Advances in differential diagnosis of cerebrovascular diseases in magnetic resonance imaging: a narrative review

Introduction

Cerebrovascular diseases (CVDs) include any disorders temporarily or permanently disturbing a brain area due to alterations in blood flow and/or blood vessels. CVDs involve pathological alterations in blood vessels of the brain and typically manifest in cerebral stroke. Cerebral stroke is a primary cause of disability and death worldwide and occurs at main branches of the cerebral arteries, basilar arteries, their associated small vessels and corresponding veins (1). Its differential diagnosis can be difficulty, particularly when it involves small vessel and complications with other CVDs (2,3). Moreover, there are many brain diseases not primarily involving cerebral vessels but presenting physical and mental symptoms similar to that of the stroke, such as hyponatremia, multiple sclerosis and brain tumors. Differential diagnosis of strokes from these secondary CVDs is essential to guide therapeutic decisions and predict the prognosis. Alongside clinical presentation and laboratory tests, neuroimaging techniques have become prevailing tools in differential diagnosis of CVDs. Magnetic resonance imaging (MRI), originally named nuclear magnetic resonance, excels other neuroimaging techniques by its features of non-invasive, diverse models/sequences and high spatiotemporal resolution and thus, becomes a powerful tool in differential diagnosis of a variety of CVDs (2,4). Previously, many excellent reviews of neuroimaging have been published. They focus on either general imaging techniques of ischemic CVDs (5,6) or a specific MRI sequence like vessel wall MRI (2,3) and multiparametric quantitative MRI (7). However, a comprehensive overview of MRI sequences and their administration in differentiation of cerebral stroke from other neurological diseases remains to be presented. This review aims to provide neurologists, neurosurgeons and radiologists with an up-to-date overview of MRI knowledge and its administration for differential diagnosis of CVDs. We present the following article in accordance with the Narrative Review reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-22-750/rc).

Methods

Studies including CVDs in MRI published over the last 10 years, including 109/141 (77.3%) published after 2020, were identified via a PubMed search using different combinations of the following search terms: “cerebrovascular diseases”, “differential diagnosis”, “magnetic resonance imaging”, “neuroimaging”, “cerebral stroke” and others as presented in Table 1. Additional papers were identified by reviewing reference lists of relevant publications. Publications with relative low credibility and non-English publications were excluded. Data were extracted based on their relevance to the topic instead of implementing a systematic approach to paper selection. More details of the method are shown in Table 2.

Overview of MRI in diagnosis of CVDs

Neuroimaging techniques include cerebral angiography, ultrasound, computed tomography (CT) scan, and positron emission tomography (PET) as well as MRI and many others. Compared to CT scans, MRIs are more effective at exposing subtle differences between soft tissues, nerves and blood vessels. Using MRI can detect flowing blood and puzzling vascular malformations as well as demyelination disease without beam-hardening artifacts and any ionizing radiation (8,9). Compared to PET, MRI completes one scan faster with a temporal resolution of ~3 seconds (9-11). These advantages make MRI tests the leading neuroimaging techniques in differential diagnosis of CVDs.

Mechanisms underlying MRIs

MRI is a non-ionizing and non-invasive technique based on the phenomenon of nuclear magnetic resonance. It usually uses a high frequency (200 MHz to 2 GHz) of electromagnetic radiation and large magnetic fields of 1–7 tesla (T). MRI applies external magnetic field to line up protons’ axes of the tissue under examination and this alignment or magnetization makes atomic nuclei in water aligned with the axis of the MRI scanner, leading to emission of detectable signals after a period of time. Two different relaxation times (i.e., T1 and T2) are commonly applied to characterize tissue magnetization. T1 is the time constant measuring the returning rate of excited protons to equilibrium status longitudinal to the main field. T2 or traverse relaxation time determines the time consumed for removing phase consistency of spinning protons among the nuclei.

Alongside detection of water movement, the MRI also measures other signals. MRI can detect the amount of brain deoxygenated blood that gives off a Blood-Oxygen-Level Dependent (BOLD) signal. The BOLD signal can be transformed into voxels that manifest as a 3 dimensional (3D) image of the brain for tracking neural activity. That is, increased neural activity can increase blood flow as well as oxygen consumption, which causes increase in deoxygenated blood and emits more BOLD signals. The strength of this technique is having good spatial resolution of 1 mm that is far beyond the resolution of other imaging techniques. Correspondingly, BOLD-based MRI is particularly useful in determining prior mini-strokes (11,12).

Detecting changes in levels of choline, lactate, myo-inositol, N-acetyl aspartate, myelin in tissues is also an important mechanism of MRI. This is achieved by magnetic resonance spectroscopic imaging (MRSI). MRSI is a molecular imaging technique that can noninvasively map metabolite distributions without labeling, and serves as biomarkers for tumor characterization in the brain (13,14). Spectroscopic imaging with MRSI can distinguish vascular from parenchymal disorders and to discern primary from secondary disease manifestations for abnormalities in cerebral blood flow. Fast MRSI of the brain is an alternative approach to shorten scanning time and thus makes MRSI more suitable for clinical application in diagnosis of neurology, multiple sclerosis, stroke and epilepsy (13,15,16). For example, myelin is an important component of the brain tissue and sensitive to multi-exponential T2 relaxation. Thus, it is useful in detecting myelin water imaging. By contrast, iron is present in multiple types of brain cells, particularly in cells involving ferroptosis-associated neurodegeneration. Similar to myelin, iron also decreases T2 signals. Combining T1 and T2 relaxometry for iron and myelin can detect the characterization of tissue alterations, recognize diverse quality in the nature of white matter hyperintensities, and implicate different pathophysiology across brain regions. Applying these techniques revealed that increase in iron deposition in cerebral small vessel disease (cSVD) is related to disability and increased local blood-brain barrier (BBB) permeability (17-19).

