1975, British Journal of Radiology, 48, 101-107

FEBRUARY 1975

Segmental intervertebral anastomosis in subclavian steal By Richard A. Baker, M.D., Arthur E. Rosenbaum, M.D. Departments of Radiology of Harvard Medical School, Peter Bent Brigham and Beth Israel Hospitals and Glenn H. Robertson, M.D. Massachusetts General Hospital, Boston {Received March, 1974) ABSTRACT

Segmental intervertebral arterial connections originate from normal vascular channels which are commonly seen on selective vertebral arteriography. In subclavian steal, these vessels can hypertrophy and form important collateral pathways. The significance of their haemodynamic contributions may be assessed by their multiplicity and calibre. Lateral or oblique projections in addition to frontal visualization may be required to differentiate the various transcervical channels which lie either anterior or posterior to the vertebral bodies.

Occlusion of the proximal segment of a subclavian artery may result in diversion of blood into the ipsilateral hypotensive vertebral artery (Contorni, 1970; Killen et al, 1966; Leivich et al., 1961; North et al., 1962; Patel and Toole, 1965; Piccone and Leveen, 1970). Descriptions of this entity, best known as subclavian steal, have not emphasized the role of hypertrophied segmental vertebral-to-verte-

FIG. 1. Case 1. Selective left vertebral arteriography, right posterior oblique projection. (A) Early arterial phase. The entire left vertebral artery (LV) is opacified. Via metameric hypertrophied intervertebral arteries (arrows), the right vertebral artery inferiorly (RV) (arrowheads) becomes visualized and fills the right subclavian artery (RS). (B) Mid arterial phase. The superior and middle portions of the right vertebral artery (double arrowheads) are now opacified retrograde and join the opacified column of the inferior portion of the right vertebral artery (single arrowheads). 101

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R. A. Baker, A. E. Rosenbaum and G. H. Robertson bral arterial connections (Djindjian, 1970; Folger and Shah, 1965; Labauge, Crozet and Castan, 1969; Labauge and Pequent, 1970; Newton and Wylie, 1964; Sokol, Narkiewicz and Billewicz, 1970; Weibel and Fields, 1969). These transcervical channels are metamerically arranged and lie along either the anterior or posterior aspect of the vertebral bodies. Their multiplicity and calibre appear to reflect their haemodynamic significance. This communication describes these intervertebral connections in normal and pathologic states.

Schaeffer, 1953). More accurate and graphic anatomic demonstrations of these connections can be found in Stilwell's injected specimens from Bassett's Atlas (Bassett, 1963) wherein the intervertebral arteries were shown to course both posteriorly and anteriorly (Fig. 5).

CASE REPORTS

Case 1

A 3 5-year-old woman with Williams' syndrome (Williams, Barrat-Boyes and Lowe, 1961) underwent cardiac surgery for correction of the supravalvular aortic stenosis. At operation, cardiac bypass required use and then sacrifice of the proximal right subclavian artery. Eight years later, she developed periodic symptoms of vertebrobasilar insufficiency. On physical examination, the blood pressures were 120/70 in the right arm (radial pulse 1+) and 140/80 in the left arm (radial pulse 3 +). Selective left vertebral angiography (Fig. 1) demonstrated dual opacification of the right vertebral artery: its inferior part was first opacified by transcervical intervertebral collaterals and its superior part filled retrograde via the opposite vertebral artery (Fig. 1A). The angiogram obtained 0-5 seconds later (Fig. 1B) showed that the midportion of the right vertebral artery became reopacified by this retrograde flow. Left thyrocervical catheterization demonstrated that the contralateral subclavian artery filled via the (left) inferior thyroid-(right) inferior thyroid anastomosis (Fig. 2). At several levels other radiculomedullary branches from the ascending cervical artery (arrowheads) communicated with the intervertebral channels.

Posterior branches When the branches were posterior (Fig. 5A), they appeared in segmental arrangement arising from the vertebral arteries. They traversed the intervertebral foramina and then coursed immediately posterior to the vertebral bodies. These vessels represent radiculomedullary branches which

Case 2

A 52-year-old woman had a nine-year history of bilateral leg claudication. Her recent illness was an abrupt, transient episode of dizziness, blurred vision, diaphoresis and nausea. Physical examination revealed blood pressures of 170/100 in the right arm and 120/90 in the left. Transaxillary catheterization of the right vertebral artery filled the opposite vertebral artery retrograde (Fig. 3A). Initially, numerous intervertebral channels had been opacified in a "stepladder" arrangement. The lateral projection proved that these vessels coursed principally anterior to the vertebral bodies (Fig. 3B). Case 3 A 5 5-year-old man had four episodes of grand mal seizures followed by transient right hemiparesis. The neurologic examination was normal except for the presence of carotid bruits bilaterally. Right countercurrent brachial arteriography showed opacification of the right common carotid slightly before that of the right vertebral artery (Fig. 4). The distally occluded contralateral vertebral artery filled from the right vertebral artery via several markedly hypertrophied intervertebral channels. The left subclavian artery was occluded. GROSS ANATOMY

