Spinal Vascular Malformations

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CHAPTER 397 Spinal Vascular Malformations

Patients with spinal arteriovenous malformations (AVMs) may have an insidious, subacute, or acute onset of symptoms, depending on the type of AVM and the mechanism of cord injury. Before recommending treatment, one must consider the expected clinical course based on the natural history of the type of vascular abnormality and the potential risks and benefits of the proposed treatment. However, knowledge of the natural history of spinal vascular abnormalities is incomplete. As with other rare disorders for which therapy is attempted, the natural history is known only from retrospective studies, and additional factors mitigate the usefulness of previous studies. Most information on the natural history of spinal AVMs was acquired when they were all considered to be congenital AVMs of the spinal cord. In the past 2 decades there have been significant advances in the understanding and treatment of spinal AVMs. Fundamental observations have been made regarding their true anatomy and pathophysiology, which in turn have enabled more effective and safer treatment. It is now generally recognized that the spinal vascular abnormalities are not a single entity but consist of several biologically distinct forms. Based on an understanding of the epidemiology, anatomy, pathophysiology, mechanism of origin, clinical findings, and prognosis, four major types of spinal vascular abnormalities are now recognized: dural arteriovenous fistulas (AVFs), AVMs of the spinal cord, perimedullary (pial) AVFs, and cavernous angiomas (Table 397-1).

TABLE 397-1 Classification of Spinal Vascular Abnormalities Based on Distinct Biologic Features

Adapted from Oldfield E, Doppman J. Spinal arteriovenous malformations. Clin Neurosurg. 1988;34:161-183.

Although the clinical manifestations suggest a specific pathophysiologic process, which implies the particular type and location of an AVM, a definite diagnosis requires a methodical imaging evaluation. Before embarking on treatment, the clinician must consider (1) the type of vascular abnormality affecting the patient, (2) the probable clinical course based on the natural history of that type of lesion in relation to the age and overall medical condition of the patient, (3) the specific vascular anatomy of the lesion and its relationship to the vessels supplying the spinal cord (Fig. 397-1), and (4) the relative risks and benefits of the proposed treatment.

History and Classification

Elsberg performed the first successful operation for a spinal AVM in 1914.1 Before surgery his patient was densely paraparetic and bedridden and had sensory loss below the T9 dermatomal level. Operative exploration revealed an abnormal posterior “dilated spinal vein” that entered the spinal dura adjacent to the dural penetration of the posterior root of the ninth thoracic spinal nerve. Elsberg excised 2 cm of the abnormal vessel as it penetrated the spinal dura. Postoperatively, the patient improved dramatically, with complete neurological recovery by 3 months after surgery.1,2

The classification of spinal AVMs has evolved with and been limited by the technology available to study them. The earliest analyses of spinal AVMs were based solely on postmortem histopathologic examination. In 1925, Sargent reviewed the 21 previously reported cases of spinal AVM and concluded that 19 of them were “venous angiomas.”3 In his 1943 review of 110 cases, Wyburn-Mason classified spinal cord vascular malformations into two histologic groups, arteriovenous angiomas and purely venous angiomas, the latter accounting for approximately two thirds of all cases.4 The venous angioma type was described as a mass of distended, blue pial vessels on the surface of the spinal cord. For consistency with Virchow’s original classification of vascular anomalies, Wyburn-Mason called this type “angioma racemosum venosum.” Thus, these early classifications suggested that a majority of spinal AVMs were venous lesions on the surface of the cord.5

The introduction of spinal aortography and then selective spinal arteriography by Doppman, Djindjian, and their coworkers in the 1960s allowed clinicians to confirm the presence of spinal AVMs and to define their anatomy in living patients for the first time. Demonstration of the radiographic anatomy of spinal AVMs in vivo resulted in a more precise arteriographic classification of these lesions based on their vascular anatomy and pattern of blood flow rather than on postmortem pathology.610 Hence, spinal AVMs were classified radiographically into three categories.6,7 Type I, the “single coiled vessel type,” constituted 80% to 85% of all spinal AVMs. Type II, or “glomus,” and type III, or “juvenile,” AVMs accounted for 15% to 20% of all lesions. Although investigators were able to demonstrate the site of the AVF only with type II and III lesions, in all three types the nidus was thought to be within the spinal cord.5

