T HE presence and significance of collateral

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1 The 0ccipital-Vertebral Anastomosis MANNIE M. SCHECIITER, M.D. Section of Neuroradiology, Department of Radiology, Albert Einstein College of Medicine, New York, New York T HE presence and significance of collateral circulation between the various branches of the intracranial circulation and branches of the intracranial and extracranial circulation have been described in the literature. With the current interest and emphasis in the medical and surgical treatment of cerebrovascular disease and with improvements in diagnostic procedures, a clearer demonstration of these collateral channels is now more frequently sought and recognized. Most of these potential collateral channels become obvious only when occlusive vascular disease interrupts the normal pathways, and the channels dilate to form alternate routes for the passage of blood to vital areas. A temporary differential in the hydrodynamics of two opposing systems may also reverse the flow of blood and demonstrate these channels. For a better understanding of vascular disease as a whole, these potential sites must be known and their presence recognized. The ophthalmic anastomosis frequently is seen and recognized in cerebral angiograms, whereas the less frequent occipital-vertebral anastomosis 2,3,7'n,15'1~,ls has not received appropriate emphasis and its role in the collateral circulation has not been fully appreciated. During carotid angiography on the right side, medium passing retrogradely down the carotid artery not infrequently enters the vertebral artery. This may result from a technically poor injection, when the tip of the needle may elevate the intima and partially obstruct the lumen of the vessel, or when occlusive disease is present in the carotid artery distal to the site of puncture. The pathway of the contrast medium in such cases is down the right carotid artery to the innominate artery, where it is then swept into the subclavian artery and into the vertebral Received for publication November 8, artery. In the past this was, in fact, the basis for techniques of indirect vertebral angiography in which the right carotid artery was compressed distal to the site of the puncture during angiography. 4,5 Similarly retrograde carotid catheterization may also be used to demonstrate the vertebral artery and its branches).1~ When filling of the vertebral artery occurs during the injection of contrast medium into the carotid artery or vice versa, the occipitalvertebral anastomosis may be demonstrated by including the cervical course of the vertebral artery in the film. Absence of contrast medium in the proximal portion of the common carotid artery and vertebral artery will be recognized readily, excluding this as the possible course of flow (Figs. 1-4). FIG. 1. Vertebral angiogram. Note filling of both vertebral arteries and filling of branches of external carotid artery via the occipital anastomosis. Marked narrowing at the origin of internal and external carotid arteries was present on the side of anastomotic filling of branches of external carotid artery.

2 Occipital-Vertebral Anastomosis 759 Fro. ~. Vertebral angiogram with filling of branches of external carotid artery via the occipital vertebral anastomosis. Note also filling of both posterior communicating arteries and branches of anterior and middle cerebral arteries. In a review by the author of 1,000 consecutive cerebral angiograms this anastomosis was seen 8 times. In ~ of these patients, stenotic disease was present in the cervical course of the vertebral arteries and the contrast medium passed from the external carotid artery to the basilar artery via this vertebral anastomosis. A third patient suffering from a ruptured aneurysm of the posterior communicating artery was treated by ligation of the common carotid artery. A postoperative angiogram was attempted above the occluded vessel and contrast medium introduced directly into the external carotid artery filled the aneurysm via the anastomosis from the occipital artery (Fig. 5a, b, c, d). The direction of flow was from the occipital branches of the external carotid artery to the vertebral artery to the basilar artery to the posterior communicating artery to the posterior communicating aneurysm. The anterior and middle cerebral arteries also filled from this injection. In the fourth patient stenotic disease was present at the origin of the external and internal carotid arteries and a vertebral angiogram performed via a subclavian puncture resulted in filling of the branches of the external carotid artery via the muscular branches of the ver- Fro. 3. Towne's projection of vertebral angiogram (Fig. 2). Note filling of occipital branch of external carotid artery. tebral artery to the occipital vessels (Fig. 1). No vascular disease was present in the other 4 cases. In one of these, a catheter introduced into the common carotid artery inadvertently entered the occipital artery: the contrast medium introduced directly into the occipital artery flooded this vessel and filled the vertebral circulation. In another, the occipital Fro. 4. External carotid angiogram. The needle is in external carotid artery. Note filling of this vessel and its branches (4), (2), and (3). The basilar artery and its branches (1) have filled via the occipital anastomosis (3).

3 760 M a n n i e M. Schechter 1~IO.5a (left). Left common carotid angiogram May ~1, 1962 with filling of internal and external carotid arteries and their branches. Note filling of an aneurysm of the posterior communicating artery (1). FIG. 5b (right). Right brachial angiogram June 1~, 196~ performed after ligation of left common carotid artery shows filling of right vertebral artery, posterior communicating artery, an aneurysm, and right carotid siphon. Note also bowing or stretching of anterior cerebral artery which is more pronounced than in Fig. 5a and apparently is caused by development of ventricular dilatation. artery had been p u n c t u r e d i n a d v e r t e n t l y a n d the contrast m e d i u m flooded this vessel a n d its tributaries a n d entered the vertebral artery, passing to the basilar artery a n d its branches (Fig. 4). Schulze a n d Sauerbery ~2examined 53 bodies post m o r t e m for the presence of this a n a s t o m o - sis b y i n t r o d u c i n g colored latex into the vessels a n d f o u n d it present in v a r y i n g degrees in all 53 cadavers. I n most of the cases, there was a direct anastomosis between b o t h occipital arteries a n d both vertebral arteries. I n 45 cases this was present on b o t h sides, in ~ cases on the right side only, in 3 cases on the left FIG. 5c (left). Right percutaneous vertebral angiogram June 1~., 196~ shows filling of right vertebral artery, filling of posterior communicating artery and aneurysm, and branches of right carotid artery. Overlapping of [)ranches of the left internal carotid artery is present. Fla. 5d (right). Left external carotid angiogram July 10, 196r shows filling of branches of external carotid artery, vertebral artery, basilar artery, the aneurysm and anterior and middle cerebral branches of internal carotid artery.

