Spinal Intradural Vascular Malformations

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Chapter 103 Spinal Intradural Vascular Malformations

Jonathan A. White, Thomas A. Kopitnik, H. Hunt Batjer

Spinal vascular malformations are a family of lesions involving abnormalities of the arteries or veins surrounding the spinal column, spinal cord, and nerve roots. They are relatively rare ¹^–³ and may manifest as a hemorrhage, myelopathy, radiculopathy, or back pain.⁴^–⁷ These lesions can be divided into two broad categories: those that are intradural and those whose abnormal arterial connections are extradural. Extradural lesions are the most common and account for approximately 80% of spinal vascular malformations and are considered in another chapter. This chapter discusses the intradural lesions and includes glomus arteriovenous malformations (AVMs), juvenile AVMs, and intradural direct arteriovenous fistulas (AVFs). Cavernous malformations of the spinal cord and intradural spinal aneurysms are also discussed. In addition to detailing the symptoms, diagnosis, treatment, natural history, and outcomes of these lesions, the demographics and symptoms of these lesions are contrasted with those of the extradural lesions.

History and Nomenclature

The early classification of spinal AVMs occurred prior to the advent of spinal angiography. Patients with signs and symptoms of myelopathy underwent surgery, and the lesions were characterized based on their pathologic appearance.⁸^–¹⁷

With the advent of spinal angiography in the 1960s, a more refined nomenclature developed based on the pattern of arterial input and venous drainage.¹⁸^–²⁰ This resulted in the creation of the terms type I, type II, and type III AVMs still in common use today.^2,^21,²²

A type I lesion is a dural AVF whose single or, occasionally, multiple arteriovenous connections lie within the dura of the nerve root sheath and result in a dilated, arterialized coronal venous plexus.^23,²⁴ Prior to angiography, this dilated vein was erroneously felt to be the site of pathology rather than the arteriovenous connection that is the true source of pathology. Surgical treatment consisted of stripping the veins, often with poor results.²⁵ With the recognition of the fistulous component of this lesion, surgical therapy has been directed at ligation of the abnormal arteriovenous connection and has led to significantly better outcomes.

Type II lesions, or glomus AVMs, are analogous to intracranial AVMs and consist of a tightly packed nidus of vessels over a short segment of the spinal cord. These lesions tend to manifest at an earlier age than the type I lesions and tend to occur at the cervicothoracic junction rather than at the thoracolumbar junction.^1,²⁶ Like type I lesions they may be amenable to surgical excision. Type III lesions, or juvenile AVMs, arise in single or multiple adjacent somites and therefore are frequently both extradural and intradural and may involve soft tissue and bone in addition to the spinal cord and dura.^27,²⁸ In the cord they form a diffuse nidus with normal spinal cord existing between loops of abnormal vessels. The embryologic term metameric was historically used in connection with these lesions because it connotes involvement of tissue derived from the entire somite.¹⁵ Surgical cure of these metameric or type III lesions (juvenile AVMs) is difficult and often requires a multidisciplinary approach.

Shortly after the introduction of the type I to III classification an additional type IV lesion was proposed by Heros et al.¹³ This lesion is a direct connection between an intradural artery and a vein in the subarachnoid space without a definable nidus. The lesions are frequently ventral and involve the anterior spinal artery. Surgical cure is possible when the lesions are small. Embolization may be a helpful adjuvant and may be palliative for the larger lesions.

The understanding and classification of spinal vascular malformations continue to evolve. Recently, a type V spinal AVM was proposed based on the observation that some type III AVMs are outside the spinal cord and dura and are therefore not truly metameric.²⁹ Their epidural location drastically changes the potential for treatment. Spetzler et al.,³⁰ in addition to their other nomenclature contributions, have proposed that juvenile AVMs of the conus medullaris be considered a separate category of spinal AVM because complex juvenile lesions at the level of the conus may have a more favorable prognosis with surgical resection.

With the advent of MRI, cavernous malformations of the spinal cord have been identified with increasing frequency.^1,^{7–9,16,31–53} Like their intracranial counterparts, they are sinusoidal venous channels that appear with stair-step neurologic decline from repeated hemorrhage. Some controversy exists over the indication for surgical resection of these lesions. Intradural spinal aneurysms are also being diagnosed with increasing frequency and may be traumatic, flow related from AVM feeding vessels, or rarely congenital such as an aneurysm of a posterior inferior cerebellar artery that has a spinal origin. These lesions appear with subarachnoid hemorrhage and may require direct surgical repair or endovascular vessel sacrifice.