The juvenile- and glomus-type malformations, despite accounting for a minority of all spinal AVMs, were initially described more accurately than the single coiled vessel type. Arteriographically, they were composed of a discrete nidus in the substance of the spinal cord and had at least one medullary artery that supplied blood to the spinal cord, as well as to the AVM. The juvenile type was considered analogous to cerebral AVMs. It occurred primarily in children and young adults, had multiple large feeding vessels supplying a large AVM, exhibited rapid shunting of blood flow, and was often associated with a spinal bruit. The glomus type also had a distinctive radiographic appearance. Typically, a single feeding artery supplied a small nidus of delicate vessels occupying a short segment of spinal cord.

The single coiled vessel lesion, the most common of the three types, was described as a single, continuous, tightly coiled vessel on the surface of the spinal cord. Blood flow through this lesion was generally slow, with nearly 20 seconds often required for clearance of contrast material. These spinal AVMs were usually supplied by one or two feeding vessels that were thought to supply the AVM but not the spinal cord. In contrast to the juvenile and glomus types, in this type the nidus of the arteriovenous shunt was not identified. The arteriographic classification was adopted by surgeons, who theorized, but were never able to demonstrate, that the nidus of the AVM was located in multiple penetrating parenchymal vessels between the dorsolateral arterial plexus and the single coiled vessel on the cord surface. This theory, concomitant with the advent of microneurosurgery in the 1960s, led to surgical stripping of the engorged, thin-walled vessels from the surface of the cord as the preferred treatment.11,12

In 1977, Kendall and Logue identified AVFs in the dural sleeve of spinal nerve roots in nine patients who had radiographic findings otherwise completely consistent with the single coiled vessel type of spinal AVM.13 After simple surgical excision of the dural AVF, the patients improved. Hence, lesions that were previously considered pial venous angiomas or single coiled vessel AVMs by earlier classifications were now recognized to be dural AVFs in the spinal nerve root sleeve and adjacent spinal dura. The typical single coiled vessel morphology of these lesions is now acknowledged to be the result of chronic metamorphosis of the vessels of the coronal venous plexus by arterialization of normal pial veins into dilated, serpentine, thin-walled vessels on the surface of the spinal cord.

Two additional advances in the understanding and classification of spinal AVMs have occurred in the past 3 decades. First was the recognition by Djindjian and colleagues in 1977 that some intradural lesions that were previously considered to be AVMs of the spinal cord are actually simple AVFs in the pia (perimedullary AVFs).14 Second was the recognition of an additional important category of vascular lesion that was previously thought to be extremely rare because there was no diagnostic study that could reveal it before the introduction of computed tomographic (CT) scanning. This lesion is the cavernous angioma (also called cavernous malformation), which has a predisposition to hemorrhage repeatedly. Its true incidence has become evident only since the introduction of magnetic resonance imaging (MRI).

With the recognition that former type I AVMs (the “single coiled vessel” type) were actually dural AVFs, identification of perimedullary AVFs, recognition of the clinical importance of cavernous angiomas, and increased understanding of the pathophysiology underlying the natural history and clinical manifestations of the different types of spinal AVMs, it has become clear that each major type is a distinct biologic entity (Figs. 397-2 to 397-7).1434 Thus, reclassification of spinal AVMs was necessary to provide terminology that accurately described the lesion and allowed logical categorization based on biologically distinct categories rather than on the use of old terms and categorization schemes that were based on a mistaken understanding of the true nature of the lesions, used abstract terms (e.g., type I spinal AVM) rather than comprehensible and clearly descriptive terms for the various lesions, and permitted different authors to use the same term in substantially different ways.6,7 Hence, four types of spinal vascular malformations with definite biologic differences (e.g., anatomy, pathogenesis, pathophysiology, epidemiology, clinical features) are now recognized: dural AVFs, intradural vascular malformations (which include AVMs of the spinal cord and intradural AVFs), and cavernous angiomas of the spinal cord (see Table 397-1 and Fig. 397-7). In dural AVFs, the arteriovenous nidus is embedded in the dura, usually in the spinal nerve root sleeve and contiguous dura (see Fig. 397-2). In intradural vascular malformations, the arteriovenous shunt is either buried in the substance of the spinal cord (AVMs; see Figs. 397-3 and 397-4) or in the pia or subarachnoid space (perimedullary AVFs; see Fig. 397-5). Cavernous angiomas (see Fig. 397-6), which are not demonstrated by spinal arteriography but have highly characteristic MRI findings, are rarely mistaken for the other types of spinal vascular abnormalities.

