Arterial Anatomy

The spinal cord is supplied by two arterial networks, the anterior and posterior arterial systems (see Fig. 397-1). The anterior plexus is derived from the anterior spinal artery, which extends along the entire length of the spinal cord in the anterior median fissure and is the origin of the sulcal arteries, which leave the anterior spinal artery at a 90-degree angle to perfuse the anterior two thirds of the spinal cord. The anterior horns, corticospinal tracts, and spinothalamic tracts are perfused by this anterior spinal arterial distribution. The posterior system is a network of plexiform collaterals between two posterolateral arteries. It supplies the posterior third of the spinal cord, including a portion of the corticospinal tracts and the entire dorsal column.^{7,8,10,31,35,36} Both the anterior and the posterior arterial systems are supplied by medullary arteries.

During the first 6 months of gestation, paired bilateral medullary arteries supply the anterior and posterolateral arteries at each segmental level of the spinal cord. By the third trimester, however, most medullary arteries have regressed, and in adults, only 6 to 10 remain to supply the spinal cord.³¹ The medullary arteries in the cervical region are derived from the vertebral arteries and branches of the thyrocervical trunk. The medullary arteries in the thoracic and lumbar regions arise from a branch of the segmental vessels from the aorta and iliac arteries, specifically the intervertebral segment of the spinal ramus of the posterior segmental (intercostal) arteries (see Fig. 397-1).

The largest and most important of these 6 to 10 medullary arteries is the arteria radicularis magna, or the artery of Adamkiewicz. It serves as the major blood supply to the mid and lower thoracic and lumbar segments of the spinal cord and typically originates on the left side between T8 and L2; however, it may arise from T3 to L4 and may be on either side.³⁷ The upper thoracic portion of the spinal cord, above the region perfused by the artery of Adamkiewicz and below the relatively well collateralized cervical region, is a “watershed” or arterial border zone. It is particularly susceptible to hemodynamic ischemia and is the site of watershed infarcts of the spinal cord induced by severe hypotension.

In addition to the medullary arteries, which supply only the spinal cord, there are two other important terminal branches of the intervertebral artery (the posterior spinal ramus of each segmental artery): the radicular arteries (which supply the nerve roots) and the dural arteries (which supply the dural root sleeves and spinal dura). These arteries persist at each segmental level into adulthood (see Fig. 397-1).

Venous Anatomy

The spinal cord venous system, like the arterial system, is composed of two radially arranged vascular networks (see Fig. 397-1). The sulcal veins in the anterior median fissure and the radial veins in the dorsal and anterolateral portions of the spinal cord drain to the coronal venous plexus on the cord surface.³⁸ This pial venous plexus is drained by medullary veins to the epidural venous plexus. The medullary veins—which like the medullary arteries are not present at each segmental level but arise sporadically along the long axis of the spinal cord—cross the subarachnoid space and penetrate the dura adjacent to the dural penetration of the nerve roots.³⁸ Venous structures within the intrathecal space lack valves, but functional valves at the level of the dural penetration of the medullary veins prevent retrograde venous flow from the epidural (Batson’s) plexus to the intradural space.^35,38 In the region of the cervicomedullary junction, the venous system of the brainstem and the spinal cord communicate freely.

Dural Arteriovenous Fistulas

Figures 397-2 and 397-8 illustrate the typical pathologic and arteriographic anatomy of spinal dural AVFs. The AVF, a low-flow shunt in the dural sleeve of a spinal nerve root, is supplied by the dural branch of the intervertebral artery. A medullary vein, the sole venous outflow from the dural AVF, carries the shunted arterial blood retrograde to the normal direction of venous flow to the coronal venous plexus.² Microarteriography of specimens in which the spinal dural AVF was excised en bloc demonstrates that the nidus in the dura is in the dural root sleeve and the adjacent spinal dura and that it is a simple network of a small number of separate vessels that converge into the medullary vein just beneath the inner layer of dura (Fig. 397-9).³⁹

FIGURE 397-8 A, Selective spinal arteriogram of a spinal dural arteriovenous fistula (AVF) embedded in the root sleeve of the ninth right thoracic nerve root and the adjacent spinal dura. The nidus of a spinal dural AVF (arrows) is typically in the intervertebral foramen and the lateral aspect of the spinal canal and drains into dilated, tortuous intradural veins on the cord surface. B, Subtraction arteriogram in which the image has been reversed so that the vascular pattern corresponds to the view at surgery (C-F) with the patient in the prone position. The upward-pointing arrowheads in B and C indicate the caudal loop of the medullary vein draining the dural AVF. Correspondence of the shape of the veins, as seen on the arteriogram (B) and at surgery (C), provides a road map to the site of the dural AVF. The left-pointing arrowhead in C indicates the right T9 sensory root, and the arrow points to the site of dural penetration of the vein draining the AVF and the sensory root. D, The forceps grasp the dura (asterisks). This intradural and extradural view shows the AVF eimbedded in the dura (to the right of the dura in the image) and the site of intradural penetration of the medullary vein draining the AVF intradurally (arrow). E and F, The dura (asterisks in E) is retracted laterally to reveal the relationship of the nerve root and the dural penetration of the arterialized medullary vein that drains the blood from the fistula intradurally to the spinal venous system. This vein typically can be identified as it penetrates the inner surface of dura next to (E) or slightly separate from (F) the dural penetration of the sensory root (arrow in F). In E and F note the convergence of the individual vessels of the AVF just beneath the thin inner layer of the dura into a single draining vessel and the normal radicular vein on the nerve root.

(A, D, and E, From Oldfield E, DiChiro G, Quindlen E, et al. Successful treatment of a group of spinal cord arteriovenous malformations by interruption of dural fistula. J Neurosurg. 1983;59:1019-1030; B, C, and F, from Oldfield EH. Spinal vascular malformations. In: Macdonald RL, ed. Neurosurgical Operative Atlas: Vascular Neurosurgery. New York: Thieme; 2008;2:190-199. Reprinted with permission.)

FIGURE 397-9 Microarteriogram. A, In this magnified view, the cannula in the dural artery is just visible at the lower end of the photograph. The shadow of the dural nerve root sleeve can be seen just above it. At the upper end, a stellate flare represents spillage of contrast agent from the cut end of the medullary vein. B, An artist’s sketch of the microarteriogram highlights the sinuous path taken by the primary vascular loops from which the shunt is constructed. The dural artery splits immediately into two loops, which coalesce in the dura at the axilla of the root and then split in the dura again into two arterial loops on the root’s shoulder. When the two vessels rejoin (midportion of the image), they penetrate the dura to join the medullary vein. Note the absence of any true glomus of capillaries, a finding indicating that these lesions are arteriovenous fistulas, not arteriovenous malformations.

(B, Drawn by Howard Bartner, National Institutes of Health; from McCutcheon IE, Doppman JL, Oldfield EH. Microvascular anatomy of dural arteriovenous abnormalities of the spine: a microangiographic study. J Neurosurg. 1996;84:215-220.)

The absence of other routes of regional venous drainage,^15,40 normally provided by the medullary veins, to carry excess blood flow from the coronal venous plexus through the dura and into the extradural venous system results in rostral flow of the arterialized blood in the coronal venous plexus, which reaches the cranial venous system in most patients. The diversion of blood under high pressure by the arterialized medullary vein from the dural AVF into the coronal venous plexus, combined with the absence of normal pathways for venous drainage, results in dilation, elongation, and tortuosity of the vessels of the coronal venous plexus. Moreover, because the intrathecal venous system is valveless, the radial and sulcal veins transmit the high pressure directly to the spinal cord, thereby producing venous congestion, venous hypertension, reduced arterial perfusion pressure, ischemia, and myelopathy (see later).

