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. 2022 Nov 3;22(4):447–458. doi: 10.2463/mrms.rev.2021-0140

Vessel Wall Imaging of Intracranial Arteries: Fundamentals and Clinical Applications

Miho Gomyo 1,*, Kazuhiro Tsuchiya 2, Kenichi Yokoyama 1
PMCID: PMC10552670  PMID: 36328569

Abstract

With the increasing use of 3-tesla MRI scanners and the development of applicable sequences, it has become possible to achieve high-resolution, good contrast imaging, which has enabled the imaging of the walls of small-diameter intracranial arteries. In recent years, the usefulness of vessel wall imaging has been reported for numerous intracranial arterial diseases, such as for the detection of vulnerable plaque in atherosclerosis, diagnosis of cerebral arterial dissection, prediction of the rupture of cerebral aneurysms, and status of moyamoya disease and cerebral vasculitis. In this review, we introduce the histological characteristics of the intracranial artery, discuss intracranial vessel wall imaging methods, and review the findings of vessel wall imaging for various major intracranial arterial diseases.

Keywords: atherosclerosis, dissection, intracranial artery, plaque, vessel wall imaging

Introduction

Stroke is the second leading cause of both morbidity and mortality worldwide.1 Atherosclerotic cerebral infarction is the most common type of ischemic stroke,2 and evaluation of the intracranial artery is essential for stroke prevention and post-treatment progress. Besides atherosclerosis, intracranial arterial diseases include cerebral arterial dissection, cerebral aneurysms, moyamoya disease, and vasculitis. The accurate differentiation and diagnosis of these diseases are essential for appropriate treatment. Conventional techniques for imaging the intracranial arteries include digital subtraction angiography (DSA), which is the gold-standard modality, computed tomography angiography (CTA), and 3D time-of-flight magnetic resonance angiography (3D-TOF MRA). However, these imaging techniques are lumenography, which is used to visualize blood flow in the vascular lumen. Meanwhile, vessel wall imaging (VWI) using MRI is useful to assess the pathophysiology of intracranial arterial diseases because not only the vascular lumen but also the vessel wall can be directly visualized.

In 2017, the American Society of Neuroradiology (ASNR) Vessel Wall Imaging Study Group (VWISG) reported the principles of intracranial VWI, clinical recommendations, and findings of VWI in major intracranial arterial diseases.3 Schaafsma et al. reported that based on the interpretation of the intracranial VWI findings in 205 patients with ischemic stroke according to the ASNR VWISG consensus, the etiology was changed in 55% of patients, that the proportion of patients classified as having intracranial arteriopathy not otherwise specified decreased from 31% to 4%, and that the proportion of patients classified as having intracranial atherosclerosis increased from 23% to 57%.4 Their report suggests that VWI is extremely important for understanding the pathological basis of intracranial arterial diseases and selecting the appropriate treatment. So far, a large amount of literatures on the usefulness of VWI in intracranial arterial diseases have been reported. In this study, we introduce the methods of intracranial VWI, elucidate the histological characteristics of various intracranial arterial diseases, and present VWI findings, including recently reported features.

Vessel Wall Imaging of the Intracranial Artery

In adults, the diameter of the M1 segment of the middle cerebral artery (MCA) and the basilar artery can be up to 3 mm. The walls of these vessels are extremely thin, at 0.2–0.3 mm, i.e., approximately one-tenth of the luminal diameter. Therefore, high spatial resolution and SNR are required to identify abnormalities in the intracranial arterial wall and lumen. Three-tesla (3 T) MRI scanners have higher SNR than 1.5 T scanners and are therefore suitable for VWI of the intracranial artery. In addition, to visualize the intracranial arterial wall, it is necessary to create a contrast between the intracranial arterial wall and the surrounding cerebrospinal fluid. It is also necessary to suppress blood flow signals that visualize the lumen of the artery as black blood (BB). The suppression of blood flow signals is crucial not only to distinguish and identify intracranial arterial walls but also to avoid misdiagnosis of artifacts caused by blood flow as lesions.