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FIGURE 397-7 Distribution of patients with spinal dural arteriovenous fistulas (AVFs) (A), intradural spinal arteriovenous malformations (AVMs) (B; most reports include AVMs and AVFs), and perimedullary AVFs (C) by gender, age at diagnosis, and level of AVF along the long axis of the spine. The distinct differences in the distribution of patients with these three types of spinal vascular abnormalities indicate that they are biologically discrete disorders and support the general classification depicted in Table 397-1.

(Data compiled from the following references: dural AVFs—gender, 1528 age, 1517,20,24,25 and level 1419,21,23,2428; intradural AVMs—gender, 16,27,28,29,30 and age and level16,27,28,30; and intradural AVFs—gender, age, and level. 27,3134 From Oldfield EH, Bennett A, Chen MY, et al. Successful management of patients with spinal dural arteriovenous fistulas and negative arteriography. J Neurosurg. 2002;9(2 suppl)6:220-229.

Vascular anatomy and Pathogenesis

Normal Vascular Anatomy of the Spinal Cord and Dura

Clinical diagnosis of the various subtypes of spinal AVMs and correct interpretation of diagnostic studies require an understanding of spinal vascular anatomy. Hence, knowledge of the normal spinal vascular anatomy is necessary to fully appreciate the blood supply, arteriographic features, and pathophysiology underlying the cord injury in each type of spinal vascular malformation.

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.

Vascular Anatomy of Spinal Vascular Abnormalities

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

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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.)

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.

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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.)

Juvenile Type

The anatomic features of juvenile-type intradural AVMs are represented in Figures 397-3 and 397-10. These lesions are fed by multiple enlarged medullary arteries via the anterior and posterolateral spinal arteries and may have a voluminous arteriovenous nidus that completely fills the thecal sac. The nidus typically has neural tissue within its interstices. Juvenile AVMs frequently involve the vertebral column and the paraspinous soft tissues (metameric form; see Fig. 397-10). Unlike dural AVFs, these lesions are high-flow AVMs; a spinal bruit may indicate their presence.

Glomus Type

The nidus in the glomus subtype of intradural AVMs is a compact tangle of blood vessels that is confined to a short segment of cord (see Figs. 397-4 and 397-11). These lesions typically lie in the anterior half of the spinal cord and are supplied by one or two medullary arteries via the anterior spinal artery or the posterolateral spinal arteries.

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.4450

Etiology, Pathophysiology, Clinical Findings, and Natural History

This section discusses the cause, pathophysiology, clinical manifestations, and natural history of each type of vascular abnormality. Dural AVFs are the most common type, have a similar pathophysiology of cord injury from patient to patient, and have a relatively stereotypic clinical course that permits prediction of a patient’s prognosis with reasonable accuracy. In contrast, the other types of AVMs are less common and have a more sporadic and less predictable clinical course, and the pathophysiology of the cord injury varies from patient to patient (e.g., hemorrhage, venous congestion, vascular steal, aneurysm formation with cord compression). Cavernous angiomas, which have conspicuously different clinical and radiographic features and do not pose a problem of differential diagnosis, are considered last.

Dural Arteriovenous Fistulas

Spinal dural AVFs are distinguished from intradural AVMs by their cause, pathophysiology, incidence, age at onset of symptoms, distribution along the spinal axis (see Fig. 397-7), and neurological findings and progression (Table 397-2).5,15 These distinguishing characteristics are important because effective treatment of such lesions requires early recognition and clinical differentiation from intradural spinal AVMs.

