INVITED REVIEW ARTICLE
Vascular Disease of the Spine Charles N. Munyon, MD* and David J. Hart, MDw
Abstract: Vascular insults to the spinal cord are substantially less common than their corresponding events in the brain; it has been estimated, for example, that spinal cord infarcts make up r1% of ischemic events in the central nervous system. Although the public health burden of spinal cord injury remains severe, the majority of this burden stems from traumatic rather than vascular events. Still, vascular injuries in the spine are common enough and their consequences devastating enough that a familiarity with the pathophysiology, diagnosis, and treatment of the more common etiologies is essential to any practitioner of the clinical neurosciences. In this educational review, we will briefly outline the normal development and anatomy of the spinal vasculature, then focus on specific mechanisms of vascular injury to the spine. In particular, we will examine spontaneous and iatrogenic ischemic insults and their associated clinical syndromes, and then review vascular neoplasms and malformations of the spine with attention to the various management strategies that currently exist for these complex lesions. Finally, we will briefly address the future areas for exploration, including investigative avenues for neuroprotection, as well as the possible influence of atherosclerotic disease on spinal degenerative disease and low back pain. Key Words: spine, vascular disease, spinal vascular malformation, spinal embryology and development, spinal radiology, spinal vascular anatomy
(The Neurologist 2015;19:121–127)
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he spine, like the brain, contains cells that are highly metabolically active and exquisitely sensitive to ischemia, requiring a robust and reliable vascular supply. The brain and spinal cord are also both vulnerable to similar types of vascular malformations, which can alter neurological function via hemorrhage, venous congestion, vascular steal, or even direct compression of neural elements. Additional similarities between cerebral and spinal vasculature include an anterior and posterior circulation with different associated clinical syndromes, as well as a severely limited capacity for regeneration in the wake of ischemic or hemorrhagic injury to the parenchyma. The spine, however, is substantially less prone to primary vascular injury (as opposed to secondary vascular injury from trauma) than the brain. The relative rarity of spinal vascular events is partly explained by the spine’s more direct and much more collateralized blood supply and its lower ratio of gray to white matter. This rarity means that the true incidence of spinal vascular disease is unknown and that its
From the *Department of Neurological Surgery, Temple University School of Medicine, Philadelphia, PA; and wDepartment of Neurological Surgery, University Hospitals Neurological Institute/Case Western Reserve University School of Medicine, Cleveland, OH. The authors declare no conflict of interest. Reprints: David J. Hart, MD, Department of Neurological Surgery, University Hospitals Neurological Institute/Case Western Reserve University School of Medicine, 11100 Euclid Avenue, Cleveland, OH 44106. E-mail: [email protected]. Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 1074-7931/15/1905-0121 DOI: 10.1097/NRL.0000000000000018
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pathophysiology and natural history remain incompletely understood. Still, more sophisticated magnetic resonance imaging (MRI) sequences, coupled with an improved safety profile and wider availability of spinal angiography, have begun to substantially improve both our understanding of the pathophysiology of spinal vascular disease and our ability to positively influence its course. The greatest obstacle to timely intervention remains the failure to include spinal vascular disease in the differential diagnosis, particularly in cases where symptoms such as severe chest pain draw the attention of the treating physician away from neurological findings. This review is therefore offered as a reminder of the many facets of spinal vascular disease, in the hopes of reinforcing awareness of these rare but potentially devastating processes.
EMBRYONIC DEVELOPMENT OF THE SPINAL VASCULATURE In the second and third weeks of embryonic life, 31 pairs of segmental vessels arise from the paired dorsal aortas and extend dorsally to the neural tube, following the path of the developing nerve roots. Each of these segmental vessels divides into a ventral and dorsal branch, which will establish a network of capillaries which become the paired ventral arterial tracts. During weeks 3 to 6, the ventral arterial tracts move medially, eventually fusing to form the anterior spinal artery (ASA). Concomitantly, a pair of dorsolateral anastomotic pial networks form which will become the posterior spinal arteries (PSAs).1,2 All 3 arteries supply a ramifying network of smaller vessels known as the perineural vascular plexus (PNVP); because the central nervous system (CNS) does not have vascular progenitor cells, the developing spinal cord must guide the ingression of the PNVP into the parenchyma. The pattern of ingression is highly stereotyped and depends on a network of glioneuronal progenitor cells called radial glia to guide the vascular endothelial cells to their targets. These endothelial cells, along with perivascular cells known as pericytes, will interact with neuronal and astrocytic progenitor cells to form the neurovascular units which compose the blood-CNS barrier.3 Although the specific molecular mediators of this process are poorly characterized, it is likely that derangements at this stage are responsible for some types of vascular malformation. As development progresses, most of the segmental vessels undergo regression to radicular vessels, supplying the nerve roots, dura, and vertebral bodies. This disconnects the anterior and PSAs from aortic supply at all but a few levels.1,2 Levels with persistent aortic supply will therefore be essential for flow augmentation in the postnatal spine, as discussed below.
NORMAL VASCULAR ANATOMY OF THE SPINE The mature spinal cord and its meninges are supplied by an anastomosing arterial network arising from 3 longitudinally oriented vessels: the paired PSAs and the solitary ASA. Although the PSAs have multiple interconnections with each other, they are not in direct communication with the ASA. This means that the spine, like the brain, has an essentially independent anterior and posterior www.theneurologist.org |
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circulation.2,4 All 3 longitudinal vessels, however, receive their rostral supply from the vertebral artery; the ASA is formed from the union of 1 vessel from each vertebral artery just caudal to the vertebrobasilar junction, whereas the PSAs arise more caudally from the ipsilateral vertebral or posterior inferior cerebellar artery. At their caudal ends, the spinal arteries receive additional blood supply from the median sacral artery. Between these termini, blood flow to the spinal arteries is augmented at variable intervals by those segmental vessels which underwent only partial regression during development. These vessels are known as anterior or posterior radiculomedullary arteries, depending on which circulation they augment. The number and configuration of the radiculomedullary arteries differs substantially among individuals. In the thoracic and lumbar spines, they are generally branches of the dorsospinal artery, but in the cervical spine, they can arise from branches of the vertebral, subclavian, or supreme intercostal artery. The largest of the radiculomedullary arteries is the “arteria radicularis anterior magna,” better known as the artery of Adamkiewicz, arises at the thoracolumbar junction and supplies the lumbar enlargement. Generally, the territories supplied by radiculomedullary arteries can be divided into the cervicothoracic, midthoracic, and thoracolumbar spines; the junctions between these territories are watershed areas particularly sensitive to systemic hypotension. Figure 1 shows a schematic of the arterial supply of the spinal cord.2 The parenchyma of the cord is also divided into vascular territories, based upon longitudinal supply. The ASA supplies the anterior horns and central gray matter of the cord via sulcocomissural or sulcal arteries which run in the anterior median fissure. Each sulcal artery supplies blood to only 1 side of the cord, with the subsequent segment alternating laterality. The ASA also sends out the arteriae vasocoronae, which course around the sides of the cord and penetrate the pia to supply the anterior and lateral funiculi. The PSAs also send out pial perforators, which supply the posterior funiculi as well as a variable portion of the posterior horns. Figure 2 shows a cross-sectional representation of the arterial supply of the spinal cord, with the approximate territories supplied by the ASA and PSAs marked out on the right.2 Venous drainage of the spinal cord occurs centrifugally along pathways similar to those taken by the arteries. The anterior median vein, however, drains both sides of the gray matter in contrast to the unilaterally alternating sulcocomissural arteries. There is also a posterior median vein, which drains out to the dorsal median sulcus. Larger veins on the surface of the spinal cord form a network of up to 6 channels, 6 ventral and 3 dorsal, which receive drainage from the anterior and posterior median veins as well as the smaller perforating veins draining the white matter. These intradural anastomotic networks send out ventral and dorsal radicular veins which then drain along the nerve roots into the internal vertebral venous plexi. These plexi are composed of the basivertebral, anterior and posterior longitudinal, and retrocorporeal veins, as well as the aforementioned radicular veins.5 They are valveless, tortuous channels which anastomose extensively with the intracranial venous sinuses rostrally and the deep pelvic and thoracic veins more caudally. The caudal anastomoses appear to be a frequent route for metastasis of pelvic malignancies to the spine, as first hypothesized by Batson in 1940.2,5,6
RADIOGRAPHIC EVALUATION OF SPINAL VASCULATURE Historically, diagnostic modalities for spinal vascular disease have lagged significantly behind those for cerebrovascular disease,
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FIGURE 1. Schematic diagram of the arterial supply to the spine (posterior view), showing typical locations for the anterior and posterior radiculomedullary arteries. The dashed lines represent divisions between the cervicothoracic, midthoracic, and thoracolumbar vascular territories, with the hatch marks showing regions of potential watershed ischemia. Reprinted with permission from Wells-Roth and Zonenshayn.2 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
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Vascular Disease of the Spine
timely manner. Technologic advancement cannot replace a thorough history and physical examination and the generation of an appropriate differential diagnosis to guide further investigations.