4 Occipital-Vertebral Anastomosis 761 FIG. 6. Vertebral angiogram shows muscular branches of vertebral artery. side only aad in 3 cases the anatomical preparation was poor and sites of anastomoses were uncertain. In Gray's 6 Anatomy of the Human Body the descending branch of the occipital artery is described as the largest branch of this vessel and descends in the back of the neck dividing into a superficial and deep portion. The deep portion anastomoses with the muscular branches of the vertebral artery (Fig. 6) and with the profunda cervicalis, a branch of the costocervical trunk. Occasionally numerous muscular branches of the vertebral artery supply the deep muscles of the neck (Fig. 6) and where the vertebral artery curves around the articular process of the atlas they anastomose with the occipital and with the ascending and deep cervical arteries. An anastomosis also exists between the ascending pharyngeal, posterior auricular and vertebral arteries. TSndury, TM in his textbook of topographical anatomy, has also described small collateral vessels between the vertebral and occipital arteries in the neck. Pernkopf, s Sabotta, 13 and Spalteholz ~4 showed these small branches in dissected cadavers. Richter 9 identified muscular branches arising from the vertebral artery in e5 out of 30 vertebral angiograms. We have only observed these in 50 per cent of our vertebral anglograms (Fig. 6). As previously mentioned, postmortem studies show the anastomosis between the occipital artery and the vertebral artery in almost every case. We recognize this in under 1 per cent of consecutive cerebral angiograms and it is seen more frequently when occlusive disease is present. The altered direction of blood flow will be fr~na vertebral to occipital or from occipital to vertebral arteries depending on the head of pressure in each system. The relative infrequency of a radiologic demonstration of this anastomosis may be because of the small caliber of the channels. Since postmortem studies have shown that such an anastomosis is present in a high proportion of cases, nonfilling may also be the result of the hydrodynamics of the situation. The anastomosis becomes radiologically evident, when the hydrodynamics have been disturbed by occlusive disease in either system or by direct introduction of contrast medium into the occipital artery, thus temporarily increasing the pressure in this level. Summary The site of anastomosis between the vertebral and occipital arteries is described. Although these channels are present invariably they are recognized in under 1 per cent of cerebral angiograms. Possible causes for their infrequent filling with contrast medium are discussed. Eight cases showing flow from carotid to vertebral system or from vertebral to carotid system were observed and illustrations of these are included. In 1 case a posterior aneurysm filled via the occipital branch of the external carotid artery. References l. BERK, M.E. Combined carotid-vertebral angiography--a method of vertebral angiography. Brit. J. Radiol., 1960, 33: ~. DECKER, K., and HOLZEI~, E. Gef~,tssverschltisse

5 76~ Mannie M. Schechter im Carotis- und Vertebralisangiogramm. Fortschr. RSntgenstr., 1954, 80: VANDER EECKEN, H. Discussions of collateral circulation of the brain. Neurology, 1961, 11, No. 4, part ~: ELVlDGE, A. R. The cerebral vessels studied by angiography. Res. Publ. Ass. nerv. inert. Dzs., 1938, 18: ENGESET, A. About the angiographic visualization of the posterior cerebral artery, especially by intracarotid injection of contrast. Acta radiol., Stockh., 1948, 30: GRAY, H. Anatomy of the human body. C. M. Goss, Ed. Philadelphia: Lea & Febiger, 1959, ~7th ed., 1458 pp. (see pp ). 7. KRAYENBLrHL, H., and RICHTER, H. n. Die zerebrale Angiographie. Stuttgart: G. Thieme, 195~, vii, 217 pp. (see p. 100). 8. PERNKOPF, E. Topographische Anatomie des Menschen. Munich: Urban & Schwarzenberg, 1957, $,pt RICHTER, H. R. Collaterals between external carotid artery and vertebral artery in cases of thrombosis of internal carotid artery. Acta radiol., Stockh., 1953, ~/): ~ SCItLCHTER, ]V[. Percutaneous carotid catheteriza- tion. Acta radiol., Stockh., 1963, n.s. 1: 417-4s 11. SCHi3RMANN, K. Darstellung der A. vertebralis und ihrer ~-ste im Angiogramm vonder A. carotis externa aus. Zbl. Neurochir., 1954, 1~: SCHLTLZr~, H. A. F., and SAUERBREY, A. Zur Frage der Anastomosen zwischen der A. vertebralis und der A. occipitalis. Zbl. Neurochir., 1956, 16: SOBOTTA, J. Atlas of descriptive human anatomy. E. Uhlenhuth, Ed. and Transl. New York: Hafner Publishing Co., 1954, SPALTEHOLZ, W. Handatlas und Lehrbuch der Anatomic des ]Y[enschen. Amsterdam: Schletema & Holkema, , 15th ed., TATELMAN, ~V[. Pathways of cerebral collateral circulation. Radiology, 1960, 75: TSNDURY, G. Angewandte und topographische Anatomie. Ein Lehrbuch fiir Studierende und ~rzte. Stuttgart: G. Thieme, 1951, 416 pp. (see p ). 17. WIEDENMANN, O. Eine extrakranielle Anastomose zwischen dem Versorgungsgebiet der A. carotis externa und der A. vertebralis. Fortschr. RSntgenstr., 1962, 96: YOUMANS, J. R., and SCARCELLA, G. Extracranial collateral cerebral circulation. Neurology, 1961, 11 :

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