intracranial and extracranial circulations in the dog: anatomic and angiographic studies

INTRACRANIAL AND

ANATOMIC AND ANGIOGRAPHIC STUDIES

EXTRACRANIAL CIRCULATIONS I N THE DOG :

EBNE8TO DE LA TORRE, MARTIN 0. NETSKY AND I. MESCHAN Sections of Neurology and Neurosurgery, and the Departmen,ts of Pathology

and Radiology of the Bowman Gray of Medicine of Wake Porest College, Winston-Salem, Nor th Carolina

NINE FIGURES

The dog has been a frequent subject f o r laboratory studies of the cerebral circulation. A detailed description of this circulation was lacking before the work of Ellenberger and Baum (1891) and Tandler (1899). Bouclcaert and Heymans ( ' 3 5 ) added some information as a result of dissections of portions of the cerebral circulation in the course of their physiologic studies. More recently, Jewel1 ('52) gave a detailed anatomic description of the blood vessels of the head of the dog, showing the numerous anastomoses between external and internal carotid systems already known to physiol- ogists. I n the process of conducting experiments on the production of infarcts in the brains of dogs, we realized there was a significant lack of information on the radiologic anatomy of the cerebral blood vessels. Localization of af- fected vessels was uncertain when seen in roentgenograms of the skull, and this problem could not be solved by referring to the literature.

To overcome this deficit, angiograms were done in the living animal. Dissections were then performed after injec-

'This investigation was supported in part by Research Grant B-1088 from the National Institute of Neurological Diseases and Blindness of the National Institutes of Health, Public Health Service.

343

344 ERNEST0 DE LA TORRE AND OTHERS

tions with latex to compare the anatomic relations with the roentgenologic findings. This essay is a report of the corre- lation of anatomic findings, angiographic appearances and the functional angiographic anatomy of the cerebral vessels of the dog.

MATERIALS AND METHODS

Serial cerebral arterial angiograms were done on 12 dogs and one monkey. The pre-anesthetic medication was 3 mg of morphine sulfate per kilogram of body weight and 0.4 mg of atropine sulfate given subcutaneously. The anesthetic was intravenous sodium pentobarbital in a dose of 30 mg per kg.

A longitudinal incision in the neck was made with the center of the incision 2.5 em from the angle of the jaw. This center was found most often to be over the site of bifurcation of the carotid artery in the neck.

A trochar with sharp stylet (Lindeman needle) of 16 or 18 gauge was inserted into the common carotid artery, and the non-traumatic outer sheath of the needle directed inside the selected vessel. Thin polyethylene tubing (PE 50) was passed through the Lindeman needle and the artery threaded as far cephalad as possible. The total length of tubing was approximately 30 cin to allow the operator to stand at a distance as a protection against direct exposure to x-rays. A three-way stopcock was attached to the proximal end of the tubing, and two 2-ml syringes were placed on the stopcock. One syringe was used to inject the radiopaque medium, the other contained heparin to prevent clotting. The injection system was filled with the opaque material prior to injection, and with heparin between Pxperiments. Lead screens and aprons then were placed to isolate the operator from the field of radiation.

The injections were made into the internal carotid artery in most instances, less commonly into the external carotid, common carotid or occipital arteries. The flow of blood was modified in some experiments by clamping other homolateral or contralateral vessels just prior to the injection of the contrast medium.

CRANIAL CIRCULATION IN DOG 345

I n the initial experiments, 2 to 3 ml of 70% Diodrast (R) were injected, but afterwards it became obvious that 1 ml was sufficient to fill the major arteries and their branches. Occasionally, 50% Hypaque (R) and in two instances, Li- piodol (R) was used. Urokon (R) in 70% concentration was tried once, but 2 ml produced convulsions, and therefore this dye was not used again. The rate of injection was usually 1 ml in two seconds, occasionally in three or 4 seconds. The resistance of the system prevented greater speeds, but the slower rate is close to the physiologic rate of flow of blood in the internal carotid artery (see section on “experimental alterations of flow’ ’).

Three different projections (ventro-dorsal, lateral and oblique) were used, but only one was made at each injection. The ventro-dorsal view was made with the animal on its back, and the head extended on the cassette. The roentgen beam was directed vertically downward. Different degrees of flexion of the head while in the supine position were used, but these were of little value because of obscuring osseous shadows. The lateral projection was attempted as a “per- fect lateral” with ear shadows superimposed. An oblique view, approximately 45” from the lateral, was also used. The injected side was toward the cassette. Each of these views proved superior for certain features, and these details will be considered later.