SPINAL CORD ISCHEMIA As a result of its rich anastomotic supply and higher ratio of white to gray matter, the spinal cord is substantially better protected than the brain from symptomatic ischemia. While reliable data on incidence are lacking, one large autopsy series showed only 9 spinal infarctions in 3784 patients (0.23%). Sandson and Friedman (1989) reported that 1.2% of the admissions for stroke at their institution were spinal ischemic events.18 It is widely accepted that spontaneous spinal cord infarctions make up less than 1% of ischemic insults to the CNS.4 FIGURE 2. Cross-sectional representation of the arterial supply of the spinal cord, including depiction of both an anterior and a posterior medullary artery. The right hand side shows the territories typically supplied by the sulcocommisural arteries (vertical stripes), the arteriae vasocoronae (horizontal stripes), and the posterior spinal arteries (diagonal stripes). Reprinted with permission from Wells-Roth and Zonenshayn.2 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
not only because of the relative rarity of spinal vascular insults, but also because of the technical challenges in imaging the vasculature of the spine. Although Moniz first described cerebral angiography in 1927, early neuroangiography relied on direct, or later catheterbased, injection of high concentrations of contrast into proximal, large-caliber vessels.7,8 Radiographic localization and characterization of vascular lesions in the spine was therefore essentially limited to looking for alterations in the bony spine through an xray or in the subarachnoid or epidural space via myelography. Distinction between vascular versus infectious or neoplastic etiologies had to be undertaken on clinical grounds, with many misdiagnoses not discovered until surgery or autopsy.4,8,9 Gradual refinements in technique and technology allowed Hook and Lidvall10 to demonstrate 2 cervical arteriovenous malformations (AVMs) by vertebral arteriography, and Djindjian et al (1962) to use aortography for gross diagnosis of spinal vascular lesions, but real progress would not begin until 1967, forty years after Moniz’s initial monograph. In that year, DiChiro, Doppman, and Ommaya first described selective catheterization of the radiculomedullary arteries, and all subsequent techniques in spinal angiography have been built upon their work.8,11 While catheter angiography remains the gold standard, in the last two decades MR angiography has become progressively better at delineating the anatomy of vascular malformations and detecting ischemic lesions with substantially better temporal and spatial sensitivity.12–15 For visualization of vascular lesions in relationship to the surrounding bony anatomy, CT angiography (CTA) has recently become a viable diagnostic modality. Utility had historically been limited by an inability to scan more than a few vertebral segments in the narrow window of peak arterial contrast concentration; this limitation appears to be mitigated, however, by the use of multidetector row helical CT (MDCT). MDCT allows for increased longitudinal resolution with shorter acquisition times, allowing for CTA of the neuraxis during peak contrast concentration.16 For precise localization, moreover, most modern fluoroscopy suites will allow for selective catheterization followed by CTA acquisition with intra-arterial contrast injection.16,17 None of these diagnostic modalities will be of any use, however, if they cannot be brought to bear in a focused and Copyright
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Anterior Spinal Artery Syndrome (ASAS)(Aka Beck’s Syndrome) Because the ASA is primarily responsible for blood supply to the anterior and lateral funiculi as well as the spinal gray matter, insults due to occlusion or hypoperfusion of the ASA lead to destruction of the corticospinal and spinothalamic tracts with relative preservation of the dorsal columns.19 ASAS is most frequently described in association with surgery for aortic aneurysm (discussed below), but can also present spontaneously.19–21 The spontaneous presentation generally involves sudden onset of severe pain in the affected dermatome, paralysis and loss of pain and temperature sensation below the lesion, and sparing of vibration sense and proprioception. Loss of bladder and bowel function is a frequent but not universal occurrence.19,21 In instances of lower cervical lesions, ASAS can be mistaken for myocardial infarction due to involvement of afferent visceral pathways from the cardiac plexus.22,23 Prognosis for recovery depends on age, longitudinal extent of signal abnormality on MRI, and evolution of proprioceptive deficits (thought to be due to cord edema causing dorsal column compression and ischemia).
Sulcal Artery (SA) Syndrome Because the sulcal (sulcocommissural) arteries alternate between supplying the left and right sides of the spine, infarction in the territory of a sulcal artery can lead to a cluster of findings relatively similar to a Brown-Sequard injury.24,25 Hemiparesis starts at the level of the lesion, with a loss of pain and temperature sensation starting roughly two dermatomes below the level of the infarct. As with ASA syndrome, there is dissociated sensory loss with preservation of dorsal column signals. Bowel and bladder effects are variable, but continence is usually preserved. SA syndrome is generally embolic in etiology, and has been described in association with dissecting thoracoabdominal aneurysms with mural thrombus,25 with iatrogenic injury from manipulation of the aorta (see below), and recently by Li et al (2010)24 in a case of vertebral artery dissection.
PSA Syndrome Posterior spinal artery syndrome (PSAS) is substantially less common than ASAS, likely due to both the dual, interconnected PSAs and the greater number of posterior radiculomedullary arteries.26 As would be expected, PSAS involves loss of proprioception and vibration sense below the level of the lesion; segmental sensory loss to all modalities can be seen with involvement of the dorsal horns, and involvement of the lateral corticospinal tracts can lead to paresis. Symptoms can be unilateral or bilateral.27 Reported causes of PSAS
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include syphilitic arteritis, cholesterol emboli, vertebral dissection, and iatrogenic injection or embolization.26–28 As with ASAS, prognosis appears to correlate with the extent of longitudinal involvement.
Fibrocartilaginous Emboli In addition to atheroemboli, thromboemboli from atrial fibrillation, paradoxical venous emboli, and mycotic emboli, the spine is susceptible to fibrocartilaginous emboli (FCE) from herniation of intervertebral disc material into the spinal vasculature.29 This rare syndrome is classically associated with axial loading to the spine with accompanying valsalva, but has also been described after minor trauma, particularly to the cervical spine. Onset of symptoms may be almost instantaneous, but can be delayed by hours or even days.4,30 Autopsy findings in patients with infarction of the cervical spine and respiratory compromise have confirmed the presence of cartilage within both the arteries and veins of the spinal cord, with a predilection for medium sized vessels.29,30 While clinical suspicion can often provide a putative diagnosis, confirmatory testing is only truly available at autopsy; FCE should therefore remain a diagnosis of exclusion, with an appropriate workup for transverse myelitis, multiple sclerosis, and other clinically appropriate syndromes remaining mandatory even in cases with classical mechanism and clinical picture.
Ischemia and Aortic Aneurysms As discussed above, the spinal arteries rely on blood from the aortic trunk to perfuse the length of the spine. The blood supply to the lumbar enlargement is particularly vulnerable to interruption if flow from the aorta is compromised, because the ASA typically becomes atretic in the lower thoracic spine, reconstituting distally with the input of the artery of Adamkiewicz.3,31 Atherosclerotic disease of the aorta can cause direct compromise of segmental vessels by atheroma formation, aneurismal dilation, or dissection causing occlusion. Thromboembolic events from mural thrombi have also been described in the literature. An imaging clue that may suggest an aortic etiology is the presence of vertebral body infarction. Vertebral body ischemia often becomes apparent on MRI before parenchymal infarction, and can help confirm infarction as the cause of new neurologic deficit.32 Cheng et al33, show that vertebral body infarction in the same vascular territory as the affected level correlates with aortic pathology in their series. Many cases of spinal infarction associated with aortic aneurysms are related to surgical or endovascular repair of the aneurysms. Paraplegia has been a known complication of aortic surgery since its inception, and multiple neuroprotective, neuromonitoring, and neuroimaging strategies have been devised to minimize the risks associated with thoracoabdominal aortic reconstruction and repair.34 The use of somatosensory evoked potentials (SSEPs), preoperative localization of the artery of Adamkiewicz, systemic hypothermia, and distal perfusion with shunting or cardiopulmonary bypass have all improved the safety profile of aortic aneurysm repair.34,35 Additional successful strategies include the preoperative drainage of CSF to reduce the intradural pressure and thus increase the perfusion pressure of the spine, as well as direct epidural cooling to obviate the need for systemic hypothermia. In addition to reducing the rate of iatrogenic injury, these strategies have helped to provide insight into potential neuroprotective measures against spontaneous vascular insult.35–37
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Other Iatrogenic Injuries There are several reports in the literature of spinal infarction complicating coronary artery bypass grafting, particularly with use of the intra-aortic balloon pump.38 While some of these injuries are likely due to systemic hypoperfusion, other causes include creation of atheroemboli due to plaque rupture by the pump, or even direct occlusion by the balloon of a segmental artery.39,40 Other thoracic procedures that require mobilization or manipulation of the aorta have also been associated with infarction, particularly transthoracic esophagectomy.41 Additionally, there are several reported cases of spinal infarction causing severe neurologic deficit or even death following epidural corticosteroid injection for the relief of radicular pain. While the mechanism of infarction is incompletely understood, the prominent hypothesis is that intra-arterial injection of steroids associated with a particulate vector may cause agglomeration and downstream occlusion of the vessel. This is borne out by the observation that some steroid formulations appear to carry significantly higher risk than others.42,43 Spinal infarction is also a known complication of spinal angiography, even in the absence of endovascular intervention.44 Finally, injury to the spinal vasculature is unsurprisingly a possible complication of spine surgery. While direct injury accounts for some of these cases, there are also many reports of ischemia related to deformity correction, particularly in larger scoliosis repair. While some of these events may be attributable in part to systemic hypotension, mechanical impingement on arterial supply or venous drainage appears to be the principal cause in many such events.45 SSEPs have therefore become indispensible to the safe correction of spinal deformity, optimally allowing for the rapid detection and reversal of mechanical disruption to the vascular supply.