Intradural Arteriovenous Malformations

The nidus of intradural AVMs (Figs. 397-10 and 397-11; see also Figs. 397-3 and 397-4) is embedded within the spinal cord or is partially intramedullary and extramedullary. Intradural AVMs are more uniformly distributed along the length of the spinal cord than are dural or perimedullary AVFs (see Fig. 397-7). They are usually supplied by one or more enlarged medullary arteries that supply the spinal cord as well.

FIGURE 397-10 Juvenile-type intramedullary arteriovenous malformation (AVM) of the cervical and thoracic segments of the spine in a 26-year-old deaf and mute woman with progressive quadriparesis that was eliminating her ability to communicate by signing. Right vertebral arteriography, anteroposterior (A) and lateral (B) views, demonstrates the superior aspect of a large intramedullary AVM that extends from C4 to T2. The nidus of the AVM fills the spinal canal from front to back and from side to side. On sagittal T1-weighted magnetic resonance imaging (C), the signal void from the AVM clearly involves not only the cross-sectional area of the spinal cord but also the anterior and posterior elements of the spine and paraspinous soft tissue, a distribution that was confirmed by additional arteriography.

(From Thompson B, Oldfield E. Spinal vascular malformations. In: Carter L, Spetzler R, Hamilton M, eds. Neurovascular Surgery. New York: McGraw-Hill; 1994:1167-1195.)

FIGURE 397-11 Selective spinal cord arteriogram demonstrating a glomus-type intramedullary arteriovenous malformation supplied by the anterior spinal artery via the artery of Adamkiewicz.

(From Oldfield EH, DiChiro G, Quindlen EA. Successful treatment of a group of spinal cord arteriovenous malformations by interruption of dural fistula. J Neurosurg. 1983;59:1019-1030.)

Perimedullary Arteriovenous Fistulas

The anatomic derangement in intradural AVFs is depicted in Figures 397-5, 397-12, and 397-14. In these lesions, a direct pial fistulous communication lies between an intradural spinal artery and the coronal venous plexus. The absence of intervening small vessels (i.e., a glomus) at the AVF defines the lesion. The fistula may arise from the anterior or posterolateral spinal arteries but is more commonly supplied by the anterior spinal artery.^14,16,32,41 Intradural AVFs are often associated with a venous varix at the arterial-to-venous transition.

FIGURE 397-12 Posterolateral perimedullary arteriovenous fistula (AVF). Left, Selective spinal arteriography demonstrating that the nidus of this relatively small pial AVF is supplied by the descending limb of a posterior spinal artery, that there is more than one arteriovenous shunt, and that the arterial-to-venous shunting occurs at a moderate pace. The site of the nidus (arrows) is identified just proximal to the site of initial venous dilation and by the site from which the venous flow diverges rostrally and caudally (middle, arrows). Right, The feeding vessel has returned to a more normal size 6 months after surgical excision and the absence of filling of the AVF.

Cavernous Angiomas

Because cavernous angiomas are usually angiographically occult, it is not surprising that the spinal cord vascular anatomy is not altered by them (see Fig. 397-6). These mulberry-like lesions are typically small (5 to 15 mm), have a low level of blood flow, and are supplied by delicate thin-walled vessels. A rim of hemosiderin and gliosis, the product of previous small hemorrhages, typically surrounds these well-demarcated lesions. Cavernous malformations may occur in association with cerebral cavernous malformations and may occur at more than one level of the spinal cord when they are associated with familial multiple cavernous angiomatosis,^42,43 which is now known to be an autosomal dominant trait that maps to chromosome 7q.^44–50

Magnetic Resonance Imaging

Because of its lower risk and capacity for multiplanar imaging, MRI has replaced myelography as the initial diagnostic procedure in patients with myelopathy. With spinal AVMs, MRI abnormalities may be produced by abnormal vessels in the subarachnoid space, by the nidus of an intramedullary AVM in the spinal cord, or by changes in the spinal cord produced by venous congestion, myelomalacia, infarction, or hemorrhage.^19,93–97 MRI is noninvasive and often provides the initial diagnosis of an AVM; it may also differentiate intramedullary AVMs from perimedullary AVFs and dural AVFs. Ideally, MRI should be performed with at least a 1.5-T machine using a spinal coil.

Patients with spinal vascular malformations, except those with cavernous angiomas, often demonstrate a serpentine pattern of low signal in the subarachnoid space on T1- and T2-weighted MRI. This pattern of signal void is due to flow in the dilated, tortuous vessels of the arterialized coronal venous plexus. These arterialized pial veins may focally indent the cord surface and produce a scalloped appearance on sagittal T1-weighted images (Fig. 397-17B and C). The abnormal signal produced by the enlarged coronal venous plexus is frequently most prominent in the posterior pia and subarachnoid space.

FIGURE 397-17 Sagittal spinal magnetic resonance imaging (MRI) scans of a 66-year-old man with a spinal dural arteriovenous fistula (AVF) at T9-10. Before injection of contrast material, T1-weighted (TE 400, TR 16) images reveal an area of focal cord expansion affecting the conus (A) and increased signal intensity on T2-weighted (TR 2000, TE 20) proton density imaging (B) in the thoracolumbar segments of a cord swollen from venous congestion. Immediately after the injection of gadolinium–diethylenetriaminepentaacetic acid (DTPA) (C), T1-weighted images (TR 400, TE 16) reveal enhancement of the vessels of the coronal venous plexus (compare the same MRI technique without enhancement in A). T2-weighted imaging techniques that show cerebrospinal fluid brightly often prominently depict the abnormal vessels on the surface of the cord (D) and in the cerebrospinal fluid. As seen on T1-weighted (TR 417, TE 16) MRI performed after the injection of gadolinium-DTPA 8 months after excison of the spinal dural AVF (E), elimination of the fistula resulted in resolution of the swollen appearance of the spinal cord and disappearance of the abnormal enhancing vessels on the cord surface.

(From Thompson B, Oldfield E. Spinal vascular malformations. In: Carter L, Spetzler R, Hamilton M, eds. Neurovascular Surgery. New York: McGraw-Hill; 1994:1167-1195.)

Magnetic resonance angiography (MRA) has become increasingly useful in the evaluation of patients suspected of harboring a spinal vascular malformation.^98,99 MRA techniques, including time-resolved spinal MRA and contrast-enhanced MRA, have evolved to the extent that it can be used to detect spinal vascular malformations and to define them in some patients (or at a minimum provide the information to focus subsequent spinal digital subtraction arteriography [DSA] when it is performed). However, it should be emphasized that MRA should not supplant dedicated spinal catheter DSA because catheter arteriography remains the “gold standard” for definitively categorizing a spinal vascular malformation and precisely defining its anatomy.

