ARTERIOVENOUS MALFORMATIONS AND FISTULAS

Types

Cortical-subcortical arteriovenous lesions recruit cortical arteries and drain into superficial veins but may also drain into the deep venous system if the transcerebral venous system is patent. These lesions are also designated gyral AVMs (Fig. 23-4). In both cortical (sulcal) and cortical-subcortical (gyral) lesions, some regions of the cortex drain to deeply located veins that should not be considered as true parts of the deep venous system. Such vessels include the medial veins of the temporal lobe and the basal vein of Rosenthal, the veins of the cerebellar vermis, and the precentral cerebellar veins.

Corticoventricular arteriovenous lesions correspond to the classic pyramidal malformations that are based on the cortex and reach the ventricular wall at their apex. These malformations are fed by both cortical and perforating arteries and drain to both superficial and deep veins. Corticocallosal AVMs belong to the corticoventricular group (Fig. 23-5). They have the same venous characteristics but do not recruit perforating arteries. Corticocallosal AVMs drain into the subependymal veins and later into the deep venous system. The arterial supply to the corpus callosum is linked to the cortical arterial network, even though it may simulate perforating arterial channels in the supraoptic region and choroidal arteries at the splenium.

Deep-Seated Arteriovenous Lesions

Deep-seated lesions are located in the depth of the telencephalon, diencephalon, brain stem, or cerebellum (Fig. 23-6). The nidi involve the deep nuclei, and the arterial and venous connections are along the long fiber tracts. The deeply seated arteriovenous lesions recruit perforating arteries exclusively and drain into the deep venous system. They may use transcerebral veins, if patent, as direct venous outlets or as collateral pathways. Arteriovenous lesions of the lenticular and striate nuclei may recruit transcortical arteries from the insular branches of the middle cerebral artery. Arteriovenous lesions of the dentate nucleus may recruit hemispheric collaterals of the cerebellar arteries. MRI and angiography will be able to distinguish these deep-seated lesions from cortical-subcortical lesions, particularly because the dominant supply of the deep intracerebral lesions arises from the perforators.

FIGURE 24-4 A to D, This corticocallosal AVM had a massively dilated thalamostriate vein draining into the internal cerebral vein that subsequently led to unilateral hydrocephalus. On MRI, the flow voids can be well appreciated on T2W images (A, B) while on T1W nonenhanced studies (C) the AVM signal is typically hypointense.

FIGURE 24-6 A to D, Infratentorial micro-AVM of the pons. On FLAIR-weighted images a hyperintensity can be seen that corresponds to a small glomerular AVM that is fed by three separate pontine perforators. The 3D rotational angiography demonstrates well the glomerular aspect of this AVM.

Arteriovenous Lesions of the Choroid Plexus

Choroid plexus AVMs are important to recognize because they are anatomically extracerebral lesions accessible to surgical and endovascular therapy. Choroidal arteriovenous lesions are fed primarily by choroidal arteries and by subependymal arterial feeders arising from the circle of Willis, including the anterior thalamoperforate arteries arising from the posterior communicating arteries that course through the walls of the third ventricle to reach its roof and the adjacent choroid fissure (Fig. 23-7). By definition, choroid plexus arteriovenous lesions have no cortical arterial supply. They drain via ventricular veins, with occasional recruitment of transcerebral veins. These extra-axial lesions can be distinguished from intra-axial AVMs by angiographic criteria.

Epidemiology

The incidence of brain AVMs is difficult to estimate. Figures from small communities and autopsy series suggest that 0.14% to 0.8% of the population may present with a brain AVM in a given year. In adults, symptomatic brain AVMs appear to be about one tenth as frequent as intracranial arterial aneurysms. The risk of hemorrhage is estimated to be about 2% to 4% per year for “unruptured” brain AVMs but 8% to 17% per year for brain AVMs that have bled previously. Overall, the major morbidity or mortality of brain AVMs is about 1% per year.