The usual presence of cervical intervertebral connections has been described and diagrammed in anatomic textbooks (Brash, 1951; Miller, 1964;

FIG. 2. Case 1. Left thyrocervical arteriography with some reflux into the subclavian artery. The enlarged anastomosis of inferior thyroid artery (IT) with right inferior thyroid artery (IT') causes filling of the right subclavian artery (RS). Radiculomedullary branches (arrowheads) are from the ascending cervical artery (AC). More proximally, the ascending cervical artery shows two sites of stenosis (open arrows) as a manifestation of Williams' syndrome. There is some visualization of intervertebral arteries (solid arrows) as seen in Fig. 1A.

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FIG. 3. Case 2. Smaller intervertebral arteries in subclavian steal (right transaxillary right vertebral arteriography). (A) Antero-posterior projection. Four "stepladder" arranged intervertebral arteries are opacified (arrowheads). (B) Lateral projection. Intervertebral arteries lie anterior to the vertebral bodies, proving that these are not radiculomedullary branches.

normally subserve the spinal cord and the local soft tissues and bone. Anterior branches The intervertebral arteries which course immediately anterior to the cervical vertebral bodies are also metameric (Fig. 5B). EMBRYOLOGY

The development of the radiculomedullary branches has been described in man (Keibel and Mall, 1912; Padget, 1948) and in lower animals (Keibel and Mall, 1912). Their embryogenesis is best illustrated in the pig: early, two longitudinal capillary networks are formed from capillary sprouts of the vertebral arteries. These networks lie along the antero-lateral aspect of the spinal cord. By the 9-mm

stage, they bridge the midline and interconnect (Fig. 6A). At the 28-mm stage, selection within the network has occurred as a result of which there is enlargement of only a few arteries oriented perpendicular to the long axis of the spinal cord and of a single channel oriented parallel to the long axis (Fig. 6B). The enlarged, transversely oriented channels persist as the transcervical radiculomedullary branches, and the single longitudinal channel as the anterior spinal artery. ANGIOGRAPHY

Normal In man the radiculomedullary branches can be visualized angiographically in the absence of abnormality (Fig. 7), but only unilaterally on selective vertebral angiograms. This unilaterality appears to

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FIG. 4. Case 3. Countercurrent right brachial arteriography (steep right posterior oblique projection). The proximal left subclavian artery was thrombosed. The left vertebral artery (LV) is occluded superiorly. Its inferior portion fills solely via multiple intervertebral channels (arrows) from the right vertebral artery (RV).

FIG. 5.* Injected human specimen from Bassett's stereoscopic atlas. (A) View of vertebral bodies from posterior after removal of the posterior portion of the neural arch. Bilateral segmental radiculomedullary branches from each vertebral artery enter the intervertebral foramina and interconnect in the midline (arrows). (B) View of cervical spine from anterior. Segmental branches (arrows) from the vertebral arteries course anterior to the vertebral bodies and interconnect. In frontal projection, these branches radiographically (Fig. 3A) may simulate radiculomedullary branches (Figs. 1 and 4).

*Reproduction with consent of Mrs. David L. Bassett and GAF Corp.

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FIG. 6. Embryologic development of radiculomedullary arteries in the pig (adapted from Keibel and Mall). (A) 9-mm stage. Bilateral networks develop from the vertebral arteries with subsequent evolution of multiple midline bridging vessels. (B) 28-mm stage. Selection has occurred whereby only a few radiculomedullary branches have enlarged further. They unite centrally with a longitudinal channel which is the anterior spinal artery.

occur because of a haemodynamic equilibrium with contralateral radiculomedullary branches.

vertebral artery is caused by a haemodynamic gradient which may also cause hypertrophy of the diminutive transcervical vessels. In Case 1, early arterial Abnormal phase radiographs demonstrate good opacification of On proximal occlusion of a subclavian artery, the opposite vertebral artery and proximally occlublood flow from the superior portion of the con- ded subclavian arteries via the intervertebral chantralateral vertebral artery into the lower pressure nels before retrograde appearance of the radio105

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C.4

C.4

A

B

7. Selective vertebral arteriography showing normal inter-vertebral radiculomedullary and prevertebral arteries in man. FIG.

