23 Surgical Management of Thoracic Spinal Arteriovenous Malformations Abstract Vascular malformations of the spinal cord are rare, but carry significant risk of spinal cord compromise, particularly in the thoracic watershed region, which is the spinal cord segment most vulnerable to ischemic injury. In this chapter we focus on arteriovenous malformations (AVMs) and arteriovenous fistulas (AVFs) of the thoracic spinal cord. We review the relevant spinal vascular anatomy, the pathologic mechanisms by which spinal vascular malformations (SVMs) can cause acute or progressive neurological deficits, and the natural history of these lesions. Selective spinal angiography is the gold standard for diagnosing and characterizing SVMs, whose highly variable and dynamic angioarchitecture, together with adjacent normal spinal vascular anatomy, must be well understood in order to plan safe, effective, individualized treatment. Finally, we discuss endovascular and microsurgical approaches to treating AVMs and dural and pial AVFs of the thoracic spinal cord. Keywords: spinal vascular malformation (SVM), spinal arteriovenous malformation (AVM), spinal arteriovenous fistula (AVF), spinal dural AVF, spinal pial AVF Clinical Pearls • Vascular malformations of the spinal cord carry significant risk of spinal cord compromise, particularly in the thoracic watershed region, which is the spinal cord segment most vulnerable to ischemic injury. • The natural history of most spinal cord vascular malformations is progressive neurological decline over a period of several years. Therefore, treatment should be aimed at safely obliterating these lesions soon after diagnosis, in order to stabilize or reverse initial neurological deficits, and to prevent future spinal cord compromise. • Selective, catheter-based spinal angiography is the gold standard for diagnosing and characterizing spinal vascular malformations (SVMs), and their highly variable and dynamic angioarchitecture, together with the surrounding normal spinal vascular anatomy, must be well understood in order to plan safe, effective, and individualized treatment. • The most appropriate treatment strategy for spinal arteriovenous malformations (AVMs) may be endovascular, microsurgical, or hybrid, depending on lesion angioarchitecture. • Spinal dural arteriovenous fistulas (AVFs) are the most common SVMs, comprising 60 to 80% of all SVMs. They are often amenable to straightforward microsurgical ligation, due to the location of the fistula in the portion of the segmental radiculomeningeal branch within the dura associated with the segmental sensory nerve root. The exposure typically requires only a one- or two-level thoracic laminectomy and small dural incision. The sensory nerve root provides a clear intradural landmark. • Spinal pial AVFs are highly variable in their angioarchitecture. Giant pial AVFs are best treated endovascularly when possible, while small and large pial AVFs are more safely managed by microsurgery, in order to protect small branches to normal spinal cord from direct catheterization. • Spinal AVMs are typically approached endovascularly when possible, and though safe and complete obliteration may not always be possible, it may not be needed in order to favorably alter the natural history of the lesion. In this chapter we review the classification, diagnosis, evaluation, and surgical and endovascular management of arteriovenous malformations (AVMs) and arteriovenous fistulas (AVFs) of the thoracic spine. The general approach to spinal vascular malformations (SVMs) at our institution has been published elsewhere, and we adhere to that framework in the present discussion.1 Many classification systems for SVMs have been described. Here, for simplicity, we classify these lesions on the basis of their angioarchitectural features. Vascular lesions that contain an arteriovenous shunt, AVMs and AVFs, are amenable to surgical and endovascular treatment. The vascular lesions that do not contain an arteriovenous shunt, capillary telangiectasias, and cavernous hemangiomas, in the rare cases in which procedural intervention is indicated, are amenable to surgical management alone, as they are anatomically inaccessible via transcatheter routes. The fundamental distinction between AVFs and AVMs is that an AVF contains a direct connection between an artery and a vein, whereas an AVM contains a network of abnormal vessels, referred to as a “nidus,” separating the arterial and venous sides of the lesion. (Some lesions may contain both nidal and direct fistulous components, making them difficult to classify.) AVMs can be further classified based on the location of the nidus, which may lie either within or at the surface of the spinal cord. The nidal location has important endovascular and open surgical treatment implications. We use a straightforward system based on the location of the nidus or fistulous connection, outlined in In order to understand SVMs and their surgical and endovascular management, it is important to establish a background understanding of normal spinal arterial and venous anatomy. This subject has been comprehensively reviewed by several authors.2 Here we briefly survey the elements of spinal vascular anatomy most relevant to the subject of this chapter. The reader is referred to The arterial supply to the spinal cord is provided by one anterior spinal artery (ASA) and two posterior spinal arteries (PSAs). The ASA is formed from small left and right ASAs, each of which arises from the corresponding vertebral artery. The ASA is located in the anterior median sulcus, and supplies approximately the anterior two thirds of the spinal cord, including the anterior horns, ventral and lateral corticospinal tracts, and the spinothalamic tracts. At thoracic levels, the aorta gives rise to segmental radiculomedullary feeding arteries that provide collateral supply to the territory of the ASA. (Each segmental artery also gives rise to radiculomeningeal branches that supply the dura at segmental levels; these branches become especially relevant in the setting of spinal dural AVFs.) The most significant of these is the great anterior segmental medullary artery (the artery of Adamkiewicz), which typically arises on the left, between the levels of T8 and L2. In part as a result of this configuration, the spinal cord watershed is located in the upper thoracic region, so compromise of the ASA carries a high risk of paralysis. Table 23.1 Topographic classification of spinal AVM
23.1 Introduction, Definitions, and Classifications
Table 23.1.