The Schonander rapid film changer was used for most of the serial radiologic studies. I n the first group of animals, two films per second were taken for 7 seconds. It then became apparent that some rapidly changing details were being missed, hence in the later experiments three films per second during 5 seconds were taken with each injection of radiopaque medium. A single exposure technique with a 500 ma x-ray unit was also used. Exposure of the film was made when approximately three-fourths of the dye had been injected.

The animals were sacrificed at the conclusion of the experiments, and dissections of the blood vessels were performed


in some instances. The brains were removed and studied for evidence of macroscopic or microscopic damage, Subcuta- neous trypan blue had been given an hour before injection for this purpose. This dye did not stain the brain unless large volumes of Diodrast (R) had been used in repeated injections during the experiment. Each animal was used for a single series of injections.

Injections of latex or vinylite containing red lead were performed on 6 additional dogs. Twenty ml were injected into the common carotid artery, with the vertebrals and the other common carotid artery clamped. The material was injected rapidly, but the pressures were not measured. Latex proved best f o r dissection. Vinylite containing red lead was useful f o r roentgenographic studies of the blood vessels in the anatomic specimen. Attempts were made to obtain three- dimensional models of the blood vessels by digesting the vinylite-injected cerebrum with sodium hydroxide. The blood vessels were too brittle and broke in the process of dissecting and handling.

Anntornq of the cephalic arter ies

The cephalic blood supply arises mainly from the two common carotid and the two vertebral arteries, but the spinal artery is a potential source of blood to the brain. The common carotid artery subdivides most frequently into two branches, the external and internal carotids (figs. 1, 2, E.C., I.C.) at a level 2 to 3 em below the angle of the jaw, approximately where the hypoglossal nerve (H.N.) crosses the artery. The level of subdivision may be identified in roentgenograms at the upper level of the alar wing (fig. 2, A.W.). Usually, the occipital (Oc.) and ascending pharyngeal (A.P.) arteries arise from the external carotid just beyond the bifurcation. The subdivision into 4 vessels on occasion may be at the same level, forming a quadrifurcation. Variants are encountered in which one or another of the vessels arise at a higher level, but for purposes of convenience, the group


may be considered as a quadripartite division. The most constant division, as in man, is into internal and external carotid arteries. The occipital artery often arises posteriorly from the external carotid immediately after formation of the latter, usually a t the same level as the very thin ascending pharyngeal artery. On one occasion, the occipital artery arose from the internal carotid, 2 em above the carotid bulb.

The internal carotid artery may be recognized easily by the bulbous enlargement at its beginning (fig. 1). The diameter of the bulb is about three times that of the more distal portion of the artery. The thinner internal carotid artery enters the skull through the foramen lacerum posterius, and follows a bony channel, the carotid canal. The artery then forms a loop bending ventrally. The bottom of the loop may or may not leave the skull. The distal end of the loop then enters the cranial cavity through the carotid foramen (figs. 1, 4). The lower part of the loop may receive an anastomotic connection from the ascending pharyngeal artery. This anastomosis, however, is rarely present. The artery then courses forward to enter the cavernous sinus, piercing the dura at the level of the posterior clinoid process of the sella turcica. Within the cavernous sinus, the internal carotid artery receives the maxillo-carotid anastomotic artery (figs. 2, 3,4, 5, M.C.A.) called the “anastomotic artery” by Tandler (1899). At this level, a small medially directed branch arises, the posterior hypophyseal artery (not shown in the figures). This arterial branch may arise bilaterally, or from one side only. Jewel1 and Verney (’57) state it may arise from the ‘ ‘anastomotic artery” in some instances. The internal carotid then passes forward and slightly laterally, gives off a posterior communicating artery (P.Co.) almost as large as the parent artery, and then subdivides into anterior (A.C.) and middle cerebral (M.C.) vessels. These arteries, with their counterparts on the opposite side, form the circle of Willis.

The anterior choroidal artery (fig. 4, A.Ch.) arises from the middle cerebral just beyond its origin. The anterior


choroidal artery courses in a caudal direction toward the choroid plexus of the lateral ventricle.

The external carotid artery is easily identified as the larger subdivision of the common carotid, and is a direct continuation of the latter. The first branches, just beyond the bifurcation, are the occipital and the ascending pharyngeal arteries (fig. 1). The external carotid then gives off branches to the face and jaw, and becomes the internal maxillary artery when it crosses niedial to the mandible (fig. 2, 1.111.). The internal maxillary artery stays close to this bone, then curves inward to the alar canal at the base of the skull. Thereafter it makes a distinctive curve, leaves the alar canal and gives origin to the orbital artery (figs. 2, 4, 7, Or.), and ends in the pterygopalatine fossa as the infraorbital artery (figs. 1, 2, 4, I. Or.)