The contrast and brightness of cerebral imaging are correlated with the intensity of MRI and can be enhanced by using contrast agents. High-resolution images can be obtained by applying 1.5T and 7T MRIs. For instance, 7T MRI provides enhanced details in cortical imaging ≤1 millimeter of tissue, and reduces blurring between gray and white matter. Thus, 7T MRI can display detailed characteristics of the small vessels that are invisible in a conventional 3T MRI. Using 7T MRI can detect early pathological alterations in small vessels and thus guide evaluation of treatment effects on vascular functions at early stage (17,20,21). Moreover, by administration of a gadolinium-based contrast agent, dynamic contrast-enhanced (DCE)-MRI can detect permeability and fluid volume fractions of blood vessels in cSVD, which overcomes the limitation of conventional MRI that is difficult to detect increase in BBB permeability (21,22).

Sequences and applications of MRIs in diagnosis of CVDs

MRIs are a continuously developing technology that evolves upon the challenges of clinical demands for high resolution and fast reports of the test. MRIs can be used in many different models/sequences and in combination with other imaging techniques.

Basic sequences of MRIs

In MRI sequences, T1-weighted and T2-weighted scans are the most commonly used. T1-weighted images (Figure 1A) can highlight fat tissue within the body by use of short “time to echo” alongside “repetition time”. T1 properties of tissues are the dominant factor determining the contrast and brightness of an image. By contrast, T2-weighted image (Figure 1B) can highlight fat and water within the body by use of longer time to echo and repetition time. These features allow MRI test to identify atherosclerosis and hemodynamic alterations. In addition, proton-density changes and subsequent signal enhancement by water protons in extravascular space can reflect cellular swelling in prefrontal cortex and other tissues interfacing air and/or bone or close to large blood vessels (23,30).

Figure 1 Basic MRI sequences. (A) T1-weighted-weighted scans. (B) T2-weighted scans. (C) DWI. (A-C). MRI from patient with acute ischemic stroke [reprinted with permission from Lin et al. (23)]. (D) SWI. Some small vessels are marked in red arrows, the red nucleus is marked in yellow arrows, the skull and extracranial lipid are marked in green arrows [reprinted with permission from Qiu et al. (24)]. (E) DCE-MRI. Images of the fast (during contrast) DCE-MRI part at the highest contrast agent concentration (a), and first dynamic phase of the slow (postcontrast) DCE-MRI part after contrast agent arrival (b). The smaller brain area (yellow border lines), planned through the superior sagittal sinus, is acquired for the fast (during contrast) part to obtain shorter dynamic scan intervals [reprinted with permission from de Canjels et al. (21)]. (F) CVR. Brain regions showing significant effects of clinical composite score 1 on the BOLD signal change from the acute to subacute phase of injury [reprinted with permission from Churchill et al. (25)]. The scales are bootstrap ratio. (G) MRA. Time of flight-MRA showing stenotic lesions in the terminal part of internal left carotid, middle and anterior left cerebral arteries (red arrows) in a patient presenting with a secondary central nervous system angiitis in the context of systemic lupus erythematosus [reprinted with permission from Ferlini et al. (26)]. (H) 4D flow MRI. Blood flow is measured in P1 and P2 segments of the posterior cerebral artery [4, 5], and the posterior communicating arteries [6] [reprinted with permission from Malm et al. (27)]. (I) T2/FLAIR. In an axial F section, lower intensity values with a greater degree of myelination [reprinted with permission from Ganzetti et al. (28)]. (J) IVW-MRI. Image shows multiple areas of concentric contrast enhancement in the proximal left and distal right of the middle cerebral arteries (arrows) in a patient presenting with primary angiitis of the central nervous system [reprinted with permission from Ferlini et al. (26)]. (K) ASL-MRI. Interictal ASL shows ipsilateral hypoperfusion in the temporal neocortex (arrows) and in the medial temporal lobe (arrowhead) [reprinted with permission from Sone et al. (29)]. (L) APTw-MRI. Image is from a patient with acute ischemic stroke [reprinted with permission from Lin et al. (23)]. MRI, magnetic resonance imaging; DWI, diffusion-weighted imaging; SWI, susceptibility-weighted imaging; DCE, dynamic contrast-enhanced; CVR, cerebrovascular reactivity; BOLD, blood-oxygen-level dependent; MRA, magnetic resonance angiogram; 4D flow MRI, four-dimensional flow magnetic resonance imaging; FLAIR, fluid-attenuated inversion recovery; IVW, intracranial vessel wall; ASL, arterial spin labeling; APTw, amide-proton-transfer weighted.

Diffusion-weighted imaging (DWI)

DWI measures water molecule diffusion in tissues (Figure 1C). As diffusing water interacts with many different obstacles throughout biological tissues, DWI can demonstrate the details of tissue architecture and quantify changes in hemodynamic. For fibrous internal structures like axons in white matter, early tissue alterations that are not detectable in conventional imaging can be quickly captured by diffusion tensor imaging. In these tissues, water diffuses faster along the axons or blood vessels than in the direction perpendicular to it. This feature is helpful in determining fractional anisotropy that has different value when measured in different direction, connectivity and other characteristics of the tissue. Thus, DWI can help reconstruct structural brain networks that excels functional network analysis for cSVD at resting condition (24,31,32).

In association with DWI, apparent diffusion coefficient (ADC) measures the average size and size distribution of alveoli and acinar airspaces and can quantify restriction of water diffusion. Calculating DWI/ADC ratio can provide optimized information about cell count, proliferation markers and other histological architecture of tissues (33,34).

Susceptibility-weighted imaging (SWI)

SWI, originally named BOLD venographic imaging, is developing from simple 2D to 3D T2-weighted sequences having better spatial resolution and contrast of susceptibility (Figure 1D). It is particularly sensitive to compounds with paramagnetic, diamagnetic, and ferromagnetic properties, which can identify deoxyhemoglobin, ferritin, hemosiderin, calcium and some other blood products. SWI has the advantage of phase and magnitude and can reveal small amounts of hemorrhage or calcium. It is also used for assessing veins as deoxyhemoglobin causes losing magnitude and shifting the phase (35).