Dural Arteriovenous Fistulas

Patients with dural AVFs have a wide range of findings on MRI.^19,94 T1- and T2-weighted images, when abnormal, often reveal an area of focal cord expansion; there is a central area of low or high signal on T1-weighted images and increased signal intensity on T2-weighted images in the thoracolumbar segments of a cord swollen from venous congestion (see Fig. 397-17A and B). In the large study of Gilbertson and coworkers, increased T2 signal in the spinal cord was the most common finding, and it occurred in all patients.¹⁰⁰ Studies performed immediately after the intravenous injection of gadolinium–diethylenetriaminepentaacetic acid (DTPA) reveal enhancement of the vessels of the coronal venous plexus (see Fig. 397-17C) and may produce enhancement of the most severely involved segments of the spinal cord; delayed imaging after gadolinium (40 to 45 minutes) may reveal an increase in the extent of enhancement to involve the entire enlarged lower portion of the spinal cord (Fig. 397-18).⁹⁷ Whether gadolinium enhancement of the spinal cord indicates edema, venous congestion, or loss of integrity of the blood-brain barrier associated with ischemic injury remains to be determined. Although the sensitivity of T2 signal changes is high, T2 signal abnormality and enhancement of the spinal cord on T1-weighted images are nonspecific features, and some patients do not have visible contrast enhancement of the congested vessels of the coronal venous plexus (see Fig. 397-18). It has recently been suggested that peripheral hypointensity on T2-weighted images of the spinal cord is a consistent and specific diagnostic feature of venous congestion associated with dural AVFs.¹⁰¹

FIGURE 397-18 T1-weighted magnetic resonance imaging (MRI) scans of a patient with severe paraparesis from a thoracic dural arteriovenous fistula (AVF). A, Note the nonspecific widening of the midthoracic portion of the cord and the low signal before the administration of gadolinium. B, Images after the intravenous administration of gadolinium show nonspecific enhancement of the central region of the spinal cord most severely affected. Note that the MRI findings in this patient do not establish the diagnosis of a spinal dural AVF or even suggest the presence of an arteriovenous malformation. Findings on MRI may be normal or only nonspecifically abnormal in patients with spinal dural AVFs.

(From Thompson B, Oldfield E. Spinal vascular malformations. In: Carter L, Spetzler R, Hamilton M, eds. Neurovascular Surgery. New York: McGraw-Hill; 1994:1167-1195.)

Contemporary spinal MRA can not only demonstrate the presence of abnormal arterial feeders or draining veins (or both) but can also often depict the site of the fistula and the location of the shunt within one vertebral level of where it is found with spinal DSA.^98,99

Surgical elimination of the spinal dural AVF results in diminishment of the swollen appearance of the spinal cord, induces resolution of the abnormal T2 hyperintensity in the spinal cord, and eliminates enhancement of the abnormal vessels of the coronal venous plexus over the weeks or months after surgery (see Fig. 397-17).^{98,99,102,103}

Intradural Arteriovenous Malformations and Arteriovenous Fistulas

At the site of intramedullary AVMs, T1-weighted images usually demonstrate a focal signal flow void comprising multiple channels with a serpentine pattern in an area of local expansion of the spinal cord (Fig. 397-19).^94,95 The position of the nidus in the axial plane of the cord is established with sagittal and axial images, which sometimes permit the exact intramedullary position of an AVM to be recognized and occasionally distinguish perimedullary AVFs from intramedullary AVMs that are partially intramedullary and extramedullary.^94,95 Subacute hemorrhage is seen as increased signal on T1-weighted studies. An aneurysm or a venous varix associated with an AVM or an AVF, respectively, is recognized as a globular-shaped region of flow void (see Fig. 397-15C and D).^93,94,104 Spinal MRA can identify the presence of an intradural AVF or AVM, but classification into the correct subtype can be difficult. Occlusion of the nidus with emboli or thrombosis of a varix after interruption of an AVF can be confirmed by loss of the signal flow void on T1-weighted images,⁹⁴ as well as by spinal MRA.

FIGURE 397-19 A and B, Magnetic resonance imaging (MRI) scans of an intramedullary arteriovenous malformation (AVM). Because of the rapid flow within the vessels of intramedullary AVMs, they have areas of flow void on MRI. A, Coronal T2-weighted (1000/75) MRI scan revealing an intramedullary nidus (arrow) at the T6 vertebral level. B, Sagittal T1-weighted (SE 600/25) MRI scan showing the nidus (arrow) more clearly. At selective spinal arteriography, the anteroposterior (C) and lateral (D) views in the early venous phase confirm the intramedullary location of the nidus (arrows).

(From Doppman J, DiChiro G, Dwyer A, et al. Magnetic resonance imaging of spinal cord arteriovenous malformations. J Neurosurg. 1987;66:830-834.)

Although MRI may suggest a spinal vascular malformation and the need for further spinal arteriographic evaluation, if MRI is performed only without contrast enhancement, the images may either be normal or show nonspecific changes in patients with dural AVFs (see Fig. 397-18). Because dural AVFs are the most common type of spinal vascular malformation and the type most amenable to treatment, patients with unexplained progressive myelopathy or radiculopathy and a normal unenhanced MRI study require additional diagnostic evaluation with contrast-enhanced MRI, spinal MRA, or both. In cases in which MRI is negative or equivocal and clinical suspicion remains, spinal DSA should still be performed.

Computed Tomographic Angiography

Computed tomographic angiography (CTA) may also be used as a screening test in patients suspected of having a spinal vascular malformation. With 4- and 16-detector and, more recently, 64-detector spiral CT imaging, CTA has been used to successfully detect spinal vascular malformations.^20,105 CTA generally clearly demonstrates the draining veins and usually depicts the feeding vessels and the fistula or fistulas.^20,105 CT scanning, however, is poor for examining the spinal cord parenchyma itself. As with spinal MRA, CTA can demonstrate the presence of the fistula and often delineates the anatomy of the fistula but cannot supplant spinal DSA. CTA is useful in helping focus DSA, thus reducing the time needed for the study and the amount of contrast material required.

Myelography

It is important to remember that myelography is a sensitive diagnostic screening test for spinal AVMs. A technically acceptable myelogram reliably demonstrates abnormal vascularity as serpentine filling voids in the subarachnoid space in all types of spinal vascular abnormalities (Fig. 397-20) except cavernous angiomas. Therefore, in a patient with equivocal findings on MRI, myelography that fails to demonstrate abnormal vessels in the subarachnoid space obviates the need for spinal arteriography. However, once the diagnosis of a spinal AVM has been confirmed with MRI or myelography, spinal arteriography is necessary to establish the type of spinal AVM, define the precise anatomic location of the nidus of the AVM, and identify the arterial supply to the AVM and to the spinal cord.

FIGURE 397-20 Myelogram of a patient with a spinal dural arteriovenous fistula. The dilated coronal venous plexus is evident on the dorsal surface of the spinal cord.

(From Muraszko KM, Oldfield EH. Vascular malformations of the spinal cord and dura. Neurosurg Clin N Am. 1990;1:631-652.)

Dural Arteriovenous Fistulas

Selective DSA of dural AVFs demonstrates intrathecal drainage of the fistula, via an arterialized medullary vein, into the dilated, tortuous veins of the coronal venous plexus (see Fig. 397-8); in most patients this occurs predominantly along the posterior surface of the spinal cord. In some patients it also discloses the nidus of the AVF in the intervertebral foramen and lateral aspect of the spinal canal (see Fig. 397-8A). A prolonged view of the venous phase after selective injection of the artery feeding the AVF fully defines the abnormal venous anatomy because these low-flow lesions often require 15 seconds or more for the contrast material to dissipate.