2D Vessel Wall Imaging

Intracranial VWI methods include 2D and 3D imaging methods. The fast spin echo method is used for T2-weighted imaging (T2WI) and proton-density weighted imaging (PDWI), and the spin echo method is used for T1-weighted imaging (T1WI). The maximum intensity projection (MIP) images obtained using 3D-TOF MRA are used for positioning, and cross-sectional scanning is performed orthogonally to the long axis of the target intracranial artery. By setting the FOV to 10–13 cm, a high in-plane resolution of 0.25–0.5 mm can be obtained. Usually, a slice thickness of 2 mm is employed. The ASNR VWISG recommends a voxel size of 2.0 × 0.4 × 0.4 mm, which provides a good balance between SNR and spatial resolution.3 2D-VWI is widely used because it can be performed without special sequences, PDWI can clearly depict vessel wall boundaries, and T1WI and T2WI can be used to evaluate plaque characteristics.5 Moreover, due to the high in-plane resolution of 2D-VWI, it is possible to evaluate the vessel wall and the lumen of the intracranial artery in more detail. However, the scanning time of 2D-VWI is generally long, and it usually takes approximately 5 min to scan a range of 2–4 cm; it is therefore not suitable for the evaluation of multiple and widespread intracranial arterial diseases. In addition, it is important to appropriately determine the cross section of the target intracranial artery, for which the double oblique setting is required. The presaturation pulse or double inversion recovery method is commonly used to suppress blood signals. The use of electrocardiogram and pulse wave synchronization is not recommended because the heart rate defines the TR, and the T1 contrast fluctuates depending on the patient’s heart rate.

3D Vessel Wall Imaging

The turbo spin echo (TSE) sequence is used in 3D-VWI. In the conventional TSE method, the refocus flip angle pulse is used at a constant angle; however, a variable flip angle that changes the flip amplitude over time according to the T1 and T2 values of the tissue is advantageous. This method makes it possible to avoid the specific absorption rate limitation with a 3 T MRI scanner. Furthermore, the use of the optimized variable flip angle yields images with good contrast with less influence of blurring (compared with that using the normal 3D-TSE method) in a short time, even if many turbo factors are used. In addition, a strong flow void effect can be obtained using the variable flip angle method because the phase dispersion of blood increases owing to the modulation of the flip angle. In 3D-VWI, data are usually collected from the sagittal section, and a wide area from the main artery to the peripheral artery can be scanned in approximately 7 min. Because 3D-VWI acquires data from 0.5 × 0.5 × 0.5 mm isotropic voxels, it can be reconstructed in any desired section after imaging, and even blood vessels with strong flexion and meandering can be evaluated using curved multi-planar reconstruction. Another advantage of 3D-VWI is the absence of inflow artifacts due to 3D data acquisition and the use of external volume suppression pulses. The following sequences have been issued for 3D-VWI: volumetric isotropic TSE acquisition (VISTA; Philips Healthcare, Best, the Netherlands), sampling perfection with application-optimized contrast using different flip angle evolution (SPACE; Siemens Healthineers, Erlangen, Germany), Cube (GE Healthcare, Wisconsin, USA), and Multi Planar Voxel (MPV; Canon Medical Systems, Tochigi, Japan).

Preparation pulse, such as delay alternating with nutation for tailored excitation (DANTE) or motion-sensitized driven equilibrium (MSDE), may also be used as additional BB imaging techniques.6–9 DANTE suppresses the signal of moving spins in the vessel flow with a series of low flip angle nonselective pulses interleaved with gradient pulses with short TRs. On the other hand, MSDE consists of a series of RF pulses with 90°/180°/− 90° flip angles and motion-sensitization gradients placed symmetrically around the 180° pulse. Moreover, improved MSDE (iMSDE) consists of two 90° excitation pulses and two 180° refocusing pulses with bipolar motion-sensitized and spoiled gradients, resulting in improved SNR and CNR compared with MSDE.10,11 Although these sequences can produce excellent black-blood images, they suffer from decreased vessel wall SNR.8,9

Anatomy of the Intracranial Artery

To understand the VWI findings of intracranial arterial diseases, it is necessary to consider the normal anatomy and pathological findings specific to the intracranial arterial wall. The external elastic plate disappears into the cavernous sinus of the internal carotid artery (ICA) and into the dural penetrating part of the vertebral artery. The intracranial arterial wall consists of the thin adventitia, which is composed of collagen fibers, the media, which is composed of smooth muscle cells, the intima, which possesses numerous micro foramen, and a strong internal elastic plate, which is located immediately below the intima. Because elastic fibers in the media are either absent or extremely thin, nutrition to the media is provided by permeation from the blood through the micropores of the intima and infiltration from the cerebrospinal fluid through the adventitia. Therefore, the intracranial artery does not require vasa vasorum, which are a microvascular network that nourishes the vessel wall in thick medial arteries such as the aorta, and enhancement of the intracranial arterial wall is usually not observed. However, in intracranial arterial diseases, such as arteriosclerosis, dissection, vasculitis, and aneurysm, vasa vasorum is present, which causes contrast enhancement of the intracranial arterial wall.12–14

