Neuroradiology 8, 149-- 155 (1974) © by Springer-Verlag 1974

Some Technique-Dependent Patterns of Collateral Flow during Cerebral Angiography* J.F. Seeger T.O. Gabrielsen, and R.E. Latehaw Department of Radiology, University of Michigan Medical Center, Ann Arbor, Mich. 48104, USA Received: January 14, 1974

Summary. During selective transfemoral catheter sage bidirectionnel de ces anastomoses, en rapport avec cerebral angiography, anastomoses between external le vaisseau injeet6. La visualisation de ces anastomoses se carotid branches and the vertebral , between the produit de facon variable d@end parrots enti6rement de vertebral and deep or ascending cervical , and la technique, refldtant une augmentation transitoire de la between the middle meningeal and ophthalmic arteries pression dans l'art~re durant l'injeetion du produit de can be demonstrated fairly frequently in patients with no contraste. Par consgquent, l'observation d'une circulation known vascular abnormalities. One can occasionally artdrielle eollat6rale extraergnienne pendant une anglo- show bidirectional filling of these anastomoses depending graphic e6r6brale ne repr6sente pas n6cdssairement un on the vessel injected. Visualization of these anastomoses phdnomgne anormal tel qu'on le rencontre darts les occurs to a variable degree and is sometimes entirely troubles art6riels occlusifs, duns les malformations vas- technique-dependent, reflecting a ~ransient increase in the culaires et dans les tumeurs vascularis6es. intraluminal pressure during the injection of contrast medium. -- Thus, demonstration of extracranial collateral Einige technische Besonderheiten des kollateralen Blut- arterial flow during cerebral angiography should not durchflusses w#thrend der cerebralen Angiographie necessarily be interpreted as an abnormal phenomenon, Zusam~z~enfassung. W/~hrend der selektiven transfe- such as may be seen with arterial occlusive disease, vas- moralen Katheter-Angiographie k6nnen sich Anastomo- cular malformation, or a very vascular tumor. sen zwischen Externa-Gefggen und der A. vertebralis, zwischen der A. vertebralis und tiefen oder aufsteigenden eervicalen Arterien und zwischen der A. meningica media Quelques particularites techniques de la circulation col- und der A. ophthalmica darstellen. Diese Befunde finden latdrale au coats de l'angiographie cdr@brale sich auch bet Patienten, bet denen keine Geffil?anomalien Rdsumd. Au cours de l'angiographie c6rdbrale par vorliegen. Gelegentlich wird ein bidirektionaler Kontrast- eath6t6rismes s61ectifs par vote f6morale, peuvent ap- mitteldurchflul3 durch diese Anastomosen nachgewiesen, paraltre des anastomoses entre des branches carobidiennes dabei ist die Kontrastmittelffillung yon der Lokalisation externes et l'art6re vert6brale, entre l'art@re vert6brale et der Kontrastmittelinjektion abh/~ngig. Es zeigt sich also, les art6res c6r6brales profondes ou aseendantcs et entre dab diese unterschiedliehen DurchstrSmungen technisch l'art6re m6ning6e moyenne et l'art6re ophtalmique. Oc- bedingt werden k6nnen und nicht immer als abnormales easionnellement, on peut mettre en 6vidence un remplis- Ph~nomen gedeutet werden k6nnen.

Introduction The presence of anastomoses between the external carotid and vertebral arteries, between the vertebral and ascending and deep cervical arteries, and between the middle meningeal and ophthalmic arteries is well known. Such communications are best demonstrated angiographieally when they serve as collateral chan- nels in patients with vascular occlusive disease or vas- cular malformations [4, 6, 19, 22, 28]. In our experience, by performing cerebral angio- graphy routinely by selective catheterization, we have shown these anastomoses fairly frequently in patients with no known vascular abnormalities. Visualization of these anastomoses is to a large degree a function of the technique of the examination.