Intracranial dural AVFs that drain inferiorly into the spinal venous system and cause myelopathy can mimic spinal dural AVFs clinically and on MRI and myelographic studies (Fig. 397-21).^21,22,106 The AVF in these patients is located in the dura of the posterior fossa convexity or the tentorium and is supplied by branches of the internal or external carotid or vertebral/basilar arteries. Myelopathy occurs when the arterialized venous drainage has access to the valveless spinal venous system. Hence, if a patient with myelopathy has MRI or myelographic findings of a dilated, tortuous coronal venous plexus but normal spinal arteriography, the patient should undergo cerebral arteriography to search for a dural AVF of the rostral portion of the cervical segments of the spinal cord, the tentorium, or the dura of the posterior fossa. In this circumstance, bilateral selective vertebral arteriography is important because unilateral injection with retrograde flow down the opposite vertebral artery will not detect some cervical spinal dural AVFs.¹⁰⁷ Similarly, because sacral dural AVFs with intrathecal medullary venous drainage and consequent myelopathy may be supplied by branches of the iliac arteries,^23,108 it is important for the arteriogram to include selective injection of all arteries potentially supplying the sacral dura if selective spinal arteriography is negative. Finally, occasionally in patients with atherosclerosis the origin of the feeding vessel is occluded and selective spinal arteriography is negative; in such patients, CTA or MRA may help localize the site of the dural AVF, or surgical exploration focused on the results of spinal MRI and knowledge that the medullary vein draining the dural AVF enters the subdural space contiguous with the dural penetration of a nerve root, usually in the lower thoracic region, can be used to locate and treat the AVF.¹⁰⁹

FIGURE 397-21 Forty-one-year-old man with progressive quadriparesis, beginning in the lower extremities, as a result of spinal medullary venous drainage of an intracranial dural arteriovenous fistula (AVF) of the tentorium at the petrous apex. A, T1-weighted (TE 550, TR 22) magnetic resonance imaging (MRI) scan revealing expansion of the spinal cord and abnormal cord signal from C2 to T1. B, T2-weighted (TE 2000, TR 80) MRI scan disclosing high signal in an expanded cord from C1 to T1. Note the absence of abnormal signal void in the subarachnoid vessels on MRI. Carotid arteriography demonstrates an intracranial dural AVF (C and D, large arrows) supplied by the tentorial branch of the right internal carotid artery (C, small arrow) and by the occipital branch of the right external carotid artery (D, small arrow). The blood enters the petrosal vein and empties into the anterior and posterior spinal veins (E, arrows) after injection into the internal and external carotid artery (E). There is prolonged spinal venous drainage (E). F, Sagittal T1-weighted (TR 417, TE 16) MRI 4 years after interruption of the AVF reveals return of normal signal intensity and remission of the expanded spinal cord.

(From Wrobel C, Oldfield E, DiChiro G, et al. Myelopathy due to intracranial dural arteriovenous fistulas draining intrathecally into spinal medullary veins: report of three cases. J Neurosurg. 1988;69:934-939.)

Intradural Arteriovenous Malformations

Selective spinal arteriography of glomus-type AVMs typically demonstrates a dense mass of blood vessels confined to a short segment of the spinal cord. These lesions may be supplied solely by the anterior spinal artery (see Fig. 397-11) or by the anterior and posterior spinal arteries.

Juvenile-type spinal AVMs have multiple feeding vessels and occupy a larger volume of the spinal cord. The nidus is usually large and contains spinal cord tissue within its interstices. In the metameric form, paraspinous soft tissues may also be involved (see Fig. 397-10).

Direct AVFs in the pia may be perfused by the anterior or posterior spinal arteries. These lesions are located on the cord surface or, rarely, on the filum terminale. The most common form, type III, is often associated with extensive venous enlargement and variceal formation. For the smaller, type I AVFs, the exact site of the fistula can often be determined as the point at which the feeding artery abruptly dilates as it joins the venous drainage (see Fig. 397-12). Angiomyelotomography is useful to detect small perimedullary AVFs (type I), to distinguish them from AVMs of the spinal cord, and to enhance precision of the definition of the vascular anatomy of the AVF before treatment.^14,30,41

Surgery

The goal of treatment of spinal dural AVFs is permanent elimination of venous congestion of the spinal cord. This goal, which may be accomplished by excision, obliteration, or occlusion of the nidus or by interruption of venous drainage from the fistula between the dura and the dilated coronal venous plexus, has not always been the objective of treatment. When spinal arteriography was first introduced in the 1960s, the AVF was not identified in the spinal dura but was thought to reside in the arterialized pial veins of the coronal venous plexus. Consequently, these dilated, tortuous, arterialized coronal veins were mistaken for the nidus of the AVM and became the target of microneurosurgical operations designed to “strip” the cord of the purported pial nidus.^{12,68,110,111} Unfortunately, this treatment often exacerbated rather than eliminated the venous congestion. Furthermore, these stripping procedures involved an extensive multilevel laminectomy, tedious and unnecessary pial dissection, and a higher risk for morbidity in the patient. Moreover, the veins being excised were the normal veins of the coronal plexus that had been altered in appearance by the reception of blood under high pressure and flow.² Recognition of the actual location of the dural AVF implied that effective treatment of most spinal vascular malformations should be directed at the dural nidus of the fistula. Simple interruption of the AVF produces permanent resolution of the venous congestion and improvement of myelopathy in many patients.^{5,13,15,21,55,62,112–114}

Operative treatment of dural AVFs begins with a laminectomy one level above and one level below the dural nidus and the intramedullary vein that drains the fistula. One useful adjunct in localization of the point of fistualization is to place a coil in the feeding artery as close to the fistula as possible at the time of the spinal arteriogram. Fluoroscopy may then be used in the operating room to easily localize the fistula. After a midline dural opening, the arterialized medullary vein is identified. This vessel almost always penetrates the dura at the site of the dural penetration of the posterior nerve rootlets (Video 397-1; see also Fig. 397-2).

VIDEO 397-1

For 6 months this 63-year-old man had experienced difficulty walking that required a cane, pain in his hips and the upper portion of his legs, and urinary urge incontinence and frequency. Magnetic resonance imaging demonstrated abnormal vessels in the subarachnoid space in the thoracic and cervical regions. Selective spinal arteriography demonstrated two dural arteriovenous fistulas (AVFs), one on the right at T7 and one on the left at T11. The arrows demonstrate the precise sites of dural penetration of the medullary veins draining the dural AVFs intradurally. At surgery, the medullary venous drainage is identified as it penetrates the dura adjacent to the dural penetration of the T7 and T11 nerve roots and then is coagulated with bipolar forceps and divided.

To confirm that the vessel to be interrupted is the medullary vein draining the dural AVF and not a medullary artery, its configuration is compared with the anatomy disclosed in the venous phase of the preoperative arteriogram, and it is followed as it crosses the subarachnoid space and joins the abnormal-appearing coronal venous plexus (Figs. 397-22 and 397-23). After identification and confirmation, the arterialized medullary vein is coagulated with bipolar forceps over a length of 4 to 6 mm and sharply divided as it penetrates the inner layer of dura between the dura and the engorged coronal venous plexus. Interruption of the medullary vein usually produces a visible change in venous turgor, and after a few minutes, the color of the arterialized coronal venous plexus may change from red to blue. However, it should be noted that interruption of the medullary vein generally does not produce an immediate or dramatic change in venous color (perhaps because of shunting of blood through a spinal cord capillary bed that is maximally dilated to supply the cord in the face of severely diminished perfusion pressure).

FIGURE 397-22 A 67-year-old woman with a 6-month history of progressive gait disturbance, lower extremity claudication, and bladder dysfunction. A, T2-weighted non–contrast-enhanced sagittal magnetic resonance image of the thoracic spine. There is abnormal bright signal (arrows) within the substance of the thoracic cord along with accompanying expansion of the spinal cord. Serpentine flow voids (arrowhead) can be seen dorsal and lateral to the spinal cord. B, Preoperative arteriogram, and C and D, intraoperative views. An anteroposterior spinal arteriogram (B; seen from the surgeon’s view; that is, it has been flipped horizontally) demonstrates filling of the spinal dural arteriovenous fistula (AVF) and the pattern of the vessels of the coronal venous plexus. Note the congruency of the vascular pattern in comparison to the intraoperative views of the dorsal surface of the spinal cord at the same level (C) and at the site of dural penetration by the medullary vein (D). By studying the vascular pattern of the arteriogram, correlation with the intradural vessels (black arrows) is possible, which allows ready identification of the intradural draining vein (white arrows). D, Intradural draining vein (medullary vein). This magnified view demonstrates the relationship of the intradural draining vein of the AVF (arrowhead) to the dural penetration of the nerve root (arrow). The fistula is effectively treated by coagulation and division of this vessel.