On the other hand, vasa vasorum extends from the extracranial segments to the intracranial internal carotid arteries and vertebral arteries at the dural penetrating part. Therefore, a mild enhancement may be observed in these sites, even in normal cases.15,16 Moreover, with aging, vasa vasorum appears and extends from the extracranial to the intracranial ICA and vertebral artery and is the cause of peripheral wall thickening and enhancement.15,17 Therefore, care must be taken not to misdiagnose the enhancement of the intracranial arterial wall due to aging as pathological (Fig. 1).

Fig. 1.

Fig. 1

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Arterial wall enhancement due to aging in a 71-year-old woman. CT angiography shows no stenosis in the intracranial artery (a). 3D-T1-weighted VWI also shows no specific wall signal of the vertebral arteries (b). Post-contrast-enhanced 3D-T1-weighted VWI shows the wall enhancement of the bilateral vertebral arteries that continue from the extracranial (arrows in c). VWI, vessel wall imaging.

Atherosclerosis

Atherosclerosis is the most important cause of cerebral infarction. When the endothelial cells of blood vessels are damaged due to hypertension, hyperglycemia, dyslipidemia, etc., the barrier function is lost. Subsequently, low-density lipoprotein (LDL) in the blood enters the intima and is oxidized. The oxidized LDL is taken up by macrophages that have invaded the intima; as a result, cholesterol and fat are accumulated, and activation of the intima results in intimal thickening. Plaques are formed via this process, which are composed of a fibrous cap, lipid core, and inflammatory cells. Cerebral infarction occurs when the lumen of a cerebral artery is narrowed or occluded owing to plaque development or a thrombus that has attached due to plaque rupture. Plaque rupture causes intra-plaque hemorrhage. With the use of VWI, it is possible to evaluate plaque instability or vulnerability, including the plaque’s properties, localization, and remodeling patterns. A systematic review of 21 papers with sample sizes ranging from 15 to 219 reported that, in approximately 50% of patients with acute and subacute ischemic stroke, 3D-TOF MRA did not reveal significant stenotic lesions in the intracranial main arteries, but VWI revealed the causative vulnerable plaque; therefore, the significance of VWI in the diagnosis of intracranial atherosclerosis has been demonstrated.18

Depiction of plaque

Plaques usually show as eccentric wall thickening in VWI. However, plaques with both eccentric and concentric wall thickening on VWI have recently been reported,19,20 and pathologically confirmed.21,22 In a retrospective study of 20 atherosclerotic basilar artery stenoses, a mixture of eccentric and concentric wall thickening was observed in about half of the patients, and symptomatic stenosis was more common in patients with mixed wall thickening compared with those with only eccentric wall thickening (100 vs. 54.5%, P = 0.038).20

T2WI shows the fibrous cap as a hyperintense region on the surface of the plaque in contact with the lumen of blood vessels. The fibrous cap is thicker in stable plaque and thinner in vulnerable plaque due to the decomposition of collagen fibers by inflammatory cells. Plaque possesses a lipid core that accumulates cholesterol and fat, and vulnerable plaque becomes lipid rich. The lipid core shows low or iso-intensity on T1WI and T2WI, which is different from the signal intensity of subcutaneous and visceral fats. This is because the main component of plaque is cholesterol, whereas subcutaneous and visceral fats are primarily composed of triglycerides.23

Plaque thickness and surface properties

It has been reported that symptomatic plaques are significantly thicker than asymptomatic plaques24 and that the surface of symptomatic plaques is irregular and discontinuous.25 A comparative study of 14 symptomatic stenoses and 16 asymptomatic stenoses of the MCA found the irregularity of plaque surface in 71% of symptomatic stenoses but only in 19% of asymptomatic stenoses (P = 0.008).25

Plaque localization

In the coronary artery, plaque is usually located on the opposite side of the branch’s origin. The lateral lenticulostriate arteries, which are the penetrating arteries of the MCA, often branch from the upper and posterior wall of the M1 segment. In a study of 40 symptomatic stenoses and 52 asymptomatic stenoses of the MCA, plaque localization was found to be significantly higher in the anterior wall (44.8%) and inferior wall (31.7%) than in the upper wall (14.3%) and posterior wall (9.0%), where the penetrating arteries originated (P < 0.001). Plaques are significantly more often located on the upper wall in symptomatic stenosis than in asymptomatic stenosis (P = 0.016). In a previous study, the group with symptomatic stenosis with penetrating artery infarction had more superior (P = 0.001) but fewer posterior (P = 0.038) and inferior (P = 0.024) plaques than those without penetrating artery infarctions.26 This indicates that plaque localization is associated with symptomatic stenosis and perforator infarction (Fig. 2).