TABLE 397-2 Comparison of Clinical Syndromes of Dural Arteriovenous Fistulas and Intradural Arteriovenous Malformations

  DURAL AVF (N = 27) INTRADURAL AVM* (N = 54)
Gender Predominantly male Male or female
Mean age at diagnosis (yr) 46 24
Onset of symptoms Gradual (85%) Acute (37%)
SAH 0 50%
First symptom Paresis (44%) SAH (32%)
Spinal bruit 0 6%
Exacerbation of symptoms by activity 70% 15%
Arms affected 0 11%

AVF, arteriovenous fistula; AVM, arteriovenous malformation; SAH, subarachnoid hemorrhage.

* Includes perimedullary AVFs.

Adapted from Rosenblum B, Oldfield EH, Doppman JL, et al. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVMs in 81 patients. J Neurosurg. 1987;67:795-802.

Although the exact mechanism underlying the origin of dural AVFs is unknown, the late onset of symptoms, lack of association with other vascular anomalies, strong predilection for the lower spinal segments, absence of medullary veins in these patients,15,40,51 predominant occurrence in men, and occasional development of similar lesions by acquired means, such as traumatic paraspinal AVFs52 and postoperative dural AVFs,53 suggest that these lesions are acquired.5,15 The pathophysiology of the progressive myelopathy produced by these lesions is clear: dural AVFs are low-flow arteriovenous shunts that induce venous hypertension. By directly measuring venous pressure in the coronal venous plexus at surgery in patients with spinal dural AVFs, Hassler and coworkers demonstrated that venous pressure in the spinal cord averages 74% of the simultaneous mean systemic arterial pressure.54 Therefore, by the time of treatment, these patients have venous hypertension severe enough to reduce spinal cord arterial perfusion pressure to less than 30% of normal (spinal cord perfusion pressure = mean arterial pressure−venous pressure), thereby resulting in venous congestion, spinal cord ischemia, and progressive cord injury with clinical myelopathy. The clinical result of progressive cord injury from venous hypertension is an insidious but progressive decline in motor and sensory function, which is the manifestation in 85% to 95% of patients with dural AVFs.15,55 However, about 5% to 15% of patients with dural AVFs experience episodes of acute myelopathic exacerbation (Foix-Alajouanine syndrome).17 The rapid worsening in such cases probably indicates profound venous congestion, which unless treated expeditiously to eliminate venous hypertension, will result in venous thrombosis and irreversible cord injury.56 An even rarer finding—and one that has been reported in only a few patients with dural AVFs—is acute hemorrhage.

For clinical diagnosis, it is important to remember that dural AVFs are distinguished from intradural AVMs by a number of clinical features (see Fig. 397-7 and Table 397-2).16 Unlike intradural AVMs, dural AVFs have a strong male predilection (>80%) and develop in the latter half of life (in 80% of patients the onset of symptoms begins after the age of 40).15 Dural AVFs have a strong tendency to occur in the lower thoracic and lumbar regions.15 Consequently, patients with spinal dural AVFs are unlikely to exhibit upper extremity involvement and typically have an insidious onset of paraparesis or sphincter dysfunction. Low back or radicular pain often precedes the onset of a gradually progressive myelopathy. Patients with dural AVFs frequently report worsening of symptoms during physical exertion (neurogenic claudication) or with certain changes in posture (see Table 397-2).15

There are no studies of the natural history of patients with untreated dural AVFs. The first report describing them was not published until 1977.13 With that report it became apparent that treatment was simple, safe, and effective. Thus, a prospective study of their natural history without treatment has not been possible and cannot be justified now or in the future. However, the natural history of dural AVFs can be deduced from studies performed before recognition of their existence and from studies of the condition of patients at treatment.57 This opportunity is based on their high prevalence in patients with spinal AVMs; their distinguishing epidemiologic and clinical features,5,15 which are distinct enough to permit their identification with reasonable accuracy in previous studies30,5860; and the consistency of their clinical course. The information available to examine the natural history comes principally from a retrospective analysis performed by Aminoff and Logue and reported in 1974.58,59 Although their study began before the introduction of selective spinal arteriography, it clearly reveals the natural history of patients with dural AVFs. The study was composed predominantly of adult men with thoracolumbar lesions (49 of the 60 patients were ≥41 years old, 43 of those 49 were men, and 55 of the 60 lesions [92%] were located in the thoracic or lumbar spinal segments)43 that had never hemorrhaged (90%), features that distinguish patients with dural AVFs from those with other types of spinal AVMs.57 The course of the disease, as defined by their study, consisted of progressive neurological decline and functional disability. Twenty percent of the 60 patients required crutches or were nonambulatory by 6 months after the onset of symptoms other than pain (Fig. 397-13). Fifty percent of the patients were severely disabled (confined to a wheelchair or bed) within 3 years of the onset of gait impairment, and 91% had restricted activity within 3 years of the onset of symptoms.58,59 Similarly, in their 1976 report, which included 23 patients with type I AVMs (now known to be dural AVFs), Tobin and Layton noted that “There seems to be a distinct natural history for patients who have the angiographic Type I arteriovenous malformation. These usually have a slowly progressive course, evolving over 2 to 3 years, leading to nearly complete paraplegia and bowel or bladder incontinence. Few of these patients seem to have other modes of presentation.”29

