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Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine Vascular anatomy of the spinal cord Alejandro Santillan, Veronica Nacarino, Edward Greenberg, Howard A Riina, Y Pierre Gobin, Athos Patsalides Division of Interventional Neuroradiology, Department of Neurological Surgery, New York Presbyterian Hospital, Weill Cornell Medical Center, New York, New York, USA Correspondence to Dr A Santillan, 525 E 68th St, Division of Interventional Neuroradiology, Department of Neurological Surgery, New York Presbyterian Hospital/Weill Cornell Medical Center, New York, NY 10065, USA; [email protected] Received 5 March 2011 Accepted 7 March 2011 Published Online First 2 May 2011 ABSTRACT In this article, a detailed description of the normal arterial supply and venous drainage of the spinal cord is provided, and the role of catheter angiography and MR angiography in depicting the vascular anatomy of the spinal cord is discussed. INTRODUCTION Improvements in endovascular and microsurgical techniques have resulted in more effective treatments for many vascular lesions of the spinal cord. A thorough knowledge of the vascular anatomy of the spine and spinal cord is a prerequisite for understanding the pathophysiology of spinal vascular lesions and is necessary for planning safe surgical and endovascular interventions. This knowledge is also important for the treatment of thoracoabdominal aortic aneurysms and for percutaneous spinal procedures. Even though digital subtraction angiography remains the gold standard for spinal vascular imaging, MR angiography (MRA) has gained widespread acceptance in the detection of large vascular structures, such as the artery of Adamkiewicz, and has demonstrated promise in detecting vascular abnormalities of the spinal cord. ARTERIAL BLOOD SUPPLY Arterial supply to the spinal column and spinal cord Segmental arteries The arterial supply to the spinal column, paraspinal muscles, dura, nerve roots and spinal cord derives from the segmental arteries. The segmental arteries in the thoracic and upper lumbar spine originate in pairs from the posterior aspect of the descending aorta adjacent to the spinal column. The segmental arteries in the thoracic spine include the posterior intercostal arteries (nine pairs) and subcostal arteries (one pair); there are typically four pairs of lumbar segmental arteries arising from the descending aorta, corresponding to the top four lumbar vertebrae (figure 1). Above T3, several segmental arteries may arise from a common origin, termed the supreme intercostal artery. The supreme intercostal artery, also called superior intercostal artery, is commonly a branch of the costocervical trunk or the aortic arch, and rarely from the vertebral artery. It provides supply to the upper thoracic region. Below T3, there is typically one pair of segmental arteries at each level which supply all of the dorsolateral tissues of a single metamere, except the spinal cord. There are extensive anastomoses between segmental arteries with important connections both above and below a given level, as well as contralaterally. The J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 descending aorta is situated to the left of the spinal column in the upper thoracic levels and descends anteromedially to become just slightly left of midline by the lumbar region, before bifurcating into the common iliac arteries at the lower level of the fourth lumbar vertebra. The segmental arteries originate from the aspect of the descending aorta adjacent to the spinal column. Thus the left segmental arteries originate from the posterior aspect of the aorta in both the thoracic and lumbar spine but the right segmental arteries originate from the medial aspect of the aorta in the upper thoracic spine and the posterior aspect of the aorta in the lower lumbar spine. There is some variability in the craniocaudal location of the ostia of the segmental arteries. In the upper thoracic spine, the segmental arteries originate about two vertebral levels caudal to the level they supply and therefore have a marked upward course. In the lower thoracic and upper lumbar spine, the segmental arteries originate just below the corresponding vertebral level, and therefore these arteries tend to have a short upward course. In the lower lumbar spine, the ostia of the segmental arteries are generally located at the level of the center of the third and fourth lumbar vertebrae, respectively.1 It is important to remember that the segmental arteries are named by the level they supply and not by the level from which they originate. When performing catheter angiography of the spine, one can correctly identify the level of a given segmental artery by identifying the (hemi) vertebral blush evident after injection of contrast material or through the use of bony landmarks (figures 5A and 11B). In the thoracic spine, each segmental artery