DCE-MRI

DCE-MRI can measure perfusion, fluid volume fractions, vessel permeability, and other microvascular parameters quantitatively. DCE-MRI can measure small changes in BBB permeability in serial T1-weighted scanning through ~25 min after using a gadolinium-based contrast agent. Through measuring the delivery rate of contrast agent to the extravascular space and its levels, DCE-MRI can demonstrate increases in BBB permeability in cSVD (Figure 1E). In addition, DCE-MRI test is very useful in prognosis and individualized management of CVDs, such as cSVD-related stroke, vascular cognitive impairment and diseases involving white matter that all change BBB permeability (21,22).

Cerebrovascular reactivity (CVR)

This MRI measurement probes cerebral hemodynamic changes following vasodilatory stimulus. Using carbon dioxide inhalation and BOLD, CVR mapping has high sensitivity and spatial resolution through simple processing, and thus can provide a better approach to detect CVDs. CVR can measure the initial BBB leakage and subsequent stiffness, which is a key to understanding the pathogenesis of stroke, cSVD and dementias. Baseline CVR may predict progress of subsequent cSVD, drug response and individualize medications. Lower CVR is related to cognitive impairment that is caused by worsened white matter hyperintensity, as shown in patients of minor stroke (Figure 1F). Assessment of CVR with BOLD MRI can yield excellent spatial resolution while having fine repeatability, reproducibility and tolerability. By administering higher field strength to increase BOLD signals, CVR imaging may yield larger and more weighted images for cSVD (25,36,37).

Magnetic resonance angiogram (MRA)

MRA can evaluate blood flow of the carotid arteries, vertebral arteries, basilar artery and branches of these vessels as well as venous sinuses in CVDs. MRA is usually performed on patients whose head and neck surgery are expected. MRA can specifically examine blood vessels and help discover blockage and aneurysms (17). Time-of-flight MRA (Figure 1G) is the dominant non-contrast bright-blood method in grading residual aneurysm, and has been introduced for imaging human vascular system, and differential subsampling with an ultrafast high-spatial-resolution head MRA (26,38,39).

Four-dimensional flow MRI (4D flow MRI)

It is a multi-modality approach using phase-contrast MRI to enhance assessments of blood flow and hemodynamic analysis in cerebral aneurysms and other CVDs. It uses a collection of high-resolution velocity fields to reconstruct the flow field (Figure 1H), which increases the spatial resolution and velocity accuracy in synthesizing MRI data, and thus provides reliable evaluation of pressure and wall shear stress in cerebral aneurisms while providing volumetric and time-resolved visualization and quantification of blood flow (27,40-42).

T2/Fluid-attenuated inversion recovery (FLAIR)

FLAIR is an inversion recovery set of MRI sequence that suppresses the intensity of fluids like cerebrospinal fluid (CSF) but highlights areas of tissue T2 prolongation, and exposes lesions adjacent to CSF clearly, such as cerebral cortical regions. Thus, FLAIR can avoid influences of CSF on detection of the periventricular hyperintense lesions (Figure 1I). In an axial F section, lower intensity values with a greater degree of myelination in the FLAIR technique (28). In T1 C+ image, peri-tumoral edema appears in ring enhancement hyperintense pattern in FLAIR image (15,16).

Intracranial vessel wall (IVW)-MRI

IVW-MRI can detect MRI signal of the thinner artery wall (relative to luminal diameter) and its thickening in vessel wall disease while suppressing the MRI signal arising from neighboring blood and CSF within the voxel. IVW-MRI has an overall sensitivity closing to that of digital subtraction angiography for vasculitis diagnosis. IVW is helpful in differentiation of vasculitis from intracranial atherosclerotic disease, intracranial arterial dissection or reversible vasoconstriction syndrome. Vasculitis in IVW is characterized by a multifocal or diffuse homogenous concentric enhancement of the vessel wall (Figure 1J). In detecting angiitis of the central nervous system, IVW has a 95% specificity and 94% sensitivity for the diagnosis (26).

Arterial spin labeling (ASL)-MRI

ASL-MRI can noninvasively measure cerebral blood flow by labeling inflowing blood magnetically. It can be used to detect hypoperfusion in dementia, assess perfusion alterations in stroke, identify blood shunting in arteriovenous malformations and dural arteriovenous fistulas, localize epileptogenic focus in epilepsy, and differentiate malignant from benign tumors (29). For example, interictal ASL detects ipsilateral hypoperfusion in the temporal neocortex in temporal lobe epilepsy (Figure 1K).

Amide-proton-transfer weighted (APTw) MRI

APTw-MRI belongs to chemical exchange saturation transfer imaging. It uses the mechanism of frequent exchange between amide protons of small molecules and the surrounding water protons as well as the transfer of nuclear spin saturation from amide protons to water protons, which reduces water proton signal. APTw values can reflect cell proliferation and serve as biomarkers of tumor malignancy while characterizing CVDs (23), such as ischemic stroke (Figure 1L).

Other MRI sequences

In addition to those that are listed above, other sequences and measurements have also been developed. Optical coherence tomography (43), ultrafast high spatial-resolution MRA (44) and other emerging techniques (45,46) also offer similar insights into CVDs. In clinical scenarios, different imaging techniques are often used together to gain mechanistic insights for a series of cerebrovascular pathologies.

Stroke and its diagnosis with MRI

CVDs mainly embrace stroke, carotid stenosis, vertebral artery stenosis, intracranial stenosis, aneurysms, and vascular malformations. Primary CVDs can change brain functions and cognition while many non-primary CVDs can influence the structure and functions of cerebral vessels as well. Rapidly and accurately differential diagnosis of these diseases using MRI is the key to managing these diseases efficiently (5,47,48).

Ischemic cerebral stroke

Stroke refers to the circulation status of lacking sufficient blood flow to irrigate brain tissue due to either intra-vessel blockage, vessel narrowing or hemorrhage. More than 80% of strokes are ischemic and the rest are hemorrhagic (49,50).