Embryology and Vascular Anatomy

The fetal spinal vascular network develops in four stages.⁵⁴ The first, or primitive segmental, stage, occurs between weeks 2 and 3 of gestation. During this stage, 31 pairs of segmental vessels originate from paired dorsal aortas and grow toward the neural tube along the developing nerve roots. The segmental vessels divide into ventral and dorsal branches and form capillary networks on the ventrolateral surface of the neural tube. These networks ultimately develop into paired primitive ventral arterial tracts, the precursors of the anterior spinal artery. The anterior spinal artery develops when these paired ventral arterial tracts fuse during the third stage of development.

The second, or initial, stage occurs between weeks 3 and 6 of development and is significant for development of dorsal arterial anastomoses, separate and distinct from the ventral spinal vascular system. At this stage, longitudinal venous channels also develop on both the ventral and dorsal spinal cord surfaces. These venous channels eventually expand and give rise to an interconnected capillary network. It is within this second stage that maldevelopment theoretically leads to the genesis of vascular malformations that persist after birth and into adulthood.

The transitional stage is the third embryologic stage of spinal vascular development and occurs between the sixth week and fourth month of fetal growth. The major development in this stage is the formation of the adult pattern of vascular supply. The primitive ventral longitudinal arterial tracts fuse, and the number of segmental arteries supplying the spinal cord is reduced.⁵⁵ By 10 weeks’ gestational age, adult patterns of superficial spinal cord vessels are present. The last stage, called the terminal stage, occurs after 4 months of development and is the phase of maturation and increased tortuosity of the major spinal cord vessels.

The most likely stage of embryologic development at which spinal vascular malformations can arise is the second stage (3–6 weeks). Maldevelopment in this stage leads to persistence of thin-walled tortuous vessels that exhibit primitive capillary interconnections, arteriovenous shunts, and poorly developed elastic and medial layers that closely resemble intracranial angiomas.¹¹ The concept that intradural vascular malformations are congenital and are the result of fetal vascular maldevelopment is supported by the fact that 20% of patients with intradural AVMs have other associated congenital vascular anomalies (Table 103-1). Furthermore, these malformations are present in younger patients and are distributed throughout the entire spinal axis. This favors a common dysembryogenic basis of intradural spinal and other vascular malformations.

TABLE 103-1 Congenital Vascular Anomalies Associated with Intradural Spinal Arteriovenous Malformations

Congenital Anomaly	Reference
Brain arteriovenous malformation	Brion et al.¹⁰; Bruni et al.³³; Di Chiro and Wener¹⁸; Hebold¹⁷; Jellinger et al.⁹¹
Cerebral aneurysm	Aminoff and Logue⁴; Djindjian⁶; Djindjian et al.⁷¹; Hebold¹⁷
Vascular agenesis	Hebold¹⁷
Rendu-Osler-Weber syndrome	Doppman et al.²¹; Hebold¹⁷
Klippel-Trénaunay-Weber syndrome	Cogen and Stein⁶⁸; Hebold¹⁷; Heros et al.⁷⁸
Soft tissue hemangiomas	Djindjian et al.⁵⁸
Hemangioblastomas	Hall et al.¹⁴

In the adult, the anterior spinal artery arises from the fusion of a contribution from each of the vertebral arteries. It supplies the ventral two thirds of the spinal cord, including the lateral corticospinal tracts. It narrows as it descends but is reinforced by blood vessels at some segmental levels of the spinal column. At each segmental level a dorsal ramus of the intercostal artery enters the intervertebral foramen and gives rise to three branches: a dural branch, a radicular branch, and a medullary branch. The radicular and dural branches go to the nerve root and dura, respectively, and the medullary branch augments the flow to the anterior spinal artery. As mentioned, in fetal life during the third stage of vascular development most of the medullary branches involute, leaving the distal portion of the cord relatively ischemic. In the upper lumbar region at one segmental level the medullary artery does not involute and augments the supply of blood to the cord. This retained medullary vessel arises somewhere between T8 and L4, most often on the left, and is known as the arteria radicularis magna, or artery of Adamkiewicz. This still leaves a zone relatively vulnerable to ischemia in the upper thoracic region. The paired posterior spinal arteries run the length of the spine and supply the dorsal third of the spinal cord.