can be named according to the rib under which it courses. Segmental arteries in the lower lumbar and sacral region originate from branches of the internal iliac artery (mainly the iliolumbar and lateral sacral arteries) and the median sacral artery (branch of the aorta at the level of the bifurcation), providing arterial supply to the L5 vertebra and the sacrum. The segmental arteries travel posteriorly (on the left) or posterolaterally (on the right) along the surface of the vertebral bodies, providing short branches to supply the anterior and lateral vertebral bodies. They divide into three major trunks: (i) lateral or ventral (posterior intercostal or lumbar artery), (ii) middle or dorsal (muscular and cutaneous branches) and (iii) medial or spinal. The spinal trunk of each segmental artery enters the spinal canal at the intervertebral foramen and divides into: (a) anterior and posterior spinal canal arteries (called retro-corporeal and pre-laminar arteries, respectively) that supply the vertebral and ligamentous structures and, to a lesser extent, the dura mater, and (b) a radicular artery that supplies 67 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine the dura and nerve root at each level, but not necessarily the spinal cord (figure 2). The radicular arteries that supply the dura and nerve roots and dura are named radiculoradial or radiculomeningeal arteries and exist at almost every spinal level.2 At several levels, the radicular artery gives branches that follow the anterior and/or posterior nerve roots to supply the spinal cord. Such branches are termed the radiculomedullary arteries, with the medullary suffix denoting their supply to the spinal cord. Therefore, the arterial supply to the spinal cord originates from only a few of the segmental arteries. The radiculomedullary arteries are further divided into anterior and posterior radiculomedullary arteries based on whether they supply the anterior or posterior spinal arteries, respectively (figure 2). The average number of anterior radiculomedullary arteries is 6 (range 2e14)3 4 whereas the number of posterior radiculomedullary arteries varies from 11 to 16.5 The arterial supply to the cervical spinal cord varies considerably among individuals. Based on embryonic development, feeding arteries to the cervical spinal cord are derived from the vertebral arteries, the deep and ascending cervical arteries (from the costocervical and thyrocervical trunks, respectively) and to a lesser degree from the ascending pharyngeal and occipital arteries. Therefore, all of these arteries need to be meticulously explored for complete angiographic evaluation of the vascular supply to the cervical cord. Superficial arterial system of the spinal cord At the surface of the cord, two arterial systems can be described: (1) the longitudinal arterial trunks that extend along the long axis of the spinal cord and are constituted by the anterior spinal artery and two posterior (or posterolateral) spinal arteries and (2) the pial plexus that covers the periphery of the spinal cord. Longitudinal arterial trunks Anterior spinal artery Figure 1 (1) Basilar artery; (2) vertebral artery; (3) anterior spinal artery; (4) posterior spinal arteries; (5) anterior radiculomedullary artery; (6) ascending cervical artery; (7) deep cervical artery; (8) subclavian artery; (9) posterior radiculomedullary artery; (10) segmental arteries (posterior intercostal arteries); (11) great anterior radiculomedullary artery or artery of Adamkiewicz; (12) segmental arteries (lumbar arteries); (13) rami cruciantes. 68 The anterior spinal artery (ASA) is typically formed at the level of the foramen magnum by the confluence of descending branches of the intracranial segments of the vertebral arteries (figure 6). Descending feeders of equal size from each vertebral artery are rather uncommon as one side is usually dominant. Descending branches from both vertebral arteries may join at the C2e4 level, or the smaller of the two branches may end separately as a centrally located artery.5 The anterior spinal artery (ASA) travels along the anterior sulcus of the spinal cord and descends (with variable interruptions) to the conus medullaris. Although the ASA has variable caliber (diameter 0.2e0.8 mm)5, it is thinnest in the thoracic cord and thickest in the region of the conus. Due to its long course, the ASA requires additional arterial supply via anterior radiculomedullary arteries in order to maintain adequate blood flow to the entire spinal cord. As a result, the ASA should not be thought of as a single straight artery but rather as a consecutive series of anastomotic vascular loops.6 Blood supply to the ASA via radiculomedullary arteries originates from three major regions: cervicothoracic, midthoracic and thoracolumbar. Because of the opposing flow from adjacent ascending and descending radicular branches that supply the ASA, watershed areas exist at