Vessel wall MR imaging of aortic arch, cervical carotid and intracranial arteries in patients with embolic stroke of undetermined source: A narrative review

Abstract

Despite advancements in multi-modal imaging techniques, a substantial portion of ischemic stroke patients today remain without a diagnosed etiology after conventional workup. Based on existing diagnostic criteria, these ischemic stroke patients are subcategorized into having cryptogenic stroke (CS) or embolic stroke of undetermined source (ESUS). There is growing evidence that in these patients, non-cardiogenic embolic sources, in particular non-stenosing atherosclerotic plaque, may have significant contributory roles in their ischemic strokes. Recent advancements in vessel wall MRI (VW-MRI) have enabled imaging of vessel walls beyond the degree of luminal stenosis, and allows further characterization of atherosclerotic plaque components. Using this imaging technique, we are able to identify potential imaging biomarkers of vulnerable atherosclerotic plaques such as intraplaque hemorrhage, lipid rich necrotic core, and thin or ruptured fibrous caps. This review focuses on the existing evidence on the advantages of utilizing VW-MRI in ischemic stroke patients to identify culprit plaques in key anatomical areas, namely the cervical carotid arteries, intracranial arteries, and the aortic arch. For each anatomical area, the literature on potential imaging biomarkers of vulnerable plaques on VW-MRI as well as the VW-MRI literature in ESUS and CS patients are reviewed. Future directions on further elucidating ESUS and CS by the use of VW-MRI as well as exciting emerging techniques are reviewed.

Keywords: atherosclerosis; cerebrovascular disease/stroke; embolic stroke of undetermined source (ESUS); imaging; stroke; vessel wall MRI.

Figure 1

Vascular beds commonly affected with atherosclerosis. Careful evaluation of high-risk plaque features using vessel wall MRI of the intracranial arteries, cervical carotid arteries, and aortic arch may aid in identifying culprit plaques in patients with cryptogenic stroke or embolic stroke of undetermined source. Such efforts may help identify causes of stroke that may have been previously overlooked.

Figure 2

Intraplaque hemorrhage in carotid plaque on Magnetization-Prepared Rapid Gradient Echo (MPRAGE) and Time-of-flight MR angiography (TOF MRA). T1 hyperintense IPH at the right carotid bifurcation (white arrowheads) on both (A) MPRAGE and (B) TOF MRA. The MPRAGE image has fat and blood flow suppression, allowing for the IPH to standout in contrast to the vessel lumen and surrounding soft tissues. The TOF MRA image also demonstrates an intact hypointense fibrous cap at this level (black arrowhead).

Figure 3

Ulcerated plaque with intraplaque hemorrhage on VW-MRI. Male patient presented with clinical and imaging evidence of a 1–2-year history of recurrent left MCA territory infarcts. (A,B) Contrast-enhanced MRA neck confirmed a left cervical carotid bifurcation stenosis with an ulcerated plaque (A, arrowhead). (C,D) 3D surface volume rendering of the left carotid plaque depicts the ulcerated surface morphology with (D) axial image through the ulceration showing marked surface irregularity (red arrows). (E,F) Carotid VW-MRI showed intraplaque hemorrhage (arrowheads), depicted as T1 hyperintense signal on a fat-suppressed T1W MPRAGE image. Based on the clinical and imaging findings, the patient underwent a left carotid endarterectomy.

Figure 4

Intrinsic T1 hyperintense signal of intracranial plaque on precontrast VW-MRI. Orthogonal view of a precontrast VW-MRI of the middle cerebral artery shows intrinsic T1 hyperintense signal (arrowhead) and positive (outward) wall remodeling (arrowhead).

Figure 5

Vessel wall thickening and atherosclerosis on VW-MRI in a symptomatic patient. (A) A patient with left parietal lobe acute ischemic infarcts (arrowheads) underwent intracranial VW-MRI. (B) Time-of-flight MRA and (C) intracranial VW-MRI shows multiple intracranial plaques (arrows) that showed both eccentric (a, b, c, e) and concentric (d) vessel wall thickening. The culprit lesion was thought to be the most stenotic lesion (c) in the left internal carotid artery.

Figure 6

Non-stenotic right middle cerebral artery enhancing culprit plaque. (A) A patient with a right basal ganglia acute infarct showed (B) mild luminal irregularity but no appreciable stenosis of the right middle cerebral artery on time-of-flight MRA imaging (arrowhead). (C) Precontrast VW-MRI showed eccentric wall thickening along the right M1 middle cerebral artery (arrowhead). (D) Precontrast and (E) postcontrast images in the orthogonal plane through the plaque shows eccentric wall thickening and enhancement of the culprit plaque, which likely caused the ischemic infarct.

Figure 7

Comparison of 3 and 7 Tesla (T) VW-MRI for intracranial atherosclerosis. A patient with history of obesity, hyperlipidemia and hypertension and ischemic stroke underwent a (A) 7T TOF-MRA, which showed left M1 middle cerebral artery severe stenosis (arrowhead). (B) 7T MRI axial T1 SPACE post-gadolinium (0.5 mm isotropic resolution) image clearly delineates arterial wall thickening and avid vessel wall enhancement in the region of stenosis (arrowhead). (C) The same patient was imaged 18 days later on a 3T MRI (T1 SPACE post-gadolinium, 0.8 × 0.8 × 1.0 mm) to assess the stenosis (arrowhead). The 7T VW-MRI shows improved conspicuity and delineation of the margins of the arterial wall compared to the 3T, an advantage of the higher magnet strength due to the higher signal to noise leveraged for higher spatial resolution and soft tissue contrast.

Figure 8

Joint VW-MRI of the extracranial and intracranial arteries. (A) Coronal precontrast VW-MRI image shows the coverage of the joint intracranial and extracranial VW-MR image. (B) A curved reformatted image of the left cervico-cranial carotid artery shows intrinsic T1 hyperintense signal at the carotid bulb (yellow arrowhead), which was favored to be the culprit source of plaque in this patient with ischemic strokes. The intracranial internal carotid artery at the siphon (white arrowhead) and M1 middle cerebral artery segment (red arrowhead) showed no significant wall thickening to suggest intracranial atherosclerosis.

Figure 9

4D Flow MRI of intracranial atherosclerosis. (A) TOF MRA image demonstrates a focal area of middle cerebral artery narrowing (arrowhead) with (B) post-contrast T1-weighted VW-MRI showing a corresponding eccentric, enhancing atherosclerotic plaque (arrowhead). (C) On 4D Flow MRI, increased velocities are seen in the area of greatest narrowing (arrowhead).

Figure 10

Aortic VW-MRI using the MR MultiTasking based 3D Multidimensional Assessment of Cardiovascular System (MT-MACS) Technique. (A) In a 71-year-old patient with aortic atherosclerosis, bright-blood lumenography, (B) dark-blood (vessel wall imaging), and (C) gray-blood (optimized to detect calcium/calcified nodules) images were acquired. In the thoracic aorta (dashed line), increased aortic wall thickness (4.491 mm) was measured and most conspicuous on the dark-blood (B) and gray-blood (C) images. [These images are re-printed with permission from Zhaoyang Fan, PhD from Magnetic Resonance in Medicine (112).]