(Adapted from Watson JC, Oldfield EH. The surgical management of spinal dural vascular malformations. Neurosurg Clin N Am. 1999;10:73-87.)

FIGURE 397-23 Selective spinal arteriogram in a 36-year-old man with a spinal dural arteriovenous fistula (AVF) at the left seventh thoracic nerve root. A, The seventh left thoracic intercostal artery provides a common origin of the arterial supply to the dural AVF (arrow) and to the artery of Adamkiewicz (arrowheads pointing to the left of the image). Note that the medullary vein draining the AVF intradurally (arrowhead pointing upward) takes a horizontal course initially. B-D, Surgical view (patient prone) after the dura (asterisks) and arachnoid have been opened and retracted laterally. B, The medullary vein draining the AVF enters the dura (arrow) just dorsal to the dural penetration of left seventh thoracic sensory root (arrowheads). C, The medullary vein draining the dural AVF has been coagulated, ligated, and divided (arrows) as it enters the subdural space (upper arrowhead). Note the dural penetration of the sensory root just deep to the site of intradural entry of the vein draining the AVF (lower arrowhead). D, The artery of Adamkiewicz (arrows) is identified by its straight course and rostral direction immediately after penetrating the dura just deep to the dural penetration of the left seventh thoracic nerve root (arrowheads). Forceps are retracting the denticulate ligament (white) medially. E, After surgical interruption of the medullary vein draining the dural AVF intradurally, the dural fistula no longer opacifies. The arrow designates the abrupt termination of the vessel previously supplying the AVF, and the arrowheads indicate the patent artery of Adamkiewicz and anterior spinal artery.

(From Oldfield E, Doppman J. Spinal arteriovenous malformations. Clin Neurosurg. 1988;34:161-183. Reprinted with permission.)

Outcome

Operative treatment of dural AVFs is safe and consistently interrupts the progression of neurological deficits.^{2,5,13,15,55,62,116,117} When the series from the National Hospital for Nervous Disease⁵⁵ and the National Institutes of Health¹⁵ are combined (total of 76 patients), 37 of the 49 severely disabled (Aminoff and Logue grades 3 to 5) patients (76%) had improved gait after surgery (Fig. 397-24). Furthermore, 26 of 27 patients (96%) with disability but unaided locomotion retained independent ambulation, and 17 of the 27 (63%) improved. Of the 76 patients, 70 (92%) either stabilized or improved. Improvement in control of micturition and independent ambulation is achieved in most patients after surgery.^15,55 Patients with more advanced preoperative disability are likely to be stabilized but are less likely to improve after surgery.^{2,13,15,55,57,62} These observations have been confirmed in more recent reports.^113,114,116 One retrospective study of 25 patients found a tendency toward moderate, but definite functional decline several years after treatment.¹¹⁸ This occurred more commonly in patients with a more prolonged clinical course before treatment and in patients with more severe neurological deficits at treatment. Thus, this functional decline may represent the additive effects of age on the original neurological damage.

FIGURE 397-24 Relationship of preoperative functional state and postoperative outcome in patients with dural arteriovenous (AV) fistulas. The outcome after surgery is directly related to the patient’s neurological status preoperatively. Generally, patients who walk independently before treatment do so after treatment. Note, however, that most patients were not treated until they had already acquired severe functional disability. Early diagnosis and therapy offer the best outcome.

(Adapted from Muraszko KM, Oldfield EH. Vascular malformations of the spinal cord and dura. Neurosurg Clin N Am. 1990;1:631-652. Data from Rosenblum B, Oldfield EH, Doppman JL. Pathogenesis of spinal arteriovenous malformations. J Neurosurg. 1987;67:795-802; Symon L, Kuyama H, Kendall B. Dural arteriovenous malformations of the spine: clinical features and surgical results in 55 cases. J Neurosurg. 1984;60:238-247.)

In summary, neurological outcome is closely related to the preoperative neurological function of the patient (see Fig. 397-24). With early diagnosis and treatment, before progression of the myelopathy and neurological impairment, patients retain their pretreatment neurological function or improve. Finally, because simple interruption of the venous drainage of a spinal dural AVF provides lasting occlusion of the fistula,¹¹² as it does for cranial dural AVFs,¹⁰⁸ this has been used to support the concept that the venous approach to the treatment of certain dural AVFs can be used successfully alone.^119,120

Embolization

Although dural AVFs can be treated by transarterial embolization, the durability of embolic occlusion and neurological improvement has been problematic despite the promise offered by the introduction of new embolic agents and increased experience.^117,121 Additionally, embolization cannot usually be safely performed in patients with a common arterial supply to the dural AVF and the spinal cord (see Figs. 397-14 and 397-24).^5,15,115

With particulate embolization, the improvement in symptoms is generally only transient because the embolized dural AVF recanalizes¹¹⁷ and recurrent myelopathy follows.^111,122 For spinal dural AVFs, particulate embolization is rarely indicated inasmuch as they are usually low-flow lesions and curative treatment is generally safe and straightforward.

Embolization with liquid polymerizing agents (N-butyl-2-cyanoacrylate [NBCA]) is used at some centers as the primary treatment of patients with spinal dural AVFs. It has been argued that embolization with liquid agents will pass distally into the feeding artery, reach the nidus of the dural AVF and the vein draining it, and provide permanent obliteration of the fistula. However, it is generally accepted that embolic occlusion with these agents does not consistently provide complete or permanent occlusion of other types of central nervous system AVFs and AVMs.¹²³ Moreover, although minimal clinical or arteriographic follow-up has been performed in patients with spinal dural AVFs occluded with liquid agents, the incidence of recanalization is high, as is the frequency with which patients require additional therapy later.^113,114,124 Merland and colleagues noted persistent flow through dural AVFs requiring immediate surgery in 14 of 45 patients who underwent embolization with liquid embolic agents.¹²⁵ Niimi and associates examined the outcomes of 47 patients in whom embolic therapy was used for spinal dural AVFs.¹²⁶ In 8 of the 47 (17%), the inadequacy of therapy was recognized immediately (partial embolization) because the acrylic did not reach the fistula or an anterior or posterior spinal artery arose at the same level. Two of these 8 patients were monitored for less than 1 month, but 5 of the 6 patients monitored for more than 1 month required additional treatment. Of the remaining 39 patients, 4 were observed for less than 1 month (in 1 of whom recanalization had already occurred), and 35 were monitored for at least 1 month, 18 of whom (51%) experienced recurrence. Overall, 26 of the 43 patients (60%) who were monitored for at least 1 month either had inadequate therapy at the outset (8 patients) or had a known recurrence of the AVF. Many of the patients who had not yet recanalized had been observed for less than 1 year,¹²⁶ an interval known to be inadequate for establishing the permanency of occlusion.¹²³

One critical issue alluded to earlier that affects durability may be attributed to inadequate penetration of the embolic agent to the site of the fistula and most proximal portion of the draining vein. Guillevin and colleagues reported a series of 26 patients with spinal dural AVFs treated with NBCA.¹²⁷ With a mean follow-up of 38 months, when glue was found in the dura mater on CT scans (in 19 patients, 73%), none of these patients had a recanalized fistula on arteriography, and the clinical status of all patients improved. However, in 7 patients (27%), glue was observed in or proximal to the foramen on CT scans, and recurrence was high in this group (5 of the 7 patients had recurrence and required surgery).

