Functional MRI

Functional MRI quantifies the local increase in oxyhemoglobin concentration secondary to increased blood flow and volume that occurs after stimulation of eloquent cortex. The images enable the clinician to recognize the relationship of AVMs to eloquent brain structures, as well as elucidate cortical reorganization secondary to the AVM.^2–4 This information may help during preoperative planning and during patient counseling, because it could, in some measure, predict the development of post-therapy deficits in patients.

Diffusion-Tensor Imaging

Diffusion-tensor imaging is a developing technology that enables in vivo visualization of multiple white matter tracts and their relationship to an AVM. The ability to use this information can help minimize treatment risks and determine the best therapeutic modality for the patient.^2,5

Provocative Injection Testing (Wada’s Test)

Prior to embolization of an AVM, Wada’s testing of selective feeding vessels can be performed. Amobarbital sodium or propofol injections have been performed on vessels in or remote from the lesion.^6–8 This pharmacologic test helps predict the effect of occluding a feeding vessel. Due to their short half-life, their effect disappears rapidly. Such evaluation helps prevent embolization of pedicles that may result in focal neurologic deficit. This preoperative functional evaluation is helpful when supraselective intranidal microcatheter placement is not achieved and there is concern that vessels to adjacent normal brain may be compromised.

Angiography

Angiography remains the gold standard for defining arterial and venous anatomy of an AVM.² Such analysis of the angioarchitecture helps in evaluating the risk of hemorrhage and selecting the best therapeutic management of the AVM.⁹ Angiographic characterization of the AVM includes identification of the main arterial feeders, size of the AVM, shape of the nidus (compact vs. diffuse, without clear borders that separate it from adjacent brain), drainage patterns (superficial drainage into cortical veins, deep drainage through deep venous system, or proximity to dural sinuses), and characteristics of outflow (presence of restriction from stenosis or sinus thrombosis). Anatomic characteristics of AVMs such as deep location, deep venous drainage pattern, presence of a single draining vein, venous stenosis, eloquent location, and small diameter are all related to increased risk of hemorrhage or neurologic deficit.^10–19

Angiography helps elucidate the presence of associated aneurysms. These aneurysms are categorized by their location (i.e., feeding artery, intranidal, circle of Willis, or venous). Associated aneurysms are found in roughly 7% to 41% of patients with AVMs.^20–25 Studies evaluating hemorrhage risks for AVMs with associated aneurysms have shown conflicting results. A 2007 study from the Columbia study group described prospectively collected hemorrhage risk factors limited to the period between the initial AVM diagnosis and the start of treatment, calculating annual hemorrhage rates in 622 patients.²⁶ In the group’s model, the presence of associated intranidal or feeding artery aneurysms did not have a significant effect on hemorrhage rates.¹¹ Other studies, however, have included intranidal aneurysms as important risk factors for hemorrhage in AVMs,^{1,13–16,21,27,28} with increased size of the aneurysm related to increased risk of hemorrhage.^21,29 These aneurysms are exposed to the same intraluminal pressures as the arterial components of the AVM. Therefore, any pressure changes following AVM embolization could lead to associated aneurysm rupture. Thus, vessels that supply intranidal aneurysms should be recognized and treated early to reduce the risk of hemorrhage.³⁰

Angiography further evaluates for the presence of pseudoaneurysms (false aneurysms), which may form in previously ruptured AVMs. These irregularly shaped cavities have abnormally structured vessel walls and are often located at the point where artery and vein make contact due to inherent weakness.³¹ Previous rupture of an AVM is an independent predictor of future hemorrhage,²⁶ and recognizing the presence of posthemorrhage pseudoaneurysm formation can help reduce the risk of future hemorrhage.

AVM-associated arteriovenous fistulas are sometimes discovered in the nidus during angiographic evaluation. The presence of these high-flow AVFs is associated with increased risk of intra- and postoperative complications, including hemorrhage.^32,33 Prior endovascular treatment of these AVFs helps decrease the chance of this complication. Reducing the flow through the AVF also helps decrease the chances of undesired embolization of the AVMs’ venous drainage, cerebral veins, dural sinuses, or pulmonary circulation.^33,34

