Neuroradiology 9, 209--214 (1975) © by Springer-Verlag 1975

Some Aspects of the Spinal Cord Circulation in Cervical Myelopathy M. Rovira, O. Torrent and J. Ruscalleda Service of Neuroradiology, Department of Radiology, Social Security Hospital Medical Center and Medical School, Barcelona, Spain Received: April 10, 1975 Summary. Under usual technical conditions, it is possible, in a great percentage of cases, to visualize angiographically the afferent radiculospinal artery feeding the anterior cervical spinal axis, coming from the vertebral arteries. The level of its emergence is varied, predominating at C5--C6. This radiculospinal artery can be directly affected by a spondylotic lesion at the foraminal level and is one of the causes of the ischemic syndrome observed in the cervical myelopathies resulting from this process.

dominance sur les niveaux C5--C6. Cene artbre radiculom6dullaire peut ~tre comprim6e directement par une l~sion spondylosique, au niveau du foramen de conjonction. Cela repr6senterait par cons6quent l'une des causes du syndrome isch'emique observ6 dans les my61opathies cervicales cons6cutives ?~ce proc6s.

Quelques aspects sur la circulation mddullaire dans la mydlopathie cervicale Rdsumd. Sous des conditions techniques courantes, il est

possible de visualiser angiographiquement, pour un pourcentage 61ev6 de cas, une artgre radiculo-mSdullaire nourricigre de l'axe spinal ant~rieur cervical, provenant des art6res vert~brales. Le niveau de son ~mergence est vari6, mais avec pr~-

einem hohen Prozentsatz der Fiille mSglich, eine radiculomedull~re Arterie des vorderen Zervikalmarks angiographisch darzustellen, die aus den Vertebralarten stammt. Diese radiculo-medulliire Arterie kann an einem Foramen intervertebrale durch spondylotische Veriinderungen abgedrfickt werden und somit eine der Ursachen des isch~imischen Syndroms sein, das schliefSlich zur zervikalen Myelopathie ffihrt.

We have been performing spinal cord angiography with selective catheterization since 1970 [6] following the techniques described by Di Chiro [1] and Djindjian [2] with the almost exclusive aim, at first, of diagnosing arteriovenous lesions and localizing them topographically thus facilitating their neurosurgical treatment. Subsequently we became interested in the study of the normal circulation of the spinal cord, using the normal and abnormal data we were getting from the diagnostic angiographic studies. We were especially attentive in observing minutely the cervical course of the vertebral arteries whenever we carried out an investigation of those vessels, either for cervical pathology, or as was much more frequent, for intracranial processes. Unfortunately, we were not able to carry out systematic anatomical studies on cadavers for social and administrative reasons. There is no doubt that this lack of experimental work has made the accumulation of adequate data to confirm or contradict our anglographic findings more difficult. As is well known, the vascularization of the spinal cord, depending principally (70Yo) on the anterior spinal arterial axis, is very precarious. This arterial axis, gives out metamerically a series of branches which

irrigate the medullary substance over an area equivalent to 2/3 the frontal part of the surface of the spinal cord where the most important structures are: the anterior and lateral tracts and anterior horns, the commisural region and part of the posterior horns and tracts, leaving only the most dorsal part of the columns of Goll and Burdach and the region where the posterior roots enter to be dependent on the posterior arterial axes. Because of this, the vascularization of the spinal cord will be assured only when a functional and anatomical integration of this anterior spinal axis exists. This axis runs through the whole spinal cord, from the oblongata to the conus terminalis where it anastomoses with the posterior axis forming the ansa described by Lazorthes [4] which is of great functional importance, to the vicarious spinal cord circulation (Fig. 1). According to the findings of Adamkiewicz at the end of the last centrury, and the most modern anatomical studies on spinal cord vascularization, the anterior spinal vascular axis originates in the most cephalic part of the vertebral arteries generally in only one before joining with the 1st h o m o n y m to form the basilar artery, coursing down through the cervical region, where the spinal cord has its greatest diameter,

Betrachtungen iiber die Blutzirkulation des RYtckenmarks bei der zervikalen Myelopathie Zusammenfassung. Unter normalen Bedingungen ist es in

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M. Rovira et

al.:

Spinal Cord Circulation in Cervical Myelopathy Based on these anatomical descriptions, we began our radiographical study with the intention of localizing these fine spinal vessels in normal conditions, with the following results.

