Spinal Cord Vascular Malformations in Children

Spinal vascular malformations comprise a diverse group of abnormalities, including arteriovenous malformations (AVMs), cavernous malformations, dural arteriovenous fistulas (AVFs), and capillary telangiectasias. These conditions each have distinct causes, presentations, radiologic appearances, natural histories, and treatments and are best considered separately. Although these lesions have been associated with a poor prognosis in the past, improvements in diagnosis and treatment have resulted in significantly better outcomes over the past 2 decades. All of these lesion types may be found in the pediatric age range. This article explores the presentation, natural history, investigation, and treatment of spinal AVMs, spinal AVFs, and spinal cavernous malformations.

Various classification schemes exist to characterize arteriovenous lesions in the spinal cord. In any system of classification, a distinction should be made between AVFs and true AVMs. In 1993, Anson and Spetzler attempted to classify spinal AVMs into 4 types. In this classification system, a type I AVM is actually a dural AVF, and types II, III, and IV are intradural lesions. A type II spinal AVM is an intramedullary glomus AVM characterized by a compact nidus of abnormal blood vessels within the spinal cord. Juvenile or metameric AVMs, referred to as type III lesions, are more extensive vascular lesions that can occupy the entire spinal canal at multiple levels and often extend into the paraspinal space. Type IV malformations are perimedullary AVFs in which the transition from feeding artery to draining vein occurs without an intervening nidus of abnormal vessels. Perimedullary fistulas can be further divided into 3 subtypes: a type IVa lesion, which is a small extramedullary fistula fed by a single arterial branch; a type IVb lesion, which is an intermediate-sized lesion supplied by multiple dilated arterial feeders; and a type IVc fistula, which is a high-flow, large-caliber, multipediculated fistula associated with dilated and tortuous vessels and a large shunt volume.

The tendency for the classification system of Anson and Spetzler to link AVFs with AVMs led Spetzler and colleagues to propose a new classification system that draws a clearer distinction between these 2 distinct entities. This new classification system emphasizes the distinction between lesion type (eg, AVF or AVM) as well as location of the lesion within the spinal axis (eg, extradural, intradural extramedullary, and intradural intramedullary). Intramedullary lesions may be further divided according to nidus type (eg, compact or diffuse). Intradural extramedullary fistulae are divided according to location (eg, ventral or dorsal).

Spinal cord AVMs

Pial spinal AVMs are lesions with a vascular nidus present within the spinal cord parenchyma. These lesions can be compact or diffuse. Compact glomus AVMs account for approximately 90% of all intramedullary spinal AVMs and are supplied by multiple feeders from the anterior and posterior spinal arteries. The venous outflow of these lesions is usually diffuse, occurring in the rostral and caudal directions and on the dorsal and ventral surfaces of the spinal cord. Glomus AVMs are most commonly seen at the dorsal cervicomedullary junction. As with cerebral AVMs, associated aneurysms may increase the risk of hemorrhage. Surgical resection is the mainstay of treatment of such lesions, and preoperative embolization is useful in select cases.

Juvenile or metameric AVMs are extensive lesions that typically have an intramedullary component and extend into the extramedullary and extradural space. These complex vascular lesions can occupy the entire spinal canal and extend into the paraspinal space. They may involve multiple spinal levels and are supplied by several large medullary arterial feeders. Diffuse intramedullary AVMs can involve the subarachnoid space, pia, and parenchyma of the spinal cord. Normal intervening neural tissue may be contained between the intraparenchymal portions of the AVM. Secondary bony remodeling changes that can be seen in patients with juvenile AVMs include enlargement of the spinal canal with a widened interpedicular distance and erosion of the laminae and pedicles. These lesions typically affect children and young adults and may involve the bone, muscle, skin, spinal canal, spinal cord, and nerve roots of an entire somite level, as seen in disorders such as Cobb syndrome. These extensive lesions are difficult to treat, with the goals of therapy being to reduce mass effect, venous hypertension, and vascular steal. Endovascular embolization is the treatment of choice, but open surgical treatment may be required for decompressive purposes as well. Surgical resection of diffuse lesions involves ligating the vascular loops at the pial surface rather than following the lesions into the parenchyma of the spinal cord.

Demographics and Incidence

Spinal AVMs are one-tenth as common as intracranial AVMs. Spinal AVMs are rare entities in children. In a recent review of 267 patients who presented with a spinal AVM in a single year, 22% of patients were 18 years or younger. Intradural spinal AVMs are more likely to affect children and young adults, whereas dural AVFs are more likely to occur in patients older than 40 years. In a study of 81 patients with spinal AVMs, the average age of patients with a symptomatic dural AVF was 49 years, whereas the average age for patients with symptomatic spinal cord AVM was 27 years. Almost two-thirds of patients with an intradural spinal AVM were younger than 25 years. Among intradural spinal AVMs, glomus-type AVMs are most common. Syndromes associated with spinal cord AVMs include hereditary hemorrhagic telangiectasia, neurofibromatosis type I, Klippel-Trénaunay-Weber syndrome, and Cobb syndrome.