23.2 Vascular Anatomy of the Thoracic Spine
Fig. 23.1 and 
Fig. 23.2, which illustrate the segmental arterial supply to the spine and spinal cord, respectively, and to 
Fig. 23.3, which illustrates the venous anatomy of the spinal cord.
Type | Location of nidus or fistula | Alternative names |
AVM | Intramedullary | Type II, “glomus AVM” |
Pial |
| |
Epidural |
| |
Intramedullary and extramedullary | Type III, “juvenile AVM,” “metameric AVM” | |
AVF | Pial | Type IV, “spinal cord AVF,” “perimedullary AVF” |
Dural | Type I, “dural AVF,” “dorsal intradural AVF” | |
Epidural |
|
|
Abbreviation: AVF, arteriovenous fistula; AVM, arteriovenous malformation. | ||
Fig. 23.1 Segmental arterial anatomy of the spine. (1) Posterior spinal arteries, (2) anterior spinal artery, (3) great anterior radiculomedullary artery (artery of Adamkiewicz), (4) medial musculocutaneous branch, (5) lateral musculocutaneous branch, (6) posterior radiculomedullary artery, (7) retrocorporeal arteries, (8) spinal branch, (9) posterior (dorsal) branch, (10) anterior (ventral) branch, (11) left segmental artery (posterior intercostal artery), (12) right segmental artery (posterior intercostal artery), and (13) aorta. (Reproduced with permission from Santillan A, Nacarino V, Greenberg E, et al. Vascular anatomy of the spinal cord. J Neurointerv Surg 2012;4:67–74.)
Fig. 23.2 Segmental arterial anatomy of the spinal cord. (1) Posterior spinal arteries, (2) anterior spinal artery, (3) spinal branch, (4) anterior radiculomedullary artery, (5) posterior radiculomedullary artery, (6) central (sulcal) arteries, and (7) vasocorona. (Reproduced with permission from Santillan A, Nacarino V, Greenberg E, et al. Vascular anatomy of the spinal cord. J Neurointerv Surg 2012;4:67–74.)
Fig. 23.3 Venous anatomy of the spinal cord. (1) Anterior median vein, (2) right deep cervical vein, (3) left deep cervical vein, (4) right vertebral vein, (5) left vertebral vein, (6) subclavian vein, (7) internal jugular vein, (8) left brachiocephalic vein, (9) superior vena cava, (10) accessory hemiazygous vein, (11) intercostal veins, (12) posterior radiculomedullary vein, (13) anterior radiculomedullary vein, (14) azygous vein, (15) hemiazygous vein, (16) lumbar veins, and (17) vein of the filum terminale. (Reproduced with permission from Santillan A, Nacarino V, Greenberg E, et al. Vascular anatomy of the spinal cord J Neurointerv Surg 2012;4:67–74.)
The PSAs also arise from the vertebral arteries, but descend along the spinal cord posterolaterally, supplying the posterior columns. At thoracic levels, the PSAs anastomose with segmental radiculomedullary branches from the intercostal arteries.