VASCULAR MALFORMATIONS OF THE SPINE Spinal vascular malformations are diverse and challenging lesions requiring a multidisciplinary approach to diagnosis and treatment. Their presentation can range from incidental radiologic finding to sudden, catastrophic neurologic injury, and the spectrum of intervening clinical syndromes can mimic such diverse pathologies as spinal stenosis, multiple sclerosis, and even intracranial aneurismal rupture.46 Classification of these complex lesions has evolved substantially based on advances in histopathologic and radiographic evaluation as well as surgical and endovascular therapies. In 2002, Spetzler and colleagues proposed a revised classification system with three broad categories: vascular neoplasms, spinal aneurysms, and arteriovenous lesions. The latter category is further subdivided into arteriovenous malformations (AVMs) and arteriovenous fistulae (AVFs). Finally, AVMs are subdivided into extradural-intradural, intramedullary, and conus medullaris subtypes, whereas AVFs are subdivided into extradural, intradural dorsal, and intradural ventral groups.46,47 An alternate classification system was also proposed in 2002 by Lasjaunias and colleagues, reflecting the suspected etiology of a spinal AVM: under this system, type I AVMs are hereditary genetic lesions (typified by the macrofistula found in patients with Hereditary Hemorrhagic Telangectasia), type II AVMs are those found in genetic but nonhereditary syndromes such as the Cobb and Klippel-Trenaunay-Weber syndromes, and type III AVMs are sporadic/isolated findings.48 Please see the above-referenced publications for a comprehensive explanation of these 2 classification schemes. The multidisciplinary management of spinal vascular malformations is beyond the scope of this review and
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continues to evolve rapidly. Strategies for endovascular, surgical, and radiosurgical approaches to these lesions abound in the literature, and selection of treatment modality will depend on multiple factors including institutional practice patterns and the preferences of the treating physician.49–53 What is universally and unsurprisingly true is that the prognosis for these lesions improves when they are detected before the onset of major deficit. Prompt diagnosis is therefore of the utmost importance. Patients with even minor neurological deficit and stigmata of vascular syndromes such as Cobb or KlippelTrenaunay-Weber syndromes should be of particular concern; examination of the skin for cutaneous angiomata as well as examination of the extremities for limb hypertrophy is essential, particularly in younger patients presenting with signs of spinal cord dysfunction.50,54,55 While these syndromes are rare enough that no guidelines currently exist, early and thorough workup (including MRI of the brain and spine as well as spinal angiography), although expensive and invasive, is likely to prove cost effective, given the available therapeutic options and the potentially devastating consequences should a malformation go undetected. Another clinical picture that should be of concern is the gradual evolution of an apparent polyradiculopathy or myelopathy in a middle-aged male. Dural arteriovenous fistulae represent the most common vascular malformation of the spine and generally present with symptoms related to venous congestion or vascular steal rather than frank hemorrhage or infarction.51,52,56,57 Fluctuating intensity of symptoms should raise particular concern for a vascular etiology, as variations in regional hemodynamics can cause claudication of the spine. As with many other spinal vascular lesions, prognosis is principally dependent on the extent of neurological deficit at time of diagnosis; it has been estimated that the mean time between symptom onset and diagnosis in dural arteriovenous fistulae is around 10.5 months.58,59 Awareness of these lesions and maintenance of an appropriate index of suspicion is therefore paramount in the avoidance of permanent neurological injury.
Vascular Neoplasms of the Spine The 2 common vascular neoplasms intrinsic to the spinal cord are hemangioblastomas and cavernous angiomas (cavernomas). Both lesions can also be found in the brain (although hemangioblastomas are generally limited to the posterior fossa), and both can present with hemorrhage or local mass effect.60 Finally, both lesions can be found in sporadic and familial forms, with hemangioblastomas associated with Von Hippel-Lindau disorder and multiple cavernomas associated with mutations in CCM1, CCM2, and CCM3.60–62 Although these lesions are primarily located along the cord, they can also be found in the epidural space or along the nerve roots.60,61,63 Treatment for symptomatic lesions is generally surgical, although hemangioblastomas can be embolized preoperatively to minimize blood loss. Figures 3 and 4 show characteristic histologic presentations of cavernomas and hemangioblastomas, respectively.
Vascular Disease of the Spine
FIGURE 3. Cavernous malformation, with large, thin walled vascular spaces uninterrupted by normal parenchyma. Reprinted with permission from Edgar.59 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
challenge of markedly decreased sensitivity of MRI within the spinal canal. Nardone and colleagues recently reported the use of motor evoked potentials to confirm spinal pathology in patients with acute ischemic insults to the spine and normal MRIs.33,65 There are also multiple recent reports of improved MR diffusion-weighted imaging techniques which may improve the sensitivity for acute spinal infarct.66 The development of improved imaging and ancillary testing will be critical to any organized effort to study the timely treatment of spinal ischemia. In the interim, iatrogenic ischemic insults to the spine, although unfortunate, provide another possible means to explore treatment options for spinal ischemia. Lee and colleagues report a recent case of spinal cord ischemia after embolization of a high cervical lesion; the patient was treated with thrombolytics, hypothermia, and hyperbaric oxygen, with improvement from hemiplegia (grade 0/5) at onset to grade 4/5 by the end of the treatment.64 Although it is impossible to generalize from this anecdotal report, it seems likely that
FUTURE AREAS OF INVESTIGATION Intervention in Acute Ischemia of the Spine As with diagnostic modalities, in the realm of therapeutic intervention, spinal vascular disease lags significantly behind its cerebrovascular counterpart. Although thrombolytic therapies would appear to have a logical role in the management of acute spinal stroke, there are substantial barriers to initiation of thrombolysis within the therapeutic window.4,32,64 In addition to the decreased clinical awareness of spinal stroke, there is the Copyright
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FIGURE 4. Hemangioblastoma, with pale, eosinophilic stromal cells surrounding sinusoidal vascular channels. Reprinted with permission from Edgar.59 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
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aggressive intervention by neurocritical care teams may have a substantive impact on the outcome in cases of spinal ischemia.
Atherosclerotic Disease and the Spinal Column Low back pain is one of the leading causes of disability in the industrialized world; although not nearly as potentially devastating in individual terms as the entities discussed above, its overall financial impact is tremendous. Observational studies have shown good correlation between atherosclerotic burden and degenerative disease of the spine, as well as between cardiovascular risk factors and evidence of low back pain. In particular, atherosclerotic stenosis of the lumbar arteries was strongly correlated with degenerative disease of the spine in 2 cadaveric studies.67–69 Given the already extraordinary burden that atherosclerotic disease inflicts upon the developed world, further prospective studies into a possible link to back pain as well as efficacy of risk factor management in alleviating back pain seem warranted.
CONCLUSIONS Vascular disease of the spine remains poorly understood and often devastating. Although substantial progress has been made since the latter half of the 20th century, it remains a fertile and potentially very rewarding area of research. Even with recent advances in diagnostic imaging and ancillary testing, the most important tool for prompt identification of a vascular insult to the spine remains a high index of suspicion. We hope that this review, although not comprehensive, will help to reinforce awareness of the myriad presentations and pathophysiological mechanisms underlying spinal vascular disease. REFERENCES 1. Kaplan KM, Spivak JM, Bendo JA. Embryology of the spine and associated congenital abnormalities. Spine J. 2005;5:564–576. 2. Wells-Roth D, Zonenshayn M. Vascular anatomy of the spine. Oper Tech Neurosurg. 2003;6:116–121. 3. Bautch VL, James JM. Neurovascular development: the beginning of a beautiful friendship. Cell Adh Migr. 2009;3:199–204. 4. Geldmacher DS, Bowen BC. Spinal cord vascular disease. Neurology in Clinical Practice. Philadelphia PA: Butterworth Heinemann; 2004:1313–1322. 5. Chaynes P, Verdie´ JC, Moscovici J, et al. Microsurgical anatomy of the internal vertebral venous plexuses. Surg Radiol Anat. 1997;20:47–51. 6. Batson OV. The function of the vertebral veins and their role in the spread of metastases. Ann Surg. 1940;112:138–49. 7. Doby T. Cerebral angiography and Egas Moniz. AJR. 1992; 159:364. 8. Akopov S, Schievink W. History of spinal cord vascular malformations and their treatment. Semin Cerebrovasc Dis Stroke. 2002;2:178–185. 9. Lahanis S, Vlahos L, Gouliamos A, et al. Arteriovenous malformation of the spinal cord mimicking a tumour. Neuroradiology. 1993;35:598–599. 10. Hook O, Lidvall H. Arteriovenous aneurysms of the spinal cord: a report of two cases investigated by vertebral angiography. J Neurosurg. 1958;15:84–91. 11. Di Chiro G, Doppman J, Ommaya AK. Selective arteriography of arteriovenous aneurysms of spinal cord. Radiology. 1967;88: 1065–1077. 12. Mascalchi M, Quillici N, Ferrito G, et al. Identification of the feeding arteries of spinal vascular lesions via phase-contrast MR angiography with three-dimensional acquisition and phase display. AJNR Am J Neuroradiol. 1997;18:351–358. 13. Binkert CA, Kollias SS, Valvanis A. Spinal cord vascular disease: characterization with fast three-dimensional contrast-enhanced MR angiography. AJNR Am J Neuroradiol. 1999;20:1785–1793.