(A) Right posterior oblique projection. The radiculomedullary channels are diminutive (solid arrows) and the anterior prevertebral arteries (open arrows) are larger. (B) On lateral projection, these radiculomedullary branches penetrate the intervertebral foramina.

paque from the superior portion of the vertebral artery (Fig. 1A). Two occlusions may obtain along the pathway of the same vertebral artery. Involvement of the subclavian artery proximal to the origin of the vertebral artery and of the more superior portion of the same vertebral artery provides a situation in which the affected vertebral artery can fill from the opposite vertebral artery only via the intervertebral channels (Case 3). The radiculomedullary system also has communications with the deep cervical artery and the as-

cending cervical artery (Fig. 2). Other important transcervical arterial pathways include superior-tosuperior thyroid, superior-to-inferior thyroid, and inferior-to-inferior thyroid connections (Bosniak, 1964) (Case 1). Differentiation of the various transcervical vessels often requires selective injections and several projections. The intervertebral arteries have a "stepladder", or metameric arrangement, which is best illustrated in the frontal projection. The lateral or oblique projections separate the radiculomedullary branches (which course posteriorly) from the other intervertebral branches

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Segmental intervertebral anastomosis in subclavian steal (Fig. 2B) and the thyroid anastomoses (which course anteriorly).

LABAUGE, L., and PEGURET, C , 1970. Opacification du

ACKNOWLEDGMENT

LEIVICH, M., HOLLING, H. E., ROBERTS, B., and TOOLE, J.

reseau perispinal de la region cervicale par l'arteriographie humerale retrograde. Journal de Radiologie, d'Electrologie et de Medicine nucleaire, 51, 592-598.

This work was supported in part by USPHS grants NS 02683, HL 05832, and HL 11668. REFERENCES BASSETT, D. L., 1963. A Stereoscopic Atlas of Human Anatomy (Sawyer's, Portland, Oregon). BOSNIAK, M. A., 1964. Cervical arterial pathways associated with brachiocephalic occlusive disease. American Journal of Roentgenology, 91, 1232-1244. BRASH, J. C. (Ed.), 1951. Cunningham's Textbook of Anatomy, pp. 1387-1391 (Oxford University Press, London). CONTORNI, L., 1970. II circolo collaterale vertebro-vertebrale nella obliterazione dell' arteriasubclavia alia sua origine. Minerva Chirurg., 15, 263—271. DJINDJIAN, R., 1970. Angiography of the Spinal Cord (University Park Press, Baltimore).

F., 1961. Reversal of blood flow through the vertebral artery and its effect on cerebral circulation. New England Journal of Medicine, 265, 878-885. NEWTON, T. H., and WYLIE, E. F., 1964. Collateral

circulation associated with occlusion of the proximal subclavian and innominate arteries. American Journal of Roentgenology, 91, 394-405. NORTH, R. R., FIELDS, W. S., DEBAKEY, M. E., and CRAW-

FORD, E. S., 1962. Brachial-basilar insufficiency syndrome. Neurology, 12, 810-820. PADGET, D. H., 1948. The development of the cranial arteries in the human embryo. Contributions to Embryology. Carnegie Institute of Washington, 32, 205—261. PATEL, A., and TOOLE, J. R., 1965. Subclavian steal syn-

drome reversal of cephalic flow. Medicine, 44, 289-303. PICCONE, V. A., jun., and LEVEEN, H. H., 1970. The sub-

clavian steal syndrome. Journal of Thoracic Surgery, 9, 51-75. patients with Blalock-Taussig anastomosis. Circulation, SCHAEFFER, J. P. (Ed.) 1953. Morris's Human Anatomy, 31, 241-248. p. 664, (New York, The Blakisjbin, Co.). KEIBEL, F., and MALL, F. P., (Eds.) 1912. Manual of Human Embryology, pp. 635-637 (J. B. Lippincott, Philadelphia). SOKOL, S., NARKIEWICZ, N., and BILLEWICZ, O., 1970. Subclavian steal syndrome after Blalock-Taussig anasKILLEN, D. A., FOSTER, J. H., GOBBELL, W. G., STEPHENtomoses. Journal of Cardiovascular Surgery, 10, 350—354. SON, S. E., jun., COLLINS, H. A., BILLINGS, F. T., and SCOTT, H. W., jun., 1966. The subclavian steal syndrome. WEIBEL, J., and FIELDS, W. S., 1969. Atlas of Arteriography in Occlusive Cerebrovascular Disease (Saunders, PhilaJournal of Thoracic Surgery, 51, 539-560. delphia). LABAUGE, L., CROZET, G., and CASTAN, P., 1969. L'exploration angiographique des hemodetournements dans les WILLIAMS, J. C , BARRAT-BOYES, B. G., and LOWE, J. B., 1961. Supravalvular aortic stenosis. Circulation, 24, 1311— arteres du cou a destinee cerebrale. Journal de Radiologie, 1318. d'Electrologie et de Medicine Nucleaire, 50, 200-210. FOLGER, G. M., and SHAH, K. D., 1965. Subclavian steal in

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Segmental intervertebral anastomosis in subclavian steal.

Segmental intervertebral arterial connections originate from normal vascular channels which are commonly seen on selective vertebral arteriography. In...
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