Occipital- Vertebral Anastomosis An anastomosis between the occipital branch of the and the was

* Presented in part at Tenth Annual Meeting of The American Society of Neuroradiology, Mexico City, Mexico, Fig. 1. 6 year old girl with histiocytoma of right orbit. February 21--24, 1972. During part of this investigation, Lateral projection of right common carotid angiogram J.F. Seeger was a. NINDS Special Fellow No. 2 FII NS shows opaeifieation of vertebral and basilar arteries 2365-02 and R.E. Latehaw was a NINDS Special Fellow (solid arrows) via prominent anastomosis with occipital No. 1 Fll NS 02476-01. artery (open arrows) 150 J.F. Seeger et aL : Technique-Dependent Collateral Flow present in all of 53 cadavers studied by Schulze and the vertebral artery even during common carotid angio- Sauerbrey [23] and usually occurred at or near the graphy (Fig. 1). superior surface of the posterior arch of the atlas. Ac- Opacification of the has also been cording to Gray [8], this communication is between the shown during vertebral angiography [20]. Richter [19] deep portion of the descending branch of the occipital mentioned that the occipital artery was opacified in artery and muscular branches of the vertebral artery. one of his 30 vertebral angiographies performed by

Fig. 2. 6 year old boy with brain stem glioma, a) Lateral projection of right common carotid angiogram demons- trates occipital (open arrows) to vertebral (solid arrow) anastomosis, b) Lateral and e) frontal projections of right vertebral angiogram show reverse filling of this same anastomosis (open arrows), with subsequent opacifieation of external carotid artery branches

Rare reports have appeared in the literature show- percutaneous puncture. With selective catheterization, ing opacification of this anastomosis in patients with- the vertebral to occipital anastomosis may be seen out known vascular disease, either due to inadvertent quite frequently during vertebral angiography even in introduction of contrast medium directly into the oc- patients who have no associated carotid occlusive dis- cipital artery [22] or deliberate or accidental external ease, vascular malformation or congenital anomaly. carotid angiography [2, 24]. If the anastomosis is Occasionally, bidirectional filling of this anastomosis large, in some cases perhaps representing a congenital can be demonstrated during selective carotid and anomaly, we occasionally have seen opacification of verteberal angiographies (Fig. 2). J.F. Seeger et al. : Technique-Dependent Collateral Flow 151

This normal anastomosis should not be confused rive external or common carotid angiographies but with various congenital anomalies such as a primitive have occasionally visualized the ascending pharyngeal hypoglossal artery or proatlantal intersegmental artery artery during selective vertebral angiographies (Figs. [26], nor should visualization of this anastomosis dur- 3, 4). Although we have not found it illustrated in text- ing common carotid angiography necessarily imply books of anatomy, the anastomosis between the as- hypoplasia or absence of the ipsilatcral vertebral artery cending pharyngeal artery and the vertebral artery in (Fig. 2). all our eases occurred anterior to the vertebral artery and inferior to the level of the vertebral-occipital anas- Ascending Pharyngeal- Vertebral Anastomosis tomosis, presumably between muscular branches of the Another anastomosis between the external carotid vertebral artery and prevertebral branches of the and vertebral arteries which rarely has been illustrated ascending pharyngeal artery [8, 18]. This localization

