Spinal Vascular Anatomy

The arterial supply to the spine is primarily derived from the segmental arteries. There are 31 paired segmental arteries corresponding to the 31 somites into which the embryo divides (rostrocaudally) during the first few weeks of development. Each segmental artery provides blood supply to its corresponding metameric derivatives: muscle, skin, bone, spinal nerve, and spinal cord. At the start of embryologic development, each segmental artery has a branch that supplies the cord. Over time, most of these branches regress, so that by the completion of embryologic development, of the 62 segmental arteries, 4 to 8 supply the anterior spinal artery and 10 to 20 supply the posterior spinal arteries.

The anterior spinal artery extends along the ventral spinal axis for the entire length of the spinal cord. Its caudal extension is known as the artery of the filum terminale. It may be recognized angiographically by its characteristic midline hairpin appearance. The normal anterior spinal artery diameter is in the range of 110 to 340 μm. The anterior spinal artery gives origin to between 200 and 400 sulcocommissural arteries, which lie within the ventral sulcus of the spinal cord. From the ventral sulcus, the arteries enter the central gray matter, at which point they give off branches to the peripheral white matter. Each sulcocomissural artery supplies either the right or the left side of the spinal cord. The sulcocommissural arteries supply the ventral half of the cord and the gray matter. The dorsal half of the spinal cord is supplied by branches of the paired posterior spinal arteries. Angiographically the posterior spinal arteries may be recognized by a similar but smaller hairpin appearance located laterally.

Each segmental artery accompanies its corresponding nerve into the neural foramen. Each segmental artery divides into dural and radicular arteries. The radicular artery provides supply to the dorsal and ventral nerve roots. Some segmental arteries provide supply to the spinal cord via branches connecting to the pial/coronal arterial network and are designated radiculopial arteries. Some segmental arteries provide direct supply to the anterior spinal artery and are designated radiculomedullary arteries. The two most significant radiculomedullary arteries are the artery of cervical enlargement and the artery of lumbar enlargement, also known as the arteria radicularis magna or the artery of Adamkiewicz.³

Venous drainage occurs through the radial and coronal veins, which in turn drain into the primary dorsal and ventral longitudinal collecting veins, which drain into the radicular veins, which drain into the ventral epidural venous plexus. The radial veins are also connected by lateral longitudinal veins. The ventral epidural venous plexus is a valveless system in which the direction of flow depends on the outflow vein at each anatomic level. In the cervical spine, the epidural venous plexus drains into the vertebral veins, which empty into the innominate veins. In the thoracic spine, the epidural venous plexus drains into the intercostal veins, which then drain into the azygos and hemiazygos veins. In the lumbar spine, the epidural venous plexus drains into the ascending lumbar vein, the azygos and hemiazygos veins, and the left renal vein. In the sacral spine, the epidural venous plexus drains into the sacral veins, which eventually empty into the internal iliac veins.

Classification of Spinal Vascular Malformations

The classification of spinal vascular malformations has evolved significantly over the last 150 years as the understanding of the complex pathophysiology of these lesions has continued to improve. The initial classification schemes that were proposed failed to properly categorize the lesions based on their anatomy. The first classification scheme for spinal vascular lesions was proposed by Virchow in 1858.⁴ Virchow subdivided vascular lesions into two types: angioma cavernosum (lesion without parenchyma between the blood vessels) and angioma racemosum (hamartoma: lesion with parenchyma between the blood vessels). Elsberg, in 1916, was the next to propose a classification scheme for spinal vascular lesions in which he divided them into three categories: aneurysm of spinal vessels, angioma in which a mass of dilated veins penetrates the spinal cord, and dilation of posterior spinal veins. In 1928, Cushing and Bailey proposed yet another classification system in which they divided spinal vascular lesions into two major groups: hemangioblastomas and vascular malformations. The broad group of vascular malformations included plexus of dilated veins, aneurismal varix, venous angioma, and telangiectasias.

Advances in neurointerventional surgery and microneurosurgery during the 1960s and 1970s combined with a clearer understanding of the true pathophysiology of spinal vascular lesions led to the development of a new classification system that divided spinal vascular malformations into types I to IV. This system, which is still widely used today, did not include neoplastic lesions (Table 91-1). The classification system proposed by Rodesch and colleagues divided spinal vascular malformations into three groups: AVMs, fistulas, and genetic classification of spinal cord arteriovenous shunts.⁵ The last group was further subdivided into three groups: genetic hereditary lesions (macrofistulas and hereditary hemorrhagic telangectasia), genetic nonhereditary lesions (multiple lesions with metameric or myelomeric associations), and single lesions (incomplete associations of either of the first two categories). The classification system for spinal vascular lesions proposed by Spetzler and colleagues also subdivided the lesions into four large groups: neoplasms, spinal aneurysms, spinal AVMs, and spinal fistulas.⁶ Arteriovenous fistulas (AVFs) were further subdivided into extradural and intradural (dorsal or ventral). AVMs were further classified into extradural-intradural or intradural. Intradural AVMs were further subclassified as intramedullary, compact, diffuse, and conus medullaris. This separate classification of conus medullaris AVMs is unique to the Spetzler system.⁶

TABLE 91-1 Common Classification of Spinal Vascular Malformations

AVF, Arteriovenous fistula; AVM, arteriovenous malformation; ASA, anterior spinal artery.

Of these classification systems, the type I through IV system remains the most commonly used. Type 1 spinal vascular malformations are actually dorsal intradural AVFs with the fistulas located in the proximal dura of the nerve root sleeve. These malformations are the most common spinal vascular malformation. They are subdivided into type A, in which the malformation is supplied by a single arterial feeder, and type B, in which the malformation is supplied by multiple arterial feeders.⁷ They occur most commonly in the lower thoracic and upper lumbar segments of the spinal cord, T4–L3, with the peak incidence between T7 and T12.⁸

In type IA malformations, the fistula is formed by an anastomosis of a dural branch of a radicular artery (very rarely a radiculomedullary artery) and a radiculomedullary vein.