Venous drainage of the cord follows the arterial supply. Radial veins coalesce from the cord and anastomose to become the coronal venous plexus, a plexus of veins on the cord surface. At segmental levels, medullary veins leave the coronal plexus and exit the intervertebral foramen to join the epidural venous plexus. This epidural plexus communicates with the venous sinuses of the cranial dura and drains into ascending lumbar veins and the azygous venous system.

Glomus Arteriovenous Malformations

Glomus, or type II, spinal AVMs are high-flow malformations in which a tightly packed malformation nidus is located within a short segment of the pia or the spinal cord parenchyma. They may occur anywhere along the longitudinal axis of the spinal cord, although some reports indicate a higher incidence of glomus AVMs in the cervicothoracic junction.^1,²⁶ The feeding arteries of glomus AVMs usually arise from distinct medullary arteries and also supply the spinal cord.⁵⁶ The malformations are frequently found in the ventral aspect of the spinal cord and derive their blood supply from medullary branches of the anterior spinal artery. Venous drainage is through the coronal venous plexus, and, unlike dural (type I) AVMs, the venous drainage usually occurs in both a rostral and a caudal direction⁵⁷ (Fig. 103-1). With dural lesions, caudal venous drainage is extremely rare.

FIGURE 103-1 Spinal cord glomus arteriovenous malformation with arterial feeding from the anterior spinal artery and bidirectional venous drainage.

The clinical symptoms of glomus-type intramedullary AVMs is usually apoplectic in nature because of sudden hemorrhage from the malformation. These AVMs usually become symptomatic before adulthood and frequently appear with subarachnoid hemorrhage (SAH). Neurologic symptoms often involve the upper extremities, if the nidus is in or near the cervical portion of the spinal cord. By comparison, upper extremity involvement is exceedingly rare in the more commonly observed dural (type I) AVMs. There is no gender predilection for intradural AVMs, whereas at least 85% of spinal dural AVMs occur in males. SAH or intramedullary hemorrhage occurs in 50% of patients with intradural vascular malformations and is attributed to the frequently associated presence of arterial or venous aneurysms.^1,^58,⁵⁹ Of 54 patients with confirmed intradural spinal AVMs who were studied at the National Institute of Health, 30 patients (52%) had experienced SAH and 24 patients (44%) had aneurysms associated with either the draining or feeding vasculature.⁵⁹ SAH occurs as the initial symptom most commonly in glomus-type malformations, whereas weakness is most common in any other spinal vascular malformation.

At the time of diagnosis, most patients with intradural AVMs have some motor and sensory deficit. Spastic paraparesis and pain and temperature sensory deficits are the most frequent neurologic findings during onset.⁵⁹ A bruit heard over the affected dermatome may also be present. With intradural AVMs, specific neurologic symptoms reflect the location of the nidus along the longitudinal axis of the spinal cord. Strenuous activity or postural changes rarely exacerbate the symptoms of intradural glomus-type AVMs, although this is a common finding with dural type I lesions or juvenile (type III) spinal malformations.

The differential diagnosis encompasses numerous conditions that may mimic the symptoms of an intradural AVM. Because of the relatively rare incidence of intradural spinal vascular malformations, other diagnoses are more tenable. They include degenerative diseases, neoplasms, infections, trauma, demyelinating or neurodegenerative diseases, and developmental and acquired conditions. The apoplectic nature of spinal SAH, which occurs in at least one half of patients with intradural glomus AVMs, is the single distinguishing event that strongly implicates an intradural vascular malformation as the etiology.

Adequate and appropriate radiologic investigation is paramount for confirming the diagnosis of an intradural vascular malformation. Plain spine radiographs may be useful to rule out other pathology and have been found by some to be abnormal in patients with high-flow intradural AVMs. Rosenblum et al.⁵⁹ found that 15% of patients with intradural AVMs had widened interpeduncular distances on plain spine radiographs. No increase in spinal canal dimension was observed with type I dural lesions.

Although total spine myelography was the radiologic test of choice for many years, most patients now undergo MRI as a screening test instead of myelography (Fig. 103-2). Although the sensitivity of myelography and CT for detecting a spinal AVM is high, the anatomic information is nonspecific.⁶⁰ Selective spinal angiography with high-resolution digital imaging remains the diagnostic test of choice to provide the most precise anatomic information (Fig. 103-3).