Fig. 3. 30 year old woman with diplopia and left periorbital pain. Right vertebral angiogram, a) Lateral projection shows ascending pharyngeal artery (open arrows) opaeified by collaterals (small arrowheads) from vertebral artery. Collaterals (small arrows) to deep cervical artery (large solid arrows) are also demonstrated, b) Frontal projection shows ascending pharyngeal (open arrows) and deep cervical (solid arrows) arteries. Note congenital hypoplasia of right vertebral artery (large arrowheads) beyond origin of posterior inferior eerebellar artery in a) and b) angiographically involves the ascending pharyngeal is in agreement with the illustrations in the two pre- artery. Wiedenmann [29] reported a case of inadvert- vious ease reports [16, 29]. ent placement of a needle into the ascending pharyn- It is interesting to note that an occasional patient geal artery with opacification of a communication with will complain of a burning sensation in the back of the the vertebral artery during injection of 5 ml of con- throat during selective vertebral angiography. This is trast material. We have seen one such ease with presumably caused by contrast material entering the unintentional catheterization of the ascending pha- ascending pharyngeal artery through vertebral anas- ryngeal artery during attempted external carotid tomoses. angiography. Another example of this anastomosis was shown by Nierling et al., [16] during common carotid Vertebral-Ascending and/or -Deep Cervical Anastomoses angiography in a patient with occlusion of the internal The ascending and deep cervical arteries anasto- carotid artery. In patients without vascular abnormal- mose with each other, with the vertebral artery, and ities, we have not seen this anastomosis during selee- with the occipital artery [18]. The ascending cervical 152 J.F. Seeger et al. : Technique-Dependent Collateral Flow artery, lying somewhat more superficial and anterior internal or external carotid angiography may in fact than the deep cervical artery, also communicates with be a reflection of a normal but prominent anastomosis the ascending pharyngeal artery [8, 18]. We occasionally [13]. The true situation often becomes obvious if both observe opacifieation of either the ascending or deep vessels are studied selectively in the same patient cervical artery during selective vertebral angiography, (Fig. 6). more commonly the latter (Figs. 3, 4, 5). Discussion Middle Meningeal-Ophthalmic Anastomosis Despite some reports to the contrary [1, 11], there An anastomosis between the middle meningeal is little doubt that a definite, though probably slight, artery and the lacrimal branch of the increase in intrahminal pressure occurs during in- passes through the superior orbital fissure. This com- jection of contrast material into either the carotid or munication was constantly seen (although variable in vertebral artery. This is perhaps best illustrated by the size) in 170 anatomical specimens studied by tIayreh fairly frequent finding of reflux from the anterior com- [10]. It is most commonly demonstrated angiographic- municating artery into the vascular bed of the opposite ally when it serves as a collateral in patients with carotid artery during selective internal carotid angio- stenosis or occlusion of either the internal or external graphy or reflux into the opposite vertebral artery carotid artery. during selective vertebral angiography. Saltzman [21] Several previous angiographie reports have de- found a much higher incidence of opacifieation of the scribed an anomalous origin of the middle meningeal posterior cerebral artery during internal than common from the ophthalmic artery [3, 7, 25], or an anomalous carotid angiography. Lodin and Ottander [15] reported origin of the ophthalmic from the middle meningeal a higher incidence of spontaneous flow through the artery [5]. Such anomalies certainly seem to occur [9, anterior communicating artery following internal than puncture and also with auto- matic pressure as opposed to manual injection of con- trast material. It seems obvious that such patterns of flow can occur only from a higher to a slightly lower pressure area. We feel that this transient increase in intravascular pressure, at least early during the injec- tion, is, in most instances, responsible for "technique- dependent" opacifieation of the previously described anastomoses. This opinion is supported by the intra- arterial pressure recordings which Lin et al., [14] ob- tained in the brachial and carotid arteries during retrograde braehial angiography. Numerous variables will, of course, affect the head of pressure during injection of contrast material: The catheter may cause partial obstruction when placed in a small vessel and spasm associated with catheter placement may contribute to the obstruction. A re- latively generous bolus of contrast material will then flood the small vascular bed and may "overflow" into existing anastomoses which are usually not visualized. It follows that the more selective the catheterization, the greater is the likelihood of demonstrating these anastomoses. This is true even with no apparent com- promise of the vessel lumen by either the catheter alone or catheter plus spasm. The rate of injection of contrast material also in- Fig. 4. 12 year old boy with papilledema and early hydro- fluences opacification of these anastomoses. Our cephalus from small tumor in the pineal region (*). Lateral projection of left vertebral angiogram. Opaeifieation of standard technique in adults and older children is to ascending pharyngeM (open arrows) and deep cervical deliver, with a pressure injector over a one second (solid arrows) arteries as in Fig. 3 period, 8 ml of meglumine iothalamate 60% (Conray) with common carotid, 7 ml with internal carotid and 10]. However, most of the angiographically illustrated 5--6 ml with selective vertebral angiographies. With cases were either common, internM, or external carotid external carotid angiography, 3--5 ml of contrast is angiographies, but not selective injections into the usually hand injected. Proportionately less contrast and the external carotid artery. material is used for cerebral angiography in infants and Demonstration of an apparent anomaly during either young children. J.F. Seeger et al. : Technique-Dependent Collateral Flow I53