The occigital artery (figs. 1, 2, 4) follows approximately the same direction as the internal carotid f o r 2 to 3 em, then curves backward for a short distance and bifurcates. The superior branch courses inward to the posterior part of the skull, is covered by occipital muscles, and sends many branches perforating the skull (posterior meningeal arteries, P.M.). The inferior branch of the occipital artery courses posteriorly and then superiorly. It then turns caudally t o anastomose with the vertebral artery (fig. 1, 4, V.).

The ascending pharyngeal artery is the smallest branch of the quadrifurcation, and may be absent. It courses cephalad ending in the superior pharyngeal muscles at the base of the skull, and may on occasion anastomose with the internal carotid artery.

The internal carotid artery beyond the cavernous sinus subdivides into anterior and posterior branches. The latter branch is the posterior communicating artery with almost the same diameter a s the internal carotid. The anterior branch courses a few millimeters dorso-medially and then bifurcates into middle and anterior cerebral arteries. This cephalad turn forms part of a loop completed by the middle cerebral


artery as it courses laterally (figs. 2, 3, 5 ) . The middle cerebral artery gives origin to the anterior choroidal, then courses in the Sylvian fissure. The artery lies superficially and is visible macroscopically on the inferior and much of the lateral surface of thc hemisphere. This is in contrast to man where the Sylvian portion of the artery is covered by the temporal lobe.

The anterior cerebral artery courses directly forward, then sweeps medially around and above the optic nerve. A fine branch, the internal ophthalmic (I.O.), arises laterally and under the 2nd cranial nerve. The anterior cerebral artery is small, but the anterior communicating artery (A.Co.) is relatively large in diameter, and completes the circle of Willis. The anterior cerebral then gives origin to the internal ethmoidal artery (I.E.). The main artery then turns up and posteriorly (fig. 4) to supply the cerebrum on either side of the midline (pericallosal and callosomarginal branches).

The vertebral arteries arise from the subclavians, and as- cend in the transverse canal formed by the transverse for- amina of the upper 6 cervical vertebrae (figs. 2, 4). The vertebral artery in its rostra1 passage supplies branches to the cervical vertebrae and muscles, and cervical region of the spinal cord. At the level of the upper margin of the wing of the atlas, the vessel turns dorsally and medially, entering the intervertebral oblique foramen. The vertebral artery receives a branch from the occipital before entering the foramen. This combined artery which we have designated the occipito- vertebral (figs. 2, 4. O.V.) pierces the dura and subdivides on each side into upper and lower branches. The upper branches unite to form the basilar artery, the lower branches join the ventral spinal artery. This anastomotjc circle is called by us the cerebrospinal circle (figs. 2, 4, Csp.C.) to indicate its position between cerebrum and spinal cord. The basilar artery often has a sinuous course on the ventral surface of the brain stem, and divides at the upper margin of the pons to form the posterior portion of the circle of Willis.


A n a s t onzoses aw d radiographic appearances

The presence of a series of anastomotic connections between the previously described blood vessels is of importance in understanding the cephalic circulation and angiographic appearances. The connections between internal and external carotid circulations have been described (Schmidt, '50) as a rete nzirabile, but this term is applicable to the cat and some other species rather than the dog. Certain principles of the connections were clarified by Jewel1 ('52) using only dissection methods, and we have confirmed many of his findings.

The anastomoses were studied functionally by angiograms in the living animal, and anatomically by dissection of the head and neck. Twelve significant anastomoses were found. These do not include anastomoses between the ipsilateral anterior, middle and posterior cerebral arteries. There were three types: those within the internal circulation, those in the external system, and those connecting the two circulations. The vertebral artery has wide anastomoses with both the cervical arteries and the anterior spinal artery, but is considered here as a vessel of the internal circulation. This is further justified because the blood in the external system may under some conditions gain entrance into the cranial contents.

A. Anastoiaoses wi th in the internul circulation

1. The two anterior cerebral arteries. The anterior communicating artery (fig. 2) was found in all animals. It is relatively large in diameter compared to the anterior cerebral artery, accounting for the frequent filling of both anterior cerebral arteries with unilateral injections. The anterior communicating artery thus is an important anastomosis between the two hemispheres. I n addition, in all the injected specimens, fine threads of inter-connecting vessels were seen bridging over the corpus callosum from the anterior cerebral artery of one hemisphere to the other.


