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iagnostic and Interventional Imaging (2012) 93, 690—697

ONTINUING EDUCATION PROGRAM: FOCUS. . .

adiographic anatomy of the intervertebral cervicalnd lumbar foramina (vessels and variants)

X. Demondion ∗, G. Lefebvre, O. Fisch,L. Vandenbussche, J. Cepparo, V. Balbi

Service de radiologie musculosquelettique, CCIAL, laboratoire d’anatomie, faculté demédecine de Lille, hôpital Roger-Salengro, CHRU de Lille, rue Émile-Laine, 59037 Lille, France

KEYWORDSSpine;Spinal cord;Vessels

Abstract The intervertebral foramen is an orifice located between any two adjacent verte-brae that allows communication between the spinal (or vertebral) canal and the extraspinalregion. Although the intervertebral foramina serve as the path traveled by spinal nerve roots,vascular structures, including some that play a role in vascularization of the spinal cord, takethe same path. Knowledge of this vascularization and of the origin of the arteries feeding it isessential to all radiologists performing interventional procedures. The objective of this review

is to survey the anatomy of the intervertebral foramina in the cervical and lumbar spines andof spinal cord vascularization.

© 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

The intervertebral foramen is an orifice located between any two adjacent vertebrae thatallows communication between the spinal (or vertebral) canal and the extraspinal region.

Although the intervertebral foramina serve as the path traveled by spinal nerve roots,vascular structures, including some that play a role in vascularization of the spinal cord,take the same path. Knowledge of this vascularization and of the source of the arteriesfeeding the spinal cord is therefore essential to all radiologists performing interventional

procedures in view of the iatrogenic risks they present. We will first review the anatomy ofspinal cord vascularization, and then the topographic anatomy of the cervical and lumbarintervertebral foramina, as these are the most frequent sites of injections performed byradiologists.

∗ Corresponding author.E-mail address: xavier.demondion@chru-lille.fr (X. Demondion).

211-5684/$ — see front matter © 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.ttp://dx.doi.org/10.1016/j.diii.2012.07.008

dx.doi.org/10.1016/j.diii.2012.07.008mailto:xavier.demondion@chru-lille.frdx.doi.org/10.1016/j.diii.2012.07.008

bar foramina 691

Figure 1. Sagittal slice through a lumbar intervertebral foramen,showing anterior (arrow) and posterior (arrowhead) radicular arte-ries circulating on the anterior side of the anterior (AR) and pos-terior (PR) roots. Also note the artery in the lower part of theintervertebral foramen (wavy arrow). The foraminal veins (curvedarrows) are located on the upper part of the foramen in front andbV

white matter of the anterolateral funiculi detach;• the radiculomedullary arteries, which feed the pial plexus

and irrigate the spinal cord. They are found mainly in the

Radiographic anatomy of the intervertebral cervical and lum

Review of the anatomy of spinal cordvascularization

Origin of the radiculomedullary arteries

While the encephalon receives blood from large arterialtrunks arising from the aortic arch (internal carotid and ver-tebral arteries), vascularization of the spinal cord comesfrom arteries of multiple and varied origins that enter it allalong the spinal canal [1], going through the intervertebralforamina.

At early stages of embryo development, each nerve rootcarries a radicular artery divided into an anterior and a pos-terior radicular artery that will help vascularize the spinalcord. This vascularization is then segmented, to correspondto the metameric structure of the cord during development.Some arteries regress while others grow larger. There is nofixed number of radicular arteries. Although the number the-oretically should be 31 on each side, in reality the numberis always lower.

In the cervical region the radicular arteries are furnishedessentially by branches of the subclavian arteries and moreparticularly by the vertebral arteries.

In the thoracic and lumbar regions, they arise fromthe parietal, thoracic and lumbar collaterals of the aorta,which in turn divide into end arteries. The anterior endarteries include the intercostal or lumbar arteries and theposterior end arteries the dorsal spinal arteries. The dor-sal spinal arteries themselves divide into a large arteryheaded toward the posterior vertebral muscle mass anda thinner radicular artery that reaches the intervertebralforamina in the company of the corresponding spinal nerve[1].

The radicular artery divides into an anterior and a poste-rior radicular artery. As a general rule, the radicular arteriescourse along the anterior side of the corresponding roots(Figs. 1 and 2). Nonetheless we want to stress that the twobranches can be separate from the beginning, that one ofthem can be missing, and that we have observed posteriorradicular arteries located behind — posterior to — posteriorroots (Fig. 3). The caliber of the radicular arteries rangesfrom 0.2 mm to 2 mm. The caliber of the anterior radicularartery is generally larger than that of its posterior counter-part.

