A Classification Proposal for Spinal Vascular Lesions

Spinal vascular lesions are rare and intriguing clinical entities. Over the past several decades, the combined expertise of our specialty has allowed important headway to be made in the diagnosis and management of these lesions. A new classification system is proposed that stratifies these lesions into neoplastic vs arteriovenous lesions. Neoplastic lesions comprised hemangioblastomas (true 3 cell line lesions) and cavernous malformations (single cell line lesions)1; arteriovenous lesions include fistulas and arteriovenous malformations. Among the neoplastic lesions, hemangioblastomas can be sporadic or occur as part of familial syndromes. Their removal is usually relatively straightforward, and surgery is tailored to their location within the spinal cord. Cavernous malformations may also occur sporadically or familially, and they can appear throughout the spinal cord. Surgical resection generally involves 1 of 3 approaches: a midline myelotomy, entry through the substantia gelatinosa or dorsal root entry zone, or a lateral approach between the nerve roots at the level of the dentate ligaments. Spinal cord arteriovenous lesions may be either fistulas or malformations.1 Fistulas may be either extradural or intradural, and intradural lesions may be either dorsal or ventral. Similarly, spinal cord arteriovenous malformations are either extradural or intradural, with intradural lesions further classified as either central or lateral intramedullary lesions or conus lesions (Figure 1). We classify these latter categories below and offer accumulated pearls for their surgical management.FIGURE 1.: A, Extradural-intradural arteriovenous malformation. B, Central intramedullary arteriovenous malformation. C, Lateral intramedullary arteriovenous malformation. D, Conus arteriovenous malformation. Used with permission from Journal of Neurosurgery Publishing Group, from Spetzler RF, Detwiler PW, Riina HA, and Porter RW: Modified classification of spinal cord vascular lesions. J Neurosurg: Spine. 2002 Mar;96(2):145-56.ARTERIOVENOUS FISTULAS Extradural arteriovenous fistulas are now routinely treated by endovascular neurosurgeons, although their intradural counterparts remain amenable to open microsurgical resection. These intradural fistulas are either dorsal or ventral and have distinct pathophysiological origins. Dorsal lesions are the most important because they are the most common. They frequently present with myelopathy caused by venous hypertension or, more rarely, hemorrhage. Angiography of these lesions shows extremely slow flow with frequent feeders from the dorsal radicular arteries. These lesions can be classified into single-feeder lesions and 2-feeder lesions. The extradural nexus of arteries and veins was formerly believed to be the pathological entity and surgical target. Actually, it is the intradural connection between the artery and vein that must be appropriately ligated to relieve venous hypertension. Importantly, the fistula may be located distal to the arteriovenous nexus, and care must be taken during preoperative imaging and surgical resection to identify it. Despite the slow flow through these lesions, venous hypertension develops because of venous outflow obstruction in a pathophysiological process similar to that which occurs in the brain. Measurement of intravascular pressure within these lesions demonstrates the profound manometric burden on the draining veins. In a study involving 22 patients with such lesions treated at our institution, the mean (SD) pressures within open lesions in the feeding artery and draining vein were found to be approximately identical: 44 (17) and 44 (16) mm Hg, respectively.2,3 Typical epidural venous pressure in such lesions was 11 (4) mm Hg, demonstrating the deviation from normal venous pressure in the draining vein and the increased gradient between these 2 venous systems, which helps to locate the pathological venous outflow obstruction. After closure of these lesions, the mean (SD) pressure in the feeding artery increased to 82 (12) mm Hg and the mean (SD) pressure in the draining vein decreased to 23 (9) mm Hg. This venous hypertension is dramatically illustrated by the case of a wheelchair-bound man in his early 30s who presented with progressive spastic paraparesis and whose physical examination findings included marked hyperreflexia and paraparesis. Imaging revealed profoundly dilated vessels throughout the cervical spinal cord (Figure 2A), and angiography in the capillary phase showed venous engorgement (Figure 2B). Attempted endovascular therapy failed. Surgical intervention with a clip placed at the arteriovenous fistulous point succeeded, and the patient recovered to ambulatory status.FIGURE 2.: A, Preoperative magnetic resonance imaging of the cervical spine showing vessel engorgement. B, Angiography in the capillary phase showing marked venous engorgement. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.Ventral intradural arteriovenous fistulas were first reported by Roberto Heros in 1986.4 Their pathophysiology differs from that of dorsal lesions in that compression from venous varices and hypoperfusion from steal phenomenon, in addition to venous hypertension, are frequently responsible for myelopathy. Ventral intradural arteriovenous fistulas may also present with subarachnoid hemorrhage from the rupture of venous aneurysms. Angiography findings indicate that these are fast-flow lesions fed by the anterior spinal artery. Their subtypes are denoted according to size, with type A lesions being small, type B lesions being intermediate in size, and type C lesions being the largest. A case example of an adolescent girl who presented with multiple episodes of transient paraplegia and was found to have a thoracic ventral intradural fistula with marked venous engorgement demonstrates that the placement of a single surgical clip at the fistulous point is enough to completely obliterate the lesion and result in negative angiogram findings and postoperative clinical improvement. ARTERIOVENOUS MALFORMATIONS Arteriovenous malformations comprise 4 discrete subtypes: extradural-intradural lesions, which respect no anatomic boundaries; central intramedullary lesions, which are fed exclusively by the anterior spinal artery; lateral intramedullary lesions, which may be partially intramedullary and partially extramedullary; and conus arteriovenous malformations (Figure 1). Extradural-intradural arteriovenous malformations are quite rare. These lesions were previously referred to as juvenile, metameric, or type III arteriovenous malformations. They respect no anatomic or tissue boundaries within the spine; angiography shows that they are high-flow lesions fed by multiple feeders. They may present with pain or progressive myelopathy stemming from direct compression, steal phenomenon, or frank hemorrhage. Surgical resection may incorporate direct injection of endovascular occlusive agents after open surgical exposure, as in the case of a child with progressive myelopathy and a large lesion resected at our institution. Preoperative endovascular embolization may assist by orienting the surgeon relative to certain angiographic landmarks during surgery. Conus arteriovenous malformations are intriguing lesions that were first defined in 2002.1,5 They are anatomically confined to the conus, where there is a connection between the anterior and posterior spinal arteries. These connections may form a “basket” around the conus, which confers a unique angioarchitecture to these lesions and gives them characteristics of both fistulas and true malformations. They are fed by multiple feeders that are both ventral and dorsal and both perimedullary and intramedullary, located within the pia and arachnoid layers. Because of their unique location, these lesions may present with myelopathy, radiculopathy, and subarachnoid hemorrhage. The case presentation of a woman in her 30s who presented with subarachnoid hemorrhage found on computed tomography of the head is representative; negative intracranial angiography findings in this case demonstrate the importance of obtaining spinal imaging in such cases. Magnetic resonance imaging of the thoracolumbar spine revealed dilated vessels in the region of the conus, and spinal angiography findings confirmed the diagnosis of a conus arteriovenous malformation (Figure 3). Successful surgical resection involves meticulous identification and preservation of normal conus vessels.FIGURE 3.: A, Preoperative and B, postoperative angiograms obtained before and after resection of a conus arteriovenous malformation. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.Conus lesions are thus unique lesions with a distinct architecture, anatomic location, and clinical presentation that frequently involve lower nerve root symptoms. They frequently require a combined endovascular and open approach with preoperative embolization. Our experience shows that favorable cure rates can be achieved, with 14 of 16 (88%) patients in our institution's series achieving cure.5 At the last follow-up, 7 (43%) of these patients were at their preoperative neurological baseline and 7 (43%) achieved neurological improvement. Among 14 cured patients, all ambulatory patients remained ambulatory postoperatively and 75% of nonambulatory patients became ambulatory after surgery.5 The final and most intriguing category of spinal vascular lesions is intramedullary arteriovenous malformations. These lesions are categorized into central lesions fed by the anterior spinal artery and lateral lesions. The lateral subtypes are far more common than anterior lesions. The pial resection technique is frequently used during resection and involves preserving the pial interface between the malformation and the spinal cord and transecting involved vessels at this interface such that the intramedullary component is left in situ. This maneuver elicits less bleeding in the spinal cord than would occur if a similar maneuver were performed in the brain. Twenty such intramedullary arteriovenous malformations treated at our institution were cured, despite partial resection that left the intramedullary component untouched. There was no uncontrolled bleeding from ligating vessels traversing across this pial margin. It may thus be the case that the arteriovenous architecture of intramedullary arteriovenous malformations in the spinal cord is distinct from that in the brain.6 CONCLUSION We present a simple classification of vascular lesions of the spinal cord. Fistulas are distinct from arteriovenous malformations, and microsurgical resection is appropriate in all cases. Preoperative endovascular embolization is of great benefit in treating intramedullary arteriovenous malformations, and standalone endovascular embolization may be curative for fistulas. Recognizing that partial resection without complete obliteration can be curative in patients with intramedullary arteriovenous malformations is crucial and may lead to improved clinical outcomes.