the border of each region, especially in the upper thoracic region. The ASA supplies the anterior two-thirds of the spinal cord tissue (including the anterior horns, and the spinothalamic and corticospinal tracts) by central and pial branches. There are 2e3 anterior radiculomedullary arteries in the cervical region. The most important supply to the cervical ASA is usually located between the C4 and C8 levels of the spinal J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine Figure 2 (1) Posterior spinal arteries; (2) anterior spinal artery; (3) great anterior radiculomedullary artery or artery of Adamkiewicz; (4) medial musculocutaneous branch; (5) lateral musculocutaneous branch; (6) posterior radiculomedullary artery; (7) retrocorporeal arteries; (8) spinal branch; (9) posterior (dorsal) branch; (10) anterior (ventral) branch; (11) left segmental artery (posterior intercostal artery); (12) right segmental artery (posterior intercostal artery); (13) aorta. cord and is termed the artery of cervical enlargement7 (figure 8). It is more often a branch of the deep cervical artery and usually accompanies the C6 nerve root. There are also numerous secondary ASA contributors arising from the vertebral arteries. These branches are usually small in caliber; however, one of the vertebral arteries usually has a large, angiographically detectable branch, at or near C3. According to Djindjan, other small contributors may arise from the costocervical trunk, thyrocervical trunk and, to a lesser extent, the ascending cervical artery. The ascending cervical artery usually supplies branches to the midcervical cord (C4eC6), and the deep cervical artery supplies the segmental arteries at C7 and C8.4 The radiculomedullary arteries (feeder arteries) branch in a ‘Y’ or ‘T’ shape in the Figure 4 (1) Anterior median vein; (2) right deep cervical vein; (3) left deep cervical vein; (4) right vertebral vein; (5) left vertebral vein; (6) subclavian vein; (7) internal jugular vein; (8) left brachiocephalic vein; (9) superior vena cava; (10) accessory hemiazygos vein; (11) intercostal veins; (12) posterior radiculomedullary vein; (13) anterior radiculomedullary vein; (14) azygos vein; (15) hemiazygos vein; (16) lumbar veins; (17) vein of the filum terminale. Figure 3 (1) Posterior spinal arteries; (2) anterior spinal artery; (3) spinal branch; (4) anterior radiculomedullary artery; (5) posterior radiculomedullary artery; (6) central (sulcal) arteries; (7) vasocorona. J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 cervical region. Duplication of the ASA is frequent in the cervical region (figure 7). The segmental levels that give rise to anterior radiculomedullary arteries in the thoracic and lumbar region are variable and unpredictable. Small radicular arteries that are difficult to visualize angiographically supply the spinal cord in the upper and mid-thoracic region. The most important 69 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine Figure 5 (A, B) Selective catheter spinal angiography (frontal view) depicts the typical ‘hairpin’ ascending branch of the artery of Adamkiewicz (arrow) which supplies the anterior spinal artery (arrowheads). The hemivertebral blush is noted in (A), confirming the midline position of the anterior spinal artery. anterior radiculomedullary arterydand the one most easily recognized in angiographydis the artery radiculomedullaris magna, also known as the artery of Adamkiewicz (AKA). It has a diameter of 0.5e1.0 mm5 and almost always arises in the thoracolumbar region, between T8 and L2 in 75% of cases.6 8e10 It has, however, been identified as superiorly as T5 and as inferiorly as L4.4 In 80% of cases, it is found in the left side. The AKA forms the classic ‘hairpin’ loop when it reaches the ASA and gives off a thin ascending branch and a larger descending branch (figures 2, 5A, 5B and 9). Portions of the thoracic and upper lumbar spinal cord are extremely vulnerable to ischemic compromise as there is minimal collateral supply to the spinal cord inferior to the junction of the AKA and ASA. Additional feeders to the ASA below the level of the AKA are rarely found, and the ASA maintains a large caliber until the end of the conus. Even though the ASA continues caudally past the conus as an insignificant branch to the filum terminale, the more important, functional continuations of the ASA are the ‘rami cruciantes’ that surround the conus and provide robust anastomoses with the posterior spinal arteries (PSAs) (figure 1). Figure 6 Selective left vertebral artery catheter angiogram (frontal view) shows the anterior spinal artery (arrowheads) originating from the left vertebral artery (arrow). PSA system can be thought of as a ‘ladder-like’ longitudinal network comprised of two trunks coursing on either side of the spinal cord, medial to the posterior root entry zone.6 Eleven to 16 feeders contribute to the PSA at various levels through the