2. Internal carotid with basilar artery. The posterior communicating artery is the backward continuation of the internal carotid, and has almost the same diameter as the latter, a condition also seen in human fetuses. The posterior communicating artery on one side fuses with the other to form the basilar (fig, 2). In its backward course, the posterior communicating artery gives off the posterior cerebral and the superior cerebellar arteries.

It is of interest to compare this with the circle of Willis in man, where a modification of this plan is seen. The posterior communicating artery in adult man is smaller compared with the fetal stages, and the posterior cerebral relatively large. The basilar artery in man divides into two posterior cerebral arteries and the superior cerebellar arteries are branches of the basilar. The posterior communicating artery is an anastomotic connection to the posterior cerebral. The basic plan is thus similar in man and dog, but the basilar artery is fused lower in the dog (de la Torre and Netsky, '60). This contrast is also apparent in the dog because of the relatively greater distance from the end of the basilar artery to the infundibular stalk. The posterior communicating arteries in both species then primarily connect the carotid and basilar systems, but also serve as a potential communication between the two internal carotids.

In one dissected animal, a direct connection was found from the basilar artery to both internal carotids. This is a remnant of the primitive trigeminal artery described by Padget ('48) in the early human fetus. It has been seen angiographically, on rare occasions, in the human adult (Har- rison and Lutrell, '53).

3. Inter-carotid anastomoses. Small anastomoses between the two internal carotid arteries were found in all cases by dissection, but were not seen in angiograms. Many individual variations were noted. The anastomoses usually were several small branches crossing the midline at the posterior part of the sella turcica. These then form the posterior hypophyseal vessels, as described by Jewel1 and Verney ( '57),

352 ERNEST0 DE L A TORRE AND OTHERS

and are analogous to the posterior hypophyseal vessels in man.

On one occasion, a relatively large single vessel was seen passing from one internal carotid artery to the other, just behind and attached to the dorsum sellae. This is typical of the horse, but had not been described in dog before the work of Jewel1 and Verney ( '57). Our findings are confirmatory. These authors describe some of the variations of the inter- carotid arteries, originating in some cases directly from the internal carotid artery as found by us, and on occasion from the maxillo-carotid anastomotic artery a t its origin in the cavernous sinus. 4. Vertebral with anterior spinal arteries. The vertebral

artery at segmental levels gives origin to branches anastomosing with the ventral spinal artery. These were seen in dissected specimens and in one post-mortem angiogram with Lipiodol. Andreyev ( ' 3 5 ) has dealt more extensively with these anastomoses.

B. Anastomoses within the emkrnal circulation 1. Occipital with internal maxillary artery. This was dem-

onstrated by dissection, but not in angiograms. The superior branch of the occipital artery courses dorsally, then turns inward around the occipital bone and beneath the muscles of the neck. Branches of this vessel then perforate the bone and constitute the posterior meningeal vessels (fig. 1, P.M.). These anastomose with the posterior branches of the middle meningeal artery arising from the internal maxillary artery.

2. Other groups of anastomoses within the external circulation have not been presented here because they are not directly related to the intracranial circulation.

C. Anastomoses hetween inter.in1 and estervtnl circulations 1. Internal carotid with internal maxillary artery. This

anastomosis is the most obvious and important between intra- and extracranial circulations. There are two separate parts,

CRANIAL CIRCULATION I N DOG 353

but they will be discussed as one. The anastomosis was easily found in the angiograms and dissections in all cases. This arterial connection was described by Ellenberger and Baum (1891) as the internal ophthalmic artery, but Tandler (1899) called it the anastornotic artery. The terms arteria amasto- vnotica or ranaus anastomoticus have also been used. These names are confusing, because there are at least three and sometimes 4 other anas tomotic channels between internal and external circulations. It is therefore suggested that the name be the maxillo-carotid anastomotic artery to indicate its connections and in part to conform to previous nomenclature. Jewel1 ( ’52) criticized the nomenclature of Ellenberger and Baum, and stated “they failed to demonstrate the very small true internal ophthalmic artery arising from the anterior cerebral.” He believed this small branch was the “true homo- logue” of the human ophthalmic artery, and the evidence to be presented in a later publication (de la Torre and Net- sky, ’60) is in accord with this.