The radicular arteries are not all of the same impor-tance, as Adamkiewicz reported in 1882 [1]. The number ofradiculomedullary arteries actually participating in the vas-cularization of the spinal cord can vary from one person toanother. Accordingly different authors have estimated theirnumbers differently: 3 to 10 for Adamkiewicz, 5 to 10 forKaydi, and 6 to 8 for Lazothes [1]. In summary, it seems thatonly one artery out of 8 to 10 actually reaches the spinalcord.

Accordingly, we distinguish:• the radicular arteries that are very small and become

lost along the roots before reaching the spinal cord.Although there are variations, these are seen essen-tially in the lower dorsal and sacral regions of the

cord;

• the radiculopial arteries, which reach the pial plexus.These arteries are part of the coronary plexus of the spinal

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ack of the nerve roots, as well as in the lower part of the foramen.B: vertebral body; ID: intervertebral disc.

cord, from which the arteries intended to vascularize the

igure 2. Medial view of a sagittal slice of the lumbar col-mn showing anterior (arrow) and posterior (arrowhead) radicularrteries circulating on the anterior sides of the anterior (AR) andosterior (PR) roots. VB: vertebral body; ID: intervertebral disc.

692 X. Demondion et al.

Figure 3. Sagittal slice through a lumbar intervertebral foramen.Note that within this foramen we identify one artery (arrow) in frontat a distance from the anterior root (AR) and another behind theposterior root (arrowhead). VB: vertebral body; ID: intervertebraldisc; SAP: superior articular process of the vertebra below; Pi: infe-rior articular process of the vertebra above; Rn: nerve root; curveda

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The radiculomedullary arteries furnish the spinal cordwith the bulk of its arterial irrigation. They feed the graymatter and the deep part of the white matter.

Arterial vascularization of the spinal cord

Cord vascularization is schematically ensured by three ver-tical systems anastomosed by a horizontal perimedullaryplexus and fed by the radiculomedullary arteries describedabove [1,2]. Accordingly, we distinguish an anterior spinalaxis and two posterolateral spinal axes traveling respec-tively in the ventral median fissure and the posterolateralsulci of the cord (Fig. 5). The anterior spinal artery, madeup of the anterior branches of the radiculomedullary arte-ries, is of considerable functional importance because by itspenetrating branches it feeds the anterior two thirds of thespinal cord. The posterior spinal arteries, made up of theposterior branches of the radiculomedullary arteries, pro-vide blood to the posterior last third of the cord, via itspenetrating branches.

The anterior spinal artery is not always a continuousanastomotic pathway. It can be divided into threefunctional parts: cervicothoracic, mid-thoracic and thora-columbar [2]. The upper or cervicothoracic region comprisesthe cervical cord and the first two or three thoracic segments(Figs. 6 and 7). The rich vascularization of this segmentcomes from several distinct sources that nonetheless alloriginate from the subclavian artery: vertebral arteries,deep and ascending cervical arteries, and finally the cervico-intercostal trunk. Within this region, we distinguish:• the upper cervical spinal cord, fed most often by two

anterior spinal arteries from the intracranial portion ofthe vertebral arteries. The anastomosis of these arteriesrarely descends below the fourth cervical segment;

rrows: foraminal veins.

region of the dorsolumbar junction. The most importantis the Adamkiewicz artery (Fig. 4). The most common arethe 9th and 10th dorsal arteries, and the 1st, 2nd, 4th and5th lumbar arteries.

igure 4. Anterior view of a dissected spinal cord, showing thertery of Adamkiewicz (arrow) and its characteristic inflection tooin the anterior arterial axis (arrowhead).

• the mid-cervical spinal cord, fed by two to three anteriorradiculomedullary arteries from the vertebral arteries;

• the lower cervical and upper thoracic spinal cord, vascu-larized by an anterior radiculomedullary artery from theright or left cervico-intercostal trunk, accompanying rootsC7, C8 or T1. It is often the principal vascular source ofcervical enlargement.

Figure 5. Macroscopic horizontal slice of the cervical cord,showing the anterior arterial axis (arrow) and the dorsolateral axes(arrowhead).

Radiographic anatomy of the intervertebral cervical and lumbar foramina 693

Figure 6. Anterior view of a dissected spinal cord showing thecontribution of radiculomedullary arteries (arrows) from the inter-

Figure 7. Medial view of a sagittal slice of the cervical columnsf

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vertebral C4—C5, C5—C6, C6—C7 and C7—T1 left and C2—C3 andC4—C5 right foramina, on the anterior spinal axis (arrowheads).