Venous drainage from the spinal cord occurs through an intradural system and an extradural system. The intradural venous system comprises the intramedullary veins and the pial veins, while the extradural system involves the veins of the spine and the epidural venous plexus (Batson’s plexus). The ventral spinal cord is drained by a longitudinal midline anterior spinal vein, as well as by anterolateral veins, which receive drainage from segmental sulcal veins. Venous drainage from the posterior columns and dorsal horns is into the longitudinal posteromedian and posterolateral veins.
23.3 Epidemiology
SVMs are overall rare, and account for approximately one-tenth of central nervous system vascular malformations. The detection rate of new cases has been estimated at less than 15 per million per year in the general population. Of these, spinal dural AVFs are the most common, constituting 60 to 80% of all SVMs.3
23.4 Presentation and Clinical Features
Patients with SVMs may present clinically with signs of myelopathy (sensory or motor deficits, bladder or bowel dysfunction, proprioceptive deficits, hyperreflexia), or with pain or a neurological deficit in a radicular distribution. They may also present with back pain or progressive spinal column deformity. The dominant pathophysiologic mechanism is determined by the hemodynamics of the lesion; the principal mechanisms are hemorrhage, ischemia due to venous hypertension or arterial steal, and mass effect.
Pain or neurological deficit that is acute in onset may signify a hemorrhage. Rupture of a spinal AVM can cause acute spinal injury due to spinal subarachnoid hemorrhage or hematomyelia (spinal intraparenchymal hemorrhage). The clinical presentation of a ruptured spinal AVM varies depending on the level and site of the injury within the spinal cord, but typically includes lower extremity motor and sensory deficits, with or without proprioceptive deficits and bowel or bladder dysfunction. Hemorrhage also typically produces a sudden onset of severe upper back or interscapular pain without nuchal rigidity. The likelihood of hemorrhage is increased in the presence of intranidal or flow-related aneurysms, particularly aneurysms of the ASA.
Conus medullaris syndrome is common in the setting of certain spinal AVMs. The reason for this is that because the spinal venous system is valveless, the degree of venous hypertension increases in the more gravity-dependent regions of the spine. As the conus medullaris is the most dependent segment of the spinal cord when posture is upright, venous hypertension is most pronounced there. Venous hypertension can be verified angiographically, by demonstrating of a prolonged venous phase on angiogram of the artery of Adamkiewicz.
Arterial steal phenomena may also arise in lesions containing high-flow arteriovenous shunts, as such shunts can divert flow from normal, adjacent spinal cord tissue. Lesions fed by the ASA are especially prone to cause arterial steal, as the ASA is poorly collateralized.
Mass effect is an uncommon mechanism for myelopathy in SVMs, but large intranidal or flow-related aneurysms or dilated venous varices may cause cord or nerve root compression.
23.5 Arteriovenous Malformations
Spinal cord AVMs typically come to attention in childhood or young adulthood, in the setting of acute spinal cord compromise due to spinal intraparenchymal hemorrhage or compression myelopathy. Most patients recover partially from an initial hemorrhage, but the probability of second and subsequent hemorrhages is high, and the tendency is for patients to experience progressive deterioration of spinal cord function.
23.6 Pial Arteriovenous Fistula
Large and giant spinal cord pial AVFs often come to attention in childhood and adolescence, while small pial AVFs typically present later in life. Large and giant lesions can present with acute spinal cord compromise in the setting of spinal subarachnoid hemorrhage (usually due to venous rupture), progressive sensorimotor deficits due to vascular steal or venous hypertension, or mass effect on the spinal cord or nerve roots from dilated veins. Small lesions rarely rupture, and typically cause slowly progressive neurological deficits due to venous hypertension.
23.7 Dural Arteriovenous Fistula
Spinal dural AVFs typically cause progressive myelopathy through venous hypertension and hypoperfusion of the spinal cord. Back or leg pain is common, and symptoms are typically exacerbated by actions that increase intraabdominal pressure, such as straining, or bending at the waist. Patients typically present in adulthood, and by the time of diagnosis many patients already experience bladder or bowel dysfunction or sexual dysfunction.
23.8 Intramedullary–Extramedullary Arteriovenous Malformation and Angiomatosis
Intramedullary–extramedullary AVMs and angiomatosis typically present in childhood and young adulthood, sometimes in the setting of an identifiable syndrome such as Osler–Weber–Rendu or Cobb syndrome. Children present with pain and progressive myelopathy due to mass effect, arterial steal, or hemorrhage.