Fig. 2.

Fig. 2

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VWI to distinguish between symptomatic and asymptomatic intracranial atherosclerotic plaques in a 73-year-old man with acute infarction of the left basal ganglia. 3D time-of-flight MR angiography demonstrated mild stenosis at the proximal M1 of the left middle cerebral artery (arrowhead in a) and the LSA arising from the left distal M1 (arrow in a). Sagittal oblique VWI was obtained in orthogonal cross section for the left M1. In the VWI at the proximal left M1 stenosis, T1-weighted VWI showed eccentric isointense arterial wall thickening (arrow in b) and T2-weighted VWI showed hyperintensity on the luminal side of the wall thickening (arrow in c) and a hypointense margin (dotted arrow in c), consistent with the thick fibrous cap and lipid core of atherosclerotic plaque. The thick fibrous cap showed mild enhancement in contrast-enhanced T1-weighted VWI (arrow in d). T1-weighted VWI of the distal M1 arising from the LSA branches revealed a plaque extending from the superior to the posterior wall (arrow in e) with strong enhancement (arrow in f) and without a T2-hyperintense thick fibrous cap (g). Therefore, this plaque was considered the cause of acute infarction in the left basal ganglia. Arterial wall thickening without luminal narrowing is known as positive remodeling. LSA, lenticulostriate artery; VWI, vessel wall imaging.

Remodeling pattern

Although the method of evaluating the remodeling pattern slightly differs among studies, when the area of the minor axis cross section of the stenotic site is larger than that of the normal artery, this is defined as positive remodeling, and when it is smaller, it is defined as negative remodeling.27 In positive remodeling, the diameter of blood vessels expands outward due to plaque growth. Such plaque is lipid rich, and the fibrous cap is thin and prone to rupture. There is a significant correlation between positive remodeling and ischemia in the coronary arteries.28 Furthermore, positive remodeling is common in symptomatic plaques in the intracranial artery.24,25 In a study of 137 plaques identified in 42 patients, larger unstable plaques and positive remodeling were observed more in posterior circulation plaques compared with anterior circulation plaques.27 Because positive remodeling involves mild or no stenosis, it is useful to evaluate the lumen using VWI. Conversely, in negative remodeling, the vessel diameter becomes narrow. Negative remodeling reflects the fibrous response and is common in asymptomatic plaques (Fig. 2).29

Intra-plaque hemorrhage and plaque enhancement

As arteriosclerosis progresses, the vasa vasorum of the intracranial artery develop from the proximal side to the distal side and sometimes develops in the distal part independently, transporting inflammatory cells to the plaque and playing an important role in its development.16,30 However, many vasa vasorum are immature and incomplete, which results in intra-plaque hemorrhage and plaque enhancement.31,32

In a study of 109 cases of MCA stenosis (46 symptomatic and 63 asymptomatic), intra-plaque hemorrhage was observed in 19.6% of symptomatic cases but in only 3.2% of asymptomatic cases, and the difference was statistically significant (P = 0.01).33 However, intra-plaque hemorrhage is less common in the intracranial artery than in the extracranial artery, and vulnerable plaque cannot be ruled out even without the presence of intra-plaque hemorrhage.34,35 The criteria for determining the signal of intra-plaque hemorrhage differ in the literature, and there are reports that the signal is higher than that of the cranial muscle and that the signal is at least 1.5 times higher than that of the adjacent gray matter.33,36