spine. The largest posterior radiculomedullary artery often enters below the level of the AKA.5 Throughout its course, each PSA gives off branches that supply the posterior third of the spinal cord, including the posterior columns, dorsal gray matter and superficial dorsal aspect of the lateral columns of the spinal cord. Pial plexus Besides the direct connections between the ASA and PSAs at the conus medullaris, there is an extensive arterial network on the entire surface of the spinal cord formed by effective anastomoses Posterior spinal arteries The two PSAs (diameter <0.5 mm) also originate at the level of the foramen magnum by branches of the ipsilateral vertebral or posterior inferior cerebellar arteries. The PSAs travel along the right and left posterolateral surface of the spinal cord (hence the alternative term posterolateral spinal arteries), receiving supply at various levels from the posterior radiculomedullary arteries (figures 3 and 11A, B). The system of posterior spinal arteries is discontinuous, and sometimes a PSA may cross over to the contralateral side to supply the contralateral spinal cord. The 70 Figure 7 Detailed view from a reconstructed image from rotational catheter angiogram of the left vertebral artery in a patient with subarachnoid hemorrhage shows an anterior spinal artery aneurysm (arrow) and duplication of the same artery (arrowheads). The duplication represents an anatomic variant. J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine Figure 8 Selective right vertebral artery catheter angiogram (frontal view) demonstrates the artery of cervical enlargement (arrow) supplying the anterior spinal artery (arrowheads). between the ASAs and PSAs. This superficial rich anastomotic network is termed the pial plexus and has been visualized on micro angiograms of the spinal cord.5 This network, which may also be referred to as the ‘vasocorona’, consists of transverse and oblique branches from the ASAs and PSAs and is responsible for supplying the periphery of the spinal cord (figure 3). Intrinsic arterial system The spinal cord parenchyma is supplied by the intrinsic arterial system, which is subdivided into a central (centrifugal) system and a peripheral (centripetal or vasocorona) system. The central system is comprised of the central arteries, also referred to as sulcal or sulcocommisural arteries, which originate from the ASAs and travel into the anterior median fissure (figure 3). After penetrating into the cord either on the left or right, they branch centrifugally, mainly within the gray matter. The peripheral system (vasocorona; diameter 0.1e0.2 mm)4 consists of small perforators (rami perforantes) that originate from the pial plexus J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Figure 9 Selective spinal angiogram in a patient with arteriovenous malformation of the spinal cord (thick arrow), demonstrates a common feeder for the anterior (thin arrows) and left posterior spinal (arrowheads) arteries. and vascularizes the periphery of the spinal cord. These small perforators course into the white matter centripetally. The territory supplied by the central arteries (diameter 0.06e0.40 mm)4 vascularizes the majority of the gray matter. The ASA also supplies the ventral half of the outer white matter tracts through its contribution to the vasocorona. As a result, the ASA supplies approximately two-thirds of the cross sectional area of the spinal cord (anterior commissure, anterior horns, Clarke’s nucleus, anterior portions of the fasciculi cuneatus and gracilis, corticospinal and spinothalamic tracts). The PSAs distribute blood to the dorsal third of the spinal cord, contributing to the apex of the posterior horns. The corticospinal pathways are nourished by both systems. VENOUS DRAINAGE Just as the arterial system can be divided into intrinsic and extrinsic systems, the venous system of the spinal cord is also composed of intrinsic and extrinsic (superficial) systems. The venous system, like the arterial system, is extremely variable in its anatomy although the variability of the anatomy of the 71 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine spinal cord venous drainage is even greater than the arterial supply (figure 4). Intrinsic venous system Although the intrinsic veins draining the spinal cord are divided into sulcal (central) and radial (peripheral) veins, the areas drained by them do not correspond to the areas harbored by the central and peripheral arterial systems. The sulcal veins collect blood from both halves of the medial aspects of the anterior horns, anterior gray commissure and white matter of the anterior funniculus. The radial veins arise from the capillaries near the periphery of the gray matter of the lateral horns, and from the dorsal nucleus of Clark or from the white matter. They are directed outward towards the surface of the spinal cord where they form a venous ring and eventually drain