Vascular Malformations

CHAPTER 24 Vascular Malformations

Four major types of primary malformations of the vascular systems can be identified: arterial, arteriovenous, capillary, and venous. Each of these malformations manifests intrinsic primary abnormalities and each causes derivative secondary change in the rest of the vascular system. Classically, these vascular malformations are grouped into four categories (1) the dural and pial arteriovenous malformations and shunts, (2) cavernous malformations (cavernomas), (3) capillary telangiectasias, and (4) developmental venous anomalies.



Pial Malformations

Arteriovenous shunts correspond to an abnormal capillary bed with a shortened arteriovenous transit time. The shunts are located in the subpial space, are fed by arteries that normally feed the brain parenchyma, and are drained by pial veins. Two categories of arteriovenous shunts—arteriovenous malformations (AVMs) and the arteriovenous fistulas (AVFs)—may be differentiated by their different angioarchitecture at the transition between feeding artery and draining vein.

AVMs are characterized by a network of abnormal channels (the nidus) interposed between the arterial feeder(s) and the draining vein(s). The shunts may be small (micro-AVMs) with a nidus less than 1 cm in diameter and normal size arteries and draining veins, or the shunts may be larger (macro-AVMs) with nidi larger than 1 cm in diameter and enlarged feeding arteries and draining veins. AVMs may be compartmentalized into portions fed and drained by separate vessels, as documented by angiography or at surgery. In many cases of pial AVMs the separate compartments exhibit differing internal angioarchitecture with more fistulous or more glomerular nidal appearances (see later) within the different compartments (Fig. 24-1).

AVFs consist of direct, fistulous transitions from an artery into a vein. They, too, can be classified as micro-AVF or macro-AVF depending on the size of the feeding artery. The AVFs are found almost exclusively on the surface of the brain or the spinal cord. Pial AVFs appear to be relatively frequent in children and rare in adults (Fig. 24-2).

Arteriovenous Malformations that Involve the Cortex

Cortical arteriovenous lesions involve the cortex, are fed exclusively by cortical arteries, and drain into superficial veins (unless secondary thrombosis of cortical veins shunts the venous flow into alternate pathways). These lesions are also designated sulcal AVMs (Fig. 23-3).

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.


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.


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.


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.



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.


“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.

High-resolution, 3D, dynamic contrast-enhanced MRA provides greater information about the velocity and direction of blood flow through each component of the AVM and can confirm the diagnosis of an AVM suggested by prior conventional MRI and MRA (Fig. 24-10). Complex subtraction techniques help to eliminate artifactual signal resulting from intraparenchymal hemorrhage. However, caution must be taken in very fast-flow AVMs, because the rapid flow results in poorer contrast of the feeding arteries compared with normal vessels and draining veins (Fig. 24-11).

Functional imaging methods such as blood oxygenation level–dependent contrast (BOLD) fMRI and perfusion imaging may give additional information about the pathophysiology of these AVMs (Fig. 24-12).

Conventional Digital Subtraction Angiography

Conventional catheter angiography remains the study of choice to evaluate all potential feeding arteries, including external carotid branches that can supply the AVM via dural and leptomeningeal collaterals. Digital subtraction angiography (DSA) also provides a full assessment of the other vascular territories to rule out multiple shunts that may indicate an underlying systemic disease (e.g., hereditary hemorrhagic telangiectasia) or a syndromic disease such as cerebrofacial arteriovenous metameric syndrome. DSA should define the angioarchitecture of all feeding arteries, determine whether the shunt is a direct or indirect type, and display all significant arterial dilatations, stenoses, and associated flow-related aneurysms (Fig. 24-13). DSA should define the nidus, including its size, fistulous versus glomerular nature, intranidal aneurysms, false aneurysms (in case of hemorrhagic AVMs), associated angioectasia, and neoangiogenesis. DSA should also display all of the draining veins to resolve deep versus superficial patterns of drainage, length of the pial segments, venous ectasias, and any stenoses that might cause flow restriction. DSA is paramount, therefore, for ascertaining the risk posed by an individual brain AVM and for selecting the therapy best suited for that specific AVM (Fig. 24-14).

Two conditions merit special imaging consideration:

Differential Diagnosis

Two significant entities must be considered in the differential diagnosis of cerebral AVMs: (1) cerebral proliferative angiopathy and (2) segmental vascular syndromes with brain AVMs.

