries in particular, may cause ischemic stroke. https://orcid.org/0000-0002-6081-890X Sung Ho Ahn To date, neuroimaging for stroke has focused on the brain parenchyma, as for other https://orcid.org/0000-0002-8376-545X neurological diseases that primarily involve this brain region. Although parenchymal im- Bum Joon Kim aging is useful for evaluating the underlying stroke mechanism, predicting the prognosis, https://orcid.org/0000-0002-3278-3252 and aiding treatment decision-making, it neglects the true culprit of arterial-wall pathol- ogy. Various modalities including computed tomography angiography (CTA), magnetic http://www.e-acn.org Copyright © 2021 The Korean Society of Clinical Neurophysiology This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// pISSN 2508-691X creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, eISSN 2508-6960 provided the original work is properly cited. Annals of Clinical Neurophysiology Volume 23, Number 1, April 2021 resonance angiography (MRA), and digital subtraction angi- ly the distal internal carotid artery (ICA), is more commonly ography (DSA) have been used to locate and measure ste- associated with artery-to-artery embolism, whereas local noses in the intra- and extracranial arteries. However, these branch occlusion is prevalent in posterior-circulation ICAS, conventional vascular imaging modalities do not provide especially in the basilar artery (BA).4 In the middle cerebral ar- adequate information regarding vessel pathology.2 Carotid tery (MCA), the mechanism differs according to the location duplex sonography does reveal the vessel-wall pathology and severity of the atherosclerotic lesion. In proximal MCA of extracranial cervical arteries,3 but is of limited use for eval- disease, and particularly in the case of proximal MCA occlu- uating intracranial artery stenosis, which is a major cause of sion, stroke most commonly results from a combination of stroke in Asian patients. mechanisms. This can be explained by plaque rupture with The use of high-resolution vessel-wall magnetic reso- occlusion causing both perforator infarction and embolism. nance imaging (VWMRI) to evaluate intracranial arterial-wall In the case of distal MCA atherosclerotic disease, artery-to-ar- pathologies is increasing in many centers. Since treatment tery embolism is the most common mechanism of stroke decision-making for ischemic stroke depends primarily on because of the location, being associated with turbulence the mechanism, it is critical to identify the true culprit. This at the distal MCA bifurcation. A longer stenosis is associated review focuses on the usefulness of VWMRI for identifying with the occurrence of a local branch occlusion.8 the etiology of arterial stenosis and for evaluating intracra- nial atherosclerotic stenosis (ICAS). The pitfalls and future Imaging techniques in VWMRI directions for the use of VWMRI in the field of stroke care are High-spatial-resolution in VWMRI is essential for character- also discussed. izing vessel-wall pathologies, enabling visualization of the morphology of both the plaque and its components. In terms of hardware, a magnetic field strength of at least 3 T VWMRI IN ICAS is needed to perform VWMRI.9 For vessel-wall assessment, a combination of multiple magnetic resonance sequences Stroke mechanism of ICAS such as T1-weighted imaging (T1WI), T2-weighted imaging It has been demonstrated that the high prevalence of ICAS (T2WI), and proton-density (PD) and time of flight (TOF) im- in Asians may be at least partially explained by vulnerability aging are used in VWMRI. Multiple tissue-weighted images to certain risk factors, levels of antioxidant enzyme activi- such as obtained in T1WI, T2WI, and PD imaging are used ty,4,5 and greater intracranial arterial tortuosity than in other for better characterization of the individual lesion, whereas races.6 The stroke mechanism also differs according to the TOF imaging is used mainly to characterize luminal abnor- location of the atherosclerosis, and most strokes related to malities and locate and assess the site of vessel narrowing. extracranial atherosclerosis are caused by artery-to-artery In brain tissue, the signal intensity (SI) on T1WI is highest for embolism. ICAS is associated with more diverse mechanisms lipids, followed in decreasing order by cerebral white matter, based on the lesion pattern presented on diffusion-weight- cerebral gray matter, and cerebrospinal fluid (CSF). Subacute ed imaging: 1) local branch occlusion, 2) artery-to-artery hemorrhages and high-protein-containing lesions such as embolism, 3) in situ thrombosis, and 4) hemodynamic. Local mucoceles also have a high SI. On T2WI, the SI in the brain is branch occlusion is caused by obliteration of the perforator’s highest in the CSF, which has the longest T2 relaxation time, orifice by the atheroma. Artery-to-artery embolism manifests followed in decreasing order by gray matter and white mat- as infarcts distal to the stenosis in the territory of the relevant ter. Brain edema, demyelinating lesions, cerebral infarcts, and artery, usually with small scattered lesions. In situ thrombosis tumors also have long T2 relaxation times and thus a high involves infarcts with extensive involvement of most or even SI on T2WI. Conversely, acute or chronic hemorrhage, calci- all of the diseased arterial territory. With a hemodynamic fication, fibrosis, and high-protein-containing lesions have a impairment, the infarcts are located in the border-zone areas low SI on T2WI. PD imaging has a better signal-to-noise ratio associated with perfusion deficits distal to the stenotic or oc- than T1WI, while contrast enhancement is less evident.9 cluded artery.4,7 ICAS in the anterior circulation, and especial- 18 https://doi.org/10.14253/acn.2021.23.1.17 http://www.e-acn.org Seung Min Kim, et al. Vessel wall MRI in stroke Typical findings of VWMRI of ICAS pears hyperintense on T2WI and may show enhancement. Atherosclerosis develops in the inner curvature of the arterial In contrast, a hypointense and nonenhanced layer in the vessel wall, where the shear stress is low.10 Atherosclerotic adjacent area is often observed on T2WI. A third, thin layer plaques are composed of lipid, fibrous components, cellular with enhancement is often observed in the periphery. These material, connective tissue matrix, and calcification. Evalu- layers observed on carotid VWMRI are correlated with find- ating these components can aid the diagnosis of vascular ings obtained from carotid endarterectomy specimens. The pathologies, thus helping to identify “vulnerable” plaques enhanced layer immediately adjacent to the lumen is the that are at high risk of causing stroke.11 ICAS lesions are often fibrous cap, the outer nonenhanced layer indicates the lipid multiple and exhibit eccentric thickening with or without a core, and the outer peripheral thin rim of enhancement rep- focal enhancement (Fig. 1). Positive vessel-wall remodeling resents an increased area of vasa vasorum in the arterial ad- can be also observed in some cases.12 Symptomatic plaques ventitia (Table 1).13 However, not all intracranial atheroscle- are associated with more positive vessel-wall remodeling,