General clinical features

The leading cause of ischemic stroke is atherosclerosis and then hypertension. Ischemic stroke can manifest as changes in levels of consciousness, and many functions of motor and sensation. With a clear history and careful physical exam, a stroke and its cerebral location can be identified. Although occlusion at different segments of the cerebral vessels can exhibit different symptoms and signs, the infarct areas present basically the same pathologic alterations (51,52), which form the basis of neuroimaging diagnosis of ischemic stroke (Figure 1C, Figure 2A).

Figure 2 MRI illustration of cerebral stroke. (A) Ischemic stroke. Representative images showing the infarct at 58-h in DWI (a, red circle), T2/FLAIR (b), cerebral blood flow (c) and oxygen extraction fraction (d). Reprinted with permission from Wu et al. (53). (B) Lacunar stroke. Stroke topography on DWI in single subcortical (a), multiple subcortical (b), cortical (c), and non-confluent cortical-subcortical regions (d). Reprinted with permission from Tan et al. (54). (C) Hemorrhagic stroke. T2 weighted axial MRI of the brain showing severe cerebral atrophy (a, red arrow); axial MRI of the brain demonstrating a linear gyriform hypointensity (b, red arrow) on SWI sequence in a cortical distribution representative of superficial siderosis; T2/FLAIR weighted MRI showing large confluent lesions (c, red arrow) with a Fazekas 3 rating and maximum intensity projection of SWI sequence of the brain showing multiple diffuse microbleeds (d, red arrow). Reprinted with permission from Karayiannis et al. (55). MRI, magnetic resonance imaging; FLAIR, fluid-attenuated inversion recovery; DWI, diffusion-weighted imaging; SWI, susceptibility-weighted imaging.

In ischemic stroke, lacunar stroke occupies about 20% and results from occlusion of small penetrating branches of cerebral vessels (Figure 2B). In this cSVD, occlusion of individual lenticulostriate arteries leads to lacunar stroke and cognitive impairment, which can be pure motor, pure sensory or ataxic hemiparetic strokes. In addition, at the early stage, signs of motor disturbance may not be obvious, and timely differential diagnosis with MRI becomes important (56,57).

Diagnosis of stroke

In general, clinical presentation is the main diagnosis of stroke. However, the diagnosis at the very early stage of stroke can be difficult, especially when stroke is complicated with brain lesions showing ischemic stroke-like injuries. Thus, MRI characterization of ischemic neuroimaging is essential for diagnosis of stroke (53,54).

DWI can detect ischemic lesions accurately (Figure 2A,2B). In general, the lesions manifest as hyperintense areas on DWI and as correlative hypointense regions on ADC maps, which appear as quick as minutes of stroke onset. Notably, MRI can detect small lesions in cortical or subcortical areas, more effortlessly than CT scan at the acute stage, especially in the posterior fossa or brain stem (58-61).

At different stages of stroke, different manifestations of neuroimaging are present. Arterial occlusion enhances DWI signal and reduces ADC values in the infarct core within minutes. Changes in blood flow appear in MRA and thromboembolism can be identified with SWI. Slow or stagnant flow due to loss of normal flow void in vessels may also be detected as high signal on FLAIR (Figure 2A) and T1 C+ intravascular enhancement. From 6 hours of stroke onset, high T2 signal can be increasingly revealed on FLAIR. After 16 hours of stroke, T1 hypointensity appears. During the first week, high DWI signal and low ADC signal persist in the infarct parenchyma while the infarct area still appears hyperintense on T2 and FLAIR. Cortical contrast enhancement usually lasts for 2–4 months (62,63). In animal study, capillary thrombosis following the venous thrombosis can be found. In rats of sexes, T2 lesion volume and neurological function is correlated with the number of T2*-positive thrombotic vessels, which is significantly greater in female than male rats (64).

Studying blood flow velocity of small perforating arteries is critical to capture earlier pathological alterations in lacunar stroke with 7T phase contrast MRI. Velocity pulsatility can be measured from these blood flow velocity. Arterial pulse pressure may be partially dampened by stiff vessels, which causes arterial transmission of higher pulsatility. Assessing pulsatility with CVR in these small vessels helps reveal the pathways underpinning cSVD (65,66). These changes are also exhibited in Figure 2A.

Hemorrhagic stroke

General clinical features

A hemorrhagic stroke is bleeding directly into the brain tissue caused by traumatic injury, hypertension, amyloid angiopathy, hemorrhagic conversion of ischemic stroke, cerebral aneurysms, arteriovenous malformations and vasculitis alongside other causes like dural arteriovenous fistula and venous sinus thrombosis (67). Acute hemorrhagic stroke includes subarachnoid hemorrhage (SAH), subdural hematoma or intraparenchymal cerebral hemorrhage. The symptoms include headache, one-sided weakness, decreased level of consciousness, neck stiffness, increased intracranial pressure, vomiting, seizures and others (68,69).

Diagnosis of hemorrhagic stroke

Neuroimaging is essential for identification of the cause, location, severity, guidance of treatment, prognosis of cerebral injury of hemorrhage. The age of the hematoma is important sign for MRI evaluation of intracranial hemorrhage (Figure 2C).

In general, hemorrhagic stroke in axial MRI appears as a hyperacute hematoma in the brain that is isointense to hypointense in axial T1-weighted image and hyperintense on T2-weighted imaging. It often manifests as low signal intensity with a small rim of vasogenic edema surrounding the hematoma. A conventional intermediate-echo T2-weighted 3.0-T image can detect hemosiderin and bleeding while SWI can further reveal diffuse microbleeds (Figure 2C) and vascular damage and highlight the veins based on their high levels of deoxyhemoglobin content (67). At 1 month, the susceptibilities, fractional anisotropy, and cerebral blood flow decrease in the perihematomal tissues relative to the contralateral side, whereas mean diffusivity enhances. In the hematomal tissues, the susceptibilities increase; however, fractional anisotropy, mean diffusivity and cerebral blood flow decrease relative to the contralesional area. At 3 months, hematoma and perihematomal volumes reduce significantly (70).