Cervical Region

Fig. 1. Normal spinal cord angiography, a) The right posterior spinal axis fills through a posterior radiculospinal artery J' and the left fills partially through the arterial connections between both axes. b) The artery of Adamckiewicz proceeding from Th9 nourishes the anterior thoracolumbar spinal axis with its ascending ( t ) and descending (~) branches which anastomose with the posterior spinal axes (~,-~)at the level of the conus terminalis

it then receives 1 to 3 feeding arteries from the vertebrals or, more rarely, from one of the ascending cervical arteries. At the level of the upper dorsal column, the anterior spinal axis receives one single afferent branch that emerges from the 4th or 5th intercostal artery, and it is not until the thoracolumbar region that the supply to the anterior spinal axis can be guaranteed by an artery of considerable diameter, the artery of Adamkiewicz. These radiculospinal arteries that feed the anterior spinal axis are usually not adequate to maintain a compensatory permeability in the whole of its long path, which means that the occlusion of one of them leaves a rather extensive area of the spinal cord ischemic. Some authors have succeded in demostrating experimentally the permeability of this axis in its entire path. While accepting that this anatomical permeability can be accompanied by a truly functional compensation in some cases, we have seen that it is not so in the majority of cases, and arterial compensation does not exist, or is notoriously insufficient, causing irreversible ischemia, except in the conus region, thanks to the anastomosis between the anterior and posterior arterial systems.

We have reviewed a series of 150 studies of vertebral arteries in their cervical path, in patients with intracranial processes without any apparent spinal pathology. Both vertebral arteries have bee~a investigated in only 20Yo of the cases, since in a certain number of circumstances we believed that a bilateral exploration would have been harmful to the patient. The artery most frequently explored was the left one because it is technically the easier, and because it has a proportionally greater diameter. We were frequently able to visualize the anterior spinal axis in the bilateral cases, 88.8Yo, while with studies carried out on single vertebral arteries the visualization of the arterial axis was 70Yo. The percentage is higher when selective vertebral angiography is performed instead of vertebral puncture [7] because in many cases, the anterior spinal axis is filled through radiculospinal arteries, emerging below the level of the puncture. The emergence of the anterior spinal axis directly from the vertebral artery in its most cephalic part was rare (12Yo). In these cases, it is frequent that, in the cervical region, other arterial intakes to the axis do not exist (Figs. 2 and 3).

Fig. 2. The anterior spinal axis t has a high emergence, directly from the vertebral, just after the fenestration of the vertebral artery

M. Rovira et aI.: Spinal Cord Circulation in Cervical Myelopathy

Fig. 3. High origin of the anterior spinal axis ( t ) , issuing from the vertebral artery before forming the trunk of the basilar. The spinal axis does not receive other afferent vessels from this vertebral artery

Fig. 4 Fig. 5 Fig. 4. Vertebral angiography -- Radiculospinal artery emerging from the left vertebral at the level of C 4 Fig. 5. Cervical myelopathy. Osteophytic curve of the right vertebral. A t the same level, there originates a radiculospinal artery, ~" deformed and with very poor filling

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Fig. 6 Fig. 7 Fig. 6. Anterior spinal axis nourished by thick, symmetrical radiculospinal branches accompanying C s roots Fig. 7, Radiculospinal artery proceeding from the left vertebral at the level of C7, t forming the ascending and descending branches of the anterior spinal axis

Fig. 8. Bilateral vertebral angiography. Only one radiculospinal artery exists forming the anterior spinal axis, emerging from the left vertebral artery at the C 7 level t