23.9 Pathophysiology
AVMs and fistulas are believed to form as a result of structural deficits in the embryologic arteriolar–capillary network that normally separates the intracranial arterial and venous circulations. Development of these capillary beds takes place in the period between 40 and 80 mm embryonic length, corresponding to gestational age between 11 and 14 weeks. Most AVMs appear to develop prior to the end of this period, but further details as to the formation of these lesions are not well understood.4
An AVM is a vascular malformation in which arterial circulation flows directly into the venous drainage system without an intervening capillary bed. The center of such a lesion, where there is a transition from the arterial to the venous system, is known as the nidus, and contains no neural parenchyma. The fundamental danger of these lesions arises from the feeding of the high-flow, high-pressure arterial system into the low-pressure venous system; these configurations establish the potential for a pressure-flow mismatch that overcomes the strength of the vascular wall, resulting in vascular rupture and hemorrhage.
Because AVMs lack a high-resistance capillary bed separating the arterial from the venous side of the circulation, they tend to have low resistance and consequently high blood flow, with an associated tendency to undergo active remodeling (mediated, in part, by vascular endothelial growth factor) and to increase in size and tortuosity over time.
23.10 Spinal Cord Arteriovenous Malformation
Spinal cord AVMs account for 20 to 30% of SVMs. They are high-flow lesions, and are supplied by at least one branch of the ASA or PSA. The spinal AVM comprises a network of arteriovenous shunts that drain into the spinal veins. Aneurysms associated with the feeding arteries and within the nidus are common.
23.11 Pial Arteriovenous Fistula
A pial AVF comprises one or more direct, intradural arteriovenous shunts, without intervening nidus, located on the pial surface of the spinal cord. The arterial supply arises from one or more branches of the ASA or PSA, and the venous shunt drains into dilated spinal cord veins. Pial AVFs can be classified further according to size and flow rate of the direct arteriovenous shunt.
The type I (small) pial AVF is a single, slow-flow shunt between a normal caliber ASA and a slightly dilated spinal vein. Type I lesions are typically located on the anterior surface of the conus medullaris or filum terminale.
The type II (large) pial AVF comprises one or more shunts in parallel, resulting in greater total flow than is observed in a small AVF, and compensatory “ampullary” (proximal) dilation of the draining vein. Large pial AVFs are most commonly located in the posterolateral aspect of the conus medullaris, in which case they are supplied by one or more slightly dilated branches of a PSA.
The type III (giant) pial AVFs contain one or more high-flow shunts, also supplied by dilated arterial branches of the ASA, PSA, or both. In the case of a giant pial AVF, however, the arterial feeders converge to a single shunt, which drains into a collection of grossly dilated, arterialized draining veins. While giant pial AVFs are most common in the conus medullaris, they are also found at cervical and thoracic levels.
23.12 Dural Arteriovenous Fistula
Spinal dural AVFs are the most common type of spinal AVF. Several synonymous terms are used to refer to these lesions: type I malformations, spinal dural AVFs, intradural dorsal AVFs, dorsal extramedullary AVFs, and angioma venosum racemosum.
Spinal dural AVFs derive their arterial supply from radiculomeningeal branches of segmental spinal arteries (anterior or posterior radicular arteries). Their venous drainage is centripetal into the spinal cord and medullary veins. A critical anatomic feature of these lesions is that the shunt itself is typically located in the dura around the sensory ganglion of the proximal nerve root.
These lesions become symptomatic due to flow reversal in the perimedullary spinal cord veins, resulting in spinal cord venous hypertension, cord ischemia, and in extreme cases, necrotizing myelopathy.
Some authors have proposed that spinal cord autoregulation is accomplished, in part, by a glomerulus-like vascular structure located within the two dural leaflets. The function of this structure is to maintain constant intraspinal venous pressure in the setting of frequent changes in intraabdominal and intrathoracic pressures. The structure comprises the terminal portion of the radiculomedullary vein, which becomes tortuous and narrow in the arachnoid and dura, preventing venous blood from flowing intradurally from the epidural plexus. The wall of the radiculomedullary vein transitions to form a meningeal cuff, which is thought to connect spinal arteries with the perimedullary veins. This model of the spinal arteriovenous anatomy is the basis for the recommendation that both endovascular and microsurgical treatment should aim to obliterate the origin of the proximal draining vein in order to permanently obliterate a spinal dural AVF.5,6
23.13 Epidural Arteriovenous Fistula
An epidural AVF represents an arterial shunt into the epidural venous plexus. This lesion carries high morbidity, though it is extremely rare, appearing in several case reports and small series. Epidural AVFs most commonly arise in the cervical spine, though they have also been described in the lumbar region, sacrum, and pelvis. We include them for completeness in describing the anatomic classification of SVMs, but will not discuss them further here, as they are hardly relevant to surgery of the thoracic spine.