into the superficial venous system, which consists of longitudinal veins in median and paramedian locations with numerous anastomoses and a rich collateral network. Superficial (extrinsic) venous system At the level of the spinal pia matter, blood is accumulated in the anterior and posterior spinal veins. The anterior median spinal vein accompanies the ASA (diameter 0.4e1.5 mm),5 is most prominent in the lumbosacral segment and typically continues along the filum terminale to the end of the dural sac as a terminal vein (vein of the filum terminale) (figure 12). The anterior median vein receives drainage from the sulcal veins and the veins of the ventral fissure. There may be as many as three posterior spinal veins,4 with the posterior median vein being the most constant and of the greatest caliber. The other posterior spinal veins are located posterolaterally, accompany each PSA and are called posterolateral spinal veins. The posterior spinal veins receive blood supply from the radial veins of the dorsal spinal cord. There is high variability of the superficial veins along the posterior surface of the cord and it is important to recognize that secondary networks of superficial veins often replace or complement the longitudinal veins. The anterior and posterior median spinal veins drain into the radiculomedullary veins, which accompany the anterior or posterior spinal nerve root. Numerous anterior and posterior radiculomedullary veins drain the spinal cord. These radiculomedullary veins drain into the paravertebral and intervertebral plexuses, which communicate with the pelvic venous plexuses. There are usually 8e14 anterior radiculomedullary veins11 but there may be as many as 20.12 The number of posterior radiculomedullary veins draining the spinal cords is 5e10.5 The great anterior radiculomedullary vein (GARV, diameter 1.5e2.0 mm), the largest vein draining the anterior thoracolumbar spinal cord, is easily mistaken for the AKA due its spatial course and location seen by MRA or angiography during the venous phase. The junction of a radiculomedullary vein with a median vein (anterior or posterior) is described as a ‘coathook’ configuration because of its more obtuse angulation, compared with the more acute ‘hairpin’ configuration of the AKA.13 The GARV usually accompanies the corresponding anterior or posterior nerve roots between T11 and L3. The posterior median spinal veins can be easily recognized on radiological images by the irregular tortuous courses and large caliber (<2 mm).5 The anterior median spinal vein and the three (usually) longitudinal posterior medial spinal veins communicate with the internal vertebral (epidural) venous plexus via the anterior and posterior radiculomedullary veins. A functional valve at the level of the dura that consists of an oblique, zigzag course of the vein coupled with a narrowed 72 lumen prevents reflux from the epidural veins into the intradural veins. Groen and colleagues14 separated the vertebral venous plexus (Batson’s plexus) into three intercommunicating divisions: (i) the internal vertebral venous plexus (anterior and posterior) which passes superiorly within the vertebral canal through the foramen magnum to freely anastomose with the intracranial venous system; (ii) the external vertebral venous plexus (anterior and posterior) which surround the vertebral column and (iii) the basivertebral veins which run horizontally within the vertebra. The vertebral venous plexus is a valveless system along the length of the spinal cord. The external vertebral venous plexus connects to the internal vertebral venous plexus via the intervertebral veins. These intervertebral veins empty into segmental veins that drain into the ascending lumbar and azygos venous systems. The three azygos vessels in the thoracic spine are the azygos on the right and the hemiazygos and accessory hemiazygos on the left. All three drain into the superior vena cava (figure 4). ROLE OF CATHETER ANGIOGRAPHY AND MR ANGIOGRAPHY IN DEPICTING SPINAL VASCULAR ANATOMY Depiction of spinal vascular anatomy, especially the AKA, is important in the diagnosis and treatment planning of spinal vascular lesions,15 16 presurgical planning for certain types of spinal surgery,17 thoracoabdominal aortic aneurysms repair18 and for planning the preoperative embolization of hypervascular spinal tumors.19 Catheter angiography Catheter spinal angiography is the gold standard for the study of spinal vascular anatomy. Despite significant advances in MRA, catheter angiography remains the most sensitive and specific modality for the diagnosis of spinal vascular lesions and localization of the AKA. The major drawbacks of catheter angiography include the small risk of major complications due to its invasive nature, the use of ionizing radiation and the administration of iodinated contrast material. For these reasons, only experienced practitioners should perform spinal