Lesions at the cortex

Arteriovenous lesions exclusively involving the cortex are exclusively fed by cortical arteries and drain into superficial veins. These lesions represent sulcal AVMs, as described by Valavanis and Yasargil.⁵

Cortical-subcortical 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 represent the gyral type of AVMs described by Valavanis and Yasargil.⁵

In both cortical and cortical-subcortical lesions, some regions of the cortex drain to deeply located veins that should not be considered as truly part 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 pyramid-shaped malformation, reaching the ventricular wall at their apex. Feeding arteries are both perforating and cortical. Draining veins are also deeply and superficially located.

Corticocallosal lesions belong to the corticoventricular group, inasmuch as they have the same venous characteristics, but they do not recruit “basal perforating” arteries. They 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 to choroidal arteries at the splenium.

Deep-seated lesions

Deep-seated lesions can be located supratentorially or infratentorially in the depth of the telencephalon, diencephalon, brainstem, or cerebellum. The nidus involves the deep nuclei and the long fiber tracts with their arterial and venous connections. They recruit exclusively perforating arteries and drain into the deep venous system. They may use transcerebral veins if patent, either as a direct venous outlet or as a collateral pathway. Transcortical arteries from the insular branches of the middle cerebral artery and the hemispherical collateral vessels of the cerebellar arteries can be involved in lenticulostriate and in dentate nuclear lesions, respectively. MRI and DSA are able to distinguish these deep-seated lesions from corticosubcortical lesions, particularly because the dominant supply of the intracerebrally located deep lesions arises from the perforators.

Choroid plexus lesions

Choroid plexus AVMs are important to recognize because of their extra-axial location. These lesions are fed by choroidal and subependymal arteries arising from the circle of Willis. There is no cortical arterial supply in this type of lesion. Drainage is via ventricular veins, with occasional recruitment of transcerebral veins. These extra-axial lesions, too, can be distinguished from intra-axial ones with angiographic criteria.

Hereditary hemorrhagic telangiectasia

HHT is an autosomal dominant disorder characterized by a multisystemic vascular dysplasia and recurrent hemorrhage.⁶ Two gene mutations have been identified: on chromosome 9 (affecting production of endoglin; this form is known as type 1)⁷ and on chromosome 12 (affecting production of activin receptor-like kinase; this form is known as type 2). An uncharacterized third mutation is also suspected. These mutations lead to the formation of abnormal vessels and abnormal connections between vessels. It has to be emphasized that the target of dysfunction in HHT is not in arteries but in venules.

In the general population of patients with BAVMs, up to 2.2% of cases may be associated with HHT.⁸ With multiple BAVMs, however, up to 25% of cases are associated with HHT.⁹ Ten percent to 20% of HHT patients have cerebral involvement.¹⁰ In these patients, the cerebral vascular malformations manifest in three main phenotypes: large AVFs, small AVMs with a nidal diameter between 1 and 3 cm, and micro-AVMs with a nidal diameter smaller than 1 cm. These AVMs are often multiple and are almost exclusively located near the cortex.^8,11 Although characteristic telangiectasia occur in the skin, oral mucosa, and the lips of patients with HHT, telangiectasia is not known to develop in the brain. High-flow type AVFs with venous ectasias are seen in children younger than 5 to 6 years of age; nidus-type lesions both large and small are seen in older children and in adults.^1,12–14 Twenty-five percent of single AVFs in children and 50% of multifocal AVFs occur in patients with HHT.

Cerebral DSA may demonstrate multiple areas of arteriovenous shunting, always cortical in location, either supratentorial or infratentorial. In addition, high-quality cerebral DSA can demonstrate tiny lesions, particularly micro-AVMs, which may appear occult on MRI, because these lesions usually have normal-sized feeding arteries and draining veins.¹⁰

However, patients with HHT who present with systemic complaints are more likely to develop acute neurological symptoms from embolic phenomena related to underlying pulmonary AVFs (recurrent brain abscesses, embolic stroke) than to the presence of a BAVM per se.

Cerebrofacial arteriovenous metameric syndromes

CAMSs,¹⁵ also called Wyburn-Mason or Bonnet-Dechaume-Blanc syndrome, are associated with ipsilateral AVMs of the brain, retina, and facial regions. Their segmental expression reflects their common origin from tissues involved in cerebrofacial vasculogenesis and angiogenesis. The metameric pattern of involvement is suggestive of a disorder of the neural crest or adjacent cephalic mesoderm¹⁵ at early segmental stages of differentiation.

Unclassified multiple brain arteriovenous malformations

Several case reports have described so-called multifocal BAVMs. They seem to be twice more frequent in children than in adults. They can be randomly spread on the cortex; mirror-image deep-seated nidi have been reported. One half of multifocal AVFs in children belong to this group.^1,14

Proliferative and hemorrhagic angiopathies

Proliferative and hemorrhagic angiopathies are entities often confused with BAVMs. They are rare, proliferative, vascular lesions seen usually in children and young women.

The appearance of proliferative angiopathy is typically that of a nidus-like cortical network of vessels intermingled with normal brain parenchyma, and the veins are either normal sized or only slightly enlarged. The “nidus” is typically diffuse, involving a hemisphere. There are no dominant arterial feeders. The early venous filling that is observed results from a faster capillary transit time rather than true arteriovenous shunting. Late proximal cerebral arterial occlusion may occur, resulting in ischemic phenomena and diffuse transdural angiogenesis. The most common clinical manifestation is seizures. Headaches and progressive neurological deficit are less common, and hemorrhage is exceptional. Treatment is directed at the management of seizures with medical therapy. Embolization is employed in exceptional cases: when there is evidence of focal angioarchitectural weakness within the lesion, for which partial targeted embolization to reduce any constraints to functional parts of the brain may be beneficial. The effects of medication on headaches and seizure are often beneficial. The role of surgery is limited to the correction of hemispherical ischemia by bur holes, as in moyamoya disease, when spontaneous transdural angiogenesis is absent or insufficient.

Hemorrhagic angiopathy is another entity that typically manifests with an episode of hemorrhage. Encountered in some rare cases of intracerebral hematomas in children most often after the age of 5 years, it corresponds to a network of intracerebral subcortical arterioles with normal structure and sequential venous drainage. Recurrent hemorrhage is frequent and therefore therapy is indicated. These lesions are extremely sensitive to radiation. Partial embolization of focal areas of weakness in the angioarchitecture can also be performed to reduce future hemorrhagic risk.

Developmental venous anomalies with ectasias

Developmental venous anomalies (DVAs) are anatomical variations that can involve one or both hemispheres and can also be located infratentorially. They involve extremes in variations in the venous drainage of white matter. Superficial DVAs represent the superficial medullary veins that drain the deeper medullary regions into the cortical veins. The deep group of DVAs drains the subcortical territories of the superficial medullary veins into the deep venous collectors. The venous channels are morphologically normal and drain normal functioning brain, although transit time through their venules is sometimes rapid and almost as rapid as that in slow-flow BAVMs. The frequent incidental appearance of DVAs on cross-sectional imaging and angiography attest to their benign nature. Any associated clinical symptom is caused primarily by associated malformations (cavernomas or arteriovenous shunts). Their lack of flexibility as a result of being an anatomical variant of the venous drainage to the brain in the region may also produce ischemic episodes of varying severity. However, because DVAs drain normal areas of the brain, they should never be eradicated. Rarely does a true AVM drain into a DVA. In this instance, a true arteriovenous shunt is demonstrated within an otherwise normal network of vessels. Treatment of such patients requires extreme care to preserve normal venous channels.