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M. Rovira et al.: Spinal Cord Circulation in Cervical Myelopathy

Fig. 12. Cervical myelopathy. Vertebral angiogram. The left radiculospinal artery C 6 suffers an evident reduction in its calibre at the level of the intervertebral foramen t Fig. 9

Fig. 10

Fig. 9. Vertebral angiography. The anterior spinal axis is formed principally by three radiculospinal arteries proceeding from the vertebral arteries, at the level of C 4 j' and C 6 left and C r of the right side Fig. 10. The anterior spinal axis possesses an abundant aferent network: 2 left radiculospinal arteries, C 5 t and C 6 and another right, C 7. Furthermore the spinal axis originates directly from the vertebral artery

Fig. 13. Cervical myelopathy. Osteophytic curve of the right vertebral. At the same level, there originates a radiculospinal artery, t deformed and with very poor filling

Fig. 11. Cervical myelopathy. Simultaneous filling of both vertebral arteries. The anterior spinal axis is not seen

T h e o t h e r c o l l a t e r a l s to the a n t e r i o r spinal axis o r r a d i c u l o s p i n a l arteries g e n e r a l l y f o l l o w e d the p a t h of a n e r v e root, so w e n u m b e r e d t h e m a c c o r d i n g to the a s s c o m p a n y i n g roots. W e were n o t a b l e to p r o v e the existence of r a d i o c u l o s p i n a l arteries at levels C~, C~ o r C8. O n the o t h e r hand, at C4 we l o c a t e d it in 20.6Yo of the cases (Figs. 4 a n d 5), at C~ in 24.1Yo, at C6 in 36.2Yo (Fig. 6) a n d at C 7 in 7.1yo (Figs. 7 a n d 8). U s i n g b i l a t e r a l studies, we h a v e b e e n able to p r o v e with g r e a t frequency, t h a t in the cervical r e g i o n there

M. Rovira et al.: Spinal Cord Circulation in Cervical Myelopathy

does exist a single radiculospinal medullary artery that is dependent on the vertebral arteries (Fig. 8). Even in a case of a bulbospinal arteriovenous lesion, which was fed partly by a very dilated anterior spinal artery, there existed only one radiculospinal artery, which came out at the C7 level [5]. Although we had believed at first that the existence of two or more radiculospinal arteries in the cervical region was an exception, we have now proven that in a large number of cases there are from 2 to 4 radiculospinal arteries which coincides with the classical anatomical description. In these cases the arterial pedicles can come from one or other vertebral artery, either symmetrically (Fig. 5) or forming a more complex net, assuring the arterial supply to this anterior spinal axis (Figs. 9 and 10). Angiographically we can distinguish three types of vascularization in the cervical cord, depending on the vertebral arteries: Type A with a poorly fed spinal axis, Type B in which the spinal axis has at least two feeding vessels and Type C in with there are a number of pedicles which assure that the anterior spinal axis receives good nutrition. It is obvious that there exist important relations between cervical myelopathy and the spinal vascularization. The pathological discovery of areas of intramedullary cavity necrosis that characterizes this process, confirms the importance of the ischemic factor in its etiology. Wilkinson [8] found demyelinating lesions of the lateral cords along with pronounced intramedullary cavitation in patients who died from this syndrome. On the other hand, Hughes' observation [3] is very interesting, and indicates that in certain cases extensive protrusion of the intervertebral disc can exist, which causes pressure on the anterior surface of the cord, without producing either clinical or pathological signs of myelopathy. The difference between the degree of cervical arthrosis and the presence of myelopathy can be explained from a vascular viewpoint. The radiculospinal arteries responsible for the vascularization of the anterior spinal axis, enter the spinal canal along with the nerve root through the intervertebral foramina and, crossing the epidural space and the dura mater, go to the anterior surface of the spinal cord. All along the route these vessels can be damaged by disc protrusions or osteophytic alterations if both are present, i.e., the radiculospinal arteries at the same level as the discarthrosis. Then ischemia can occur and cause a spinal cord lesion. If both factors are not present the artery will not be damaged; thus it is important to realize that