23.14 Intramedullary–Extramedullary Arteriovenous Malformation and Angiomatosis
Intramedullary–extramedullary (also referred to as intradural–extradural) AVMs represent metameric vascular lesions that may involve any or all tissue compartments within one or more adjacent spinal levels, including spinal cord, dura, vertebral bodies, paravertebral soft tissues, and skin. They commonly involve multiple feeding arteries over adjacent spinal levels. Many cases of intramedullary–extramedullary spinal AVMs are associated with developmental syndromes. Cobb syndrome, in particular, is associated with complete AVM involvement of affected somite levels.
23.15 Genetics and Associated Syndromes
AVMs are not congenital; as discussed in the previous section, they are the result of developmental errors that arise during embryogenesis. However, several syndromes have known associations with SVMs, including some with both cutaneous and vascular manifestations: Osler–Weber–Rendu, Klippel–Trénaunay–Weber, Parkes Weber, and Cobb syndromes, as well as neurofibromatosis type I. Ventral intradural AVFs have particular associations with these syndromes. Cobb syndrome involves the skin, vertebrae, and spinal cord of the affected metameres, and AVMs are found in a metameric distribution.6
23.16 Diagnosis and Evaluation
23.16.1 Noninvasive Imaging
Magnetic resonance imaging (MRI) has nearly 100% sensitivity for detecting spinal cord AVMs, and is the imaging modality of choice for initial evaluation and follow-up of these lesions. On MRI, spinal AVMs appear as signal voids within or on the surface of the spinal cord, corresponding to dilated arteries or veins. Other features of these lesions are also detected on MRI, including hematomyelia and spinal cord edema.
Decisions with regard to treatment and the feasibility of surgical or endovascular intervention are almost always based on spinal angiography, which is considered the definitive imaging modality for evaluating spinal cord vascular malformations.
23.16.2 Spinal Angiography
Even in the era of high-quality MRI and noninvasive vascular imaging, conventional catheter spinal angiography remains the definitive imaging modality for diagnosis and classification of SVMs. Catheter angiography still provides maximal spatial resolution, and, most importantly, an ability to isolate segments of the vascular system, and to visualize and study the dynamic flow patterns through lesions of interest.
Spinal angiography under general anesthesia can provide higher quality images of the thoracic region, as longer periods of apnea can be maintained during angiography, to reduce motion artifact, without causing discomfort to the patient.
We routinely perform spinal angiography through a 5 French sheath in the femoral artery, using a 5 French diagnostic catheter. In the thoracic spine, the catheters we most commonly use for catheterization of segmental arteries are the Cobra 2 or Simmons 2 (Terumo Medical, Somerset, NJ) and the Mikaelson and Modified Hook (Merit Medical, South Jordan, UT).
A nonselective angiogram from the aorta can be obtained by power injection through a pigtail, high-flow catheter positioned in the descending aorta at a midthoracic level (injecting at 10 mL/s for a total volume of 35 mL). Similarly, a retrograde bilateral femoral angiogram can be used to study the lumbar and lower thoracic levels nonselectively. In this technique, using bilateral 5 French femoral sheaths, 40 mL of contrast is injected at 20 mL/s into each femoral artery, resulting in opacification of the dorsal aorta at abdominal and lower thoracic levels up to the level of T10. This technique fills the lower thoracic and lumbar segmental arteries without filling the visceral arteries.
Individual segmental arteries must be selectively catheterized and evaluated in almost every case of a SVM. It is important to note that even though a vascular lesion may localize to the thoracic spine, its arterial supply may arise from lumbar or cervical levels, so catheter angiography must take this into account.
