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Advanced MRI techniques, including 4D flow, arterial spin labeling, diffusion, and susceptibility imaging, expand conventional anatomic assessments to physiologic evaluation.
Understanding the underlying physics and properties of these sequences informs their complementary application in the assessment of iAVMs, including detailed evaluation of blood flow, parenchymal perfusion, fiber tract injury and location, and the presence of extravascular blood products.
Improvements in these MRI-based techniques have allowed broader applications in the assessment of baseline iAVM risk and the efficacy of multimodal treatments.
Intraoperative applications of 4D flow are additionally covered in Chapter 29 .
Several advanced MRI techniques have emerged in the last few decades to improve the diagnosis and management of neurovascular disease. Traditionally intracranial arteriovenous malformations (iAVMs) were characterized primarily by invasive angiography, but MRI has matured to become the mainstay for diagnosis, treatment planning, and long-term management of complications. In this chapter, we survey several complementary advanced MRI techniques, which expand beyond anatomic delineation to physiologic assessments. Each of these MRI techniques touches upon important and complementary facets of cerebrovascular anatomy, physiology, and pathophysiology, helpful for optimizing the care of patients with iAVMs.
These advanced MRI techniques include (1) volumetric phase contrast, also known as 4D flow, for the visualization of arterial supply and quantification of blood flow; (2) arterial spin labeling (ASL) for quantifying tissue perfusion and detecting arteriovenous shunting; (3) diffusion techniques, including diffusion tensor imaging (DTI) for delineation of fiber tracts and diffusion-weighted imaging (DWI) for assessment of ischemic injury; and (4) susceptibility imaging for detecting areas of previous hemorrhage or calcification.
Early studies of intracerebral hemodynamics utilized transcranial Doppler ultrasonography to assess flow within large feeding arteries. However, the spatial and temporal resolution of this technique is limited and identification of feeding and draining vessels with transcranial Doppler ultrasound is highly dependent on the ability of a trained technologist to identify an open acoustic window. In recent years, volumetric phase-contrast (also known as 4D flow) MRI has emerged as an effective, noninvasive technique for visualizing and measuring hemodynamics within cerebral blood vessels without limitations of operator dependence ( Fig. 4.1 ). Measurements of cerebral blood flow from phase-contrast MRI have been found to correlate well with measurements made with transcranial Doppler ultrasound.
Acquisition of phase-contrast MRI is performed by applying two opposite, flow-encoding gradients and measuring a phase shift, which is proportional to the speed of protons moving along the direction of the magnetic field gradient. While planar phase-contrast MRI is generally performed with velocity encoding only in the direction perpendicular to the imaging plane of interest, 4D flow MRI is performed with velocity encoding in all three directions. Velocity data become usable after correction of background phase errors, Maxwell terms, and gradient field nonlinearity. Historically, 4D flow MRI required long acquisition times, but recent advances, including parallel imaging and compressed sensing, have brought this technique into the realm of clinical feasibility, with acquisition times within 5–10 minutes. Although more commonly performed for assessment of cardiovascular pathologies, 4D flow MRI has shown potential for quantification and visualization of complex feeding arterial and draining venous flow in AVMs as well. Moreover, neurovascular 4D flow measurements have demonstrated high multicenter and interobserver reproducibility.
4D flow MRI can provide valuable insights into the hemodynamic characteristics of AVMs and has potential to stratify patients who are at greatest risk of hemorrhage. For example, early studies using 4D flow MRI have shown that higher draining vein flow on MRI tends to correlate with higher Spetzler-Martin grade; altered venous-arterial pulsatility, especially in high-grade iAVMs; and observed flow reversal within the contralateral arteries. The increase in ipsilateral artery flow at the expense of contralateral artery flow is often referred to as steal phenomenon. Although the relationship of this observation to neurologic deficit has been questioned, there is nevertheless potential for hemodynamic parameters measured on 4D flow MRI to predict downstream events such as hemorrhage. In one small study, patients with severe symptoms exhibited higher wall shear stress in ipsilateral arteries compared to contralateral arteries, and there was a correlation between higher AVM flow in preoperative studies and greater venous vessel wall thickness in resected AVMs, presumably related to response to elevated wall shear stress. However, increased AVM flow and altered hemodynamics may not always be associated with more severe clinical presentations, such as seizure or hemorrhage. In a small study of 17 patients with iAVMs, there was no correlation found between AVM flow and clinical presentation. 4D flow MRI may play an important future role in prognostication for patients with iAVMs, but not in isolation—its interpretation will require the context of other relevant clinical and imaging findings.
4D flow MRI is beginning to show promise for monitoring the treatment response of iAVMs after resection, embolization, or radiosurgery. Following embolization, AVMs decrease in mean flow volume within feeding arteries and change in the distribution of flow in vessels surrounding the nidus. Following stereotactic radiosurgery, flow volume and pulsatility are similarly affected. As early as 6 months after radiosurgery, 4D flow MRI shows a notable decrease in blood flow within the ipsilateral supplying arteries and draining veins, before structural remodeling can be seen on standard MR angiography (MRA) images. These data suggest that 4D flow imaging may be used as an earlier indicator of treatment response than conventional MRI.
Over the years, phase-contrast MRI has also been explored for several cerebrovascular diseases beyond AVMs, including aneurysms and moyamoya disease. For example, Sekine et al. demonstrated that radial artery grafts have more retrograde flow and higher blood flow volume compared to superficial temporal artery grafts used in extracranial-intracranial bypass, and Moftakhar et al. demonstrated that bifurcation aneurysms often have recirculation blood flow patterns and intraaneurysmal pressure measurements. Further work will be required to determine whether these hemodynamic observations are predictive of downstream outcomes.
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