Plaque enhancement is frequently found in the fibrous cap and adventitia. In autopsy cases, neovascularization in the plaque of the MCA has been found to be correlated with ipsilateral infarction.35 A systematic review of 330 cases reported a significant correlation between plaque enhancement and cerebral infarction.37 In another systematic review and meta-analysis of 20 reports of intracranial VWI with sample sizes of ≥ 10 (1126 patients, 1233 intracranial stenotic lesions), plaque enhancement, positive remodeling, and plaque surface irregularities were significantly associated with cerebral infarction. In particular, plaque enhancement was reported to be the most reliable indicator of vulnerable plaque.38 The extent of plaque enhancement is correlated with clinical signs; in a study of 20 cases of acute cerebral infarction, strong enhancement equal to or greater than that of the pituitary stalk was observed only in the responsible plaque, and non-responsible plaque had no or weak enhancement (Fig. 2).39 Plaque enhancement is extensive within 1 month after the onset of cerebral infarction and diminishes after several months.40 However, a study of 55 plaque enhancements in 14 patients with cerebral infarction reported that the responsible plaque enhancement persisted, whereas the non-responsible plaque enhancement was diminished at a median follow-up period of 140 days. Both the degree and persistence of plaque enhancement at follow-up can be diagnostic markers for identifying vulnerable plaques, as well as the future risk of stroke recurrence.41

The usefulness of dynamic contrast-enhanced (DCE) perfusion as a method to quantitatively evaluate the effect of plaque enhancement has been demonstrated.42 DCE perfusion is a perfusion imaging method that necessitates the use of a contrast medium. Various parameters can be analyzed using software; among them, Ktrans corresponds to the constant of transfer speed from the plasma to the extracellular matrix and is used as an index of permeability. In a study that investigated carotid plaque, Ktrans was correlated with macrophage infiltration (inflammation) and neovascularization,43–45 which were reduced by hyperlipidemia treatment.45 A study that investigated the correlation between the number of days since the onset of cerebral infarction in 10 patients with intracranial arteriosclerosis and Ktrans reported that Ktrans showed a higher correlation than plaque enhancement and intra-plaque hyperintensity; therefore, Ktrans has potential to serve as a biomarker of plaque activity (Fig. 3).42

Fig. 3.

Fig. 3

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Assessment of intracranial atherosclerotic plaque activity using dynamic contrast-enhanced MR perfusion in a 68-year-old man with acute infarction of the right temporal lobe. Diffusion-weighted imaging showed an acute infarction in the right temporal lobe in the right middle cerebral artery territory (arrow in a). Sagittal-oblique contrast-enhanced T1-weighted VWI of the right M1 showed homogeneous enhanced plaque at the posterior wall (arrow in b). The Ktrans map of the right M1 obtained using dynamic contrast-enhanced MR perfusion revealed that the interior of the enhanced plaque was heterogeneous, and the upper part of the plaque showed the highest value (arrow in c), which is considered to indicate the activity of the plaque. VWI, vessel wall imaging.

Vasculitis

Vasculitis is usually classified by the Chapel Hill Consensus Conference classification (2012) and is broadly divided into primary and secondary vasculitis. Primary vasculitis is classified into single-organ-vessel and systemic, and systemic vasculitis is further classified into four types according to the size of the affected blood vessels. Although primary central nervous system (CNS) vasculitis is a single-organ vasculitis of unknown cause, the causes and symptoms of vasculitis in the CNS are variable, and a biopsy may be required for the final diagnosis. In CNS vasculitis, lumenography reveals focal or multiple stenoses, whereas VWI shows smooth, uniform, concentric thickening, and enhancement of the vessel wall, which suggests that the stenosis may be caused by vasculitis. However, it has been reported that among 13 cases of CNS vasculitis, 3 cases exhibited eccentric wall thickening and enhancement.46 Therefore, the differentiation from atherosclerosis requires comprehensive evaluation combined with other findings, such as age, course, underlying disease, and laboratory data. In vasculitis, the arterial wall shows hyperintensity in T2WI, reflecting inflammation and edema of the arterial wall. This was found in 94% of clinically active patients but was also confirmed in 56% of non-clinically active patients, revealing a discrepancy between the findings of VWI and clinical activity.47 However, histopathological findings confirmed active vasculitis in 44% of patients with no clinical activity,48 which suggests that VWI may more accurately reflect the pathology. The vessel wall enhancement of vasculitis is considered to be a result of the increase in permeability of endothelial cells and the leakage of contrast medium into the arterial wall by the vasa vasorum that is present on the side of the adventitia. Vessel wall enhancement is more pronounced in clinically active patients, and it is helpful when determining the biopsy site. However, when steroid treatment was administered, the ability to detect the vessel wall enhancement decreased after 2 days.49 Therefore, when diagnosing vasculitis using VWI, it is necessary to perform VWI before or immediately after the start of steroid treatment (Fig. 4).

Fig. 4.

