Classification of Spinal AVMs

The classification of spinal AVMs has evolved with and been limited by the technology available to study them. Before the advent of selective spinal angiography, all spinal vascular malformations were attributed to venous lesions situated on the surface of the spinal cord. In 1914, Dr. Charles Elsberg of New York performed the first successful operation on a spinal AVM.1 Elsberg excised a 2-cm segment of an abnormal dilated spinal vein as it penetrated the dura of the T9 spinal nerve root. Postoperatively, the patient improved and made a complete neurological recovery 3 months after surgery.

In the 1960s, selective spinal angiography demonstrated the precise radiographic anatomy of spinal AVMs and led to a new classification based on their vascular anatomy and pattern of blood flow rather than on postmortem pathology.2 Thereafter, spinal AVMs were classified radiographically into three categories. Type I AVMs (single-coiled vessel) were thought to comprise 80 to 85% of all spinal AVMs. Type II (glomus) and type III (juvenile) AVMs accounted for 15 to 20% of the lesions. In all three types, the nidus was believed to lie within the spinal cord or pia mater. In 1977, Kendall and Logue demonstrated that the single-coiled vessel spinal AVM (type I) was the result of an arteriovenous (AV) fistula at the level of the dural sleeve of a spinal nerve root.3 After undergoing simple surgical excision of the fistula without surgical stripping of the single-coiled vessel, the patients uniformly improved or stabilized.

Kendall and Logue′s work resulted in a revised classification scheme for spinal AVMs.4 Based on differences in origin, epidemiology, anatomy, pathophysiology, and clinical presentation, three categories of spinal vascular malformations were recognized: (1) spinal-dural AV fistulae arising at the nerve root dural sleeve (radiculomedullary AV fistulae), (2) intradural vascular malformations (glomus, juvenile, or perimedullary), and (3) cavernous malformations of the spinal cord. Intradural vascular malformations are further classified into three subgroups: type II or glomus AVMs, type III or juvenile AVMs, and type IV or direct perimedullary AV fistulae. This classification continues to serve as the classic view of spinal AVMs.

The past decade has brought many advances in three-dimensional (3D) imaging technology and, as such, several groups have called for a reappraisal of the classification of spinal AVMs.5–8 Although other classification systems have been proposed, the classic type I to IV nomenclature persists throughout the literature. In 2002, Spetzler and colleagues initially proposed a modification to the classic classification system based on anatomical location and pathophysiological factors.7 The system divided spinal AVMs based on anatomical descriptors, such as extradural or intradural, extramedullary or intramedullary, and ventral or dorsal. From this work, a new classification proposed by Kim and Spetzler evolved.5 The new classification system is important because it not only divides lesions based on anatomical location but makes an important distinction between AV fistulae and AVMs, which carry separate classifications of natural history, pathophysiology, treatment, and prognosis. Their classification scheme divides vascular lesions of the spinal cord into six categories: (1) extradural AV fistulae, (2) intradural dorsal AV fistulae, (3) intradural ventral AV fistulae, (4) extradural–intradural AVMs, (5) intramedullary AVMs, and (6) conus medullaris AVMs. Full descriptions of each of these lesions are provided in this chapter.

Anatomy

The correct interpretation of diagnostic studies and clinical evaluation and management of the various subtypes of spinal AVMs require a precise understanding of spinal vascular anatomy. Planning and implementation of surgical and non-surgical treatments must be based on a clear understanding of venous and arterial anatomy.

Arterial Anatomy

The spinal cord is supplied by variably collateralized anterior and posterior arterial systems ( Fig. 15.1 ).9 The anterior distribution arises from the anterior spinal artery, extends the entire length of the spinal cord in the anterior median fissure, and supplies the anterior two-thirds of the spinal cord. The posterior system, an arterial network of collaterals between two posterior arteries, supplies the posterior third of the spinal cord. The anterior arterial system supplies the anterior horns, corticospinal tract, and spinothalamic tracts. The posterior arterial system supplies a smaller portion of the corticospinal tracts and the entire dorsal columns. Both arterial systems receive blood from medullary arteries, one of the three terminal branches of intercostal arteries.