A newer liquid embolic agent, Onyx (ethylene vinyl alcohol copolymer), offers additional promise in the endovascular treatment of spinal dural AVFs (Fig. 397-25). Onyx possesses some advantages over NBCA as an embolic agent: it can be delivered slowly in more controlled fashion over a period of several minutes, it has a lower risk for premature venous occlusion or occlusion of a large intradural portion of the draining vein, and it carries a low risk for a retained catheter. Large series of spinal dural AVFs do not exist. Although the experience with Onyx in treating intradural spinal vascular malformations¹²⁸ and cranial dural AVFs^129–131 suggests that Onyx may be effective for treatment of spinal dural AVFs, insufficient experience exists for conclusions to be reached on its utility.

FIGURE 397-25 A 74-year-old woman with leg pain, myelopathy, and mild bladder dysfunction was found to have a thoracic dural arteriovenous fistula (AVF). Because of multiple medical comorbid conditions and the patient’s strong preference, she underwent spinal angiography with the intent of endovascular treatment if possible. A, Anteroposterior spinal angiogram demonstrating a dural AVF fed by the right T11 intercostal artery. B, Superselective angiogram through the microcatheter near the point of fistualization further defining the anatomy. Provocative testing with 50 mg of lidocaine produced no symptoms. C, The fistula was treated with Onyx. On the left is an image immediately before the injection of Onyx (the white arrows indicate the position of the microcatheter tip). The right image is a fluoroscopic image in which the radiopaque Onyx is seen to penetrate the fistula into the most proximal portion of the draining vein (black arrow). D, Final angiogram after the microcatheter was removed demonstrating complete obliteration of the fistula.

As summarized earlier, regardless of the therapy used, most patients with neurological deficits at treatment have some degree of residual deficit. Because of the risk for incomplete therapy or therapy that is transient, the patient has the anxiety of not knowing whether the residual neurological impairment is the result of partial treatment or recanalization of the AVF, which might be treatable. It also requires frequent radiologic reassessment to establish whether recurrence has occurred.

Finally, hemorrhage¹³² and delayed paraplegia^40,65 after embolization of spinal dural AVFs with NBCA have been reported. This suggests either propagation of venous thrombosis into the coronal venous plexus or passage of embolic material through the AVF and into the coronal venous plexus, thereby exacerbating the venous hypertension and leading to hemorrhage or venous infarction.

One clear indication for embolization of spinal dural AVFs is to treat patients with Foix-Alajouanine syndrome and incipient venous thrombosis and spinal cord infarction. A patient with an untreated dural AVF and rapid progression of symptoms has perilously high venous hypertension and is at risk for venous thrombosis and irreversible cord injury. Transarterial embolization of the fistula in these patients provides an immediate reduction in venous congestion until definitive surgical treatment can be performed.⁵⁶

Thus, treatment limited to simple interruption of the vein draining the AVF intradurally is optimal in most patients because it eliminates venous hypertension without risk to the normal vessels that supply the spinal cord and provides lasting and curative treatment. Furthermore, it is a relatively simple microneurosurgical procedure that can be performed successfully by most neurosurgeons, in contrast to embolization, which must be done by an experienced endovascular specialist.

Surgery

A number of general principles apply to the surgical management of all intradural AVMs.^{12,65,68,133–135} Surgery should be attempted only after careful consideration of the vascular anatomy of the lesion and the adjacent spinal cord as depicted by selective spinal arteriography. After acute subarachnoid or intraparenchymal hemorrhage, surgery is best delayed to permit lysis and absorption of the clot. Preoperative embolization with particulate or liquid embolic material or occlusion of giant feeders by balloon occlusion reduces the blood flow and tension in the AVM or AVF. Because it commonly leaves small particles in feeding vessels to a greater extent than in venous drainage vessels (E.H.O., personal observations), preoperative particulate embolization can also assist the surgeon in defining the feeding arteries during surgery. An operating microscope and appropriate microsurgical instrumentation are mandatory. Operative exposure must extend at least one level above and one level below the nidus of the AVM. The dura should be opened in the midline, and the arachnoid is preserved to avoid laceration of any delicate, distended, or adherent vessels underlying the dural opening. The use of small (2 to 3 mm × 10 to 15 mm) rectangular cotton pledgets or stay sutures secured to the pia-arachnoid facilitates the retraction and exposure provided by myelotomy for intramedullary vascular malformations. Painstaking hemostasis is crucial to maintain optimal visualization of the nidus of the AVM. The vascular anatomy defined on the preoperative angiogram must be carefully correlated to that seen intraoperatively to identify and confirm the major feeding and draining vessels and to plan the sequence of steps for excision.

Intraoperative ultrasonography with a directional flow probe or intraoperative arteriography^136,137 may be helpful to localize the intramedullary nidus and to distinguish afferent from efferent vessels. Bipolar cautery, used judiciously, can reduce the size and turgor of the AVM. Continuous bipolar irrigation maintains optimal visualization and prevents adherence to friable vessels. Large feeding vessels may require ligatures or clips, but metallic clips are generally avoided so that they do not interfere with the results of postoperative imaging. Generally, one major draining vein is preserved until the last arterial feeders have been taken. Intraoperative arteriography can be used to detect any residual AVM that is still patent,^136,137 but it may not detect small portions of thrombosed nidus that recanalize later. Hemostasis is reassessed completely before closure. The dura is closed in watertight fashion.

For certain ventral AVMs or AVFs, Martin and coworkers¹³⁸ and Markert and colleagues¹³⁹ described exposure of the ventrolateral quadrant of the spinal cord through an extended posterolateral approach that can be used in the cervical and thoracic regions. This technique includes a midline skin incision with a transverse extension at the level of the lesion, unilateral division and retraction of the paraspinous muscles, laminectomy and unilateral removal of the facets and pedicles, dural incision over the dorsal root entry zone, multilevel division of the ipsilateral dentate ligaments, and elevation and rotation of the spinal cord with dentate traction stitches. This technique provides exposure of the ventral root entry zone, the ipsilateral half of the ventral surface of the spinal cord, and the anterior spinal artery, although the surface of the spinal cord beyond the anterior spinal artery is not seen well. On rare occasion, anterior approaches (including cervical corpectomy and transthoracic variants) have been reported to successfully treat challenging intradural spinal vascular malformations, but closure and avoidance of cerebrospinal fluid leakage complications remain challenging. Additionally, these approaches often require fusion with its associated problems.^140–142

Intramedullary Arteriovenous Malformations

Circumferential dissection is carried out along the gliotic plane between the intramedullary AVM and the adjacent neural tissue (Fig. 397-26). To facilitate dissection of deeper portions of the AVM, the dorsal portion of the spinal cord is gently retracted laterally with small cottonoids or fine pial sutures attached to the dura laterally. Although the outcome of operative treatment of spinal intramedullary AVMs is, in general, less satisfactory than the results of treatment of dural AVFs, there are several characteristics of glomus-type intramedullary AVMs that often render them technically less problematic than juvenile-type lesions. Unlike juvenile-type AVMs, glomus lesions are generally compact, lack intertwined neural elements, and usually have a single arterial feeding vessel.¹⁵ In addition, the cervical region has a more abundant collateral system than do the thoracolumbar cord segments, thus permitting total surgical excision of certain cervical intramedullary lesions.^{12,15,24,65,68,143} However, if a relatively large lesion is situated entirely intraparenchymally in the anterior half of the spinal cord, complete excision may yield unacceptable neurological deficits. Operative intervention may be inadvisable in this circumstance.