In the differential diagnosis, if the patient has severe sharp headache, SAH should be considered. Within 48 hours of traumatic brain injury, relative to non-SAH patients, lower perfusion in the acute phase of SAH indicates higher risk for brain volume loss (71,72). Consistently, in rat SAH model with endovascular perforation or sham surgery, T2 and T2* MRI tests at 24 h after SAH onset exhibit increase in the numbers of T2* hypointense vessels. The increased vessel number correlates to SAH severity in MRI-based grading of bleeding (64).

In addition, MRI can localize the hemorrhage while providing information about local oxygen partial pressure in the tissues, patient’s hematocrit, local glucose concentration, the regional acidity, hemoglobin concentration, and integrity of the BBB. Lastly, SWI excels CT scan in differentiation of hemorrhagic transformation of ischemic infarction, hemorrhagic venous infarct, cerebral venous sinus thrombosis, and hypertensive microhemorrhage as well as cerebral amyloid angiopathy (55,73).

Differential diagnoses of stroke from other CVDs with MRI

While atherosclerosis is the predominant cause of various strokes, transient ischemic attack (TIA), cerebral aneurysm, vascular malformations, carotid stenosis and moyamoya disease can also change cerebral hemodynamic and even evoke stroke-like disorders in brain functions and cognition. Thus, these CVDs need to be differentiated from atherosclerotic stroke.

TIA

General clinical features

When a cerebral artery is blocked temporarily, TIA occurs. TIA may exhibit stroke-like symptoms; however, this temporary event does not cause permanent damage. TIA often results from transient blockage of cerebral blood vessel by an embolus or thrombus and their subsequent dissolve allows blood flow to resume without permanent damages. Vasospasm is another etiology leading to temporary narrowing of the blood vessel lumen. The patients may develop into strokes, especially shortly after a TIA attack. To prevent strokes in patients with TIA, urgent evaluation and intervention should be performed (74,75).

Diagnosis of TIA

The occurrence of TIA is generally too short to be detected in MRI (Figure 3A). However, MRI may show evidence of an infarct or hemorrhage to rule out a TIA or to identify the reason of TIA, such as carotid plaques (80). In inpatients, MRI is the most sensitive imaging method of detecting TIA or minor stroke; acute DWI hyperintense lesions on brain MRI can match 29.3% patients with a clinical diagnosis of TIA (74). However, the hyperintensity on DWI decreases after 10 days and totally disappears at 2–3 weeks after the original attack. Thus, it is recommended to complete diagnosis of TIA in DWI within 24 hours of symptom onset since TIA differs from stroke in the symptoms that usually last less than an hour without permanent brain damage in MRI (76,81,82).

Figure 3 MRI illustration of CVDs other than stroke. (A) TIA: images showing no abnormality on the initial DWI scan (a), a hyperintense area in the right basal ganglia on the baseline mean kurtosis map (b, white arrow) and a new ischemic lesion is present in a similar location in the right middle cerebral artery territory on follow-up DWI (c, black arrow) and apparent diffusion coefficient maps (d, white arrowhead) 10 days later, respectively [reprinted with permission from Zhou et al. (76)]. (B) Aneurysm: CT brain axial section showing a dilated basilar artery, suggestive of an aneurysm, compressing the left pons (a, arrow); MRI brain sagittal section showing a partially thrombosed basilar artery aneurysm (b, arrow); MRI brain coronal section showing a dilated basilar artery, and basilar artery aneurysm (c, arrow) and cerebral angiogram confirming a fusosaccular aneurysm arising from V3, V4 segments of left vertebral artery and basilar artery (d, arrow) [reprinted with permission from Bhat et al. (75)]. (C) Malformations. MRI (T1-weighted) detects a lesion located in the left cerebellar hemisphere (a, black arrow) when the patient with cerebral cavernous malformations has the first hemorrhage. At the second hemorrhage, MRI (T2 weighted) shows a lesion in the left frontal lobe (b, which is surgically removed) and a small lesion in right basal ganglia (c and d, black circle) [reprinted with permission from Zhang et al. (77)]. (D) Carotid stenosis. MRA shows stenosis of the proximal internal carotid artery (a, white arrow) and contralateral carotid artery stenosis (a, black arrow). In perfusion-weighted imaging, increased cerebral blood volume (b) and delayed time to peak (c) are shown. FLAIR shows hyperintense vessel signal in FLAIR (d, white arrows) [reprinted with permission from Park et al. (78)]. (E) Moyamoya disease. FLAIR reveals a subacute postischemic lesion in the left-hemispheric white matter (a) and time-of-flight magnetic resonance angiography shows multiple changes of arterial vascular calibers (b). Super-selective 4D ASL-based MRA and digital subtraction angiography of the right-sided ICA (c) and left-sided ICA (d) shows aberrant interhemispheric supply patterns in time-resolved manner [reprinted with permission from Sollmann et al. (79)]. TIA, transient ischemic attack; CVDs, cerebrovascular diseases; DWI, diffusion-weighted imaging; MRI, magnetic resonance imaging; MRA, magnetic resonance angiogram; FLAIR, fluid-attenuated inversion recovery; ASL, arterial spin labeling; ICA, internal carotid artery.

Cerebral aneurysm

General clinical features

When an area of artery wall in the brain weakens, part of the vessel wall expands to form cerebral aneurysm. Cerebral aneurysm can result from aging, high blood pressure, atherosclerosis, head trauma or other conditions that weaken vessel walls. Unruptured intracranial aneurysms exist in 1–5% of the general population. Only 0.25–0.5% percentage of aneurisms rupture and form SAH. Patients with unruptured intracranial aneurysms usually appear mild to severe headaches, vision impairment and many other symptoms depending on the site and size of the aneurisms (83,84).