The mid-thoracic spine, from the 3rd to the 9th thoracicsegment, is usually fed by a single thin anterior radicu-lomedullary artery (internal diameter: 0.2—0.4 mm) [3]. Itnormally arises from the posterior dorsal spinal branch ofthe 4th or 5th intercostal, artery, more often on the left(80% of cases) than the right.

The lower — thoracolumbar — area is little vascularized,unlike the areas above and below it. This area is usuallyfed by the radiculomedullary artery of the lumbosacral

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Figure 8. Schematic diagram of the vertebral venous system: a: in tinferior vena cava; ALV: ascending lumbar vein; BVV: basivertebral vein; LV: lumbar vein; PEVP: posterior epidural venous plexus; AEVP: anterior

howing a radiculomedullary artery from a C3—C4 intervertebraloramen.

nlargement (artery of Adamkiewicz), with an internaliameter ranging from 0.5 to 0.8 mm [3] (Fig. 4). Depen-ing on the series, this artery originates on the left side in5% of cases and between Th9 and L2 in 85%, according toasjaunias and Berenstein [4]; on the left side in 67.7% andetween Th12 and L3 in 83.9%, according to Biglioli et al.5].

enous vertebral system

enous drainage of the spinal cord

he system of venous vascularization of the spinal cords basically modeled on that of arterial vascularization.rom the capillary network, blood is drained by vessels

he axial plane; b: in the frontal plane, in a posterior view. IVC:RTVP: retrocorporeal transverse venous plexus; FV: foraminal vein;epidural venous plexus.

694 X. Demondion et al.

Figure 9. Transverse slice at the lumbar level showing the ante-rior epidural venous plexuses, highly developed (arrow) as well astp

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Figure 11. Parasagittal T1-weighted MRI slice, after injection ofgadolinium and fat saturation, showing the foraminal veins (curvedaf

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he posterior epidural venous plexuses (curved arrow). Note theresence of foraminal veins (arrowheads).

n a radial arrangement that flows into the perimedullaryeins [1].

We also find longitudinal pathways at these veins: twonpaired and median, situated in the anterior and pos-erior sulci (anterior and posterior spinal veins) and twother smaller lateral pairs on each side, traveling the entire

ath along which the spinal roots emerge. From theseongitudinal veins venous blood drains into the anteriornd posterior radicular veins and then into the epidural

igure 10. Parasagittal T1-weighted MRI slice of the lumbarolumn, showing the ascending lumbar vein (arrows), a lumbar veincurved arrow), and a lumbar artery (arrowhead).

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rrows) as well as the nerve roots (Rn) inside a lumbar intervertebraloramen. ID: intervertebral disc; VB: vertebral body.

enous plexuses. The epidural venous plexuses communi-ate with the extravertebral system through the foraminaleins.

he epidural veins

he large veins comprising the epidural venous plexusesravel through the epidural space. The spinal venous sys-

em is extremely important physiologically [6—8]. It isn avalvular venous system that serves, together withhe superior and inferior venae cavae, as the body’s

igure 12. Horizontal mid-cervical slice, showing the relationsf the nerve roots in the intervertebral foramen. Ra: anterior root;p: posterior root; gg: spinal ganglion; VA: vertebral artery; shortrrow: uncus; long arrows: posterior facet joint.

Radiographic anatomy of the intervertebral cervical and lumbar foramina 695

Figure 13. Mid portion of a cervical intervertebral foramen studied in an oblique sagittal plane perpendicular to the axis of the transversec: CT

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processes: a: anatomical slices; b: MRI T1-weighted sagittal slice; inferior articular process; SAP: superior articular process; Rn: nerve

posterior drainage network. This venous system, becauseof its numerous anastomoses with the caval venous sys-tem, can function as a backup network in the case of cavalcompression or obstruction. The anatomy of the venousplexuses can be described at the vertebral segment levelbecause the anastomoses of the different superimposedvenous segments form a continuous chain that makes upthe longitudinal venous network of the spine. The epiduralvenous plexuses are constituted by the anterior and pos-terior longitudinal plexuses (Figs. 8 and 9). The anteriorlongitudinal plexuses are the most developed and can bebest analyzed in axial and coronal slices. They appear tocomprise on each side two longitudinal venous networks,one lateral and the other medial. The anterior epiduralvenous plexuses are located within connective adipose are-olar tissue between the posterior longitudinal ligament andthe posterior side of the vertebral body (Fig. 9). The tworight and left longitudinal plexuses come closer to oneanother at the pedicle and move further apart at the inter-vertebral disc. A study in the axial plane shows that theinternal vertebral plexuses are linked by transverse plexusespassing in front of and behind the dural sheath, formingan epidural venous ring that is more developed in its ante-rior segment (Fig. 9). The largest transverse plexuses arebehind the middle part of the vertebral body, where theyreceive the anastomosis of the basivertebral veins (posteriordrainage vein of the vertebral bodies). The epidural venousplexuses communicate through the foraminal veins and,depending on the segment considered, with the vertebral,intercostal, lumbar or sacral veins (Figs. 1, 3, 9—11, 13).Any radiologist practicing vertebroplasty procedures musttherefore know the anatomy of this spinal venous sys-

tem, given the possibility that cement will leak into theepidural space during the filling of the vertebral body[8].