Fig. 5. 6 year old girl with right temporal epidural hema- toma. a) Frontal and b) and e) lateral projections of left vertebral angiogram. Prominent anastomosis between vertebral artery and deep cervical artery (open arrows) with retrograde filling of the latter (4,) on early film and antegrade clearing from below ( ]' ) 3/4 see later

Any process which increases the peripheral re- monstrated during vertebral angiography, had a con- sistance to flow or decreases the size of the peripheral genitally hypoplastic vertebral artery between the vascular bed tends to enhance the transient elevation orgin of the posterior inferior and the of pressure in an injected vessel and thus should lead to basilar artery (Fig. 3), which presumably offered an in- a greater frequency of opaeifieation of available creased resistance to flow of contrast material similar anastomoses. In our experience, there is a particularly to that which may occur with peripheral arterial spasm. high incidence of opaeifieation of these collaterals in We have also noted that these anastomoses are patients who have increased intraeranial pressure from seen more frequently in children than in adults. Visual- any cause (Fig. 4) or intracranial arterial spasm. One ization depends to some extent on the size of the patient in whom the vertebral-ascending pharyngeal anastomoses, which can vary from minute communiea. and vertebral-deep cervical anastomoses were de- tions to what some might consider congenital anom- 154 J.F. Seeger et al. : Technique-Dependent Collateral Flow

Fig, 6. 25 year old woman with papilledema, a) Lateral and b) frontal projections of right internal carotid angio- gram show opacification of anterior branch of (open arrows) via anastomosis (arrow- heads) with ophthalmic artery (solid arrows), c) Lateral and d) frontal projections of right external carotid angiogram show reverse direction of flow through same anastomosis (arrowheads) with opacification of ophthalmic artery (solid arrows) from middle meningeal artery (open arrows' J.F. Seeger et al. : Technique-Dependent Collateral Flow 155 alies. It is reasonable to assume that many of the com- the intraarterial injection of contrast media, l~adio- munications between the carotid and vertebrobasilar logy 86, 615--633 (1966) 12. I-tuber, P., Handa, J.J.: Effect of contrast material, systems, which are prominent during embryological hypereapnia, hyperventilation, hypotonie glucose and development [17], would tend to be larger in infants papaverine on the diameter of . In- and children than in adults, in the absence of vascular vest. Radiol. 2, 17--32 (1967) oeehsive disease. 13. Kuru, Y.: Meningeal branches of the ophthalmic artery. Aeta radiol. (Diagn.) 6, 241--251 (1967) Some patients, especially children who are studied 14. Lin, J.P., Krieheff, I.I., Chase, N.E. : Blood pressure without anesthesia, may hyperventilate to a variable changes during retrograde brachial angiography. degree because of anxiety. Ityperventilation leads to Radiology 83, 640--646 (1964) decreased arterial pC02 and increased intraeranial vas- 15. Lodin, t{., Ottander, tI. : The circulation through the anterior communicating cerebral artery on automatic cular resistance [12], which, in turn, probably leads to contrast injection. Clin. Radiol. 18, 268--271 (1967) a higher incidence of opaeifieation of available extra- 16. Nierling, D.A., Wollsehlaeger, P.B., Wollschlaeger, cranial anastomoses. 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