Fig. 4

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Vasculitis and changes after steroid treatment using VWI in a 62-year-old woman. The top row shows MR images before treatment and the bottom row shows MR images after treatment. 3D time-of-flight magnetic resonance angiography revealed a severe stenosis at the end of the left internal carotid artery (arrow in a). Axial vessel wall imaging at the severe stenosis of the left internal carotid artery showed concentric wall thickening with strong enhancement (arrows in b and c). After steroid treatment for severe stenosis, the findings were improved (arrows in d, e, and f). VWI, vessel wall imaging.

Radiation-induced Vasculitis

Radiation-induced vasculitis is caused by radiation injury and is indicated by peripheral wall thickening and enhancement.50 If there is a history of radiation therapy, including the lesions of vasculitis, it is less likely to be missed in diagnosis. It has been reported that the vessel wall enhancement persists even after several years.

Reversible Cerebral Vasoconstriction

Reversible cerebral vasoconstriction (RCVS) develops with a strong headache, known as a thunderclap headache, accompanied by multiple reversible cerebral vasoconstrictions. Vasospasm causes shortening and folding of smooth muscle cells, resulting in circumferential wall thickening.51,52 However, histologically, it has been proved that there is no inflammation in the arterial wall, and unlike in vasculitis, wall enhancement is mild or absent.52,53 Both RCVS and vasculitis frequently cause vascular stenosis. RCVS is treated via follow-up examination or with calcium channel blockers, whereas vasculitis is treated with steroids or immunosuppressants. Therefore, early differentiation between the two diseases is important for determining the treatment policy. As both RCVS and vasculitis cause circumferential vessel wall thickening, the presence or absence of vessel wall enhancement on VWI is useful for their differentiation.

Moyamoya Disease

Moyamoya disease causes stenosis or occlusion of unknown cause in the terminal ICA, proximal MCA, and proximal anterior cerebral artery, resulting in the formation of an abnormal vascular network. Moyamoya disease is categorized into the bilateral and unilateral types. Endometrial hyperplasia and medial thinning result in reduced vessel diameter, circumferential wall thickening, and afferent luminal stenosis.54–56 A previous study on wall thickening and outer diameter of the MCA according to the stage of moyamoya disease by 3D-TOF MRA reported that there was no significant difference in wall thickening depending on the stage but that the outer diameter was significantly smaller in stage 3 and 4 than in stage 1.55 Another study reported that moyamoya disease creates vessel wall enhancement regardless of whether it is symptomatic or asymptomatic.54 Conversely, a study of 47 cases of moyamoya disease, including 25 cases of acute cerebral infarction, reported that vessel wall enhancement equal to or stronger than that of the pituitary stalk was present in 76.5% of patients with ischemia, and enhancement was present in 23.5% of patients without ischemia, indicating that strong vessel wall enhancement was observed in many cases with ischemia.57 Unilateral moyamoya disease is occasionally difficult to distinguish from atherosclerosis, but moyamoya disease is known as vanishing MCA, which makes it impossible to identify the MCA because the blood vessels shrink afferently.58 This is inconsistent with the negative remodeling of atherosclerosis (Fig. 5).

Fig. 5.

Fig. 5

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Moyamoya disease in a 35-year-old man. 3D time-of-flight MR angiography revealed occlusion at the terminus of the right internal carotid artery (arrow in a). The diameter of the right M1 was small, so the trunk MCA was not visible in the sylvian fissure on coronal VWI (vanishing MCA) (circle in b). MCA, middle cerebral artery; VWI, vessel wall imaging.

Cerebral Arterial Dissection

Arterial dissection is a disease in which a dissected cavity is formed by blood flow into the arterial wall through a tear in the intima. In subintimal dissection, in which a dissected cavity is formed between the intima and media, a luminal stenosis or obstruction is caused by a false lumen that bulges toward the true lumen. In subadventitial dissection, a dissected cavity is formed between the adventitia and the media, and an aneurysm is formed by a false lumen that bulges outward.