In type IB malformations, there are anastomoses between branches of several adjacent radicular arteries and a radiculomedullary vein. The radiculomedullary vein becomes arterialized owing to increased flow and pressure, which it transmits to the valveless coronal plexus and the longitudinal veins. The radiculomedullary vein becomes enlarged and tortuous, leading to its classic angiographic appearance. Studies have shown that the mean intraluminal venous pressure is increased to 74% of the systemic arterial pressure.⁹ The normal pressure in the coronal venous plexus is approximately twice that of the epidural venous plexus. This significant pressure gradient is necessary for normal venous drainage. When it is compromised, as in the case of type I spinal AVMs, venous hypertension develops. Venous hypertension then leads to the development of progressive myelopathy due to transmission of increased venous pressure to the spinal cord parenchyma, resulting in multiple pathologic changes including demyelination.

Type II spinal vascular malformations are true AVMs of the spinal cord with multiple arterial feeders, a nidus, and draining vein(s). They are structurally similar to cerebral AVMs. They are the second most common spinal vascular malformation. They are high-flow, low-resistance, high-pressure lesions.⁶ The arterial feeders are usually branches of the anterior spinal artery or the posterior spinal arteries.

Type III spinal vascular malformations, also known as juvenile AVMs or metameric AVMs, are more diffuse lesions that can encircle the entire spinal cord. Involvement of all the derivatives of a metamere in the AVM (skin, bone, muscle, dura, nerve roots, and spinal cord) has been described as Cobb’s syndrome.

Spinal artery aneurysms or venous aneurysms are found in 20% to 40% of patients with intramedullary AVMs. The presence of a spinal artery aneurysm has been associated with an increased risk of hemorrhage.¹⁰

Type IV spinal vascular malformations are actually perimedullary AVFs and were first described by Djindjian and colleagues. The fistula occurs ventrally and in the midline between the anterior spinal artery and the coronal venous plexus.¹¹ In contrast to type I dural AVFs, type IV lesions are high-flow fistulas. These lesions are further classified into three subtypes. Type A (Merland subtype I) is a solitary AVF fed by the anterior spinal artery (ASA) and located at the conus medullaris or the filum terminale. There is moderate venous hypertension without enlargement of the ASA. The ascending draining vein is only minimally dilated. Type B (Merland subtype II) is a small group of AVFs located at the conus and supplied by the anterior and posterior spinal arteries. The feeding arteries and draining veins are moderately dilated. Venous ectasia is present at the site of the fistula, and the ascending perimedullary veins are tortuous and enlarged. Type C (Merland subtype III) is a single large AVF supplied by the anterior and posterior spinal arteries and located in the cervical or thoracic spinal cord.¹² The draining vein is significantly dilated and ectatic and may be embedded within the spinal cord.

Clinical Presentation and Natural History

Type I spinal dural AVFs typically manifest with signs and symptoms of progressive myelopathy. They are more common in men and usually present in the sixth decade of life. Gradually worsening paraparesis accompanied by sensory loss is the most common presentation. Patients can also present with back pain, leg pain, sphincter dysfunction, and sexual dysfunction. Although gradual progression of symptoms is the most likely presentation, patients can present with acute exacerbation of their symptoms. Hemorrhage is very rare.

Type II spinal AVMs typically manifest with hemorrhage, intramedullary or subarachnoid, which results in acute myelopathy. Patients can also present with progressive myelopathy secondary to arterial steal. Pain may also be a presenting symptom. The majority of patients present before age 40 years. Type II spinal AVMs demonstrate no gender preference.

Type III spinal AVMs, similar to type II spinal AVMs, can manifest with hemorrhage resulting in acute neurologic deficit or with progressive myelopathy secondary to steal phenomenon. They occur more commonly in children.

Type IV spinal vascular malformations commonly manifest with progressive paraparesis secondary to myelopathy caused by venous congestion, but they can also manifest with acute neurologic deficit secondary to rupture of a feeding artery aneurysm. They occur more commonly in adults but can be seen in children.¹⁰ Patients typically present before the age of 40 years.

Osler-Weber-Rendu syndrome (hereditary hemorrhagic telangectasisa) type 1 is an autosomal dominant disorder associated with spinal arteriovenous shunts. The syndrome is typically associated with type IV, subtype C intradural AVFs. Klippel-Trenaunay and Parkes-Weber syndromes are associated with vascular malformations of the lower limbs and can involve spinal cord vascular malformations.³

The pathophysiology of spinal vascular malformations was elegantly detailed by Aminoff and Logue¹³ in a paper published in 1974 in which they refuted the previous theories of compression of the cord by the malformation being the primary cause of symptoms and argued that the most likely mechanism of neurologic deterioration was secondary to ischemia caused by venous hypertension. Aminoff and Logue further argued that support could be garnered for this theory by the fact most symptomatic spinal vascular malformations are located in the lower thoracic or thoracolumbar spine, where there are fewer large veins draining into the coronal plexus, compared to the cervical or upper thoracic spine. Histopathologic support for this theory has subsequently been provided by Matsuo and colleagues, who performed autopsies on three patients with progressive myelopathy and found evidence of venous congestive myelopathy. The spinal cord parenchyma at the affected levels demonstrated neuronal loss and gliosis with increased numbers of hyalinized vessels.¹⁴ Autopsy also demonstrated tortuous, dilated venous vessels on the dorsal surface of the spinal cord at the affected levels.

Endovascular Management