Vascular Malformations of the Spine

History and Nomenclature

Spinal vascular malformations encompass a broad family of angiopathic abnormalities affecting the blood supply to the spinal cord and its associated structures. They are generally rare, usually presenting clinically with myelopathies, radiculopathies, and other neurological deficits secondary to hemorrhage, ischemia as a consequence of vascular steal, or cord compression. The earliest description of spinal vascular malformations was put forth by pathologist Rudolf Virchow in 1863, who detailed two groups of what he termed “neoplasms”: angioma cavernosum, without parenchyma between the affected blood vessels, and angioma racemosum or hamartoma, in which affected vessels were separated by parenchyma. ^, The work of Cushing and Bailey in 1928 and Bergstrand et al. in 1936 recategorized spinal arteriovenous malformations (AVMs) as both neoplastic and vascular malformations, the latter category was further supported by the work of Wyburn-Mason in 1943 who referred largely to Virchow’s original terminology. Although these classifications were useful in pathological terms, the clinical management of spinal AVMs (SAVMs) did not advance substantially until 1971 following the work of Di Chiro and colleagues, who described the first classification of spinal arteriovenous (AV) shunts based on angiography, and Kendall and Logue’s 1977 study using selective angiography to initially demonstrate the fistulous component of AVMs as their true pathological component. ^,

Broadly speaking, AVMs can be grouped into two broad categories: nidal (AVMs) or fistular (arteriovenous fistulae [AVFs]). Nidal types are distinguished by a network of abnormal connections between arterial feeders and draining veins, and in contrast, fistulae are a direct artery-to-venous connection. In the discussion of SAVMs specifically, a series of multicenter collaborations between the 1960s and 1980s produced the first of several overarching classification systems, initially consisting of three types of lesions: type I/dural AVFs (angioma racemosum), type II/glomus AVMs, and type III/juvenile AVMs. This classification was expanded upon with the addition of type IV/intradural perimedullary (direct) AVFs by Heros et al. in 1986. Alternatively, a system proposed in 2002 by Spetzler et al. distinguished four broad categories of spinal vascular malformations: spinal AVFs and AVMs (including conus medullaris AVMs), neoplastic vascular lesions, and spinal aneurysms. ^{, , ,}

Embryology and Vascular Anatomy

Blood supply to the fetal spinal cord develops in four stages . In the first several weeks of development, 31 somites are formed in a craniocaudal direction, adjacent to the notochord/developing neural tube. Formation of these structures is induced by the adjacent mesoderm and notochord. The first, or primitive segmental, stage is marked by each somite level receiving two segmental arteries growing dorsally from the paired dorsal aortae. These segmental vessels divide into dorsal and ventral branches, the latter forming a capillary network on the ventrolateral surface of the neural tube and developing further into paired ventral arterial tracts, which eventually fuse to become the anterior spinal axis during the third stage of development. Dorsal longitudinal tracts develop secondarily alongside intrinsic blood supply to the cord (sulcal arteries that branch from ventral longitudinal axes). The second, or initial, stage, thought to be key for the development of dorsal anastomoses forming the pair of future posterior spinal arteries (PSAs), and thus the likely stage of genesis for most SAVMs, occurs from weeks 3 to 6 of fetal development. During this stage, the formation of venous networks on the ventral and dorsal aspects of the spinal cord are formed as well, eventually expanding to form an interconnected capillary network. The third, or transitional, stage occurs between week 6 and month 4 of development, wherein we see the formation of the adult pattern of vascular supply take place, typically around week 10. The primitive longitudinal tracts of the ventral surface fuse in this stage, and we see a reduction of the medullary branches of segmental arteries augmenting the now largely formed anterior spinal axis, the eventual anterior spinal artery (ASA). Those dorsal and ventral medullary branches (sometimes referred to as segmental medullary arteries) still in place provide supportive flow to the main longitudinal arteries of the spinal cord. Following the transitional stage after month 4, the fourth and final, or terminal, stage is marked by maturation of the formed vessels and an increased tortuosity of vasculature. Of those discussed, the second stage is thought to be key to formation of vascular malformations, as maldevelopment in this stage can lead to persistence of primitive capillary anastomoses, AVFs and thin-walled, tortuous vessels, all potentially key pathological contributors.

The blood supply for the fully formed adult spinal cord consists of three main arteries––the previously discussed paired PSAs and singular ASA. The PSAs run the length of the spinal cord, branching off of either the posterior inferior cerebellar artery or the vertebral artery to supply its dorsal third. The ASA is the main source of blood supply to the spinal cord, supplying its anterior/ventral two-thirds. The ASA is formed from a fusion of branches from each of the bilateral vertebral arteries at the level of the foramen magnum and descending along the ventral aspect of the spinal cord, overlying the anterior longitudinal fissure. The ASA/PSAs narrow caudally and are fed by additional connecting arteries, medullary branches of segmental arteries. At the thoracic, lumbar, and sacral levels there are segmental spinal arteries branching posteriorly from the intercostal arteries, lumbar or iliolumbar arteries, common iliac arteries, or lateral sacral arteries. Each segmental artery proceeds to pass through the intervertebral foramen as a spinal branch, dividing into dural and radicular arteries, and at some levels medullary branches, all after penetration of the outer dural layer covering the nerve roots of the foramina. The dural arteries supply the dura, the radicular arteries supply the anterior and posterior nerve roots, and, at levels where present, the medullary arteries follow nerve roots inside the dura to anastomose with the ASA or one of the PSAs. Because of the potential ischemia induced with the partial involution of a number of medullary branches, which is a particular risk in the thoracolumbar region, there is a great radicular artery of Adamkiewicz, or arteria radicularis magna, a key blood supply structure typically observed branching from the left side of the descending aorta, at a variable vertebral level between T5–L3. The venous drainage of the spinal cord generally follows that of the arterial pattern, but most anatomic specimens demonstrate a single anterior and single posterior median spinal vein, with both connected by multiple circumferential veins following the curvature of the cord, combining to form the coronal venous plexus on the cord surface, which proceeds to drain out via the medullary veins. These leave the dural sheath to join the epidural venous plexus or internal vertebral venous plexus within the extradural adipose tissue, also known Batson’s channels, and draining posteriorly via basivertebral veins to the external vertebral venous plexus (anterior and posterior), draining out via the deep cervical vessels, the azygous system, and the lumbar veins.