During the first 6 months of gestation, paired medullary arteries supply the anterior and posterior arteries at each segmental level of the spine. By birth, however, most of the medullary arteries involute. In adults, only 6 to 10 medullary arteries remain to supply the entire spinal cord.9 In the cervical region, these medullary arteries are derived from terminal branches of intervertebral arteries (a branch of the posterior spinal ramus of the segmental arteries, which in turn are derived from the vertebral and branches of the subclavian arteries). In addition to the medullary arteries, which supply only the spinal cord, there are two other important terminal branches of the intervertebral arteries—the radicular and dural arteries. Unlike the medullary artery, radicular arteries, which supply the nerve root, and dural arteries, which supply the nerve root sleeves surrounding spinal dura, persist at each segmental level on both sides ( Fig. 15.1 ).

Pathophysiology

Extradural Arteriovenous Fistulae

Extradural AV fistulae are known as epidural fistulae under the classic nomenclature based on the work of Kendall and Logue. These lesions arise from an anomalous connection between an extradural artery (usually a radicular artery branch) and an epidural venous plexus ( Fig. 15.2 ). Increased flow under arterial pressure to the epidural venous system can result in venous hypertension and engorgement of the plexus. The mass effect of the engorged venous plexus causes compression of the spinal cord and nerve roots, often resulting in myelopathy and radiculopathy ( Fig. 15.3 ).

Intradural Dorsal Arteriovenous Fistulae

These lesions correlate with the type I AV fistulae of previous nomenclature and involve a radicular artery with an abnormal communication to the venous system of the spinal cord along the dural sleeve of the nerve root ( Fig. 15.2 ). Its low-flow shunt system results in venous hypertension with engorgement, elongation, and tortuosity of the venous system, thereby causing local mass effect with concomitant myelopathy and propensity for hemorrhage. These fistulae are believed to result initially from venous outflow obstruction, which presumably contributes to fistula formation via arterialization of the venous plexus. A medullary vein is usually the sole venous outflow from the fistula and carries the shunted arterial blood in a retrograde fashion (opposite the normal direction of venous flow) along the coronal venous plexus. The absence of other regional venous drainage creates venous engorgement and venous hypertension. The diversion of blood under high pressure by the arterialized medullary vein into the coronal venous plexus results in further venous dilatation. Because the intrathecal venous system has no valves, the varicocele-like radial and sulcal veins transmit venous hypertension to the spinal cord, producing venous congestion and myelopathy. Although intradural dorsal AV fistulae are truly rare in the cervical spine, similar direct dural AV fistulae at the skull base have been found to drain arterialized venous blood through the coronal venous plexus at the foramen magnum, resulting in the stereotypical engorged spinal venous system and myelopathy ( Figs. 15.4 and 15.5 ).10

Clinical Presentation and Natural History

The clinical presentation of spinal AV fistulae and AVMs is generally related to compression from local mass effect or acute hemorrhage. Pain and radiculopathy can result from nerve root compression, and progressive myelopathy can result from venous congestion, local spinal cord compression, and vascular steal. In the setting of hemorrhage, acute myelopathy and spinal cord injury often are the clinical presenting symptoms. Extradural, intradural dorsal, and intradural ventral fistulae all tend to present with progressive myelopathy. Extradural–intradural AVMs present with pain or progressive myelopathy, whereas intramedullary AVMs may present with acute myelopathy in the setting of hemorrhage or progressive myelopathy from chronic venous engorgement.