Clinical Presentation and Pathophysiology

Children with spinal AVMs can present with acute, subacute, or chronic symptoms of back or radicular pain, sensorimotor deterioration, bowel or bladder dysfunction, and myelopathy. Most patients with a spinal AVM are diagnosed as young adults; however, patients often become symptomatic during childhood. Thus, a spinal AVM should be included in the differential diagnosis for any child who presents with slowly progressive or acute symptoms of radiculopathy or myelopathy.

Sudden focal pain with a neurologic deficit is thought to reflect an acute hemorrhage and is the most common presentation of a spinal AVM in children; 40% of patients younger than 14 years present with acute symptoms. Children may also present in a subacute fashion with recurrent events associated with a neurologic deficit from which there is some element of recovery; with time, however, there is a gradual deterioration in baseline neurologic function because of repeated hemorrhages and alterations of blood flow associated with the malformation.

Subarachnoid and/or intramedullary hemorrhage is associated with intradural AVMs and produces acute symptoms. In the series reported by Rosenblum and colleagues, 52% of patients with an intradural spinal AVM experienced a subarachnoid hemorrhage (SAH), whereas none of the patients with a dural AVF suffered SAH. SAH was the initial presenting symptom in 31% of patients with an intradural spinal AVM; among intradural AVMs, SAH most commonly occurred in patients with glomus malformations. Thus, for patients who present with nontraumatic SAH and who have a negative cerebral angiogram, obtaining cervical spine magnetic resonance imaging (MRI) is imperative for evaluation of a spinal cord vascular malformation. An acute onset of neurologic deficit is more often found in children with glomus lesions, reflecting the higher incidence of SAH in these patients. Less commonly, patients with glomus AVMs may present with progressive myelopathy due to mechanical compression or venous obstruction.

High-pressure, high-volume, turbulent blood flow through intradural spinal AVMs can also lead to an arterial steal phenomenon that diverts blood away from the spinal cord parenchyma and results in ischemia. Venous hypertension can also contribute to spinal cord ischemia, associated with progressive distention and engorgement of veins that drain intramedullary AVMs. Progressive weakness is the most common initial symptom in patients with juvenile AVMs and perimedullary AVFs. A sensory level may also be present in patients with spinal AVMs and reflects the spinal localization of the AVM nidus. High-flow AVMs may also be associated with a spinal bruit or heart failure.

Imaging

MRI is a sensitive modality for detecting spinal AVMs. Common findings include intradural signal voids reflecting dilated arteries or ectatic veins in or on the surface of the spinal cord, thrombosed veins, hematomyelia, spinal cord edema, syringomyelia, or spinal cord myelomalacia. Intramedullary flow voids that are present in spinal cord AVMs appear as areas of hypointensity within the center of the spinal cord on axial T1-weighted images and as areas of hyperintensity on T2-weighted images ( Fig. 1 ). In addition, ectatic perimedullary veins and prominent flow voids in the subarachnoid space around the spinal cord are often visualized.

Spinal angiography is the gold standard for diagnosing and defining the anatomy and angioarchitecture of spinal AVMs. The nidi of intradural AVMs are most commonly present within the spinal cord (80% of cases) but may less frequently be present on either the dorsal or ventral surface of the spinal cord. Intradural spinal AVMs are often fed by multiple arterial feeders, are high-flow lesions, and can have single or multiple aneurysms associated with the arterial feeders or draining veins.

Treatment and Outcomes

Given the risk of hemorrhage and the cumulative risk of progressive neurologic deficit, treatment of spinal AVMs in the pediatric population is indicated in cases in which the estimated morbidity from treatment is acceptably low. Neurologic outcome after treatment has been directly correlated to preoperative motor function. Other variables such as the age at symptom onset, degree of preoperative sensory loss, and rate of progression of neurologic deficit have not been shown to correlate with outcome.

Surgical removal of glomus AVMs may be performed with similar principles that guide resection of intracranial AVMs. Specifically, care is taken to identify and preserve draining veins until after the nidus is separated from the feeding vessels and surrounding parenchyma. Intraoperative angiography can be technically challenging to perform for spinal malformations but may have a role in carefully selected cases. Preoperative endovascular embolization may have a role in select cases. Arterial side embolization as a treatment of intramedullary spinal AVMs is usually palliative at best and is rarely recommended as a primary treatment. For endovascular treatment of spinal cord malformations, liquid embolic agents such as n -butylcyanoacrylate (NBCA) are preferred because they allow for easier filling of the distal nidus of a vascular malformation, they can be deposited in a more precise fashion, and they have a lower recanalization rate. Complications from endovascular therapy can arise from inadvertent occlusion of arterial feeders supplying the spinal cord or venous branches draining the spinal cord. Intraoperative monitoring of somatosensory evoked potentials and motor evoked potentials is routinely performed during both open microsurgical excision and endovascular embolization of spinal cord AVMs.

Spinal AVFs

Spinal AVFs, which lack an intervening nidus of vessels in the transition between arterial feeders and draining veins, can be further divided into extradural and intradural AVFs. An extradural AVF is a rare, abnormal communication between an extradural arterial branch that arises from a radicular artery and an epidural venous plexus. This can result in venous engorgement with subsequent mass effect on adjacent nerve roots and the spinal cord ( Figs. 2 and 3 ). On spinal angiography, slow retrograde venous drainage of the lesion can be demonstrated in association with enlarged medullary veins. Endovascular embolization is often an effective therapy.