Historical Perspective and Previous Classifications

Spinal AVMs were first described by Gaupp in 1888.¹² Twenty-three years later, Krause described the first surgically treated spinal dural fistula.¹³ In 1931, 5 years after its original clinical description, Foix-Alajouanine syndrome (subacute necrotic myelopathy) was linked to acute thrombosis of pathologic spinal AVM vessels.^14–16

In 1943, Wyburn-Mason analyzed 110 patients with spinal AVMs.² In his classic monograph, he recognized two main types of spinal vascular lesions: venous angioma (angioma racemosum venosum) and arteriovenous angioma (angioma racemosum arteriovenosum). The venous type consisted of a mass of turgid pial veins, usually located in the posterior aspect and below the midthoracic portion of the spinal cord. He described it microscopically as thick-walled pial vessels with marked “proliferation of intramedullary capillaries, precapillaries and venules.” The arteriovenous type was described as a fistulous capillary bed, most commonly found in the cervical or lumbar enlargement and often recognized early in life. Microscopically, there were many vessels of different size and structures, some resembling arteries and others veins.²

As spinal angiographic techniques have improved,^4,5,17–19 authors have moved from descriptive pathologic analysis toward anatomically based classifications for spinal AVMs. Di Chiro and other investigators proposed the most common recent classification scheme in which spinal AVMs were divided into three types.^4,5–8 Type I lesions are dural AVFs in which a dural branch from a radicular artery forms an abnormal communication with the dural veins at the nerve root sleeve. Type II lesions are glomus or intramedullary lesions. Type III lesions are juvenile or metameric AVMs associated with both extradural and intradural extension of the spinal AVM. Subsequently, Djindian and associates proposed a new category of ventral perimedullary fistula supplied by the anterior spinal artery (ASA).⁷ Heros and colleagues further characterized this type of lesion as a type IV spinal AVM.⁶

Borden and coworkers described a three-point anatomic classification of spinal dural AVFs and used the term dural arteriovenous fistulous malformation (AVFM).⁹ Type I AVFMs involve Batson’s epidural venous plexus. Type II lesions drain into both the epidural and perimedullary venous plexus. Type III AVFMs are supplied by meningeal branches of a radicular artery, which drain into the coronal venous plexus.⁴

Niimi and Berenstein divided vascular lesions of the spine into spinal vascular lesions and spinal cord vascular lesions.¹⁰ They subdivided spinal vascular lesions into dural and extradural fistulas. Spinal cord vascular lesions were referred to as spinal cord vascular malformations, of which there are two types: isolated, which includes AVMs and AVFs, and multiple, which includes metameric and nonmetameric forms.

Bao and Ling classified spinal cord vascular lesions as intramedullary AVMs, intradural AVFs, dural AVFs, paravertebral AVMs, and Cobb’s syndrome.¹¹ Intramedullary lesions include glomus and juvenile forms. Based on their size and degree of blood flow, intradural AVFs were subdivided into types I, II, and III. Paravertebral AVMs involve the paravertebral muscles and the paravertebral and epidural space. Cobb’s syndrome involves multiple structures within the same metamere.

Rosenblum and coworkers described two major types of spinal AVMs in 81 patients based on the location of the vascular nidus: dural versus intradural.³ Intradural AVMs were divided into intramedullary and dural AVFs. Intramedullary lesions were further subclassified into glomus (compact) and juvenile (diffuse) AVMs. Dural AVFs were supplied by a dural artery, with fistulous drainage into spinal veins, at least partially within the cord or pia. Intramedullary lesions were supplied by medullary arteries, and the arteriovenous shunt was located partially in the spinal cord or pia mater. Dural AVFs were supplied by a radicular branch along the dural nerve root sleeve that drained via an AVF into the coronal venous plexus. This classification system included no description of extradural-intradural or conus AVMs.

As detailed earlier, the previous nomenclature used to describe spinal vascular malformations was purely descriptive and based on incomplete understanding of the angioarchitecture and pathophysiology of these lesions. Our system reclassifies previously described entities according to the improved understanding of the anatomic location and pathophysiology of each lesion (see Table 395-1).^20,21 Accurate characterization of these lesions allows correct diagnosis of them and optimization of treatment.

Finally, we believe that spinal vascular malformations are so complex that some lesions will defy any proposed classification system. As lesions that do not fit the current scheme are better defined, the classification system must be updated to include these malformations. For this reason, we added the separate category of conus medullaris AVMs. In his vast experience treating spinal vascular malformations, R.F.S. has encountered these lesions several times. Because their specific characteristics fit no existing category, a new one was created.^1,22 By recognizing conus AVMs, our classification system is the first to include all currently recognized spinal vascular malformations and fistulas.