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FIGURE 397-13 Degree of functional disability at 6 months and 3 years after the onset of symptoms in 49 patients aged 41 years or older reported by Aminoff and Logue.59 Almost all these patients had spinal dural arteriovenous fistulas. Note that the greatest change in function between 6 months and 3 years is in patients with minimal neurological deficit who progressed to severe functional disability. By 3 years, half the patients were confined to wheelchairs or had to use crutches to ambulate.

(From Oldfield E. Spinal vascular malformations. In: Swash M, ed. Outcomes in Neurological and Neurosurgical Disorders. Cambridge, UK: Cambridge University Press; 1998.)

In contrast to the gradual, slowly progressive decline in motor and sensory function over a period of 2 to 3 years,5,13,15,29,55,59,61,62 about 15% of patients with dural AVFs have more rapid, subacute neurological worsening (Foix-Alajouanine syndrome). This deterioration is unpredictable and indicates severe venous congestion, which unless treated immediately will lead to venous thrombosis, infarction, and irreversible loss of neurological function.17,56

Intradural Arteriovenous Malformations

Spinal cord AVMs, unlike dural AVFs, occur in males and females at a nearly equal incidence (see Fig. 397-7). Furthermore, intradural vascular malformations of the spinal cord have an earlier onset of symptoms, a higher incidence of association with other vascular anomalies, and a more uniform distribution along the spinal axis than do dural AVFs (see Fig. 397-7).15 Collectively, these observations suggest that AVMs of the spinal cord are congenital lesions, most likely the result of inborn errors of vascular embryogenesis (Table 397-3). The embryologic insult probably occurs before day 18 of gestation because the spinal cord vasculature is fully developed by that time.

TABLE 397-3 Comparison of Acquired versus Congenital Vascular Malformations

  ACQUIRED DURAL AVF CONGENITAL AVM OF THE SPINAL CORD
Gender Predominantly male Male or female
Onset of symptoms Later half of adulthood Child or young adult
Associated congenital malformation Never Occasionally
Distribution along the spine Lower half Diffuse
Normal spinal venous pathways Absent Present

AVF, arteriovenous fistula; AVM, arteriovenous malformation.

From Oldfield E, Doppman J. Spinal arteriovenous malformations. Clin Neurosurg. 1988;34:161-183.

Although current understanding of the pathophysiologic basis of the myelopathy in medullary AVMs (juvenile and glomus types) suggests that the mechanism may not be the same in all patients, the high flow rates associated with this type of spinal AVM underlie all putative mechanisms. In contrast to patients with dural AVFs, an acute initial manifestation consisting of the sudden onset of back pain, suboccipital pain, and meningismus or sudden loss of consciousness occurs in many patients with AVMs of the spinal cord; subarachnoid or intramedullary hemorrhage occurs as the initial finding in about 35% of patients; and by the time of diagnosis, about 50% of patients have had one or more hemorrhages (Table 397-4; see also Table 397-2).15,60,6365 The incidence of hemorrhage is even higher in children. In 38 children younger than 15 years with AVMs of the spinal cord reported by Riche and colleagues, 84% had an acute initial onset of symptoms, 59% of which were associated with sudden impairment of motor function.18 The high incidence of associated arterial aneurysms and the 13% to 37% incidence of associated vascular abormalities elsewhere in the central nervous system15,60,63 may partially explain the high incidence of hemorrhage.