Pathophysiology

The vascular malformation and the rest of the vasculature evolve with age. Assessment of a vascular malformation, therefore, requires consideration of (1) the presumably congenital defect that expresses itself as a malformation and (2) the response of the individual host harboring the malformation. AVMs are believed to be initially stable lesions, which become destabilized over time owing to hemodynamic increases in venous flow or mechanical compromise resulting in decreased venous outflow. Destabilization of the AVM leads to hemorrhage. Destabilization of the brain leads to seizures or progressive neurologic deficits.

The vessels surrounding the AVM are affected by the congenital malformation and by the hemodynamic alterations it produces. These secondary, acquired effects influence the clinical presentation and outcome. Pial AVMs may be found incidentally or because of headache, seizures, or hemorrhage. Children, especially those with high-flow fistulas, may manifest somatic symptoms and psychomotor retardation when venous congestion is a prominent feature of the malformation. Headaches are more commonly seen in children and are typically pseudomigrainous. AVMs in occipital locations and AVMs that have transdural supply, venous ectasia, and venous congestion show increased incidence of headaches. Most seizures associated with brain AVMs are focal and may reflect venous congestion or small hemorrhages that irritate healthy brain tissue near the brain AVM.

FIGURE 24-7 Acute intraventricular hemorrhage in a 68-year-old woman without prior history of hypertension led to CTA that was able to demonstrate a choroidal type AVM with large venous outpouchings (A). CTA demonstrates a tangle of pathologic and enlarged vessels as a sign for the AVM that was verified on DSA (B). Typical for a choroidal AVM, feeders are recruited from the pericallosal artery via the limbic arch and from the lateral posterior choroidal arteries of the posterior cerebral artery.

Pathology

The normal adult brain does not express growth factors such as vascular endothelial growth factor (VEGF) or transforming growth factor-β (TGF-β). These factors may be present in AVMs and may be induced by proliferation of new vessels, hemodynamic stress, ischemia, and/or hemorrhage. VEGF is predominantly expressed in the subendothelial layer and media of vessels in AVMs. Ultrastructurally, brain AVMs show preservation of mature vessel walls with phenotypic alterations due to high flow and hemodynamic stress, including arterial, nidal, and venous aneurysms. In contrast to the ultrastructure of cavernous malformations (CCM), AVMs maintain normal vessel wall and structural integrity with endothelial cell denudation. There may be intense laminin expression localized in and around the internal elastic lamina. Type IV collagen seems to be expressed intensely in the subendothelium at the level of the basal lamina. Type III collagen is observed in the media and perivascular tissue. Immunohistochemical analyses on activin, myosin, and smoothelin indicate the disappearance of contractile properties in vascular smooth muscle cells of AVM vessels due to the hemodynamic stress of turbulent blood flow through these lesions. The levels of certain proteinases are increased in the endothelial/periendothelial cell layer of cerebral AVMs, consistent with vascular remodeling and instability within the AVM. Endothelial cells cultured from AVMs have reduced secretion of endothelin-1, a molecule involved in vascular cell phenotypes, and demonstrate increased proliferation.

On histopathology, “classic” cerebral AVMs consist of a tangle of abnormal arteries and veins with no intervening capillary bed. Gliotic and nonfunctional brain parenchyma may be present between the abnormal vascular channels. The walls of the feeding arteries show abnormal lamination with reduplication, interruption, and distortion of the internal elastic lamina, focal increase of arterial muscle fibers, and focal thinning of the muscularis to form arterial aneurysms. The walls of the veins are typically thickened by collagenous tissue. There may be secondary signs of vascular degeneration, including fibrosis, atheroma, and calcification. The surrounding cortex shows neuronal loss and increase in fibrillary glia. The neural tissue originally present between the abnormal blood vessels is restricted to thin gliotic bands, with no identifiable neurons. Signs of prior hemorrhage, such as hemosiderin-laden macrophages, may be present.