Diagnosis of cerebral aneurysm

MRI can produce detailed images of cerebral aneurysms in phase-contrast sequence that can enhance blood flow measurements and hemodynamic analysis in patients (85). After endovascular treatment, DCE-MRA through differential subsampling with Cartesian ordering-MRA has higher accuracy and time-efficiency in detection of cerebral aneurisms with ultrafast process and high-spatial-resolution. It shows dramatic changes in inflow hemodynamic, inflow jet patterns, and vortex; the highest velocity differences are present at tissues close to the wall and vessel bifurcation along with change in parent vessel pulsatility (44,75,86,87). Figure 3B shows neuroimaging of an aneurysm of the basilar artery in several sequences of MRI relative to that in CT.

Vascular malformations

General clinical features

Vascular malformation is due to abnormal connection of an artery, vein or both of them. It often manifests as arteriovenous malformation, dural arteriovenous fistula, cavernous malformation or hemangioma and venous malformation. The malformation is usually congenital and has abnormal blood flow in the brain. The main symptoms of the vascular malformations include headaches, seizures, strokes, or hemorrhage (88-90).

Diagnosis of vascular malformations

The wide range of pathological conditions of vascular malformations makes some present typical neuroimaging features (Figure 3C) and others appear untypical. The MRI diagnosis of vascular malformations involves spin echo or fast spin echo T1-weighted imaging for regional anatomy, and spin echo T2-weighted imaging for delineating the degrees of the abnormality. Spin echo T2-weighted imaging can differentiate areas of bleeding from high-flow or hemosiderin deposition. DCE-MRI can quickly acquire image with high specificity for differentiating venous malformation from non-venous malformations, which yields a volumetric dataset of high spatial and temporal resolution. Time-resolved angiography techniques can differentiate high-flow from low-flow lesions based on their hemodynamic based on its assessments of flow direction, feeder arteries and drainage veins (77,89,91,92).

Carotid stenosis

General clinical features

Atherosclerosis or other etiologies occurring at the carotid arteries can cause reduction in the diameter of the internal carotid arteries and even blockage, forming carotid stenosis. Carotid stenosis often results in TIA or stroke when pieces of plaque get into the brain, and subsequently temporal or permanent signs of cerebral ischemia. Carotid stenosis should be differentiated from carotid web and carotid dissection in diagnosis (93-95).

Diagnosis of carotid stenosis

MRI can identify stenotic carotid arteries, and characterize the size, composition, and activity of atherosclerotic plaque (Figure 3D). In patients with carotid stenosis, using gradient-echo MRI can detect the absence of plaque calcification, deep white matter hyperintensity and susceptibility vessel sign while using perfusion-weighted MRI can show increase in cerebral blood volume (96,97). Patients with severe carotid stenosis can exhibit multiple hypointense vessels in the cerebral hemisphere ipsilateral to vessel occlusion/stenosis in SWI. In addition, changes in blood flow are correlated with the extent of carotid stenosis (4,78,98).

Moyamoya disease

General clinical features

Moyamoya disease usually results from progressive disorders in the carotid arteries and their major branches that cause irreversible blockage of cerebral vessels. Children with this disease can accompany with many other complications including strokes, TIA, slowly progressive cognitive decline, seizures or involuntary movements of the extremities. Adult patients without surgery treatment often have intracranial hemorrhages that can change the cerebral structure and organization of the structural covariance network (99-101).

Diagnosis of moyamoya disease

Using structural MRI and graph theory in moyamoya disease can demonstrate the structural covariance network (Figure 3E). Moyamoya disease can change both overall and local properties of this network with and without major stroke or hemorrhagic damage. Patients often show a suboptimal structural covariance network with decreased integrity and pronounced volume loss, and regional nodal betweenness centrality (a measure of central situation in a graph based on shortest paths) of the bilateral medial orbitofrontal cortices is significantly decreased (79,98,102,103).

Other brain diseases mimicking CVDs

Many brain diseases do not involve cerebral vessels initially; however, their development can cause disorders in brain functions, disturbance in hemodynamic and even disruption of vessels structures, thereby exhibiting stroke-like symptoms. Alongside clinical manifestations and other neuroimaging tests, MRI tests are critical tool in differentiating vascular from parenchymal abnormalities as well as the management of post-disease rehabilitation.

Functional neurological disorders

Some diseases do not have significant structural changes in brain but show neurological disorders. These diseases include hypoglycemic encephalopathy, hyponatremia, syncope, conversion disorder and hemiplegic migraine, at least.

Hypoglycemic encephalopathy

This brain injury is caused by prolonged or severe hypoglycemia. On both T2 and FLAIR, it manifests as bilaterally increased signals at the posterior limb of the internal capsule, and impaired parieto-occipital cortex, insula, hippocampus and basal ganglia. Diffusion is restricted at early stage and the changes are commonly reversible (38,104-106).

Hyponatremia

Hyponatremia refers to the condition that sodium levels are less than 135 mili-equivalents per liter. Severe hyponatremia occurs when sodium levels down to <120 mili-equivalents per liter in ~30% of patients in intensive care units. In MRI scan at 1.5T at initial presentation of day 1, there is no signal abnormality in the brain parenchyma. Similarly, there are no detectable acute infarct, intracranial hemorrhage, or any focal lesion in DWI with ADC maps, T1-weighted and T2-weighted fast spin-echo images, and FLAIR sequences. In the occurrence of demyelination due to inappropriate correction of hyponatremia, reduced myelin signal in medulla white matter may be identified (38,104-106).

Syncope

When blood flow to the brain drops at low blood pressure, syncope occurs and appears abrupt and transient loss of consciousness. The patient usually has no any illnesses or symptoms after recovery from syncope, such as headache, cognitive deficits, or somnolence. DCE-MRI may detect BBB disruption following syncope and show bright blue colored lines within the sulci throughout the cerebral cortex in severe case (107,108).

Conversion disorder

Patients exhibit motor and sensory symptoms that are unrelated to brain structural lesions although that may sustain this functional neurological disorder. In conversion disorder, microstructural changes in sensory-motor integration occur in both the hand and foot regions (109). Functional MRI of the brain in people with conversion disorder can detect reduced volumes of right and left basal ganglia and right thalamus (110). Moreover, aberrant functional connectivity of limbic-motor regions has been identified in MRI, which exhibits bottom-up hyperactive neural activity in limbic regions and a potential failure of top-down regulation from prefrontal regions (111).