angiography. The individual thoracic and lumbar segmental arteries must be selectively catheterized and evaluated. The vertebral, deep cervical and ascending cervical arteries must be catheterized for evaluation of the cervical cord. The internal iliac and iliolumbar arteries must be catheterized to detect abnormalities in the lumbosacral region. The sensitivity of spinal angiography in detecting the AKA is very high and approaches 100%.10 20e23 MR angiography Modern MRA techniques using contrast agent bolus injection allow for evaluation of the arterial supply and venous drainage of the spinal cord.24 Thus MRA provides important information about the exact location of the AKA as well as spinal vascular lesions, reducing the need for catheter angiography (figure 10). Contrast enhanced MRA performed at 1.5 T has a success rate for the detection of the AKA ranging from 67% to 100%.9 25e28 MRA of the cervical spinal cord is also feasible and useful, with a detection rate of 96% for the ASA.29 Recently, Bley et al30 identified the AKA and ASA in 88% of patients by using 3.0 T MRA. They also showed that the AKA and ASA can be differentiated from the GARV, even in patients with substantially altered hemodynamics.30 Yoshioka et al28 demonstrated continuity of the aorta, intercostal artery, radiculomedullary artery, AKA and anterior spinal artery in 85% of patients on MRA at 1.5 T. Multiplanar reformatted images and maximum intensity projection images are crucial for detection and analysis J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine Figure 11 (A, B) Selective catheter spinal angiogram depicts a right posterior radiculomedullary artery (arrow) supplying the posterior spinal artery (arrowheads). The hemivertebral blush is noted in (B), confirming the lateral position of the posterior spinal artery. Figure 10 MR angiography of the lumbar spine shows the artery of Adamkiewicz (arrow) that continues to the anterior spinal artery (arrowheads). J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Figure 12 The late phase contrast enhanced MR angiography shows the anterior median vein (arrow) which continues as the vein of the filum terminale (arrowheads). 73 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Spine of the AKA, drainage vein and spinal vascular malformations.9 24 25 31 Watanabe and colleagues32 reported the use of a contrast enhanced MRA technique termed double subtraction postprocessing. By utilizing pre-contrast imaging and repeated sequences after bolus contrast, the authors were able to subtract the subtracted venous phase image from the subtracted arterial dominant phase image in order to depict the AKA and differentiate it from the drainage vein. Later, Hyodoh and colleagues9 utilized this same technique to differentiate the AKA, which was detected in 82.4% of patients, from the drainage vein, which was detected in 78.2% of patients. As MRI continues to improve, it is likely that in the near future it will play a major role in the diagnosis of vascular lesions of the spinal cord. Correction notice This article has been corrected since it was published Online First. The section head has been amended to Spine. 13. 14. 15. 16. 17. 18. 19. 20. Competing interests None. Provenance and peer review Not commissioned; internally peer reviewed. 21. REFERENCES 22. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. Shimizu S, Tanaka R, Kan S, et al. Origins of the segmental arteries in the aorta: an anatomic study for selective catheterization with spinal arteriography. AJNR Am J Neuroradiol 2005;26:922e8. Manelfe C, Lazorthes G, Roulleau J. Arteries of the human spinal dura mater. Acta Radiol Diagn (Stockh) 1972;13:829e41. Piscol K. Blood supply of the spinal cord and its clinical importance. Schriftenr Neurol 1972;8:1e91. Brockstein B, Johns L, Gewertz BL. Blood supply to the spinal cord: anatomic and physiologic correlations. 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Watanabe Y, Dohke M, Okumura A, et al. Dynamic subtraction contrast-enhanced MR angiography: Technique, clinical applications, and pitfalls. Radiographics 2000;20:135e52. PAGE fraction trail=7.75 74 J NeuroIntervent Surg 2012;4:67e74. doi:10.1136/neurintsurg-2011-010018 Downloaded from http://jnis.bmj.com/ on May 27, 2016 - Published by group.bmj.com Vascular anatomy of the spinal cord Alejandro Santillan, Veronica Nacarino, Edward Greenberg, Howard A Riina, Y Pierre Gobin and Athos Patsalides J NeuroIntervent Surg 2012 4: 67-74 originally published online May 2, 2011 doi: 10.1136/neurintsurg-2011-010018 Updated information and services can be found at: http://jnis.bmj.com/content/4/1/67 These include: References Email alerting service Topic Collections This article cites 29 articles, 6 of which you can access for free at: http://jnis.bmj.com/content/4/1/67#BIBL Receive free email alerts when new articles cite this article. 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