Timing of imaging after a hemorrhage must be considered. Performing an angiogram immediately after hemorrhage can result in a false negative secondary to compression of the nidus by the hematoma.^35–38 Therefore, a late angiogram, performed 3 months after the hemorrhage, remains the gold standard for detection of an AVM.³⁵

n-Butyl Cyanoacrylate

n-BCA is a liquid monomer that permanently polymerizes to a solid compound after contact with solutions containing anions like blood.⁴⁶ This compound must be combined with Ethiodol, an iodine-based oil that serves as a radiopaque contrast agent. Tantalum powder can also be added to increase its opacity, although its use is not common currently. Embolization with n-BCA initiates an inflammatory endothelial response and subsequent occlusion of target vessels.⁴⁷ A variety of factors influence the effectiveness of n-BCA in treating AVMs, namely, viscosity and polymerization time. Increasing the concentration of Ethiodol in the mixture increases the viscosity, which delays the transit within the lesion. Increasing the concentration of Ethiodol delays the polymerization time, which is useful in lesions that exhibit slow flow. Temperature, homogeneity of the mixture, and changes in the pH of the solution also play a role in polymerization time.^48,49 The distance between the microcatheter and the nidus, tortuosity of the vessels, and intranidal flow are factors that influence the choice of n-BCA viscosity and polymerization time. Manipulation of viscosity and polymerization time allows for control of injection speed. Diluted glue permits prolonged injection times and dense casting of the nidus with less microcatheter retention risk.³⁴ In general, a 1:1 dilution of n-BCA to Ethiodol is used when the hemodynamic flow of the AVM is very fast and the catheter is close to the nidus. Different concentrations, such as 1:2 or 1:3, are used when the flow is slower. We frequently use a 1:2 or 1:3 n-BCA-to-Ethiodol ratio. Acid compounds such as glacial acetic acid have been used to decrease the pH, which delays polymerization time without compromising viscosity.⁵⁰ Dextrose 5% can also be used to improve distal progression of the n-BCA through small, tortuous feeders. In this technique, dextrose is injected through the guide catheter and n-BCA is simultaneously injected through the microcatheter. The dextrose injection delays the contact of the blood with the n-BCA and, in this way, delays its polymerization.⁵¹ Sometimes, as the microcatheter tip reaches smaller distal vessels, it can potentially occlude blood flow. This technique is known as “flow control” and can be utilized to prevent blood from contacting the n-BCA, thus allowing for its prolonged distal penetration.³⁴ Injection of n-BCA is stopped when glue reaches the venous system through the nidus or if there is backflow toward the catheter. The microcatheter must be removed quickly to prevent catheter retention.^47–4952

Onyx

Onyx is a newer liquid embolic agent composed of ethylene–vinyl alcohol copolymer (EVOH) mixed in a dimethyl sulfoxide (DMSO) solvent. This nonadhesive, cohesive solution is mixed with micronized tantalum for radiopacity and must be shaken together for at least 20 minutes⁵³ to achieve homogeneity of the mixture. It is available in different concentrations of the EVOH polymer, with lower concentrations being associated with decreased viscosity and thus more distal penetration of the AVM.⁵⁴ When the mixture comes into contact with aqueous solutions, the polymer begins to precipitate on the surface while the core remains liquid. This produces what has been described as a “lavalike flow pattern” within blood vessels of a soft and nonadherent mass that does not fragment during the injection.⁵⁴ Similar to n-BCA, Onyx is a nonabsorbable agent. Therefore, theoretical permanent occlusion of the AVM can be achieved.⁵⁵ However, recent evidence suggests that there exists a risk of recanalization or reperfusion of the AVM following Onyx embolization.^56,57 Its nonadhesive nature enables longer, slower, and more controlled injections, which allow for the embolization of a larger percentage of the AVM from a single catheter position. However, only partial reflux around the catheter is permissible, because catheter withdrawal can become difficult. Its nonadhesive nature also enables cerebral angiography between injections to monitor the progress of embolization,^54,55,58,59 a big advantage over the use of n-BCA. Care must be taken to use slow infusion rates and thus avoid the angiotoxicity associated with DMSO.⁶⁰ Chaloupka et al., using a swine rete mirabilis embolization model, report that a DMSO injection of 0.5 to 0.8 ml over 30 to 90 seconds, while causing mild transient acute vasospasm, results in no adverse clinical sequelae and less angiotoxicity than reported in prior studies.⁶⁰ Separation of tantalum from the Onyx is another pitfall that can increase the difficulty of viewing smaller feeding pedicles.^59,61 Onyx injection is limited to DMSO-compatible microcatheters only, such as the Marathon and the Echelon.

Polyvinyl Alcohol

PVA consists of particles available in different diameters depending on the size of target vessels.^52,62–64 PVA produces slower occlusion than liquid embolic agents. PVA particles occlude low pressure shunts first, causing an increase in intranidal vessel pressure and subsequent immediate risk of hemorrhage prior to nidal obliteration.⁶⁵ In addition, PVA is associated with high recanalization rates, ranging from 12% to 43%.^66,67 The development of collateral feeders secondary to proximal occlusion of the AVM with large size particles may contribute to such high recanalization rates.^52,62–64 Given these characteristics of PVA, it has been used with success preoperatively to reduce AVM flow prior to open or radiosurgical treatment.