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14. Bowen BC. MR angiography of spinal vascular disease: what about normal vessels? AJNR. 1999;20:1773–1774. 15. Friedman DP, Flanders AE, Tartaglino LM. Vascular neoplasms and malformations, lschemia, and hemorrhage affecting the spinal cord: MR imaging findings. AJR. 1994;62:685–692. 16. Terae S, Kudo K, Asano T, et al. CT angiography with multidetector-row helical CT in spinal arteriovenous malformation. J Clin Imaging. 2004;28:23–27. 17. Hasegawa M, Fukisawa H, Kawamura T, et al. The efficacy of CT arteriography for spinal arteriovenous fistula surgery: technical note. Neuroradiology. 1999;41:915–919. 18. Sandson TA, Friedman JH. Spinal cord infarction—report of 8 cases and review of the literature. Medicine. 1989;68:281–292. 19. Lee YS, Teh HS. Anterior spinal artery infarction: MR imaging and clinical findings. Eur J Radiol Extra. 2006;60:49–50. 20. Zuber WF, Gaspar MR, Rothschild PD. The anterior spinal artery syndrome, a complication of abdominal aortic surgery: report of five cases and review of the literature. Ann Surg. 1970;172: 909–915. 21. Sohal AS, Sundaram M, Maliewa M, et al. Anterior spinal artery syndrome in a girl with down syndrome: case report and literature review. J Spinal Cord Med. 2009;32:349–354. 22. Combarros O, Vadillo A, Gutie´rrez-Pe´rez R, et al. Cervical spinal cord infarction simulating myocardial infarction. Eur Neurol. 2002;47:185–186. 23. Cheshire WP Jr. Spinal cord infarction mimicking angina pectoris. Mayo Clin Proc. 2000;75:1197–1199. 24. Li Y, Jenny D, Bemporad JA, et al. Sulcal artery syndrome after vertebral artery dissection. J Stroke Cerebrovasc Dis. 2010;19:333–335. 25. Harlander M, Bajrovic´ FF, Blinc A, et al. Monoparesis due to spinal cord infarction associated with thoracoabdominal aneurysm. Heart Vessels. 2008;23:359–362. 26. Mascalchi M, Cosottini M, Ferrito G, et al. Posterior spinal artery infarct. AJNR Am J Neuroradiol. 1998;19:361–363. 27. Gutowski NJ, Murphy RP, Beale DJ. Unilateral upper cervical posterior spinal artery syndrome following sneezing. J Neurol Neurosurg Psychiatry. 1992;55:841–843. 28. Bergqvist CA, Goldberg HI, Thorarensen O, et al. Posterior cervical spinal cord infarction following vertebral artery dissection. Neurology. 1997;48:1112–1115. 29. Han JJ, Massagi TL, Jaffe KM. Fibrocartilaginous embolism—an uncommon cause of spinal cord infarction: a case report and review of the literature. Arch Phys Med Rehabil. 2004;85: 153–157. 30. Piao YS, Lu DH, Su YY, et al. Anterior spinal cord infarction caused by fibrocartilaginous embolism. Neuropathology. 2009; 29:172–175. 31. Biglioli P, Roberto M, Cannata A, et al. Upper and lower spinal cord blood supply: the continuity of the anterior spinal artery and the relevance of the lumbar arteries. J Thorac Cardiovasc Surg. 2004;127:1188–1192. 32. Faig J, Busse O, Salbeck R. Vertebral body infarction as a confirmatory sign of spinal cord ischemic stroke: report of three cases and review of the literature. Stroke. 1998;29:239–243. 33. Cheng MY, Lyu RK, Chang YJ, et al. Concomitant spinal cord and vertebral body infarction is highly associated with aortic pathology: a clinical and magnetic resonance imaging study. J Neurol. 2009;256:1418–1426. 34. Ogino H, Sasaki H, Minatoya K, et al. Combined use of adamkiewicz artery demonstration and motor-evoked potentials in descending and thoracoabdominal repair. Ann Thorac Surg. 2006;82:592–596. 35. Ogino H. Is hypothermia a reliable adjunct for spinal cord protection in descending and thoracoabdominal aortic repair with regional or systemic cooling? Gen Thorac Cardiovasc Surg. 2010;58:220–222. 36. Tabayashi K, Saiki Y, Kokubo H, et al. Protection from postischemic spinal cord injury by perfusion cooling of the epidural space during most or all of a descending thoracic or thoracoabdominal aneurysm repair. Gen Thorac Cardiovasc Surg. 2010;58:228–234.
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37. Griepp RB, Griepp EB. Spinal cord perfusion and protection during descending thoracic and thoracoabdominal aortic surgery: The Collateral Network Concept. Ann Thorac Surg. 2007; 83:S865–S869. 38. Spielmann PM, Campanella C. Spinal infarction following coronary artery bypass grafting. Interact Cardiovasc Thorac Surg. 2004;3:606–607. 39. Orr E, McKittrick J, D’Agostino R, et al. Paraplegia following intra-aortic balloon support. Report of a case. J Cardiovasc Surg (Torino). 1989;30:1013–1014. 40. Stavridis GT, O’Riordan JB. Paraplegia as a result of intra-aortic balloon counterpulsation. J Cardiovasc Surg (Torino). 1995; 36:177–179. 41. Zantl N, Stein HJ, Bru¨cher BL, et al. Ischemic spinal cord syndrome after transthoracic esophagectomy: two cases of a rare neurologic complication. Dis Esophagus. 2000;13:328–332. 42. Wybier M. Transforaminal epidural corticosteroid injections and spinal cord infarction. Joint Bone Spine. 2008;75:523–525. 43. Kennedy DJ, Dreyfuss P, Aprill CN, et al. Paraplegia following image-guided transforaminal lumbar spine epidural steroid injection: two case reports. Pain Med. 2009;10:1389–1389. 44. Moseley IF, Tress BM. Extravasation of contrast medium during spinal angiography: a cause of paraplegia. Neuroradiology. 1977; 13:55–57. 45. Inamasu J, Guiot BH. Vascular injury and complication in neurosurgical spine surgery. Acta Neurochir (Wien). 2006;148: 375–387. 46. Da Costa L, Dehdashti AR, TerBrugge KG. Spinal cord vascular shunts: spinal cord vascular malformations and dural arteriovenous fistulas. Neurosurg Focus. 2009;26:E6. 47. Spetzler RF, Detwiler PW, Riina HA, et al. Modified classification of spinal cord vascular lesions. J Neurosurg (Spine 2). 2002;96:145–156. 48. Rodesch G, Hurth M, Alvarez H, et al. Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Biceˆtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery. 2002;51:375–380. 49. Jehan R, Vinuela F. Vascular anatomy, pathophysiology, and classification of vascular malformations of the spinal cord. Semin Cerebrovasc Dis Stroke. 2002;2:186–200. 50. Johnson WD, Petrie MM. Variety of spinal vascular pathology seen in adult Cobb syndrome—report of 2 cases. J Neurosurg Spine. 2009;10:430–435. 51. Sivakumar W, Zada G, Yashar P, et al. Endovascular management of spinal dural arteriovenous fistulas. Neurosurg Focus. 2009; 26:E15. 52. Krings T, Thron AK, Geibprasert S, et al. Endovascular management of spinal vascular malformations. Neurosurg Rev. 2010; 33:1–9. 53. Clarke MJ, Patrick TA, White J, et al. Spinal extradural arteriovenous malformations with parenchymal drainage: venous drainage variability and implications in clinical manifestations. Neurosurg Focus. 2009;26:E5.
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54. Espinosa PS, Pettigrew LC, Berger JR. Hereditary hemorrhagic telangectasia and spinal cord infarct: case report with a review of the neurological complications of HHT. Clin Neurol Neurosurg. 2008;110:484–491. 55. Benhaiem-Sigaux N, Zerah M, Gherardi R, et al. A retromedullary arteriovenous fistula associated with the Klippel-TrenaunayWeber syndrome. Acta Neuropathol (Bed). 1985;66:318–324. 56. Jellema K, Tjissen CC, van Gijn J. Spinal dural arteriovenous fistulas: a congestive myelopathy that initially mimics a peripheral nerve disorder. Brain. 2006;129:3150–3164. 57. Kai Y, Hamada J, Morioka M, et al. Correlation between magnetic resonance images and draining patterns in dural arteriovenous fistulas with leptomeningeal venous drainage. Acta Neurochir (Wien). 2000;142:413–419. 58. Carabine LP Jr, Halbach W, Ng PP, et al. Vascular myelopathies—vascular malformations of the spinal cord: presentation and endovascular surgical management. Semin Neurol. 2002;22:123–131. 59. Krings T, Lasjaunuas P, Reinges M, et al. Spinal vascular malformations: diagnostic and therapeutic management. Clin Neuroradiol. 2006;16:217–227. 60. Edgar M. Pathology of vascular lesions affecting the spine and spinal cord. Oper Techn Neurosurg. 2003;6:122–124. 61. Goyal A, Singh AK, Gupta V, et al. Spinal epidural cavernous haemangioma: a case report and review of literature. Spinal Cord. 2002;40:200–202. 62. Roessler K, Dietrich W, Haberler C, et al. Multiple spinal “miliary” hemangioblastomas in von Hippel-Lindau (vHL) disease without cerebellar involvement. Neurosurg Rev. 1999;22:130–134. 63. Escott EJ, Kleinschmidt-DeMasters BK, Brega K, et al. Proximal nerve root spinal hemangioblastomas: presentation of three cases, MR appearance, and literature review. Surg Neurol. 2004;61: 262–273. 64. Lee K, Strozyk D, Rahman C, et al. Acute spinal cord ischemia: treatment with intravenous and intra-arterial thrombolysis, hyperbaric oxygen and hypothermia. Cerebrovasc Dis. 2010;29:95–98. 65. Nardone R, Bergmann J, Kronbichler M, et al. Magnetic resonance imaging and motor-evoked potentials in spinal cord infarction: report of two cases. Neurol Sci. 2010;31:505–509. 66. Marcel C, Kremer S, Jantroux J, et al. Diffusion-weighted imaging in noncompressive myelopathies: a 33-patient prospective study. J Neurol. 2010;257:1438–1445. 67. Ahn N, Ahn U, Nailamshetty L, et al. Lumbar spine pathology and multiple atherosclerotic risk factors: a 53-year prospective study of 1,337 patients. Proceedings of the NASS 16th Annual Meeting. Spine J. 2002;2:34S. 68. Kauppila Ll. Atherosclerosis and disc degeneration/low-back pain—a systematic review. Eur J Vasc Endovasc Surg. 2009;37: 661–670. 69. Turgut AT, So¨nmez I, Cakıt BD, et al. Pineal gland calcification, lumbar intervertebral disc degeneration and abdominal aorta calcifying atherosclerosis correlate in low back pain subjects: a cross-sectional observational CT study. Pathophysiology. 2008; 15:31–39.