Hemiplegic migraine

Migraine affects 15–20% of people and hemiplegic migraine makes up <1% of these cases. This rare variety of migraine with aura can exhibit many visual symptoms, like flashes of light and zigzag patterns, which happen before or during a migraine episode. Loss-of-function mutations of the gene of alpha 1A subunit of P/Q type voltage-dependent calcium channel can account for this disease. In MRI, patients of hemiplegic migraine can exhibit a mild atrophic cerebellum and many hyperintense lesions of the cerebral white matter without symptoms. However, the remarkable MRI presentation lacks specificity while other examinations appear normal (112-114).

Structural neurological disorders or lesions

Structural neurological disorders represent structural changes; however, the involvements in cerebral vessels or their functions are minor or secondary. These disorders include hydrocephalus, brain abscess, cerebral neoplasm and many others.

Hydrocephalus

Hydrocephalus is a pathological condition that has excess CSF within the ventricular system of the brain, which may or may not increase intracranial pressure. It can be either obstructive or communicating patterns. Communicating hydrocephalus without elevation of CSF pressures can be caused by traumatic injury, prior SAH, and meningitis. Idiopathic normal-pressure hydrocephalus in some patients has the characteristics of the triad of gait apraxia or ataxia, urinary incontinence, and dementia (115-117).

In MRI, hydrocephalus exhibits enlargement of the lateral and third ventricles more than the cortical sulcal enlargement (Figure 4A). Moreover, sites of obstructive hydrocephalus can also be identified, such as the fourth ventricle where tumors block the fluid flow (123). A patient-specific 3D geometry of the CSF spaces can be presented in structural MRI. Using phase contrast MRI can measure maximum velocity at the cerebral aqueduct and validate the computational fluid dynamic simulation, thereby highlighting patient-specific boundary conditions. Using volumetric flow-rate boundary conditions can account for deformation of brain tissue through calculation of the conservation of mass. Childhood hydrocephalus commonly has high grade venous stenosis and cerebral hyperemia wherein high grade stenosis can cause conservative management failure while hyperemia is a sign of good prognosis (115,124,125).

Figure 4 MRI illustration of other brain diseases mimicking CVDs. (A) Hydrocephalus: image showing the periventricular hyperintensities including adjacent changes, but excluding non-adjacent changes in deep white matter. The red arrows mark some of the areas detected as isolated deep white matter changes [reprinted with permission from Snöbohm et al. (115)]. (B) Brain abscess. In the left basal ganglia area, an aberrant, circular space-occupying lesion with long T1 and long T2 signal shadows is present. Its ring wall has relatively even thickness, manifesting as slightly short T1 and T2 signal shadows. The lesion-surrounding area contains patches of apparent edema; the left ventricle displays slight compression-resulted deformation; and the midline structures display minor rightward shift [reprinted with permission from Zhou et al. (118)]. (C) Brain tumors: representative images of patients with astrocytoma (a) and glioblastoma (b) [reprinted with permission from Sartoretti et al. (119)]. (D) Sporadic Creutzfeldt-Jakob disease. DWI shows typical basal ganglia abnormalities (a) and typical features of ‘cortical ribboning’ in the frontal and parietal cortex (b) [reprinted with permission from Rudge et al. (120)]. (E) Multiple sclerosis. 7 T FLAIR-SWI data show several typical white matter hyperintense lesions and global brain atrophy (a) and one large periventricular hyperintense lesion with an encircling hypointense rim (white rectangle, b). Within this lesion, tubular hypointense structures suggestive of veins and circumscribed nodular hypointensities are visible [reprinted with permission from Dal-Bianco et al. (121). (F) Ataxic hemispheres. Image exhibits small, round, high, and central low-signal-intensity lesions in the right frontal lobe and internal capsule in T2/FLAIR [reprinted with permission from Lee et al. (122)]. Red arrows in B-F point to the typical lesions. MRI, magnetic resonance imaging; CVDs, cerebrovascular diseases; DWI, diffusion-weighted imaging; FLAIR, fluid-attenuated inversion recovery; SWI, susceptibility-weighted imaging.

Brain abscess

A brain abscess has the feature of a pus-filled swelling caused by bacterial or fungal infection of the brain tissue or severe head injury (126,127). Neuroimaging of a brain abscess relies on the stage of the abscess at imaging and the etiology of the abscess. Brain abscess presents as clear ring-enhancing lesions (Figure 4B) (118,128,129) in DWI and perfusion imaging, which is clearly different from necrotic tumors.

Cerebral neoplasm or brain tumors

They are abnormal brain tissue masses resulting from excessive growth of brain cells or a metastatic tumor from other organ systems. Brain tumors can be malignant and grow quickly or benign and grow slowly, and their size and exact position can be identified with MRI optimally (Figure 4C). Since primary cerebral neoplasm is uncommon, other parts of the body, such as lungs, colon or breasts, should also be examined to see if the tumor has spread in advanced MRIs, such as diffusion, perfusion, spectroscopy, tractography, and functional MRI. Contrast-enhancing tumor region with high baseline magnetic susceptibility can be reduced markedly by hyperoxic challenges and enforced by hypercapnia relative to hyperoxia. Malignant tumor tissue magnetic susceptibility at baseline under normoxia is correlated with the corresponding susceptibility reduction under hypercapnia. By contrast, necrotic tissue and edema regions do not have dramatic changes in paramagnetic shift (119,130-132).

Others

Many other diseases also show brain lesions and can be specifically diagnosed with MRI, such as sporadic Creutzfeldt-Jakob disease. In MRI, basal ganglia abnormalities and ‘cortical ribboning’ in the frontal and parietal cortex are typical features of sporadic Creutzfeldt-Jakob disease (Figure 4D). Among several types of sporadic Creutzfeldt-Jakob disease, MM2-cortical-type is difficult to be diagnosed on the basis of clinical presentation and laboratory tests. However, MRI has high sensitivity and specificity for it at the early stage by identification of cortical distribution of hyperintensity lesions on DWI in a slower disease progression (120,133).