slice, constant. CV: vertebral body; id: intervertebral disc; IAP:s; curved arrows: foraminal veins; arrows: arteries.

opographic anatomy of the intervertebraloramina in the cervical and lumbaregions

he cervical intervertebral foramen

he containern the cervical spine, the intervertebral foramen must betudied with the two anatomic regions adjacent to it (medi-lly and laterally), because the anatomical continuum makesny division impossible (Figs. 12 and 13). That is, the nerveoot must cross three successive areas to go from thentradural to the extravertebral region [9]. We thereforeescribe:a medial area equivalent to the lateral lumbar recesswhere the roots have a relatively large amount of space,just within the medial orifice of the intervertebral fora-men; the yellow ligament forms its posterior wall;a narrow intermediate area between the uncus in frontand the posterior facet (zygapophyseal) joint behind,with the pedicle below, constitutes the intervertebralforamen, strictly speaking. The uncus truly serves as aprotective wall for the vertebral artery and the spinalganglion, vis-à-vis the intervertebral disc [10];a lateral area, which is no longer involved with the nerveroots but with the spinal nerve, which rests in the furrowof the transverse process. The bottom of this transversefurrow is perforated by the vertebral foramen, provid-ing passage to the vertebral artery, and thus constitutingan essential relation to the cervical nerve (in particularduring injections). On a transverse slice, we can clearlysee at the transverse furrow an ovoid space that shelters

the vertebral artery in front of it and the spinal ganglionbehind it.

6 X. Demondion et al.

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segment. We must underline the importance of the changesin the dimensions of the intervertebral foramen on move-ment [14,15]. In extreme flexion, all the diameters of theintervertebral foramen are at their maximum; the pedi-cles move apart from each other, disc convexity is minimal,because of the tension of the posterior longitudinal liga-ment; the posterior facet capsule and the yellow ligamentpress against the posterior articular processes [14]. Duringextension, all the diameters diminish; the pedicles movecloser to each other, reducing the height of the foramenby approximately 20% [15,16].

The greater the collapse of the intervertebral disc, thegreater the reduction in foraminal height. Accordingly, thepassage of nerve components in the bony upper part ofthe foramen protects the root somewhat from disc protru-sion, posterior facet joint osteoarthritis, and ascension ofthe inferior articular process during extension movements(as long as the height of the intervertebral space remainssatisfactory).

The contentsNumerous components are mixed closely together in theintervertebral foramen: nerve roots and spinal ganglions,foraminal fat, foraminal veins, radicular arterioles, lymphvessels, the meningeal nerve (sinuvertebral nerve) andforaminal ligaments (Figs. 1, 3, 9, 11). The total area ofthe neurovascular bundle accounts for 20 to 50% of the totalforaminal area [15]. The anterior motor root joins the poste-rior sensory root just after the birth of the spinal ganglion to

TAKE-HOME MESSAGES

• The intervertebral foramina, regardless of thesegment considered, are traveled by nerve roots butalso by vein and arteries, some going to the spinalcord.

• The radicular arteries are branches of the subclavianarteries at the cervical spine and of the aorta at thethoracic and lumbar spines. They divide into twobranches, anterior and posterior, usually travelingdown the side of the corresponding nerve roots.

• They vary in position, number, caliber, and division.• Some radicular arteries help feed the spinal cord.• The foraminal veins drain the epidural venous

plexuses, particularly developed on the anterioraspect of the spinal canal, at the middle level of thevertebral bodies.

• The drainage veins of the vertebral bodiescommunicate with the epidural veins and theperivertebral veins.

• In the cervical intervertebral foramen, the nerveroots are usually located at or below the disc plane,protected from it by the uncus.