In the setting of a spinal AVM, spinal angiography should also be used to evaluate spinal cord venous drainage. This can be accomplished by selective angiography of the artery of Adamkiewicz. When thoracolumbar myelopathy is due to severe venous hypertension, venous drainage after injection of the artery of Adamkiewicz is prolonged or absent. Improvement in venous drainage after treatment of the lesion is a good prognostic factor.6
23.17 Natural History and Implications for Treatment
The natural history of untreated SVMs varies according to lesion type and location. The thoracic spinal cord is particularly vulnerable to ischemia, as it is less well collateralized than the cervical and lumbar segments, so special care must be taken when considering treatment of thoracic SVMs.
23.18 Spinal Cord Arteriovenous Malformation
The natural history of untreated spinal cord AVMs is toward progressive neurological deterioration following an initial event, with a prognosis that varies according to specific lesion type. Extramedullary AVMs tend to present later in life, with 85% of patients asymptomatic until age 40. After an initial event, however, there is a tendency toward steady, progressive decline in neurological function, with major neurological impairment by 4 to 6 years from the initial event. Intramedullary AVMs, by contrast, present prior to age 40 in more than 85% of cases. For intramedullary AVMs of the thoracic spine, 40% of patients are no longer independent 5 years from presentation, and at 15 years 60% are no longer independent.7
As these lesions are often curable, and almost always at least partially treatable in ways that favorably alter the natural history, there is a general agreement that treatment soon after diagnosis is advisable. Microsurgical, endovascular, and combined approaches are possible, and will be discussed in the sections that follow.
23.19 Dural and Pial Arteriovenous Fistula
The natural history of dural and pial AVFs of the spinal cord is incompletely understood, as no cohort has been observed longitudinally without intervention. The best data are derived from observational studies performed in the 1970s, which suggest that within 3 years of initial presentation, 50% of patients with untreated SVMs develop severe neurological disability, as defined by requiring crutches to walk, or being wheelchair bound and unable to stand independently.8
Treatment considerations for dural and pial AVFs are therefore similar to those for spinal cord AVMs with respect to the timing and indications. The choices of modality are also similar, and will be discussed in the sections that follow.
23.20 Intramedullary–Extramedullary Arteriovenous Malformation and Angiomatosis
Intramedullary–extramedullary AVMs and angiomatoses are the most complex SVMs, and they are consequently the most difficult to treat. No optimal treatment strategy has been described. Curative treatment via microsurgical, endovascular, or combined approaches is extremely difficult, and carries high likelihood of procedural morbidity, as the lesions are entangled within normal spinal cord parenchyma. Treatment of these lesions is typically palliative, directed toward relief of symptoms caused by hematoma, arterial steal, venous hypertension, or mass effect.
23.21 Preoperative Assessment and Planning
In the present era, treatment of thoracic SVMs is almost always multimodal. Some lesions can be treated through endovascular techniques alone, some can be treated through open surgical techniques alone, and some require combined endovascular and open surgical approaches. In almost all cases, however, the treatment begins with selective spinal angiography, and partial or complete embolization is considered prior to open surgery.
The primary considerations when planning treatment of a SVM are the location of the lesion in the axial and longitudinal planes, the hemodynamics and angioarchitecture of the lesion, and the neurological status of the patient. Posttreatment status is highly correlated with preoperative neurological function, so early treatment, prior to neurological deterioration, is recommended. Nevertheless, stabilization or partial improvement in neurological function is sometimes achievable when a lesion is treated even after it has severely compromised spinal cord function.
Some lesions require surgical management. Superselective angiography through a microcatheter must be performed prior to embolization of a SVM, in order to rule out the presence of a branch to an anterior or PSA originating from a vascular pedicle common to the lesion. In particular, spinal dural AVFs that have arterial feeders arising from a pedicle common to an anterior or PSA branch should be treated with open surgery rather than endovascular embolization. In such cases, open microsurgical occlusion of the pathologic branch can be performed with greater selective precision, avoiding the potential complication of occluding arterial supply to a spinal cord artery.
As comprehensive management of SVMs requires collaboration between open microsurgical and endovascular surgical teams, it is important for each to understand the capabilities and limitations of the other. We therefore discuss both treatment modalities here.
23.22 Endovascular Treatment
In approaching a spinal cord vascular malformation, several general anatomic considerations must be addressed: anterior or PSA supply, collateral supply to or from adjacent spinal levels, collateral supply via pial collateral vessels, venous drainage, and the optimal point at which to occlude the arteriovenous shunt or shunts. It is particularly important to realize that spinal vascular lesions are dynamic, and their flow patterns and architecture may change during treatment.