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127
Vascular Disease of the Spine Charles N. Munyon, MD* and David J. Hart, MDw
Abstract: Vascular insults to the spinal cord are substantially less common than their corresponding events in the brain; it has been estimated, for example, that spinal cord infarcts make up r1% of ischemic events in the central nervous system. Although the public health burden of spinal cord injury remains severe, the majority of this burden stems from traumatic rather than vascular events. Still, vascular injuries in the spine are common enough and their consequences devastating enough that a familiarity with the pathophysiology, diagnosis, and treatment of the more common etiologies is essential to any practitioner of the clinical neurosciences. In this educational review, we will briefly outline the normal development and anatomy of the spinal vasculature, then focus on specific mechanisms of vascular injury to the spine. In particular, we will examine spontaneous and iatrogenic ischemic insults and their associated clinical syndromes, and then review vascular neoplasms and malformations of the spine with attention to the various management strategies that currently exist for these complex lesions. Finally, we will briefly address the future areas for exploration, including investigative avenues for neuroprotection, as well as the possible influence of atherosclerotic disease on spinal degenerative disease and low back pain. Key Words: spine, vascular disease, spinal vascular malformation, spinal embryology and development, spinal radiology, spinal vascular anatomy
(The Neurologist 2015;19:121–127)
T
he spine, like the brain, contains cells that are highly metabolically active and exquisitely sensitive to ischemia, requiring a robust and reliable vascular supply. The brain and spinal cord are also both vulnerable to similar types of vascular malformations, which can alter neurological function via hemorrhage, venous congestion, vascular steal, or even direct compression of neural elements. Additional similarities between cerebral and spinal vasculature include an anterior and posterior circulation with different associated clinical syndromes, as well as a severely limited capacity for regeneration in the wake of ischemic or hemorrhagic injury to the parenchyma. The spine, however, is substantially less prone to primary vascular injury (as opposed to secondary vascular injury from trauma) than the brain. The relative rarity of spinal vascular events is partly explained by the spine’s more direct and much more collateralized blood supply and its lower ratio of gray to white matter. This rarity means that the true incidence of spinal vascular disease is unknown and that its
From the *Department of Neurological Surgery, Temple University School of Medicine, Philadelphia, PA; and wDepartment of Neurological Surgery, University Hospitals Neurological Institute/Case Western Reserve University School of Medicine, Cleveland, OH. The authors declare no conflict of interest. Reprints: David J. Hart, MD, Department of Neurological Surgery, University Hospitals Neurological Institute/Case Western Reserve University School of Medicine, 11100 Euclid Avenue, Cleveland, OH 44106. E-mail: [email protected]. Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 1074-7931/15/1905-0121 DOI: 10.1097/NRL.0000000000000018
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pathophysiology and natural history remain incompletely understood. Still, more sophisticated magnetic resonance imaging (MRI) sequences, coupled with an improved safety profile and wider availability of spinal angiography, have begun to substantially improve both our understanding of the pathophysiology of spinal vascular disease and our ability to positively influence its course. The greatest obstacle to timely intervention remains the failure to include spinal vascular disease in the differential diagnosis, particularly in cases where symptoms such as severe chest pain draw the attention of the treating physician away from neurological findings. This review is therefore offered as a reminder of the many facets of spinal vascular disease, in the hopes of reinforcing awareness of these rare but potentially devastating processes.
EMBRYONIC DEVELOPMENT OF THE SPINAL VASCULATURE In the second and third weeks of embryonic life, 31 pairs of segmental vessels arise from the paired dorsal aortas and extend dorsally to the neural tube, following the path of the developing nerve roots. Each of these segmental vessels divides into a ventral and dorsal branch, which will establish a network of capillaries which become the paired ventral arterial tracts. During weeks 3 to 6, the ventral arterial tracts move medially, eventually fusing to form the anterior spinal artery (ASA). Concomitantly, a pair of dorsolateral anastomotic pial networks form which will become the posterior spinal arteries (PSAs).1,2 All 3 arteries supply a ramifying network of smaller vessels known as the perineural vascular plexus (PNVP); because the central nervous system (CNS) does not have vascular progenitor cells, the developing spinal cord must guide the ingression of the PNVP into the parenchyma. The pattern of ingression is highly stereotyped and depends on a network of glioneuronal progenitor cells called radial glia to guide the vascular endothelial cells to their targets. These endothelial cells, along with perivascular cells known as pericytes, will interact with neuronal and astrocytic progenitor cells to form the neurovascular units which compose the blood-CNS barrier.3 Although the specific molecular mediators of this process are poorly characterized, it is likely that derangements at this stage are responsible for some types of vascular malformation. As development progresses, most of the segmental vessels undergo regression to radicular vessels, supplying the nerve roots, dura, and vertebral bodies. This disconnects the anterior and PSAs from aortic supply at all but a few levels.1,2 Levels with persistent aortic supply will therefore be essential for flow augmentation in the postnatal spine, as discussed below.
NORMAL VASCULAR ANATOMY OF THE SPINE The mature spinal cord and its meninges are supplied by an anastomosing arterial network arising from 3 longitudinally oriented vessels: the paired PSAs and the solitary ASA. Although the PSAs have multiple interconnections with each other, they are not in direct communication with the ASA. This means that the spine, like the brain, has an essentially independent anterior and posterior www.theneurologist.org |
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circulation.2,4 All 3 longitudinal vessels, however, receive their rostral supply from the vertebral artery; the ASA is formed from the union of 1 vessel from each vertebral artery just caudal to the vertebrobasilar junction, whereas the PSAs arise more caudally from the ipsilateral vertebral or posterior inferior cerebellar artery. At their caudal ends, the spinal arteries receive additional blood supply from the median sacral artery. Between these termini, blood flow to the spinal arteries is augmented at variable intervals by those segmental vessels which underwent only partial regression during development. These vessels are known as anterior or posterior radiculomedullary arteries, depending on which circulation they augment. The number and configuration of the radiculomedullary arteries differs substantially among individuals. In the thoracic and lumbar spines, they are generally branches of the dorsospinal artery, but in the cervical spine, they can arise from branches of the vertebral, subclavian, or supreme intercostal artery. The largest of the radiculomedullary arteries is the “arteria radicularis anterior magna,” better known as the artery of Adamkiewicz, arises at the thoracolumbar junction and supplies the lumbar enlargement. Generally, the territories supplied by radiculomedullary arteries can be divided into the cervicothoracic, midthoracic, and thoracolumbar spines; the junctions between these territories are watershed areas particularly sensitive to systemic hypotension. Figure 1 shows a schematic of the arterial supply of the spinal cord.2 The parenchyma of the cord is also divided into vascular territories, based upon longitudinal supply. The ASA supplies the anterior horns and central gray matter of the cord via sulcocomissural or sulcal arteries which run in the anterior median fissure. Each sulcal artery supplies blood to only 1 side of the cord, with the subsequent segment alternating laterality. The ASA also sends out the arteriae vasocoronae, which course around the sides of the cord and penetrate the pia to supply the anterior and lateral funiculi. The PSAs also send out pial perforators, which supply the posterior funiculi as well as a variable portion of the posterior horns. Figure 2 shows a cross-sectional representation of the arterial supply of the spinal cord, with the approximate territories supplied by the ASA and PSAs marked out on the right.2 Venous drainage of the spinal cord occurs centrifugally along pathways similar to those taken by the arteries. The anterior median vein, however, drains both sides of the gray matter in contrast to the unilaterally alternating sulcocomissural arteries. There is also a posterior median vein, which drains out to the dorsal median sulcus. Larger veins on the surface of the spinal cord form a network of up to 6 channels, 6 ventral and 3 dorsal, which receive drainage from the anterior and posterior median veins as well as the smaller perforating veins draining the white matter. These intradural anastomotic networks send out ventral and dorsal radicular veins which then drain along the nerve roots into the internal vertebral venous plexi. These plexi are composed of the basivertebral, anterior and posterior longitudinal, and retrocorporeal veins, as well as the aforementioned radicular veins.5 They are valveless, tortuous channels which anastomose extensively with the intracranial venous sinuses rostrally and the deep pelvic and thoracic veins more caudally. The caudal anastomoses appear to be a frequent route for metastasis of pelvic malignancies to the spine, as first hypothesized by Batson in 1940.2,5,6
RADIOGRAPHIC EVALUATION OF SPINAL VASCULATURE Historically, diagnostic modalities for spinal vascular disease have lagged significantly behind those for cerebrovascular disease,
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FIGURE 1. Schematic diagram of the arterial supply to the spine (posterior view), showing typical locations for the anterior and posterior radiculomedullary arteries. The dashed lines represent divisions between the cervicothoracic, midthoracic, and thoracolumbar vascular territories, with the hatch marks showing regions of potential watershed ischemia. Reprinted with permission from Wells-Roth and Zonenshayn.2 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
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Vascular Disease of the Spine
timely manner. Technologic advancement cannot replace a thorough history and physical examination and the generation of an appropriate differential diagnosis to guide further investigations.