Compared with intradural dorsal and ventral fistulae, intramedullary AVMs are associated with a younger age at symptom onset, a higher coincidence with other vascular anomalies of the central nervous system, and a more uniform distribution along the spinal axis. These observations suggest that intramedullary AVMs are congenital lesions and most likely the result of inborn errors of vascular embryogenesis. Conversely, extradural and intradural fistulae are thought to be acquired lesions resulting from arterialization of venous plexuses.5,6,8,12–15

Many patients with intramedullary AVMs have a less dramatic neurological deterioration than typically accompanies hemorrhage. This finding suggests the probability of other mechanisms of spinal cord injury. Possible alternative mechanisms include spinal cord compression by an aneurysm or venous varix, medullary venous congestion, and ischemia related to vascular steal. Because intramedullary AVMs are high-flow shunts, a vascular steal phenomenon may be the most likely cause.

The natural history of intramedullary spinal AVMs remains incompletely defined. Most patients present in the third decade of life, but the pediatric population may represent up to 20% of patients presenting with hemorrhage.12 The onset and progression of symptoms may be gradual or acute. Subarachnoid and intramedullary hemorrhage is the initial symptom in a third of patients, and 50% of patients have had one or more hemorrhages before treatment.16 Data on the long-term disability that occurs without therapy are unavailable because these lesions are usually treated when diagnosed. Studies of the natural history of spinal vascular malformations began before the advent of selective spinal angiography and before the recognition that the incidence of intradural dorsal spinal AV fistulae far exceeds that of intradural AVMs. However, it is interesting that, in Aminoff and Logue′s large series, more than half of the patients who presented with acute symptoms—those who were unlikely to have the intradural dorsal type of spinal AVM (type I)—experienced no subsequent neurological progression.17,18

Spinal dural fistulae represent a different category of epidemiology and natural history. These lesions tend to present in the fifth and sixth decades of life and have a male predominance.19,20 However, lesions are seen in the pediatric population. Rodesch and colleagues reported the results of a small series of intradural spinal fistulae and found hemorrhage to be the presenting symptom in 44.8% of adults and 70% of children.21 Narvid and colleagues determined that 52% presented with lower extremity weakness, 30% with paresthesias, 24% with back pain, and 6% with urinary retention.20 The study made no distinction between progressive and acute presentation. Foix-Alajouanine syndrome historically has been known as a necrotic myelopathy caused by progressive spinal cord venous thrombosis. Such endomesovasculitis was originally believed to be due to a poorly characterized spinal vascular lesion but, based on the original authors description of progressive myelopathy and their histological findings, this syndrome is likely due to what we now know as intradural dorsal AV fistulae.22

Diagnostic Evaluation

Effective management of spinal AVMs depends on precise radiographic evaluation to define the anatomy of the lesion so that the appropriate intervention may be selected. Imaging evaluation has two components: screening studies for the initial evaluation of patients with acute or progressive radiculomyelopathy and vascular imaging studies for diagnostic confirmation and anatomical definition of the lesion for surgical planning.

The evaluation of progressive radiculomyelopathy includes plain radiography of the spine, magnetic resonance imaging (MRI), computed tomography (CT), and myelography. These studies are used to direct the choice of further investigations.

Because it is less invasive and usually more informative, MRI has replaced myelography as the initial diagnostic procedure of choice in patients with progressive myelopathy.23–25 MRI in patients with spinal AVMs may demonstrate abnormal vessels in the subarachnoid space ( Fig. 15.8 ), the nidus of an intramedullary AVM, or changes in the spinal cord produced by venous congestion, infarction, or hemorrhage.23 MRI often provides the initial diagnosis of an AVM and readily distinguishes between intramedullary and perimedullary AVMs and AV fistulae.

Due to the excess blood flow in the coronal venous plexus in patients with spinal AVMs, T1- and T2-weighted images often demonstrate a serpentine pattern of blood flow in the subarachnoid space. This “flow-void” signal is derived from dilated tortuous vessels of the arterialized coronal venous plexus or from an enlarged artery feeding an intramedullary AVM of the spinal cord. Tortuous, dilated, arterialized pial veins (varicoceles) of the coronal venous plexus may exert mass effect and compress the spinal cord, producing a scalloped appearance on sagittal T1-weighted images. T2-weighted images and short TI-inversion recovery sequences may demonstrate increased signal intensity within the spinal cord, representing spinal cord edema or hematoma. The enlarged coronal venous plexus often is most prominent posteriorly and may be seen more clearly on axial images.