The angioarchitecture and hemodynamics of a SVM must be precisely defined prior to any treatment, and they must be understood in the context of the surrounding normal vascular anatomy of the spinal cord. The ASA supplies the anterior two-thirds of the spinal cord, including the majority of the spinal cord grey matter and the corticospinal and spinothalamic tracts. The PSAs supply the dorsal one-third of the spinal cord, and have more anastomoses than the anterior system. As a result, there may be sufficient collateral circulation for the spinal cord to tolerate occlusion of a posterior radiculomedullary branch supplying a PSA, or at least for such an occlusion to result in at most a posterior column syndrome. However, occlusion of an anterior radiculomedullary branch to the ASA carries high risk for causing a spinal cord stroke and anterior cord syndrome.
Vascular anastomoses at levels adjacent to a SVM must be characterized prior to embolization. Anastomoses to the ASA from adjacent levels must be understood and protected during embolization. Such anastomoses are not always apparent prior to treatment, as high-flow malformations may “steal” from small anastomoses. Hemodynamic changes must therefore be anticipated during treatment. In particular, when a high-flow lesion is occluded, collateral anastomoses from which the lesion had been stealing flow may reopen. If one of these anastomoses with a spinal artery, inadvertent embolization of the newly patent artery must be avoided.
Pial anastomoses must also be understood. The pial perimedullary network connects the anterior and PSAs, so embolization of a posterior radiculomedullary artery can result in inadvertent embolization of the ASA.
The optimal occlusion point of an arteriovenous shunt must be determined prior to occlusion. The venous drainage of arteriovenous shunts must be preserved. In an AVM, occlusion of the venous drainage can cause increased pressure in the nidus, resulting in hemorrhage. In an AVF, occlusion of the venous drainage can lead to venous hypertension and cord ischemia. On the other hand, proximal occlusion of an arterial feeder to an arteriovenous shunt can be worse than ineffective, for two reasons. First, collateral arterial anastomoses supplying normal cord can be recruited to supply the shunt, and when this happens the shunt steals flow from normal cord, resulting in steal-induced cord ischemia. Second, proximal occlusion precludes further access for subsequent embolization.
23.23 Spinal Cord Arteriovenous Malformation
The goal in treating spinal cord intramedullary AVMs is to favorably alter the natural history, intervening at an early stage to stabilize or reverse neurlogic deficits and reduce future risk of hemorrhage. Curative treatment without compromising normal spinal cord is not always possible through endovascular, microsurgical, or even combined approaches; however, even partial embolization can preserve neurological function and improve overall prognosis.
Endovascular embolization is an important, first-line treatment strategy for intramedullary spinal cord AVMs, either in isolation or as an adjunct to microsurgical resection.
The angioarchitecture of an intramedullary spinal cord AVM does not always favor definitive cure. As a result, repeated, partial embolization may be an acceptable approach to treatment, favorably altering the natural history by slowing or arresting progressive cord compromise, without obliterating the lesion. Successive particle embolization can be used in this manner. Particle embolization permits slow, stepwise embolization, in a carefully controlled manner, with an ability to observe dynamic changes in the lesion and surrounding normal arterial anatomy during embolization. Particle embolization tends to permit recanalization over time, so periodic (usually annual) retreatment is necessary. In a series of thoracic AVMs treated with periodic particle embolization, 57% of patients improved neurologically after the initial embolization, and 63% improved neurologically after the final embolization. Repeated treatments were required because the recanalization rate was 80%, but there was a clear clinical benefit, with favorable alteration of the natural history, with persistence of clinical improvement after treatment even in the setting of AVM recanalization. It is hypothesized that successive embolization preserves some neurological function by protecting the spinal cord from prolonged exposure to the AVM.9
When the configuration of the AVM permits, liquid embolic agents such as n-butyl cyanoacrylate (n-BCA) and Onyx (ev3, Irvine, CA) should be used to embolize the lesion from within or as close to the AVM nidus as possible. These agents provide essentially permanent occlusion, with very low rates of recanalization. A hazard of these agents is the speed with which they act, resulting in a risk to small perforating arteries supplying normal spinal cord, which may only reappear angiographically as the steal from high-flow components is reduced during embolization.