Cerebral Proliferative Angiopathy

Cerebral proliferative angiopathy (CPA, diffuse nidus type AVM) is a clinical entity distinct from the “classic” brain AVMs in its clinical presentation, natural history, angioarchitecture, and treatment. CPA is present in 2% to 4% of all brain AVMs. It is more common in females by 2 : 1 and presents at a mean age of 20 years. Seizures, headaches, and transient ischemic attacks are far more frequent in CPA than in classic AVMs, whereas hemorrhages are exceedingly rare. On CT and MRI, CPA presents as a diffuse network of densely enhancing vascular spaces intermingled with normal brain parenchyma. T1W and T2W images show small, widely distributed flow voids that may involve multiple lobes or the entire hemisphere (Fig. 24-16). In most cases, the primary lesion extends from the surface into the basal ganglia and thalamus and involves more than one vascular territory. Compared with the size of the nidus, relatively few draining vessels are seen on CT or MRI, and these are only moderately enlarged. Perfusion-weighted MRI demonstrates perfusion abnormalities far beyond the boundaries of the morphologic malformation seen on conventional MR sequences, so the disease actually affects the entire hemisphere. The nidus shows increased cerebral blood volume, slightly decreased time to peak (TTP), and prolonged mean transit time (MTT). Remote from the nidus, in normal-appearing cortical and subcortical areas, the TTP is increased and the blood volume is decreased, indicating remote, widespread hypoperfusion (Fig. 24-17). Angiography shows no dominant feeders. Instead, CPA is fed by multiple arteries that are not enlarged or are only moderately enlarged. Unlike classic AVMs, all arteries of the affected region contribute equally to the malformation. Stenoses of the proximal arteries are present in 40% and affect the internal carotid artery (ICA) and the proximal horizontal segments of the middle cerebral artery (M1) and anterior cerebral artery (A1). Most cases show transdural supply to both the malformation and the normal brain tissue. The nidus has a classic appearance with scattered areas of “puddling” of contrast medium within what looks like capillary ectasias. These persist into the late arterial and early venous phases. The nidus is usually fuzzy, poorly circumscribed, and larger than 6 cm in diameter. Intranidal vessels show a capillary angioectasia. Perinidal angiogenesis is often present and difficult to distinguish from the nidus proper. There is no high-flow fistulous component to the arteriovenous shunt, so early opacification of draining veins is uncommon. The size of the draining veins, the “shunt volume,” and the time until the veins are visualized never “correspond” to the size of the nidus. Histopathology demonstrates the presence of normal-appearing neural tissue intermingled between these vascular channels. Perivascular gliosis is only mild. There is additional capillary angiogenesis within the subcortical region (Fig. 24-18). The implication is that the brain tissue within the “nidus” of the CPA is functional, similar to the brain tissue found between the abnormal vascular channels of capillary telangiectasia. This alters therapeutic strategies. Because these lesions appear to result from ischemia, therapy should be directed toward revascularization procedures, such as burr-hole therapy, not at the lesion proper.

The name “cerebral proliferative angiopathy” implies that new vessel formation is an important component of the disease. This is very different from classic AVMs. Meningeal vessels contribute to the lesion directly and contribute to the healthy brain tissue bilaterally via supratentorial and infratentorial transdural supply. Presumably the angiogenesis is induced by the (relative) cortical ischemia demonstrated with perfusion-weighted MRI, although the signaling mechanism remains unknown. It is not related to previous hemorrhage and does not suggest increased risk of hemorrhage in the future.

The combination of segmental stenoses of proximal arteries and distal angioectasia suggests that the pathogenesis of this lesion may be abnormal proliferation of the vessel wall. In their 1975 classification of vascular lesions in childhood and infancy, Mulliken and Glowacki differentiated between (1) vascular lesions that demonstrate cellular proliferation and endothelial hyperplasia (“hemangiomas” or true vascular tumors as in PHACES syndrome) and (2) vascular lesions that have normal endothelial turnover but structural abnormalities of the capillary, venous, lymphatic, or arterial channels (e.g., vascular malformations like brain AVMs). CPA can be regarded as an intermediate or transitional form between these two major types of vascular lesion. CPA exhibits both proliferative features (less prominent than in hemangiomas) and malformative features (less prominent than in true AVMs).

Segmental Vascular Syndromes with Brain AVMs

The significance of concurrent AVMs of the face, retina, and brain was first recognized in Lyon, France, by Bonnet, Dechaume, and Blanc, who reported two cases in 1937. Six years later, Wyburn-Mason published a detailed analysis of all similar case reports and nine new cases. The association of retinal, facial, and cerebral vascular malformations became known as Bonnet-Dechaume-Blanc syndrome in France and continental Europe and as Wyburn-Mason syndrome in the English literature.

Recent genetic/biologic contributions suggest that disorders of neural crest and cephalic cell migration may be the link common to all components of this syndrome. The neural crest and neural plate share a common lineage from cells of the lateral border of the developing neural plate (i.e., the neural folds). Under inductive influence of the adjacent epithelium (and possibly mesoderm) these cells develop into neural crest cells, hence their common metameric origin with the cells of the hindbrain. The insult producing the underlying lesion has to be before the migration occurs and thus before the fourth week of development.

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Jan 22, 2016 | Posted by in NEUROLOGICAL IMAGING | Comments Off on Vascular Malformations

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