FIGURE 397-26 A and B, After separating the arachnoid from the arteriovenous malformation (AVM), a diamond knife is used to incise the pia at the edge of the nidus. To obtain the exposure necessary for excision of the deep portion of the AVM, the pial incision is extended a few millimeters rostrally and caudally, usually in the midline. C and D, The superficial feeding vessels are interrupted sharply after they have been coagulated with bipolar cautery. Gentle retraction with a microsucker (with the tip of a small cottonoid and suction on low setting), dissection with the tips of the bipolar forceps in the gliotic plane between the malformation and the spinal cord, and elevation of the malformation while working from one pole upward or downward to expose, coagulate, and interrupt the vessels entering and leaving the malformation ventrally result in dissection of the nidus of the malformation from the surrounding spinal cord. Small custom-cut cottonoids and, if necessary, pial traction sutures are used to maintain adequate separation of the spinal cord from the nidus of the AVM for dissection. As the margins of the malformation are dissected, bipolar coagulation is used to gradually shrink the AVM and render it less susceptible to rupture during manipulation. Progressive shrinking of the AVM by coagulation also reduces turgidity in the nidus as the dissection proceeds. Generally, at least one of the major draining veins is preserved patent until dissection around the periphery of the malformation has been completed and all feeding vessels have been occluded. However, when the AVM is occluded by presurgical embolization, this may not be necessary.

(Drawing by Howard Bartner, National Institutes of Health; from Oldfield EH. Spinal vascular malformations. In: Rengachary S, Wilkins R, eds. Neurosurgical Operative Atlas. Rolling Meadows, IL: American Association of Neurological Surgeons; 1994.)

Because of their relative infrequency, no adequate long-term study comparing surgical and embolic treatment of intramedullary AVMs in the cervical region has been conducted. However, intramedullary AVMs in the thoracic and lumbar regions pose substantially greater operative risk because of their more tenuous collateral blood supply. Ventral intramedullary lesions in these segments are usually treated with repeated arteriographic embolization (see later).⁶⁴

Because they are voluminous, high-flow lesions that usually contain neural tissue within the interstices of the component vessels of the AVM and derive their arterial supply from multiple medullary arteries that also supply the spinal cord, most juvenile-type intramedullary AVMs are considered inoperable. For patients with progressive myelopathy or hemorrhage, embolization is usually recommended (see later).⁶⁴ An exception is a dorsally located lesion that is partly intramedullary and partly extramedullary.^{12,25,65,68,133,143} Presurgical or intraoperative embolization permits easier and safer excision and may improve the chance for total excision of these lesions.^26–28143

Outcome

Reports of the results of surgery for intramedullary AVMs are all influenced by selection bias. Although the results of surgery have been reported for small series of patients, many have been isolated cases, and none of the surgical series indicated the population of patients from which the surgical patients were selected. Clearly, patients were selected to undergo surgery because of the likelihood of successful and safe excision rather than submitting all patients with AVMs to surgical therapy.

Furthermore, the natural history of intramedullary AVMs is variable (see earlier), and the arteriographic outcome of surgery is known for only 3 years after surgery (Table 397-7). Early postoperative arteriography revealed persistent AVMs in as many as 40% of patients treated surgically during the 1960s and 1970s.¹⁵ At 3 years after surgery, about 30% to 50% of patients are improved, 30% to 50% remain unchanged, and 10% to 20% are worse. However, there are limited data on the incidence of persistent AVMs, even as early as 3 years, and no long-term data exist on the incidence of clinical relapse or progression because of incomplete surgical excision. Moreover, there are no studies of delayed arteriographic follow-up of greater than 1 year after surgical treatment of intradural AVMs. The short-term clinical results (3-year follow-up) of surgery clearly indicate superior outcomes in patients who receive treatment before serious neurological deficits arise (Fig. 397-27). However, this must be balanced against the knowledge that some patients have an innocuous clinical course for many years without any treatment (see earlier and personal observations of E.H.O.).

TABLE 397-7 Results of Treatment of Intradural Arteriovenous Malformations

FIGURE 397-27 Relationship of preoperative functional state and postoperative outcome in patients with intramedullary arteriovenous malformations (AVMs). As in patients with dural arteriovenous fistulas (AVFs), the outcome after surgery is directly related to the patient’s neurological status preoperatively. Generally, patients who walked independently before treatment do so after treatment. Note, however, that many patients were not treated until they had already acquired severe functional disability. As in patients with dural AVFs (see Fig. 397-24), early diagnosis and therapy offer the best outcome for patients in both groups.

(From Muraszko KM, Oldfield EH. Vascular malformations of the spinal cord and dura. Neurosurg Clin N Am. 1990;1:631-652. Data from Rosenblum B, Oldfield EH, Doppman JL. Pathogenesis of spinal arteriovenous malformations. J Neurosurg. 1987;67:795-802.)

Embolization

Embolic occlusion of spinal AVMs developed as a natural extension of the introduction and refinement of selective spinal arteriography.^10,27,144 With certain intradural AVMs, embolization is used alone. Because the incidence of recanalization after embolic occlusion is quite high,^122,145 embolization may be used before surgery for lesions that can be excised with acceptable risk. The nidus of an intramedullary AVM, as occurs in hemangioblastomas,⁹³ is often composed of several independent vascular compartments with varying degrees of overlapping common supply. Embolization, including the use of liquid embolizing materials such as the polymerizing acrylics, rarely permanently occludes the entire nidus of the AVM. For this reason, some clinicians who once advocated the routine use of glue for embolizing intradural spinal AVMs no longer do so because of the low incidence of lasting occlusion and the frequency of complications associated with it.^63,64 However, more recent reports have created new enthusiasm for embolization of spinal AVMs with liquid embolic agents, including NBCA glue and Onyx.^{121,128,146,147}

Consideration of embolization requires careful assessment of the anatomy of the blood supply, including the size of the vessels supplying the AVM, and the level of the lesion. For success, one must occlude the nidus of the AVM but not obstruct a vessel that is supplying the AVM and the spinal cord proximal or distal to the nidus. Because the feeding artery is frequently a medullary artery or the anterior spinal artery, occlusion may immediately interrupt the blood supply to the spinal cord, especially with lesions below the upper thoracic level. Cervical AVMs are safer to embolize because of the presence of greater collateral sources of blood supply in that region.

Arteriography is used frequently during progressive embolic occlusion. Selection of the catheter depends on how close the tip of the catheter must be to the nidus of the AVM for selective occlusion of the AVM while preserving the blood supply of the spinal cord and on whether particulate or liquid embolic material is used.

Although several particulate materials have been used to occlude spinal AVMs, including Gelfoam, PVA sponge microparticles, silk threads, and clot, the most commonly used particulate is PVA in the 150- to 250-µm-diameter range. Selection of the size of the particles is based on the desire to have them pass freely through the conducting vessels, the medullary arteries, the anterior or posterior spinal artery, and the enlarged sulcal vessels to the AVM without occluding the normal sulcal vessels. Because the diameter of the normal anterior spinal artery is 340 to 1100 µm and the diameter of the normal sulcal ateries is 60 to 72 µm, PVA particles 150 to 250 µm in diameter should pass through the anterior spinal artery, not enter the normal sulcal arteries, and pass into the enlarged sulcal arteries supplying the AVM.^148,149 When the vessel providing the most direct route to the AVM is particularly difficult to engage with a catheter, such as feeding arteries from the cervical segment of the vertebral artery, the particles can be embolized in a flow-directed manner toward the nidus via temporary or permanent balloon occlusion of the artery just distal to the origin of the feeding vessel. With particulate embolization, progressive occlusion of the malformation is carefully monitored with repeated arteriographic examination, and the embolization is terminated when the lesion is almost completely occluded (in situ PVA continues to cause clot to form and propagate after completion of the procedure) or when there is retrograde reflux of contrast medium proximal to the catheter tip, a finding indicating that flow-directed targeting of the nidus will no longer occur. Liquid materials (e.g., NBCA, Onyx), which are less embolic, require placement of the catheter tip at the edge of the nidus of the AVM and injection of a small amount of the polymer. Once again, prolonged injections may be achieved with Onyx.