Conversely, about half of all patients with intramedullary AVMs do not experience the acute deterioration that accompanies hemorrhage. The gradual loss of neurological function in these patients suggests a different mechanism of cord injury.15 Several mechanisms for this progressive form of myelopathy have been proposed, including ischemia resulting from vascular steal,66,67 mechanical compression by an aneurysm, and medullary venous congestion.15 Because intradural AVMs are high-flow shunts, because the medullary arteries that supply the arteriovenous nidus of these lesions also routinely supply the spinal cord, and because visible, often enlarged medullary veins provide venous drainage into the extradural venous system in most of these lesions,15 a vascular steal phenomenon may be the most logical explanation in many patients with progressive loss of neurological function.

The natural history of intradural AVMs, similar to the pathophysiologic mechanism of cord injury, is incompletely defined and variable. Data on long-term disability without therapy are unavailable because these lesions are usually treated when they are diagnosed. Many reports suggest that AVMs of the spinal cord cause recurrent hemorrhages or progressive neurological disability over the first few months or years after they are diagnosed (see Table 397-4). In the 90 patients with intradural AVMs of all types reported by Hurth and associates, 69% had acute episodes of stepwise neurological progression, and 39% of the patients with previous hemorrhage had at least one additional hemorrhage (fatal in one patient).60 Similarly, in the 38 patients with thoracic medullary AVMs treated by Biondi and colleagues by repeated, yearly embolization with particles of polyvinyl alcohol (PVA), 31% relapsed with neurological worsening between treatments (average of 6 years of treatment).64 Pregnancy, vigorous exertion, and minor trauma may cause rapid progression of symptoms or be associated with increased risk for hemorrhage (see Table 397-4).

Most authors characterize the prognosis of these patients as grave and consider the natural history sufficiently unpredictable and hazardous to justify the risks related to treatment.5,15,18,41,60,64,65,68 However, it must be acknowledged that the natural history varies greatly in individual patients and that the prognosis in some of them is not always grim. Retrospective evaluation of Aminoff and Logue’s series57 indicates that in half the patients whose manifestation was acute—one more likely to be associated with intradural AVMs—there was no subsequent neurological progression.58,59 Similar observations were made by Tobin and Layton in their report on the natural history of patients with spinal AVMs, in which they reported a progressive course leading to paraplegia over a period of 2 to 3 years in patients with features that now suggest dural AVFs, but “such a relationship was not as clear” for intradural AVMs.29 Hurth and associates noted that 80% of the 17 untreated patients with AVMs in the cervical segments of the spinal cord were independent and capable of carrying out their jobs 5 years after diagnosis and that 5 patients who were untreated or incompletely treated were unchanged 15 years after diagnosis, thus demonstrating the “slow progression of disease … in a limited number of cases.” Furthermore, 60% of their 17 untreated patients with thoracic AVMs at 5 years and 41% of 17 untreated or incompletely treated patients at 15 years were “self-sufficient and relatively well.”60 The dilemma in making decisions for individual patients is that we have no reliable guidelines that permit us to identify these patients prospectively.

Thus, although the neurological prognosis is guarded for untreated adults with intradural AVMs, it may not be as dismal as it is for patients with dural AVFs. This must be considered when undertaking treatment of intradural AVMs because in some cases, attempts to permanently eliminate the AVM are associated with significant risk.

An exception to this occurs in children with symptomatic AVMs of the spinal cord. In the retrospective assessment of 38 children younger than 15 years by Riche and colleagues, symptoms had a sudden onset in 84%, and in 60% of these patients there was sudden impairment of motor function, often associated with physical effort.18 The sudden onset was commonly followed by a period of remission, but with successive attacks in 71% and subarachnoid hemorrhage in 55%. Unlike the situation in adults, a gradually progressive evolution of the syndrome occurred in just 17% of the 38 children.