• The lumbar intervertebral foramen has two parts,one superior and rigid, where nerve componentspass and usually the radicular or radiculomedullaryarteries; the other inferior part is more mobile and

96

These three areas are aligned according to an axis ori-nted at 45◦ forward compared with the sagittal plane, thehole constituting a canal 20 mm in length [10]. Because of

his oblique angle, the bony borders of the cervical inter-ertebral foramen are visible only on three-quarter images.

he contentshe cervical nerves result from the confluence of an anteriornd a posterior root (Figs. 12 and 13). The anterior motoroot is thin, made up of four to seven rootlets from thenterior collateral sulcus of the spinal cord. The posteriorensory root, which is three times larger than the anterioroot, is composed of four to 10 rootlets that penetrate theosterior collateral sulcus [11]. The anterior root thus con-tituted develops close connections with the vertebral uncusn front of it and with the pedicle of the vertebra beneath it.he usual position of the posterior root is behind and abovehe anterior root [12,13]. Its connections are with the supe-ior articular process of the vertebra below it. Each posterioroot carries a spindle-shaped swelling containing the cellodies of sensory neurons: the spinal ganglion. The spinalanglion is thus positioned between the vertebral arteryn front of it and the posterior facet joint behind it. On aarasagittal slice with the posterior aspect of the vertebralody in the front, at the level of the uncus, the pedicle ofhe overlying vertebra above, and the pedicle of the verte-ra below, we find the anterior and posterior root, either athe same level as or below the disc plane. The very abun-ant epidural veins in the cervical region communicate withhe venous plexuses located around the vertebral artery,hus serving as shock absorber in crossing the interverte-ral foramen. At the cervical level, the nerve componentsttach more to the venous components than to the epidu-al fat, as at the lumbar level. A herniated cervical oftenends to manifest laterally just behind the junction betweenhe uncus and the vertebral body, causing not only venoustasis that engenders edema but also direct compressionf the root and the ganglion, causing the pain and mus-le disorders encountered during cervicobrachial neuralgia.he nerve roots within the intervertebral foramen becomelosely connected to the radicular artery and the branchesf its division, as we described above, with as a general rulene anterior branch traveling along the anterior aspect ofhe anterior root and a posterior branch along the anteriorspect of the posterior root.

he lumbar intervertebral foramen

he containerhis orifice has two parts: one anterosuperior, in the formf a rigid immobile ring, made up of the inferior part of theedicle and the posteroinferior part of the vertebral body;he other is inferior and mobile; it is formed by the posteriorrticular lamina covered by the yellow ligament, in the back,nd by the posterolateral aspect of the intervertebral disc inront (Figs. 1, 3, 9) [13]. This second articular part is the onehat undergoes motion-related or degenerative changes. At

he lumbar level, the foramen has an oval shape with a largeertical axis. The L5-S1 foramen is the roundest and themallest of the lumbar intervertebral foramina. The spinalanglion occupies the largest part of the foramen at this

exposed to disc changes. It is difficult to systematizethe veins, which can be found in both parts.

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Radiographic anatomy of the intervertebral cervical and lum

form the mixed spinal nerve. The spinal ganglion is locatedbelow the pedicle, on which it sometimes leaves its imprint[17].

At the foramen exit, the spinal nerve usually dividesinto a relatively large anterior branch and a thinner pos-terior branch. It is difficult to systematize the foraminalveins. They allow connections between the internal andexternal vertebral venous plexuses, as at the cervicallevel. The foraminal veins can nonetheless be individu-alized at the upper part of the foramen in back andfront, above the spinal ganglion, and at the lower part[6]. As we have seen, the radicular arteries are usu-ally found on the anterior side of the anterior andposterior roots. Foraminal fat plays an especially impor-tant functional role, similar to that of orbital fat,allowing flexible maintenance of the vascular structures[10].

Disclosure of interest

The authors declare that they have no conflicts of interestconcerning this article.

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14] Revel M, Mayoux-Benhamou MA, Aaron C, Amor B. Variationsdes trous de conjugaison lombaires lors de la flexion-extensionet de l’affaisement discal. Rev Rhum 1988;55:361—6.

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Spine 1996;21:2412—20.

17] Hasegawa T, Mikawa Y, Watanabe R, Howard S. Morphometricanalysis of the lumbosacral nerve roots and dorsal root gangliaby magnetic resonance imaging. Spine 1996;21:1005—9.

Radiographic anatomy of the intervertebral cervical and lumbar foramina (vessels and variants)Review of the anatomy of spinal cord vascularizationOrigin of the radiculomedullary arteriesArterial vascularization of the spinal cord

Venous vertebral systemVenous drainage of the spinal cordThe epidural veins

Topographic anatomy of the intervertebral foramina in the cervical and lumbar regionsThe cervical intervertebral foramenThe containerThe contents

The lumbar intervertebral foramenThe containerThe contents

Disclosure of interestReferences