Imaging Techniques

The management of SAVMs has progressed substantially in the last century. One of several keys to this progress has been the enhancement of imaging techniques, which has allowed surgeons to transition from prior high-risk exploratory laminectomy to a carefully planned approach. Since its first reported use in studying SAVMs in 1967, spinal angiography has been considered the crucial component of preprocedural planning, but the use of less invasive imaging techniques to provide initial diagnosis, visualize adjacent neurological structures, and guide subsequent steps have been a point of some debate. ^,

Myelography, or x-ray studies with injected contrast agents, first allowed the static visualization of tortuous vessels as flow voids in the subarachnoid space. Subsequently this technique was combined with computed tomography (CT) scanning, referred to as a CT myelogram, which shows 100% sensitivity, allowing an enhanced visualization of the spinal cord’s margins. The MRI followed soon after, and has all but replaced myelography in SAVM assessment, given its status as a relatively noninvasive alternative with superior soft tissue contrast, with the exception of patients unable to undergo an MRI. MRI studies use T1-weight imaging and T2-weighted imaging sequences to evaluate for suspected myelopathy to potentially show key features of underlying SAVM. The most classically described findings on initial MRI include evidence of underlying edema/vascular congestion presenting as a hyperintense signal on T2-weighted imaging (or mixed hypo/hyperintense signal on T1-weighted imaging), and of potential vessel dilation appearing as flow voids, ^{, ,} with a 2012 study showing that the standard T2-weighted imaging MRI has 100% sensitivity in showing lesions, also ruling out multiple other potential pathologies with relatively high sensitivity. Whereas clinical diagnosis of SAVMs at this point rests mainly on MRI, digital subtraction angiography (DSA) still is necessary.

In localization and identification of specific feeding arteries, magnetic resonance angiography can be helpful and avoid superfluous injections of all possible feeders; however, given the comparatively large field of view, there is poor spatial resolution. CT angiography has also been used for procedures with relatively high sensitivity. In the event the arterialized veins are too small to visualize, contrast enhancement may additionally play a pivotal role at diagnosis. With contrast-enhanced magnetic resonance angiography, the fistulous connection can be traced by following the small size and relatively slow flow structure of feeding intercostal or radiculomeningeal artery to the fistula itself. Also used is time-resolved imaging of contrast kinetics (four-dimensional magnetic resonance angiography [4D MRA]), which in one study showed higher specificity in identifying the location of the arterial feeder to within one vertebral level in 81.8% of patients. Additionally, 4D MRA can follow the first pass of contrast through the vasculature to also show flow dynamics over time, a key addition in the event of arteriovenous shunting, retrograde flow, or delayed vessel enhancement. ^, However, these sequences are to be considered a supplement to guide diagnostic DSA, rather than a replacement for DSA itself. In the case of MRA, should the examination suggest the level of malformation, spinal conventional angiography may then include at least injection of the segmental arteries, on both sides, one level above and below the suggested level.

DSA has long been considered the gold standard of imaging when performed under optimal technical conditions, particularly in SAVM classification and diagnosis. Occasionally DSA can be performed with an aortogram, which has proved helpful in the setting of an atherosclerotic or dilated aorta where segmental artery catheterization may be difficult. In some cases feeding arteries and local lesion angioarchitecture may be difficult to appreciate, in which case cerebral angiography may also be indicated. ^, There is some evidence that for some complex cases, such as conus medullaris lesions, the use of three-dimensional digital subtraction angiography is also useful in differentiating intramedullary from perimedullary surface lesions, as well as feeding arteries. Other variations on spinal angiography have been studied and shown to be effective, such as three-dimensional rotational subtraction angiography, fusion techniques combining multiple three-dimensional angiographic scans to improve capture of detail, and a time-resolved method, four-dimensional DSA, illustrates contrast in- and outflow with time, among others, but none have yet supplanted DSA as the primary diagnostic modality in SAVM treatment.

Extradural Arteriovenous Fistulas

A spinal extradural arteriovenous fistula (SEDAVF) is a rare and unique spinal arteriovenous lesion, defined as a direct connection between one or more arteries, usually the dorsal somatic branch, to the extradural venous plexus within the spinal canal and/or intervertebral foramen ( Fig. 53.1A ). The bone structure adjacent to the fistula may be involved. SEDAVFs have also been described as “epidural,” “paravertebral,” or “osteodural” AVFs, as well as spinal dural arteriovenous fistulas (DAFs) with epidural venous drainage. SEDAVFs are more likely to have bilateral segmental artery supply than their dural counterparts. They may or may not have secondary retrograde intradural venous drainage. ^{, , ,}

Type 1 Dural Arteriovenous Fistulas