SPINAL CORD ISCHEMIA As a result of its rich anastomotic supply and higher ratio of white to gray matter, the spinal cord is substantially better protected than the brain from symptomatic ischemia. While reliable data on incidence are lacking, one large autopsy series showed only 9 spinal infarctions in 3784 patients (0.23%). Sandson and Friedman (1989) reported that 1.2% of the admissions for stroke at their institution were spinal ischemic events.18 It is widely accepted that spontaneous spinal cord infarctions make up less than 1% of ischemic insults to the CNS.4 FIGURE 2. Cross-sectional representation of the arterial supply of the spinal cord, including depiction of both an anterior and a posterior medullary artery. The right hand side shows the territories typically supplied by the sulcocommisural arteries (vertical stripes), the arteriae vasocoronae (horizontal stripes), and the posterior spinal arteries (diagonal stripes). Reprinted with permission from Wells-Roth and Zonenshayn.2 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
not only because of the relative rarity of spinal vascular insults, but also because of the technical challenges in imaging the vasculature of the spine. Although Moniz first described cerebral angiography in 1927, early neuroangiography relied on direct, or later catheterbased, injection of high concentrations of contrast into proximal, large-caliber vessels.7,8 Radiographic localization and characterization of vascular lesions in the spine was therefore essentially limited to looking for alterations in the bony spine through an xray or in the subarachnoid or epidural space via myelography. Distinction between vascular versus infectious or neoplastic etiologies had to be undertaken on clinical grounds, with many misdiagnoses not discovered until surgery or autopsy.4,8,9 Gradual refinements in technique and technology allowed Hook and Lidvall10 to demonstrate 2 cervical arteriovenous malformations (AVMs) by vertebral arteriography, and Djindjian et al (1962) to use aortography for gross diagnosis of spinal vascular lesions, but real progress would not begin until 1967, forty years after Moniz’s initial monograph. In that year, DiChiro, Doppman, and Ommaya first described selective catheterization of the radiculomedullary arteries, and all subsequent techniques in spinal angiography have been built upon their work.8,11 While catheter angiography remains the gold standard, in the last two decades MR angiography has become progressively better at delineating the anatomy of vascular malformations and detecting ischemic lesions with substantially better temporal and spatial sensitivity.12–15 For visualization of vascular lesions in relationship to the surrounding bony anatomy, CT angiography (CTA) has recently become a viable diagnostic modality. Utility had historically been limited by an inability to scan more than a few vertebral segments in the narrow window of peak arterial contrast concentration; this limitation appears to be mitigated, however, by the use of multidetector row helical CT (MDCT). MDCT allows for increased longitudinal resolution with shorter acquisition times, allowing for CTA of the neuraxis during peak contrast concentration.16 For precise localization, moreover, most modern fluoroscopy suites will allow for selective catheterization followed by CTA acquisition with intra-arterial contrast injection.16,17 None of these diagnostic modalities will be of any use, however, if they cannot be brought to bear in a focused and Copyright
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Anterior Spinal Artery Syndrome (ASAS)(Aka Beck’s Syndrome) Because the ASA is primarily responsible for blood supply to the anterior and lateral funiculi as well as the spinal gray matter, insults due to occlusion or hypoperfusion of the ASA lead to destruction of the corticospinal and spinothalamic tracts with relative preservation of the dorsal columns.19 ASAS is most frequently described in association with surgery for aortic aneurysm (discussed below), but can also present spontaneously.19–21 The spontaneous presentation generally involves sudden onset of severe pain in the affected dermatome, paralysis and loss of pain and temperature sensation below the lesion, and sparing of vibration sense and proprioception. Loss of bladder and bowel function is a frequent but not universal occurrence.19,21 In instances of lower cervical lesions, ASAS can be mistaken for myocardial infarction due to involvement of afferent visceral pathways from the cardiac plexus.22,23 Prognosis for recovery depends on age, longitudinal extent of signal abnormality on MRI, and evolution of proprioceptive deficits (thought to be due to cord edema causing dorsal column compression and ischemia).
Sulcal Artery (SA) Syndrome Because the sulcal (sulcocommissural) arteries alternate between supplying the left and right sides of the spine, infarction in the territory of a sulcal artery can lead to a cluster of findings relatively similar to a Brown-Sequard injury.24,25 Hemiparesis starts at the level of the lesion, with a loss of pain and temperature sensation starting roughly two dermatomes below the level of the infarct. As with ASA syndrome, there is dissociated sensory loss with preservation of dorsal column signals. Bowel and bladder effects are variable, but continence is usually preserved. SA syndrome is generally embolic in etiology, and has been described in association with dissecting thoracoabdominal aneurysms with mural thrombus,25 with iatrogenic injury from manipulation of the aorta (see below), and recently by Li et al (2010)24 in a case of vertebral artery dissection.
PSA Syndrome Posterior spinal artery syndrome (PSAS) is substantially less common than ASAS, likely due to both the dual, interconnected PSAs and the greater number of posterior radiculomedullary arteries.26 As would be expected, PSAS involves loss of proprioception and vibration sense below the level of the lesion; segmental sensory loss to all modalities can be seen with involvement of the dorsal horns, and involvement of the lateral corticospinal tracts can lead to paresis. Symptoms can be unilateral or bilateral.27 Reported causes of PSAS
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include syphilitic arteritis, cholesterol emboli, vertebral dissection, and iatrogenic injection or embolization.26–28 As with ASAS, prognosis appears to correlate with the extent of longitudinal involvement.
Fibrocartilaginous Emboli In addition to atheroemboli, thromboemboli from atrial fibrillation, paradoxical venous emboli, and mycotic emboli, the spine is susceptible to fibrocartilaginous emboli (FCE) from herniation of intervertebral disc material into the spinal vasculature.29 This rare syndrome is classically associated with axial loading to the spine with accompanying valsalva, but has also been described after minor trauma, particularly to the cervical spine. Onset of symptoms may be almost instantaneous, but can be delayed by hours or even days.4,30 Autopsy findings in patients with infarction of the cervical spine and respiratory compromise have confirmed the presence of cartilage within both the arteries and veins of the spinal cord, with a predilection for medium sized vessels.29,30 While clinical suspicion can often provide a putative diagnosis, confirmatory testing is only truly available at autopsy; FCE should therefore remain a diagnosis of exclusion, with an appropriate workup for transverse myelitis, multiple sclerosis, and other clinically appropriate syndromes remaining mandatory even in cases with classical mechanism and clinical picture.
Ischemia and Aortic Aneurysms As discussed above, the spinal arteries rely on blood from the aortic trunk to perfuse the length of the spine. The blood supply to the lumbar enlargement is particularly vulnerable to interruption if flow from the aorta is compromised, because the ASA typically becomes atretic in the lower thoracic spine, reconstituting distally with the input of the artery of Adamkiewicz.3,31 Atherosclerotic disease of the aorta can cause direct compromise of segmental vessels by atheroma formation, aneurismal dilation, or dissection causing occlusion. Thromboembolic events from mural thrombi have also been described in the literature. An imaging clue that may suggest an aortic etiology is the presence of vertebral body infarction. Vertebral body ischemia often becomes apparent on MRI before parenchymal infarction, and can help confirm infarction as the cause of new neurologic deficit.32 Cheng et al33, show that vertebral body infarction in the same vascular territory as the affected level correlates with aortic pathology in their series. Many cases of spinal infarction associated with aortic aneurysms are related to surgical or endovascular repair of the aneurysms. Paraplegia has been a known complication of aortic surgery since its inception, and multiple neuroprotective, neuromonitoring, and neuroimaging strategies have been devised to minimize the risks associated with thoracoabdominal aortic reconstruction and repair.34 The use of somatosensory evoked potentials (SSEPs), preoperative localization of the artery of Adamkiewicz, systemic hypothermia, and distal perfusion with shunting or cardiopulmonary bypass have all improved the safety profile of aortic aneurysm repair.34,35 Additional successful strategies include the preoperative drainage of CSF to reduce the intradural pressure and thus increase the perfusion pressure of the spine, as well as direct epidural cooling to obviate the need for systemic hypothermia. In addition to reducing the rate of iatrogenic injury, these strategies have helped to provide insight into potential neuroprotective measures against spontaneous vascular insult.35–37
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Other Iatrogenic Injuries There are several reports in the literature of spinal infarction complicating coronary artery bypass grafting, particularly with use of the intra-aortic balloon pump.38 While some of these injuries are likely due to systemic hypoperfusion, other causes include creation of atheroemboli due to plaque rupture by the pump, or even direct occlusion by the balloon of a segmental artery.39,40 Other thoracic procedures that require mobilization or manipulation of the aorta have also been associated with infarction, particularly transthoracic esophagectomy.41 Additionally, there are several reported cases of spinal infarction causing severe neurologic deficit or even death following epidural corticosteroid injection for the relief of radicular pain. While the mechanism of infarction is incompletely understood, the prominent hypothesis is that intra-arterial injection of steroids associated with a particulate vector may cause agglomeration and downstream occlusion of the vessel. This is borne out by the observation that some steroid formulations appear to carry significantly higher risk than others.42,43 Spinal infarction is also a known complication of spinal angiography, even in the absence of endovascular intervention.44 Finally, injury to the spinal vasculature is unsurprisingly a possible complication of spine surgery. While direct injury accounts for some of these cases, there are also many reports of ischemia related to deformity correction, particularly in larger scoliosis repair. While some of these events may be attributable in part to systemic hypotension, mechanical impingement on arterial supply or venous drainage appears to be the principal cause in many such events.45 SSEPs have therefore become indispensible to the safe correction of spinal deformity, optimally allowing for the rapid detection and reversal of mechanical disruption to the vascular supply.