Proposed Classification System

Extradural Arteriovenous Fistulas

Extradural AVFs (Fig. 395-1) are extremely uncommon. They represent a direct connection between a branch of a radicular artery and the epidural venous plexus, which leads to the development of an extradural high-flow AVF. These fistulas are usually characterized by significant engorgement of the epidural venous complex, which leads to a mass effect on the nerve roots or the spinal cord, or on both. Venous congestion of the spinal cord can also cause myelopathic symptoms. In addition, shunting of large amounts of arterial blood into the venous system can steal blood flow from the spinal cord with resultant ischemia and worsening myelopathy.^10,23–27

FIGURE 395-1 A, Axial illustration of an extradural arteriovenous fistula along a perforating branch of the left vertebral artery. B, Posterior view showing that engorgement of epidural veins can produce a symptomatic mass effect on adjacent nerve roots and spinal cord.

(Used with permission from Barrow Neurological Institute.)

Intradural Dorsal Arteriovenous Fistulas

Intradural dorsal AVFs are the most common type of spinal AVF and usually occur in the thoracic region. Intradural dorsal AVFs (Fig. 395-2), which correlate with type I dural AVFs, are composed of a direct connection between a radicular feeding artery and the coronal venous plexus. A glomerular network of tiny branches of the radicular artery coalesces at the fistulous site, which is in the dural sleeve of the nerve root. Arterialization of the coronal venous plexus leads to myelopathic venous congestion and subsequent myelopathy.

FIGURE 395-2 A, Axial illustration of an intradural dorsal arteriovenous fistula (AVF) showing an abnormal radicular feeding artery along the nerve root on the right. The glomerular network of tiny branches coalesces at the site of the fistula along the dural root sleeve. B, Posterior view showing dilation of the coronal venous plexus. In addition to venous outflow obstruction (not shown), arterialization of these veins produces venous hypertension. Focal disruption of the point of the fistula by endovascular or microsurgical methods will obliterate the lesion. C, Illustrative case of a 55-year-old man with progressive myelopathy and bowel and bladder incontinence. A sagittal T2-weighted magnetic resonance image of the thoracic spine reveals serpiginous vessels dorsal to the spinal cord. D, Selective injection of right T7 segmental vessel showing a dorsal intradural AVF. Angiographic examination of the entire spine showed no other feeder vessels. E, Intradural intraoperative photograph revealing multiple dilated vessels over the dorsal aspect of the spinal cord. F, A single feeding arterial pedicle is isolated exiting at the right T7 nerve root sleeve as expected. G, Indocyanine green angiography confirms the fistulous site (arrow).

(Used with permission from Barrow Neurological Institute.)

The pathophysiology of intradural dorsal AVFs is thought to be obstruction of venous flow. Such obstruction leads to arterialization of the coronal venous plexus, which results in venous hypertension and myelopathy.

Intradural Ventral Arteriovenous Fistulas

Intradural ventral AVFs (Fig. 395-3) consist of an abnormal connection between the ASA and the coronal venous plexus. They are midline lesions located in the ventral subarachnoid space. Intradural ventral AVFs have been divided into three types based on size.²⁸ Type A fistulas are small shunts with slow blood flow and a moderate amount of venous hypertension. Types B and C have increasingly larger shunts, which often lead to a markedly distended coronal venous plexus. As flow through the fistula increases, progressive vascular steal and spinal cord compression take place and lead to worsening myelopathy.

FIGURE 395-3 A, Axial illustration of an intradural ventral arteriovenous fistula, a midline lesion derived from a fistulous connection between the anterior spinal artery (ASA) and the coronal venous plexus. B, Anterior view showing the fistula along the anteroinferior aspect of the spinal cord. Proximal and distal to this type A lesion, the course of the ASA is normal.

(Used with permission from Barrow Neurological Institute.)

Extradural-Intradural Arteriovenous Malformations

Extradural-intradural AVMs (Fig. 395-4) are rare. In the past they have been called juvenile, metameric, or type III AVMs. As their old name implies, they tend to be most common in children but can also occur in adults. Typically, they respect no tissue boundaries and can involve bone, muscle, skin, spinal canal, spinal cord, and nerve roots along an entire spinal level. Such complete involvement of the AVM along an entire somitic level has been termed Cobb’s syndrome.

FIGURE 395-4 Axial (A) and anterior (B) illustrations of an extradural-intradural arteriovenous malformation (AVM). These treacherous lesions can encompass soft tissues, bone, spinal canal, spinal cord, and spinal nerve roots along an entire spinal level. Considerable involvement of multiple structures makes these malformations extremely difficult to treat. C, Illustrative case. A sagittal T1-weighted magnetic resonance image of the thoracolumbar spine shows flow voids in the vertebral bodies, pedicles, posterior elements, and intradural and epidural spaces. D, Sagittal reconstruction computed tomography of the thoracolumbar spine showing the moth-eaten appearance of the vertebral bodies involved by the AVM. Native (E) and subtracted (F) angiographic views of the right T9 spinal artery show the intradural and epidural components of the AVM. Native (G) and subtracted (H) angiographic views of the right T12 spinal artery show the involvement of the posterior elements and paravertebral musculature.