In VWI, when the dissected cavity is patent, both the true and false lumens are visualized as BB, and an intimal flap can be observed between them. Conversely, if the dissected cavity is thrombotic, an intramural hematoma is visualized (Fig. 6). Intramural hematomas become hyperintense within a few days to 2 months on T1WI, and the signal intensity changes with time.59–61 However, intramural hematomas may not be hyperintense depending on the status of the obstruction of the false lumen. If the intramural hematoma is formed by a slight dissection before onset, high signal intensity may be observed on VWI on the day of onset. In 27 cases of vertebral arterial dissection, Hashimoto et al.62 reported that the spontaneous cure rate was 100% in cases in which the signal of intramural hematoma changed over time, but that in cases without signal change, the spontaneous cure rate was only 23%, and the difference was statistically significant. In this report, the relative signal intensity (RSI) of intramural hematoma against the posterior cervical muscle on T1WI VWI was calculated, and the ratio of chronological RSI was calculated using both the maximum RSI (RSI max) and minimum RSI (RSI min) during the follow-up. The RSI max was 2.5 ± 0.79 in the group with time-dependent changes and 1.1 ± 0.20 in the group without changes. The spontaneous cure rate was significantly higher in cases with changes compared with that of without chronological RSI changes (RSI max/min ≥ 1.48). It has been suggested that hyperintense intramural hematoma may be useful not only for diagnosing dissection but also for predicting spontaneous healing. In addition, in cases of subadventitial dissection in which the false lumen is occluded, it may not be possible to visualize the stenosis of the true lumen by lumenography, and a VWI method that can directly visualize the vascular lumen is useful for diagnosis.

Fig. 6.

Fig. 6

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VWI to evaluate the arterial lumen in a 53-year-old woman with dissecting aneurysm of the bilateral vertebral arteries. 3D time-of-flight MR angiography revealed a fusiform aneurysm of the bilateral vertebral arteries (arrows in a). The curved multi-planar reconstruction of the right vertebral artery obtained using T1-weighted VWI revealed a hyperintense intramural hematoma of the false lumen (arrows in b) and stenosis of the true lumen. Moreover, the axial T1-weighted VWI revealed that intramural hematoma was located at the opposite site of the origin of the right PICA, which did not extend to the PICA (arrow in c). Oblique axial T1-weighted VWI of the left fusiform vertebral aneurysm showed the intimal flap as unclear (d). Post-contrast-enhanced T1-weighted VWI revealed enhancement of both the fusiform aneurysmal wall (arrowhead in e) and the intimal flap (arrow in e), and showed that both true and false lumens were patent. PICA, posterior inferior cerebellar artery; VWI, vessel wall imaging.

Post-contrast VWI can be useful for the diagnosis of dissection as it enhances the vessel wall and intimal flap of the dissected artery (Fig. 6). The mechanism of enhancement of the dissected vessel wall is not completely clear, but it is speculated to result from inflammation and vasa vasorum formation.63,64 However, it is not uncommon for vertebral arteries to develop arterial wall enhancement with aging. Therefore, care must be taken in interpreting vessel wall enhancement, such as confirming its presence or absence on the opposite side without dissection.

Cerebral Aneurysm

It has been shown that chronic inflammation of the arterial wall due to the load of blood flow stress is involved in the development and rupture of cerebral aneurysms. During the early stages of aneurysm development, fragmentation and disappearance of the internal elastic plate and endothelial cell damage occur. Inflammatory changes due to macrophages and cytokines are induced in the arterial wall, and, as a result of progressive degeneration, the aneurysmal wall becomes thin and weak, resulting in an increase in their size or rupture.65 The development and neovascularization of vasa vasorum due to inflammation of the aneurysmal wall can cause aneurysmal wall enhancement, but the coexistence of inflammatory cell infiltration, neovascularization, and vasa vasorum of the enhanced aneurysmal wall are not always observed. In addition, some aneurysms have only vasa vasorum, and the causes of aneurysmal wall enhancement differ among cases.66 There are many reports on the enhancement of the aneurysmal wall, and enhancement is reported to be useful for predicting aneurysm rupture and identifying ruptured aneurysms among multiple cerebral aneurysms (Fig.7).67,68 However, some unruptured cerebral aneurysms also show wall enhancement, indicating that cerebral aneurysms with wall enhancement may not necessarily rupture. In an examination of 248 cases of asymptomatic unruptured aneurysmal wall enhancement, 78 cases (31.5%) exhibited wall enhancement (localized: 34, circumferential: 44). Aneurysms with wall enhancement have an estimated 5-year rupture risk that is more than three times higher than that of aneurysms without wall enhancement. Aneurysms with strong and widespread wall enhancement exhibit a positive correlation with an estimated 5-year rupture risk and an estimated 3- to 5-year growth risk. Therefore, it is advisable to consider the risk of rupture in an aneurysm with wall enhancement.69

Fig. 7.