VASCULAR MALFORMATIONS OF THE SPINE Spinal vascular malformations are diverse and challenging lesions requiring a multidisciplinary approach to diagnosis and treatment. Their presentation can range from incidental radiologic finding to sudden, catastrophic neurologic injury, and the spectrum of intervening clinical syndromes can mimic such diverse pathologies as spinal stenosis, multiple sclerosis, and even intracranial aneurismal rupture.46 Classification of these complex lesions has evolved substantially based on advances in histopathologic and radiographic evaluation as well as surgical and endovascular therapies. In 2002, Spetzler and colleagues proposed a revised classification system with three broad categories: vascular neoplasms, spinal aneurysms, and arteriovenous lesions. The latter category is further subdivided into arteriovenous malformations (AVMs) and arteriovenous fistulae (AVFs). Finally, AVMs are subdivided into extradural-intradural, intramedullary, and conus medullaris subtypes, whereas AVFs are subdivided into extradural, intradural dorsal, and intradural ventral groups.46,47 An alternate classification system was also proposed in 2002 by Lasjaunias and colleagues, reflecting the suspected etiology of a spinal AVM: under this system, type I AVMs are hereditary genetic lesions (typified by the macrofistula found in patients with Hereditary Hemorrhagic Telangectasia), type II AVMs are those found in genetic but nonhereditary syndromes such as the Cobb and Klippel-Trenaunay-Weber syndromes, and type III AVMs are sporadic/isolated findings.48 Please see the above-referenced publications for a comprehensive explanation of these 2 classification schemes. The multidisciplinary management of spinal vascular malformations is beyond the scope of this review and
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continues to evolve rapidly. Strategies for endovascular, surgical, and radiosurgical approaches to these lesions abound in the literature, and selection of treatment modality will depend on multiple factors including institutional practice patterns and the preferences of the treating physician.49–53 What is universally and unsurprisingly true is that the prognosis for these lesions improves when they are detected before the onset of major deficit. Prompt diagnosis is therefore of the utmost importance. Patients with even minor neurological deficit and stigmata of vascular syndromes such as Cobb or KlippelTrenaunay-Weber syndromes should be of particular concern; examination of the skin for cutaneous angiomata as well as examination of the extremities for limb hypertrophy is essential, particularly in younger patients presenting with signs of spinal cord dysfunction.50,54,55 While these syndromes are rare enough that no guidelines currently exist, early and thorough workup (including MRI of the brain and spine as well as spinal angiography), although expensive and invasive, is likely to prove cost effective, given the available therapeutic options and the potentially devastating consequences should a malformation go undetected. Another clinical picture that should be of concern is the gradual evolution of an apparent polyradiculopathy or myelopathy in a middle-aged male. Dural arteriovenous fistulae represent the most common vascular malformation of the spine and generally present with symptoms related to venous congestion or vascular steal rather than frank hemorrhage or infarction.51,52,56,57 Fluctuating intensity of symptoms should raise particular concern for a vascular etiology, as variations in regional hemodynamics can cause claudication of the spine. As with many other spinal vascular lesions, prognosis is principally dependent on the extent of neurological deficit at time of diagnosis; it has been estimated that the mean time between symptom onset and diagnosis in dural arteriovenous fistulae is around 10.5 months.58,59 Awareness of these lesions and maintenance of an appropriate index of suspicion is therefore paramount in the avoidance of permanent neurological injury.
Vascular Neoplasms of the Spine The 2 common vascular neoplasms intrinsic to the spinal cord are hemangioblastomas and cavernous angiomas (cavernomas). Both lesions can also be found in the brain (although hemangioblastomas are generally limited to the posterior fossa), and both can present with hemorrhage or local mass effect.60 Finally, both lesions can be found in sporadic and familial forms, with hemangioblastomas associated with Von Hippel-Lindau disorder and multiple cavernomas associated with mutations in CCM1, CCM2, and CCM3.60–62 Although these lesions are primarily located along the cord, they can also be found in the epidural space or along the nerve roots.60,61,63 Treatment for symptomatic lesions is generally surgical, although hemangioblastomas can be embolized preoperatively to minimize blood loss. Figures 3 and 4 show characteristic histologic presentations of cavernomas and hemangioblastomas, respectively.
Vascular Disease of the Spine
FIGURE 3. Cavernous malformation, with large, thin walled vascular spaces uninterrupted by normal parenchyma. Reprinted with permission from Edgar.59 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
challenge of markedly decreased sensitivity of MRI within the spinal canal. Nardone and colleagues recently reported the use of motor evoked potentials to confirm spinal pathology in patients with acute ischemic insults to the spine and normal MRIs.33,65 There are also multiple recent reports of improved MR diffusion-weighted imaging techniques which may improve the sensitivity for acute spinal infarct.66 The development of improved imaging and ancillary testing will be critical to any organized effort to study the timely treatment of spinal ischemia. In the interim, iatrogenic ischemic insults to the spine, although unfortunate, provide another possible means to explore treatment options for spinal ischemia. Lee and colleagues report a recent case of spinal cord ischemia after embolization of a high cervical lesion; the patient was treated with thrombolytics, hypothermia, and hyperbaric oxygen, with improvement from hemiplegia (grade 0/5) at onset to grade 4/5 by the end of the treatment.64 Although it is impossible to generalize from this anecdotal report, it seems likely that
FUTURE AREAS OF INVESTIGATION Intervention in Acute Ischemia of the Spine As with diagnostic modalities, in the realm of therapeutic intervention, spinal vascular disease lags significantly behind its cerebrovascular counterpart. Although thrombolytic therapies would appear to have a logical role in the management of acute spinal stroke, there are substantial barriers to initiation of thrombolysis within the therapeutic window.4,32,64 In addition to the decreased clinical awareness of spinal stroke, there is the Copyright
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FIGURE 4. Hemangioblastoma, with pale, eosinophilic stromal cells surrounding sinusoidal vascular channels. Reprinted with permission from Edgar.59 Copyright [Elsevier], [Cleveland, OH]. All permission requests for this image should be made to the copyright holder.
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aggressive intervention by neurocritical care teams may have a substantive impact on the outcome in cases of spinal ischemia.
Atherosclerotic Disease and the Spinal Column Low back pain is one of the leading causes of disability in the industrialized world; although not nearly as potentially devastating in individual terms as the entities discussed above, its overall financial impact is tremendous. Observational studies have shown good correlation between atherosclerotic burden and degenerative disease of the spine, as well as between cardiovascular risk factors and evidence of low back pain. In particular, atherosclerotic stenosis of the lumbar arteries was strongly correlated with degenerative disease of the spine in 2 cadaveric studies.67–69 Given the already extraordinary burden that atherosclerotic disease inflicts upon the developed world, further prospective studies into a possible link to back pain as well as efficacy of risk factor management in alleviating back pain seem warranted.
CONCLUSIONS Vascular disease of the spine remains poorly understood and often devastating. Although substantial progress has been made since the latter half of the 20th century, it remains a fertile and potentially very rewarding area of research. Even with recent advances in diagnostic imaging and ancillary testing, the most important tool for prompt identification of a vascular insult to the spine remains a high index of suspicion. We hope that this review, although not comprehensive, will help to reinforce awareness of the myriad presentations and pathophysiological mechanisms underlying spinal vascular disease. REFERENCES 1. Kaplan KM, Spivak JM, Bendo JA. Embryology of the spine and associated congenital abnormalities. Spine J. 2005;5:564–576. 2. Wells-Roth D, Zonenshayn M. Vascular anatomy of the spine. Oper Tech Neurosurg. 2003;6:116–121. 3. Bautch VL, James JM. Neurovascular development: the beginning of a beautiful friendship. Cell Adh Migr. 2009;3:199–204. 4. Geldmacher DS, Bowen BC. Spinal cord vascular disease. Neurology in Clinical Practice. Philadelphia PA: Butterworth Heinemann; 2004:1313–1322. 5. Chaynes P, Verdie´ JC, Moscovici J, et al. Microsurgical anatomy of the internal vertebral venous plexuses. Surg Radiol Anat. 1997;20:47–51. 6. Batson OV. The function of the vertebral veins and their role in the spread of metastases. Ann Surg. 1940;112:138–49. 7. Doby T. Cerebral angiography and Egas Moniz. AJR. 1992; 159:364. 8. Akopov S, Schievink W. History of spinal cord vascular malformations and their treatment. Semin Cerebrovasc Dis Stroke. 2002;2:178–185. 9. Lahanis S, Vlahos L, Gouliamos A, et al. Arteriovenous malformation of the spinal cord mimicking a tumour. Neuroradiology. 1993;35:598–599. 10. Hook O, Lidvall H. Arteriovenous aneurysms of the spinal cord: a report of two cases investigated by vertebral angiography. J Neurosurg. 1958;15:84–91. 11. Di Chiro G, Doppman J, Ommaya AK. Selective arteriography of arteriovenous aneurysms of spinal cord. Radiology. 1967;88: 1065–1077. 12. Mascalchi M, Quillici N, Ferrito G, et al. Identification of the feeding arteries of spinal vascular lesions via phase-contrast MR angiography with three-dimensional acquisition and phase display. AJNR Am J Neuroradiol. 1997;18:351–358. 13. Binkert CA, Kollias SS, Valvanis A. Spinal cord vascular disease: characterization with fast three-dimensional contrast-enhanced MR angiography. AJNR Am J Neuroradiol. 1999;20:1785–1793.