T1-weighted images of intramedullary spinal AVMs usually demonstrate a focal flow-void signal with local expansion of the spinal cord, suggesting an intramedullary lesion. Axial and sagittal images localize the intramedullary position of an AV nidus. This information is particularly useful for high cervical AVMs, which often are located more dorsally than AVMs occurring in more caudal regions of the spinal cord. Subacute hemorrhage appears as increased signal intensity on T1-weighted images, whereas associated aneurysms or venous varices may be recognized as a globular region of flow void. After an AV fistula has been interrupted or embolized, occlusion of the nidus or venous varices can be confirmed by the absence of the flow-void signal on T2-weighted images.

More recently, magnetic resonance angiography (MRA) has become a powerful diagnostic tool for viewing spinal AVMs.23,24 A standard 3D contrast-enhanced MRA uses time-of-flight sequences with phase contrast and pre- and postgadolinium contrast along with conventional coils to produce a 3D rendering of the spinal vessels. Repetition time values are typically 20 to 50 ms, and acquisition times are quite long. Usually only the largest arteries and veins are demonstrated in normal spinal vascular anatomy, but vessel dilatations may be easily detected in the case of an AVM or fistula. Fast 3D contrast-enhanced MRA uses high-performance coils and rapid gradient pulse sequences to achieve lower repetition time values in the 10-ms range and much faster scan acquisition times (often less than 1 min).24 This technique can produce high-quality images and detect vessels of smaller diameter.26

Multirow-detector CT angiography has also become a powerful imaging tool when spinal AVM or fistula is suspected.27–29 This modality involves obtaining phase-injected contrast images on a helical CT with a 16-row detector, using slices from 0.5 to 1 mm. Postcomputer processing of source images can produce a maximum intensity projection sequence that demonstrates the spinal vascular anatomy in 3D. A few small studies have reported that this technique easily demonstrates stigmata of spinal AVMs and fistulae, such as arterialized vessels. However, delineating between AVMs and intradural and extradural fistulae is very difficult.29

Although MRI often provides sufficient evidence of an AVM to require subsequent spinal angiography, it may be normal or show only nonspecific changes in patients with type I or type IV spinal AV fistulae. Hence, patients with an unexplained progressive myelopathy in addition to normal MRI require additional diagnostic evaluation with myelography.

Myelography was once the most sensitive diagnostic screening tool for spinal AVMs but has been replaced by the gold standard of MRI and MRA. A technically well-done myelogram reliably demonstrates abnormal vascularity in the subarachnoid space for all types of spinal AVMs and can be very helpful in patients who are unable to undergo MRI. Therefore, a technically proficient myelogram that fails to demonstrate abnormal vessels obviates the need for subsequent spinal angiography. However, once the diagnosis of spinal AVM has been confirmed with MRI or myelography, spinal angiography is necessary to define the vascular supply and the precise anatomical location of the nidus of the AVM.30,31

Spinal angiography remains the gold standard for confirmatory diagnosis and for delineating the exact angioarchitecture needed for operative and endovascular treatment ( Fig. 15.9 ). Modern spinal angiography involves the use of biplanar flat panel detectors with digital subtraction and roadmapping capabilities. In addition to standard angiographic runs, this technology allows for 3D digital subtraction angiography to be performed for 3D roadmaps of the lesion′s angioarchitecture. CT and CT angiography can be obtained in the angiography suite for additional information on soft tissues and bony anatomy surrounding the lesion. The Phillips XperCT system (Phillips Medical Systems, Eindhoven, The Netherlands) combines 3D digital subtraction spinal angiography with 3D CT on a single machine for this purpose ( Figs. 15.6, 15.9, and 15.10 ).