Perimedullary Arteriovenous Fistulas

Perimedullary AVFs, which lie in the pia on the surface of the spinal cord, constitute about 10% to 20% of all spinal AVMs.14,15,30 They are distributed equally between males and females, and most are associated with an onset of symptoms in the first half of adult life; the average age at diagnosis is older than that of patients with AVMs of the spinal cord but younger than that of patients with dural AVFs (see Fig. 397-7). However, they may also be diagnosed in childhood as early as 3 weeks of age.69,70 Their anatomic distribution along the spinal axis is bimodal, predominantly in the thoracolumbar region, particularly at the conus medullaris, and to a lesser extent in the upper cervical region (see Fig. 397-7).14,15,30,33,69

The existence of these lesions in early childhood suggests a congenital mechanism of origin. However, they may initially be diagnosed in late adulthood, and there are cases in which a perimedullary AVF was acquired. In one instance, an AVF arose in the conus medullaris in a 28-year-old 5 years after resection of a teratoma of the filum terminale.41 In another case, a perimedullary AVF in the conus medullaris developed in a 35-year-old 1 year after resection of an ependymoma at the same site.69 In two patients the origin of an AVF in late adulthood is argued to have occurred in association with deficient medullary venous drainage of the spinal cord.34

The initial clinical finding is a slowly progressive myelopathy or radiculopathy, which occurs in about 80% of patients, or subarachnoid hemorrhage, which affects about 20% of patients.15 For therapeutic purposes, Merland and colleagues categorized perimedullary AVFs into three distinct types (Table 397-5). Type I is a small, simple fistula supplied by a single feeder, usually the terminal portion of a thin anterior spinal artery, but in some instances a posterior spinal artery. Flow through the fistula is usually slow and ascending in the vessels of the coronal venous plexus, which are only slightly tortuous and dilated (Fig. 397-14). Type II AVFs are supplied by one or two main arterial feeders via several distinct arterial pedicles that converge to form multiple discrete shunts and drain into a dilated and tortuous venous system at a relatively high flow rate (see Fig. 397-12). Type III AVFs, which account for the majority of pial AVFs, are single giant AVFs with very high blood flow located in the cervical or lower thoracolumbar level. They are fed by several branches of the posterior or anterior spinal arteries, which are hugely dilated and converge into a single shunt draining into a giant venous ectasia (Fig. 397-15).30,41

Initially, it appeared as though there were no distinctive clinical features among the various types of perimedullary AVFs, but with more experience it has become apparent that only type II and III AVFs hemorrhage or produce compression of the spinal cord by venous ectasia.30 Nonetheless, most patients have a gradually progressive neurological loss15,30 that is similar to the progression associated with the venous hypertension underlying the myelopathy of spinal dural AVFs. Barrow and colleagues directly quantified venous hypertension in the venous drainage of two patients with intradural AVFs and progressive myelopathy and related the venous pressures with the clinical and MRI findings.69 This mechanism probably accounts for the myelopathy in most patients with type I AVFs because they do not hemorrhage, they are not associated with venous ectasia and cord compression, and the rate of transit from the arterial to the venous system is much too slow to produce vascular steal. However, because type II and III AVFs are always supplied by an artery that also supplies the spinal cord, it is likely that vascular steal accounts for the myelopathy in at least some of these patients with rapid shunting of blood and generous venous drainage pathways on arteriography.

Retrospective studies of the clinical history before treatment provide the only information on the natural history of this type of AVM. They suggest a relentless progression from myelopathy to paraplegia within 5 to 7 years of the onset of symptoms in patients with myelopathy but without hemorrhage, and there is a high incidence of repeated hemorrhage in patients with hemorrhage.14,15,41,30,69

Cavernous Angiomas

Cavernous angiomas, also known as cavernous malformations, cavernous hemangiomas, and cavernomas, are distributed along the entire length of the neuraxis and represent 5% to 12% of all spinal vascular abnormalities.44,71 They are distributed proportional to the volume of nervous tissue, so many more arise in the brain than in the spinal cord.72 Cavernous angiomas in the spinal cord are histologically identical to those in the brain. They typically occur as an intramedullary mass but may be seen as an epidural lesion.

Studies have identified a familial variant of the disease (familial multiple cavernous angiomatosis) characterized by multiple cavernomas and autosomal dominant transmission.42,43,7378 Genetic studies on patients from affected families have localized the genetic abnormality to chromosome 7q.4550,7884

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