Classification

The Spetzler-Martin classification of pial brain AVMs is based on the size of the AVM, the pattern of venous drainage, and the eloquence of the portions of brain adjacent to the AVM. The classification was devised to anticipate the risk of treating brain AVMs surgically but has been extended to predict the (presumed) natural history of the entire group of AVMs. We believe this generalization to be improper because (1) the classification does not assess the special characteristics of an AVM in an individual patient (e.g., associated aneurysms), (2) the classification does not recognize that an AVM with high-grade risk for surgery is not necessarily dangerous to the patient, and (3) the classification does not allow assessment for alternate therapy by endovascular techniques and radiosurgery.

To determine whether endovascular therapies are suitable for a brain AVM, one must assess the angioarchitecture of the malformation, including the nature of the feeding artery, the number of separate compartments of the malformation, any arterial or venous ectasias near to or within the malformation, and the nature of the venous drainage. There are two basic types of feeding artery. Direct arterial feeders end in the AVM. Indirect arterial feeders supply the normal cortex and also supply the AVM “en passage” via small vessels that arise from the normal artery (see Fig. 24-5). Intranidal arterial aneurysms or venous varices indicate weak points in the system. Drainage into the deep venous system and stenoses that restrict venous outflow indicate increased risk of spontaneous hemorrhage. A long pial course of the draining vein may indicate that venous drainage is restricted over a large area, increasing the risk of venous congestion and subsequent epilepsy. Conversely, a short vein that drains almost directly into a dural sinus is unlikely to interfere with the normal pial drainage.

FIGURE 24-5 A to C, Cingular or corticocallosal type of AVM. These AVMs are linked to the cortical arterial network and are drained into the deep venous system. In this case the type of feeding arteries are “en passage” rather than terminal-type feeders.

Small AVMs may be difficult to discern (Fig. 24-8). Larger AVMs usually display (1) tangled “serpiginous” parenchymal vessels that appear slightly dense due to blood pooling and (2) large draining veins in the subarachnoid space. Calcifications are present in about one third of brain AVMs. Focal hemorrhage, focal mass, or focal atrophy may also be present. Contrast enhancement opacifies the enlarged feeding arteries, the tangle of vessels in the parenchyma, and the dilated draining veins.

FIGURE 24-8 This patient presented to the emergency department with a first-ever seizure. A and B, Routine non–contrast-enhanced cranial CT revealed an ill-defined area of gray matter/white matter differentiation in the right frontal lobe (arrowheads) and a tubular extra-axial structure (small arrow) extending to the superior sagittal sinus, indicative of a vascular malformation with a large draining vein. This was verified on DSA (C).

MRI

T2-weighted (T2W) imaging shows punctate to linear flow voids in the subarachnoid space over the brain, reflecting the dilated surface vessels. Within the brain, the punctate flow voids often lie within hyperintense, gliotic parenchyma. This gliosis may extend to the surrounding brain tissue. T1-weighted (T1W) imaging shows highly variable signal within the AVM, due to turbulent flow, blood degradation products, and the variable flow rate in the veins (Fig. 24-9). There is usually intense contrast enhancement of the vessels themselves. T2*-weighted images may detect smaller areas of hemorrhage.

FIGURE 24-9 A to C, MR aspect of a cortical AVM. A conglomeration of dilated vascular masses can be seen on both T2W (A) and T1W (B, C) images. The signal (especially on T1W sequences) depends on the velocity and direction of flow with both flow-void and/or enhanced areas. Remnants of recent or old bleeding have to be specifically sought using T2W GRE sequences (not shown) because AVMs that have bled once have a higher propensity to rebleed. FLAIR and T2W sequences should be evaluated for perifocal gliosis. Classically, the cortical AVMs extend wedge shaped into the subcortical areas within a sulcus.

MRA

“Static” magnetic resonance angiographic (MRA) sequences (such as time-of-flight [TOF] and phase contrast [PC] MRA) may detect the lesion but do not detail the angioarchitecture of the malformation (see Fig. 24-3). Static MRA provides little information about the presence of flow-related or intranidal aneurysms or the direct/indirect nature of the feeding arteries. Venous stenoses and ectasias are poorly displayed due to turbulent flow. Static MRA also fails to define the hemodynamics of the AVM, including the principal feeding arteries, the early venous drainage pattern, and the flow velocity.