(Used with permission from Barrow Neurological Institute.)

Intramedullary Arteriovenous Malformations

Much like their intracranial counterparts, intramedullary AVMs are located in the substance of the spinal cord. These lesions can be supplied by single or multiple branches of the ASA and posterior spinal artery (PSA). They are classified as compact or diffuse (Figs. 395-5 and 395-6), depending on the tightness of the nidus. These lesions are usually low-resistance, high-pressure, and high–blood flow vascular malformations. Associated nidal aneurysms are common.²⁹

FIGURE 395-5 A, Axial illustration of a compact intramedullary arteriovenous malformation (AVM). In this figure, an arterial feeder from the anterior spinal artery is identified. Note the discrete, compact mass of the AVM. B, Posterior view showing additional feeding branches from the posterior spinal artery and re-emphasizing the compact nature of this type of spinal AVM. Portions of the AVM are evident along the surface of the spinal cord.

(Used with permission from Barrow Neurological Institute.)

FIGURE 395-6 A, Axial illustration of a diffuse intramedullary arteriovenous malformation (AVM) showing areas of intervening neural tissue between the intraparenchymal loops of the AVM. Portions of the AVM also course along the pial surface and subarachnoid space. B, Oblique posterior view showing loops of the AVM coursing in and out of the spinal cord. Normal neural tissue is evident between intraparenchymal portions of the AVM. This view accentuates the diffuse character of these lesions. C, Illustrative case of a 12-year-old boy with a history of subarachnoid hemorrhage. A sagittal T1-weighted magnetic resonance image of the cervical spine shows abnormal vessels in the spinal cord. D, Right vertebral artery injection shows a diffuse cervical intramedullary AVM with feeders from the anterior spinal artery and muscular branches. E, Intradural view through the operating microscope showing the diffuse cervical intramedullary nidus. Most of the vessels are thrombosed from multiple sessions of endovascular embolization.

(Used with permission from Barrow Neurological Institute.)

Intramedullary spinal cord AVMs usually become symptomatic with acute myelopathy from hemorrhage or compression. Vascular steal can lead to progressive myelopathy.³⁰

Conus Medullaris Arteriovenous Malformations

Conus medullaris AVMs (Fig. 395-7) are separate entities because they fit none of the aforementioned categories.¹ These lesions typically exhibit complex nidal angioarchitecture with multiple direct shunts from the ASA, PSA, and radicular arteries and drainage into both the anterior and posterior venous plexuses. In addition to the multiple AVFs, these AVMs also usually contain a true AVM nidus. The nidus is of the glomus type and is typically extramedullary and pial based, but it can also have an intramedullary component.

FIGURE 395-7 A, Axial illustration of a conus medullaris arteriovenous malformation (AVM) showing the feeding arteries and draining veins from both the anterior and posterior aspects of the spinal cord. Note the proximity of the AVM to branches of the cauda equina. B, Posterior view recapitulating the complexity of the angioarchitecture of these lesions. The anterior spinal artery (ASA), posterior spinal artery (PSA), radicular arteries, and anteriorly and posteriorly draining veins are simultaneously involved. Portions of the AVM can consist of direct arteriovenous shunts, as well as regions of the true AVM nidus. During endovascular treatment, surgical treatment, or both, it is crucial to identify en passage branches of the ASA and PSA. C, Illustrative case of a 15-year-old boy who experienced an acute onset of back pain and subarachnoid hemorrhage. An angiogram shows an AVM with a large draining vein at the thoracolumbar junction. D, Intradural view of a tortuous arterialized draining vein. E, Intradural view of the nidus at the conus.

(A and B, Used with permission from Barrow Neurological Institute; C-E, from Koos WT, Spetzler RF, Lang J. Color Atlas of Microneurosurgery: Microanatomy, Approaches, and Techniques, 2nd ed. Stuttgart, Germany: Thieme; 2000. Reprinted with permission.)

These lesions become symptomatic because of venous hypertension, ischemia, hemorrhage, and a mass effect from the hugely dilated venous system. They are location specific (i.e., they are always located in the conus medullaris and cauda equina) and can extend along the entire filum terminale. Because of their location, conus AVMs frequently cause both radiculopathy and myelopathy.

Conclusion

In the past several years, our ability to identify and treat spinal AVMs has advanced tremendously. This chapter describes a modified classification system of spinal arteriovenous lesions based on this current anatomic and pathophysiologic understanding. This system eliminates the potential confusion inherent in older nomenclature. Use of such a comprehensive and anatomically based system improves the efficacy of treatment.