Fig. 7

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VWI to identify a ruptured aneurysm among multiple cerebral aneurysms with subarachnoid hemorrhage in a 54-year-old woman. 3D time-of-flight MR angiography revealed saccular aneurysms at the anterior communicating artery and the left vertebral artery (arrows in a). Coronal post-contrast-enhanced T1-weighted VWI revealed wall enhancement in the left vertebral aneurysm (arrow in b), but enhancement was not observed in the anterior communicating artery aneurysm (arrow in c). Coil embolization was performed on the left vertebral artery aneurysm, and hemostasis was restored. VWI, vessel wall imaging.

A study of DCE perfusion of 29 unruptured cerebral aneurysms reported that the Ktrans in the aneurysmal wall was higher than that in the normal arterial wall and that Ktrans was correlated with the aneurysm size and PHASES score.70 One of the two cases of aneurysms that ruptured during follow-up did not exhibit wall enhancement, but the Ktrans of the aneurysmal wall was significantly higher than that of the other aneurysmal walls. Therefore, the Ktrans shows potential as a new biomarker for the risk of aneurysm rupture.70 However, as discussed in this report, some ruptured aneurysms do not exhibit wall enhancement, and the risk of aneurysm rupture and the reliable visualization of ruptured aneurysms remain controversial.

In an aneurysm phantom study, Cornelissen et al.71 reported that that signals generated from slow flow along the aneurysm wall were observed on 3D-TSE VWI and become more clearly after injecting the contrast agent. Gadolinium shortens the T1 relaxation time of blood, resulting in decreased blood suppression on VWI decreases after injecting the contrast material. Insufficient blood suppression can make mistaken for wall enhancement. In this report, the lower velocities near the aneurysm wall showed a pseudo-wall enhancement, suggesting that the wall enhancement of unstable aneurysms may be related to slow flow in addition to inflammation of the aneurysm wall. The aneurysm wall-mimicking enhancement can be improved by sufficient slow-flow suppression using MSDE and DANTE pulses. MSDE and DANTE sequences also suppress flow artifacts in aneurysms and are useful for assessing the presence or absence of thrombi in giant aneurysms (Fig. 8).72

Fig. 8.

Fig. 8

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Suppression of flow artifacts within aneurysm using preparation pulse (MSDE). 3D time-of-flight MR angiography revealed a fusiform aneurysm of the basilar artery (arrow in a). The axial image of CT angiography shows homogeneous enhancement in the lumen of the basilar artery aneurysm (arrow in b). 3D-T1-weighted VWI shows an isointense signal in the aneurysm (arrow in c). Post-contrast-enhanced 3D-T1-weighted VWI shows wall enhancement (dotted arrow in d) and enhancement within the aneurysm (arrow in d). The combined use of MSDE suppressed the signal within the aneurysm and showed no artifactual enhancement within the aneurysm (e). MSDE, motion-sensitized driven equilibrium; VWI, vessel wall imaging.

Visualization of the Stented Artery Lumen

Stent-assisted endovascular treatment is often used for the transcatheter embolization of wide-necked aneurysms using the neck-remodeling technique or anatomically difficult for clipping. As stents are known to cause intimal hyperplasia and thrombi, evaluation of the stented artery is important. However, DSA and CTA are invasive and, because they necessitate the use of contrast media, there is a risk of contrast media nephropathy and side effects. As 3D-VWI using a variable flip angle is a spin echo-based sequence, it is less affected by the magnetic susceptibility artifact produced by the stent, thrombi in the stent can be visualized,73 and the diameter of the stented artery can be evaluated more accurately.74 In addition, by postprocessing via partial minimum intensity projection (MinIP) in the source data of 3D-VWI to create a BB-MRA, it becomes easier to visually evaluate the stent lumen, as can be seen in MIP images of 3D-TOF MRA.74

Summary

In this review, we have introduced VWI methods and have described the anatomical characteristics of the intracranial artery and the findings of VWI in various cerebral arterial diseases. Because VWI can be used to directly visualize the vascular lumen and vessel wall, it is an imaging method that is useful for the assessment of the pathophysiology of intracranial arterial diseases and can contribute to the investigation of the cause of stroke. However, it is difficult to obtain histopathological specimens of the intracranial arterial wall, and it is difficult to compare the findings of VWI with pathological findings. For this reason, the signal changes and enhancement of the arterial wall have not been fully revealed, but many studies using intracranial VWI have been reported in recent years, and further elucidation of pathological conditions is expected in the future.

This work was presented as an educational lecture at the 48th annual meeting of the Japanese Society for Magnetic Resonance in Medicine (EL4-2). The content is solely the responsibility of the authors and does not necessarily represent the social views of Magnetic Resonance in Medical Sciences.

Footnotes

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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