Several series confirm that it is possible to embolize more than half of the target lesion in more than 80% of patients, with good clinical outcome in more than 80% of patients, and fixed neurological deficit in fewer than 15% of patients (severe deficits in fewer than 5%). The completeness of the embolization is not clearly correlated with clinical outcome.10,11
Most procedural morbidity in the setting of spinal AVM embolization is associated with catheterization of the ASA. We recommend use of a flow-guided catheter for this purpose, when possible. The catheter should be positioned within or as close to the nidus as possible, ideally in a sulcal branch that has turned off the longitudinal axis of the ASA, so as to minimize inadvertent embolization of a small, normal branch.
23.24 Pial Arteriovenous Fistula
The guiding principle behind treatment of pial AVFs is to obliterate the fistula at the point of arteriovenous connection, and to intervene early at an early stage, soon after presentation, to prevent spinal cord compromise and neurological deterioration. Endovascular embolization may also be used as an adjunct to microsurgical treatment, but any treatment approach must achieve complete and permanent occlusion of the point of arteriovenous connection in order to achieve cure and prevent long-term recurrence.
Liquid embolic materials, alone or in conjunction with detachable coils as a scaffold, are ideal for endovascular treatment of pial AVFs, as their degree of penetration into the nidus, to the point of arteriovenous connection, can be controlled. Particle embolization should be used only when endovascular therapy is used as an adjunct to microsurgical treatment, as particle-based occlusions are prone to recanalization. Furthermore, particles may pass through the shunt into the venous circulation, resulting in venous thrombi or pulmonary embolism.
As discussed in a previous section, pial AVFs vary greatly in their angioarchitecture. As a result, endovascular treatment must be individualized to each specific lesion.
Endovascular embolization is typically the treatment modality of choice for giant (type III) pial AVFs. These lesions are amenable to safe microcatheterization of the feeding arteries, which are dilated in response to high flow. Giant pial AVFs can be treated by deploying coils into the fistula as a scaffold for a liquid embolic agent such as n-BCA glue or Onyx (ev3, Irvine, CA). The objective of this approach is to prevent migration of the embolic agent through to the venous side of the high-flow shunt. Embolization must be performed at the fistulous connection and proximal draining vein, but not more proximally on the arterial side, so as to prevent subsequent recruitment of inaccessible collateral feeding arteries and recanalization of the fistula.
Embolization of large (type II) pial AVFs can be challenging, as these lesions typically contain at least one transmedullary or perimedullary feeding artery that is unsafe to catheterize. Small (type I) pial AVFs can be difficult to treat endovascularly, as superselective catheterization and microcatheter placement within the fistula may be dangerous when the feeding artery is a small, distal branch of the ASA. When the angioarchitecture of an AVF poses these technical challenges, microsurgical treatment may be preferable, particularly when the lesion is located on the dorsal or dorsolateral surface of the spinal cord.
23.25 Dural Arteriovenous Fistula
Endovascular management of spinal dural AVFs is similar to that of spinal AVMs, with several logical differences. Catheterization of dural AVFs typically requires microwire-assisted navigation, as these lesions are usually slower-flow lesions than AVMs, which may be catheterized using flow-guided microcatheters. Prior to embolization, superselective angiography should be performed through the microcatheter to ensure that no small branch to the ASA was missed on an initial angiogram from the segmental artery.
Importantly, spinal dural AVFs that receive arterial branches from the same pedicle as either the ASA or a PSA should be treated by microsurgical ligation, rather than by endovascular embolization.
23.26 Surgical Management
23.26.1 Spinal Cord Arteriovenous Malformation
Microsurgical obliteration of intramedullary spinal cord AVMs has been described in small case series, but is rarely achieved in practice.12,13 Nevertheless, a microsurgical approach must be considered when safe angiographic access to the AVM cannot be achieved, as in cases in which the feeding spinal artery branches are long and tortuous. In these cases, microsurgical resection may be appropriate. In the cervical spine and in the filum terminale, both dorsal and ventral lesions can be approached safely for resection. In the thoracic spine, however, dorsal intramedullary AVMs are considerably safer and more straightforward to approach microsurgically than ventral lesions. In all cases, a superficial location makes the AVM more amenable to safe resection.
The microsurgical approach to intramedullary spinal cord AVMs is similar to that of cranial AVMs. Bipolar coagulation and ligation of the arterial feeders must be performed first, while preserving the venous drainage, in order to avoid intraoperative rupture of the lesion. Associated aneurysms may be remodeled with bipolar cauterization, or they may be resected.