The most common side effect of complete embolic occlusion of spinal AVMs is new neurological deficits that arise 24 to 48 hours after embolization. These deficits may be related to propagation of venous thrombosis in the enlarged coronal venous plexus, which is sluggishly carrying only the venous drainage of the spinal cord. To avoid this complication, patients may undergo anticoagulation with heparin for 48 to 60 hours after the procedure. Repeat arteriography is performed 7 to 10 days later, with additional embolization performed as needed and at intervals of 1 to 2 years or when neurological symptoms or signs recur.

Even though embolization of spinal AVMs with PVA does not provide lasting elimination of flow through the AVM, it plays an important role in the current management of patients with intradural AVMs. Presurgical particulate embolization makes surgery easier, and when used as the only therapy, it reduces the risk for hemorrhage (which could cause quadriplegia or death), mollifies the severity of spasticity in some patients, and most important, delays neurological progression in most patients. The results obtained by Biondi and colleagues—who advocate routine yearly arteriography and embolization with PVA (Ivalon) particles, regardless of symptoms—suggest that serial endovascular embolization with PVA provides safe and successful management of most patients with AVMs in the thoracic region of the spinal cord.⁶⁴ Their long-term follow-up (mean, 6 years) of 35 patients showed that although no patients had complete, permanent obliteration of the AVM (most patients had <50% reduction in AVM size), nearly two thirds were clinically improved at the end of the study. One of us (E.H.O.) has several patients with thoracic or lumbar ventral intramedullary AVMs that receive their blood supply from the anterior spinal artery whose neurological status has been stabilized for several years by repetitive particulate embolic occlusion when symptoms recur.

Experience with the use of Onyx for the embolization of spinal intramedullary AVMs has been reported recently.¹²⁸ Seventeen patients with symptomatic spinal intramedullary AVMs were treated exclusively with Onyx. Thirteen patients underwent a single treatment session and 4 underwent two treatment sessions. The mean follow-up was 24 months. Total AVM obliteration was achieved in 6 patients (35%), subtotal obliteration was achieved in 5 patients (29%), and partial obliteration was achieved in 5 patients (29%). Improvement in neurological or functional status (or both) was noted in 14 patients (82%). Intraprocedural complications occurred in 2 patients without neurological sequelae. Although further follow-up is necessary to critically evaluate durability, the encouraging results of this study demonstrate the potential of Onyx for the treatment for spinal intramedullary AVMs.

As with surgery for intradural AVMs, the best results with embolization are achieved in patients without major neurological deficits before treatment.^{9,15,27,63,64,132,145,148,149} Selective catheterization and embolization are associated with risks of occlusion of the anterior spinal artery and paraplegia or quadriplegia, perforation of an intradural vessel with the catheter and subarachnoid or intramedullary hemorrhage,¹⁴⁵ and passage of emboli through the AVM into the venous system and subsequent hemorrhage or venous infarction¹³² or into the distal vessels of the parent artery, such as the basilar artery when using the vertebral artery to reach the AVM.

Radiosurgery

Radiosurgery has been established as a potentially effective treatment option for select AVMs of the brain. However, a possible role for radiosurgery in the management of intramedullary spinal AVMs has not been extensively investigated. Sinclair and coauthors reported on the Stanford experience using multisession CyberKnife radiosurgery for intramedullary spinal AVMs.¹⁵⁰ Their report included seven patients with a follow-up of greater than 3 years after treatment. Six of the seven patients had significant reductions in AVM volume on MRI. Five patients underwent follow-up arteriography, four of whom had residual AVMs (although reduced in size), and one patient with a conus AVM had obliteration of it. No evidence of further hemorrhage or neurological deterioration attributed to the radiosurgical treatment was noted. Taken together, this study demonstrates the feasibility of stereotactic radiosurgery for the treatment of intramedullary spinal AVMs. However, 3 years of follow-up is too early for radiation-induced myelopathy to appear, and thus its incidence, as well as the incidence of delayed recanalization, remains to be determined. This treatment needs further investigation before its role in the treatment of spinal AVMs can be assessed.

Summary of Treatment Selection for Intramedullary Malformations

As a result of rapidly and simultaneously evolving classification schemes, diagnostic techniques, surgical instrumentation, catheter sophistication, advances in embolic agents, and other factors, the results of contemporary surgery, alone or after embolization, for intradural AVMs are incompletely known. The information on surgery is limited to series that began 2 to 3 decades ago. The three surgical and single embolization series included in Table 397-7 are the only published series with more than 10 patients that permit tabulation of the data. Furthermore, for individual patients, there appear to be prominent selection biases for the use of surgery, embolization, or combined treatment in all series, surgical or embolization, large or small. For instance, although most intradural AVMs are located in the thoracic or thoracolumbar segments of the spinal cord, with few exceptions⁶⁸ the published reports emphasizing surgical success focus on patients with cervical lesions,^9,65,143 which arise in segments of the spinal cord with the greatest collateral blood supply. Moreover, there is a conspicuous bias for surgery on lesions in the dorsal half of the spinal cord, as exemplified by the tendency to provide surgical therapy for “long dorsal AVMs” before they were recognized to be the products of dural AVFs. Dorsal intramedullary AVMs are less likely to receive their blood supply from the anterior spinal artery and are associated with less surgical risk than ventral lesions are.¹³³ The tendency to avoid subjecting patients in good condition to a therapeutic procedure that risks leaving them paraplegic results in a longer delay from diagnosis to surgical treatment with more difficult AVMs. In one series the average duration from the onset of symptoms to treatment was 2.7 years for dural AVFs versus 4.2 years for intradural AVMs, and patients with intradural AVMs were more likely to have worse functional grades at treatment than were patients with dural AVFs.¹⁵

Some of the factors that underlie the bias in selection of surgical or embolic therapy may act in opposite ways at different centers. Some centers reserve the surgery-only option for patients who cannot be treated effectively with embolization, whereas others select the more accessible, “safer” lesions (smaller well-defined AVMs, direct AVFs, cervical AVMs, dorsal lesions) for surgery. In addition, there are nuances in the manner of reporting outcomes that must be acknowledged. Patients who are treated when they are paraplegic or quadriplegic are rarely made worse as a result of therapy. Thus, those who treat patients earlier can easily have a greater percentage of patients who are worse after treatment than before despite superior long-term preservation of neurological function.

Many of the outcome data from early reports do not reflect significant advances in diagnostic techniques, current knowledge of the various subtypes of AVMs, details of anatomy that can now be obtained before treatment with MRI and the rapid-sequence imaging available with intra-arterial digital techniques, the advantages of more selective arteriography, or the significant advances in the equipment and techniques of interventional radiology and surgery. Furthermore, certain lesions are treated more effectively with surgery, whereas certain others are treated best with embolization. Still others are more effectively treated by combining preoperative particulate embolization with surgery afterward. Thus, direct comparisons of surgical and embolic therapy cannot be reliably made and, in the modern era of treatment, may not be very meaningful.

In most patients with intradural spinal AVMs, treatment should be recommended when the diagnosis is established. When arteriography reveals that an intradural AVM or AVF can be completely excised with limited risk because of its permanence, surgery alone or surgery after embolization should be considered. When lesions are identified, by arteriography or during surgery, as having unacceptable risks associated with complete excision, embolization should be considered. Radiosurgery remains investigational, although it could conceivably be considered in unusual circumstances.