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14. Bowen BC. MR angiography of spinal vascular disease: what about normal vessels? AJNR. 1999;20:1773–1774. 15. Friedman DP, Flanders AE, Tartaglino LM. Vascular neoplasms and malformations, lschemia, and hemorrhage affecting the spinal cord: MR imaging findings. AJR. 1994;62:685–692. 16. Terae S, Kudo K, Asano T, et al. CT angiography with multidetector-row helical CT in spinal arteriovenous malformation. J Clin Imaging. 2004;28:23–27. 17. Hasegawa M, Fukisawa H, Kawamura T, et al. The efficacy of CT arteriography for spinal arteriovenous fistula surgery: technical note. Neuroradiology. 1999;41:915–919. 18. Sandson TA, Friedman JH. Spinal cord infarction—report of 8 cases and review of the literature. Medicine. 1989;68:281–292. 19. Lee YS, Teh HS. Anterior spinal artery infarction: MR imaging and clinical findings. Eur J Radiol Extra. 2006;60:49–50. 20. Zuber WF, Gaspar MR, Rothschild PD. The anterior spinal artery syndrome, a complication of abdominal aortic surgery: report of five cases and review of the literature. Ann Surg. 1970;172: 909–915. 21. Sohal AS, Sundaram M, Maliewa M, et al. Anterior spinal artery syndrome in a girl with down syndrome: case report and literature review. J Spinal Cord Med. 2009;32:349–354. 22. Combarros O, Vadillo A, Gutie´rrez-Pe´rez R, et al. Cervical spinal cord infarction simulating myocardial infarction. Eur Neurol. 2002;47:185–186. 23. Cheshire WP Jr. Spinal cord infarction mimicking angina pectoris. Mayo Clin Proc. 2000;75:1197–1199. 24. Li Y, Jenny D, Bemporad JA, et al. Sulcal artery syndrome after vertebral artery dissection. J Stroke Cerebrovasc Dis. 2010;19:333–335. 25. Harlander M, Bajrovic´ FF, Blinc A, et al. Monoparesis due to spinal cord infarction associated with thoracoabdominal aneurysm. Heart Vessels. 2008;23:359–362. 26. Mascalchi M, Cosottini M, Ferrito G, et al. Posterior spinal artery infarct. AJNR Am J Neuroradiol. 1998;19:361–363. 27. Gutowski NJ, Murphy RP, Beale DJ. Unilateral upper cervical posterior spinal artery syndrome following sneezing. J Neurol Neurosurg Psychiatry. 1992;55:841–843. 28. Bergqvist CA, Goldberg HI, Thorarensen O, et al. Posterior cervical spinal cord infarction following vertebral artery dissection. Neurology. 1997;48:1112–1115. 29. Han JJ, Massagi TL, Jaffe KM. Fibrocartilaginous embolism—an uncommon cause of spinal cord infarction: a case report and review of the literature. Arch Phys Med Rehabil. 2004;85: 153–157. 30. Piao YS, Lu DH, Su YY, et al. Anterior spinal cord infarction caused by fibrocartilaginous embolism. Neuropathology. 2009; 29:172–175. 31. Biglioli P, Roberto M, Cannata A, et al. Upper and lower spinal cord blood supply: the continuity of the anterior spinal artery and the relevance of the lumbar arteries. J Thorac Cardiovasc Surg. 2004;127:1188–1192. 32. Faig J, Busse O, Salbeck R. Vertebral body infarction as a confirmatory sign of spinal cord ischemic stroke: report of three cases and review of the literature. Stroke. 1998;29:239–243. 33. Cheng MY, Lyu RK, Chang YJ, et al. Concomitant spinal cord and vertebral body infarction is highly associated with aortic pathology: a clinical and magnetic resonance imaging study. J Neurol. 2009;256:1418–1426. 34. Ogino H, Sasaki H, Minatoya K, et al. Combined use of adamkiewicz artery demonstration and motor-evoked potentials in descending and thoracoabdominal repair. Ann Thorac Surg. 2006;82:592–596. 35. Ogino H. Is hypothermia a reliable adjunct for spinal cord protection in descending and thoracoabdominal aortic repair with regional or systemic cooling? Gen Thorac Cardiovasc Surg. 2010;58:220–222. 36. Tabayashi K, Saiki Y, Kokubo H, et al. Protection from postischemic spinal cord injury by perfusion cooling of the epidural space during most or all of a descending thoracic or thoracoabdominal aneurysm repair. Gen Thorac Cardiovasc Surg. 2010;58:228–234.
Copyright
r
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37. Griepp RB, Griepp EB. Spinal cord perfusion and protection during descending thoracic and thoracoabdominal aortic surgery: The Collateral Network Concept. Ann Thorac Surg. 2007; 83:S865–S869. 38. Spielmann PM, Campanella C. Spinal infarction following coronary artery bypass grafting. Interact Cardiovasc Thorac Surg. 2004;3:606–607. 39. Orr E, McKittrick J, D’Agostino R, et al. Paraplegia following intra-aortic balloon support. Report of a case. J Cardiovasc Surg (Torino). 1989;30:1013–1014. 40. Stavridis GT, O’Riordan JB. Paraplegia as a result of intra-aortic balloon counterpulsation. J Cardiovasc Surg (Torino). 1995; 36:177–179. 41. Zantl N, Stein HJ, Bru¨cher BL, et al. Ischemic spinal cord syndrome after transthoracic esophagectomy: two cases of a rare neurologic complication. Dis Esophagus. 2000;13:328–332. 42. Wybier M. Transforaminal epidural corticosteroid injections and spinal cord infarction. Joint Bone Spine. 2008;75:523–525. 43. Kennedy DJ, Dreyfuss P, Aprill CN, et al. Paraplegia following image-guided transforaminal lumbar spine epidural steroid injection: two case reports. Pain Med. 2009;10:1389–1389. 44. Moseley IF, Tress BM. Extravasation of contrast medium during spinal angiography: a cause of paraplegia. Neuroradiology. 1977; 13:55–57. 45. Inamasu J, Guiot BH. Vascular injury and complication in neurosurgical spine surgery. Acta Neurochir (Wien). 2006;148: 375–387. 46. Da Costa L, Dehdashti AR, TerBrugge KG. Spinal cord vascular shunts: spinal cord vascular malformations and dural arteriovenous fistulas. Neurosurg Focus. 2009;26:E6. 47. Spetzler RF, Detwiler PW, Riina HA, et al. Modified classification of spinal cord vascular lesions. J Neurosurg (Spine 2). 2002;96:145–156. 48. Rodesch G, Hurth M, Alvarez H, et al. Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Biceˆtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery. 2002;51:375–380. 49. Jehan R, Vinuela F. Vascular anatomy, pathophysiology, and classification of vascular malformations of the spinal cord. Semin Cerebrovasc Dis Stroke. 2002;2:186–200. 50. Johnson WD, Petrie MM. Variety of spinal vascular pathology seen in adult Cobb syndrome—report of 2 cases. J Neurosurg Spine. 2009;10:430–435. 51. Sivakumar W, Zada G, Yashar P, et al. Endovascular management of spinal dural arteriovenous fistulas. Neurosurg Focus. 2009; 26:E15. 52. Krings T, Thron AK, Geibprasert S, et al. Endovascular management of spinal vascular malformations. Neurosurg Rev. 2010; 33:1–9. 53. Clarke MJ, Patrick TA, White J, et al. Spinal extradural arteriovenous malformations with parenchymal drainage: venous drainage variability and implications in clinical manifestations. Neurosurg Focus. 2009;26:E5.
Copyright
r
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54. Espinosa PS, Pettigrew LC, Berger JR. Hereditary hemorrhagic telangectasia and spinal cord infarct: case report with a review of the neurological complications of HHT. Clin Neurol Neurosurg. 2008;110:484–491. 55. Benhaiem-Sigaux N, Zerah M, Gherardi R, et al. A retromedullary arteriovenous fistula associated with the Klippel-TrenaunayWeber syndrome. Acta Neuropathol (Bed). 1985;66:318–324. 56. Jellema K, Tjissen CC, van Gijn J. Spinal dural arteriovenous fistulas: a congestive myelopathy that initially mimics a peripheral nerve disorder. Brain. 2006;129:3150–3164. 57. Kai Y, Hamada J, Morioka M, et al. Correlation between magnetic resonance images and draining patterns in dural arteriovenous fistulas with leptomeningeal venous drainage. Acta Neurochir (Wien). 2000;142:413–419. 58. Carabine LP Jr, Halbach W, Ng PP, et al. Vascular myelopathies—vascular malformations of the spinal cord: presentation and endovascular surgical management. Semin Neurol. 2002;22:123–131. 59. Krings T, Lasjaunuas P, Reinges M, et al. Spinal vascular malformations: diagnostic and therapeutic management. Clin Neuroradiol. 2006;16:217–227. 60. Edgar M. Pathology of vascular lesions affecting the spine and spinal cord. Oper Techn Neurosurg. 2003;6:122–124. 61. Goyal A, Singh AK, Gupta V, et al. Spinal epidural cavernous haemangioma: a case report and review of literature. Spinal Cord. 2002;40:200–202. 62. Roessler K, Dietrich W, Haberler C, et al. Multiple spinal “miliary” hemangioblastomas in von Hippel-Lindau (vHL) disease without cerebellar involvement. Neurosurg Rev. 1999;22:130–134. 63. Escott EJ, Kleinschmidt-DeMasters BK, Brega K, et al. Proximal nerve root spinal hemangioblastomas: presentation of three cases, MR appearance, and literature review. Surg Neurol. 2004;61: 262–273. 64. Lee K, Strozyk D, Rahman C, et al. Acute spinal cord ischemia: treatment with intravenous and intra-arterial thrombolysis, hyperbaric oxygen and hypothermia. Cerebrovasc Dis. 2010;29:95–98. 65. Nardone R, Bergmann J, Kronbichler M, et al. Magnetic resonance imaging and motor-evoked potentials in spinal cord infarction: report of two cases. Neurol Sci. 2010;31:505–509. 66. Marcel C, Kremer S, Jantroux J, et al. Diffusion-weighted imaging in noncompressive myelopathies: a 33-patient prospective study. J Neurol. 2010;257:1438–1445. 67. Ahn N, Ahn U, Nailamshetty L, et al. Lumbar spine pathology and multiple atherosclerotic risk factors: a 53-year prospective study of 1,337 patients. Proceedings of the NASS 16th Annual Meeting. Spine J. 2002;2:34S. 68. Kauppila Ll. Atherosclerosis and disc degeneration/low-back pain—a systematic review. Eur J Vasc Endovasc Surg. 2009;37: 661–670. 69. Turgut AT, So¨nmez I, Cakıt BD, et al. Pineal gland calcification, lumbar intervertebral disc degeneration and abdominal aorta calcifying atherosclerosis correlate in low back pain subjects: a cross-sectional observational CT study. Pathophysiology. 2008; 15:31–39.
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