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advanced cervical arthrosis can be present without impairment of spinal cord function. Our experience is limited to 8 patients with a clinical picture of cervical arthrosic myelopathy with obvious changes in the gas myelogram. In these cases, bilateral vertebral angiography has given a much lower percentage of visualization of the radiculospinal arteries, 32Uo against 88.8Uo where myelopathy did not exist (Fig. 11). On two occasions we observed stenosis of this artery as it entered the dura mater (Figs. 12 and 13). It is probable, therefore, that the mechanical factor of vascular compression played an important role in this process.

Discussion The anterior cervical spinal arterial axis possesses a more or less numerous network of radiculospinal afferent arteries that maintain its flow, assuring the nourishment of the greater part of the substance of the spinal cord. These radiculospinal vessels, most of which proceed from the vertebral arteries and which follow the trajectory of the nerve roots, offer a greatly varied topography, localizing themselves at arbitrary metameric levels although they predominate at the level of the lower cervical roots (Fig. 14). The compression of one of these radiculospinal arteries at some point of its course or in the anterior spinal axis itself, by disc protusions or bars, can produce ischemia of the spinal cord with zones of softening and necrosis, characteristic of cervical myelopathy.

C3C4 20%o C4 C5 2~ C5C6 36,2Yo /r.~.~ C 6

C7 7,1%

Fig. 14. Scheme of the level of emergence of the nourishing branches of the anterior cervical spinal axis, dependent on the vertebral arteries

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M. Rovira et al.: Spinal Cord Circulation in Cervical Myelopathy

I n o r d e r for this ischemia to be p r o d u c e d , the level of the d i s c a r t h r o s i c lesion m u s t c o i n c i d e with the e n t r a n c e of the r a d i c u l o s p i n a l artery, which, on the o t h e r h a n d , m u s t b e the p r i n c i p a l afferent n u t r i e n t via of the a n t e r i o r spinal axis. O n the o t h e r h a n d , this m e c h a n i s m of ischemia w o u l d e x p l a i n the fact so often o b s e r v e d t h a t severe cervical arthrosis m a y cause m i n i m a l clinical s y m p t o m o l o g y while in o t h e r cases, s m a l l a r t h r o s i c a l t e r a tions can b e the cause of severe m y e l o p a t h i c lesions.

3. Hughes, J. T.: Pathology of the spinal cord. London: LloydLuke 1966 4. Lazorthes, G., Gouaze, A., Djindjian, R.: Vascularisation et circulation de la moelle 6pini~re. p. 286, Paris: Masson 1973 5. Rovira, M., Rius, J.: Angiografia de la medula espinal. Radiologia 13, 301--324 (1971) 6. Rovira, M., Rius Chornet, J. M., Bacci, F., Torrent, O.: La angiografia selectiva en los aneurismas arterio-venosos medulares. Radiologfa 12, 3 5 5 - 360 (1970) 7. Schechter, M. M., Zingesser, L. H.: The anterior spinal artery. Acta Radiol. Diagn. 3, 489--496 (1965) 8. Wilkinson, M.: Espondilosis cervical, p. 189, Barcelona: Salvat 1972

References 1. Di Chiro, G., Doppman, J., Ommaya, K.: Selective arteriography of arterio venous-aneurysms of spinal cord. Radiology 88, 1065-- 1077 (1967) 2. Djindjian, R.: Technique de l'art~riographie de la moelle ~pini~re par aortographie s~lective. Presse m~d. 76, 159-162 (1968)

Dr. M. Rovira Service of Neuroradiology Residencia General Ciudad Sanitaria "Francisco Franco" Barcelona 16 Spain

Some aspects of the spinal cord circulation in cervical myelopathy.

Under usual technical conditions, it is possible, in a great percentage of cases, to visualize angiographically the afferent radiculospinal artery fee...
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