Demyelinating lesions of multiple sclerosis can cause many cerebral symptoms including ophthalmoplegia (134). In relapsing-remitting multiple sclerosis patients underwent a 7T MRI, relative to the contralateral normal appearing white matter, both enhancing and non-enhancing lesions significantly decrease the amplitude of myelin water but increase interstitial and axonal water (Figure 4E). In addition, longer relaxation time is present at interstitial and axonal water, and lower frequency shift appears in axonal water in comparison with the contralateral normal appearing white matter (121,135). Another example is ataxic hemiparesis caused by corticospinal tract impairment. Ataxic hemiparesis possesses typical lacunar syndrome involving homolateral ataxia. It often shows central low-signal-intensity lesions in internal capsule in T2/FLAIR image alongside multiple small hyperintensity lesions in both cerebral hemispheres (Figure 4F). It can be caused by many different factors including ischemic stroke, mutations in POLR3A characterized by high phenotypic heterogeneity including central hypomyelination in MRI (122,136).

Strengths, limitations and perspectives

Strengths of this review

MRIs do not use radiation that is used by X-rays, CT scan and PET scans and thus can assess brain function noninvasively. However, MRIs can produce very high resolution, and thus become the imaging technique of choice for diagnosing CVDs. In addition, MRI can be used for treatments as a surgical guidance and assistance in cancer removal (137). For instance, in radiotherapy to treat cancers, MRI-guided linear accelerator can categorize tissues with a high level of spatial and temporal resolution and distinguish malignant from or non-malignant tissues anatomically and functionally while monitoring changes in tissue blood flow. The “real-time” nature of MRI is more suitable for treatment of motile soft-tissue organs, e.g., blood vessel and normal breathing (138-140).

Limitations and contraindications

While MRI represents the frontiers of modern neuroimaging techniques, there are restrictions and contraindications in using MRI techniques due to magnetic fields, machine structure, and gadolinium contrast agents. In general, relative to other neuroimaging techniques, MRIs are more expensive, require the person being scanned to stay completely still for capturing a clear image, take longer for the scan and are not suitable for emergencies like stroke and traumatic injuries. MRIs may also risk the health of specific persons including those who have implants like artificial joints, eye implants, an intrauterine device and a pacemaker. The strong static magnetic field can draw ferromagnetic objects toward MRI scanners of the machine and thus produce projectile effect, twisting, burning, and artifacts. Thus, MRIs may cause displacement of metal implants and device malfunction of foreign bodies, increase body temperature during long MRIs and result in claustrophobia. The loud noises can cause hearing issues. In some MRI scans that need injection of contrast agent, side effects like feeling or being sick may occur.

In the application of MRIs, one major challenge is that MRIs can provide clues of a specific malfunction, but are unable to determine whether abnormal image of tissues are functioning abnormally. As an optimal imaging technique, most MRI sequences are insufficient for diagnosing the functional states. For example, occlusion of a small branch of a cerebral artery may not cause malfunction of the brain region receiving its irrigation because collateral circulation from the Circle of Willis can compensate deficits in blood circulation. Another limitation is that MRIs could not determine functional change involving neurons and non-neuronal cells. Because certain brain areas highlighting on MRIs may represent many functionally diverse neuronal populations, even in one millimeter square area, exact interpretation of brain activity represented by the regional image is difficult. Thus, over-examination with MRIs without specific clinical signs and symptoms may cause confusion rather than clarification of the patient’s diseases. Occasionally, false positives or negatives of imaging findings are present in association with functional impairments.

Perspectives of MRI using in diagnosis of CVDs

In order to overcome the limitations potentially associated with the use of MRI in CVDs, it is necessary to have a full understanding of the indications and limitations of MRIs for individual patients. Meanwhile, reducing the expenses, noises, and uncomfortable environment should be the targets of medical industry while standard practice in MRI examination should be followed, such as screening all patients individually for foreign bodies before performing an MRI scan. To remove the labeling of “a high-tech version of phrenology”, it is important to combine MRIs with other functional methods, such as combinations of the time resolution of electroencephalogram, source localization in MRI, and multivariate modeling (141). Further detection of changes in regional ionic and neurochemical levels that change accompanying with alterations in local neural activity may provide a more complete and precise picture of brain activity, thereby compensating the insufficiency of neuroimaging techniques.

Conclusions

While stroke and other CVDs can be diagnosed with the support of clear and unique MRI results, differential diagnosis between them with MRI is naturally available in combination with clinical presentation, laboratory tests and other neuroimaging techniques. In MRIs, different CVDs alone or in combination with other primary or secondary cerebral vessel disorders exhibit different hemodynamic, water movement, blood components, myelin, and different association with vessel walls. In ischemic stroke, high DWI/ADC alongside slow or stagnant flow and thromboembolism in vessels are the key MRI signs for early diagnosis with or without other complications. In hemorrhagic stroke, the presence of hematoma and reduced brain volume are the representative neuroimaging. Other CVDs usually have clear signs of cerebral lesions with or without hemodynamic alterations; however, changes in hemodynamic are largely secondary. With the progress of diseases and proceeding of treatments, MRI signs exhibit corresponding changes that provide further hints for differential diagnosis, understanding the underlying mechanisms, prediction of disease progression and treatment options. Thus, MRI techniques are powerful for differentiating the causes of CVDs, either resulting from cerebral vessel pathogenesis, functional disorders or structural alteration in parenchymal cerebral abnormalities. Fully using the advantages of MRI tests while breaking its limitations is increasingly important for enhancing overall capacity of clinical management of CVDs.

Acknowledgments

We thank Zhengzhou Wenxing Translation Service Co., Ltd. (51scihelp, Certificate No. 298FGY6Y896) for language editing service.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-22-750/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-22-750/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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