The internal maxillary artery, before it becomes the infraorbital, gives off a medially directed short branch called the orbital artery (figs. 2, 4, 7 ) . The latter almost immediately subdivides into three branches, each having a role in the connections between internal and external circulations : the maxillo-carotid anastomotic (M.C.A.), the external ophthalmic (E.O.) and the external ethmoidal (E.E.) arteries. Less commonly, the three branches arose directly from the internal maxillary artery without the intervention of a common orbital trunk. The maxillo-carotid anastomotic division (figs. 1, 2, 3, 4, 5, 7 , 8) courses backward and medially in the style of an accordion, forming two or three coils, then straightens and meets the internal carotid artery at the level of the posterior clinoid process. The angiographic studies demonstrate that flow may occur in either direction under different conditions, but that normally the flow is toward the internal carotid artery, as was shown originally by Bouckaert and Heymans ( ’35). These authors showed also that the maxillo- carotid anastomotic artery could maintain the cerebral cir-


culation when the other sources of blood were eliminated. Jewel1 states “it is contributory to, and not a branch of, the internal carotid artery,” but the reasons for this statement are not given.

We prefer to believe that the maxillo-carotid anastomotic artery is embryologically a branch of the internal carotid and develops from the primitive maxillary artery. The usual direction of flow in the adult animal is not against this con- cept: it is known that the internal carotid artery is larger early in development, and only later does the external carotid gain importance with the development of the large man- dibular and maxillary territories. Flow therefore may be out of the internal carotid artery toward the contents of the orbit in early life, but later is reversed by greater pressure in the external circulation. A similar reversal of flow occurs in the human stapedial artery as it becomes vestigial (Piersol, ’23).

A second part of this anastomotic system is a branch from the middle meningeal artery which meets the maxillo-carotid anastomotic artery in some cases quite near the internal carotid, but often at a more rostra1 point (figs. 3,5). This middle meningeal anastomotic artery was seen uniformly in the dissections and in the angiograms. It was quite variable in length and course, sometimes being short and straight, but in some cases long and looped. Flow normally was toward the internal carotid, just as with the larger maxillo-carotid anastomotic artery.

2. Internal ophthalmic with external ophthalmic artery. The external ophthalmic artery is a branch of the orbital artery and appears to be a continuation of the maxillo-carotid anastomotic artery. On occasion, as already indicated, it may arise directly from the internal maxillary artery. The external ophthalmic artery courses forward and laterally in the orbit, close to the optic nerve. It joins the internal ophthalmic artery, a branch of the anterior cerebral, just before they enter the eye. This anastomosis was seen in dissections and in angiograms (figs. 2, 4, 8).


3. Internal ethmoidal with external ethmoidal artery. The anterior cerebral artery gives off the internal ethmoidal as well as the internal ophthalmic artery. The internal ethmoidal courses near the midline and meets the third branch of the orbital artery (the external ethmoidal) in the medial and rostra1 part of the orbit. The external ethmoidal initially courses upward and laterally, then turns abruptly inward at the roof of the orbit. It therefore crosses over the external ophthalmic and forms a characteristic “x” as seen in the angiogram (figs. 2, 3, 4). The anastomosis of the ethmoidals was not seen in the angiograms, but the distal portions of both arteries were well visualized. 4. Internal carotid with ascending pharyngeal artery. The

pharyngeal artery described by Jewel1 ( ’52) as anastomosing with the internal carotid at the level of the loop in the carotid canal was not verified in any but one of the anatomic dissections, and never in the angiographic studies. An attempt was made to visualize the artery in the living dog by tying all other branches from the carotids in the neck except the ascending pharyngeal, but the anastomosis was still not func- tioning. It is probably of insufficient caliber to be significant under the usual conditions.

5. Vertebral with inferior branch of occipital artery. The inferior branch of the occipital artery courses dorsally, then turns medially at the level of the atlas (figs. 1, 2, 4). The artery then enters the intervertebral oblique foramen of the atlas, where it meets the ascending vertebral artery to form the anastomosis. This combined artery, which may be called the occipito-vertebral, divides on either side to form the cerebrospinal circle (figs. 2, 4).

6. Vertebral with cervical arteries. These anastomoses were seen both in dissections and in angiograms. The connections are segmental, and are between muscular branches of the cervical arteries and small laterally directed branches of the vertebral artery.

7. Pial vessels with posterior branches of middle meningeal artery. The latex injections permitted a view of pos-

356 ERNEST0 DE L A TORRE AND OTHERS

terior branches of the middle mengingeal artery penetrating the skull and crossing the subdural space to anastomose with the adjacent pial vessels. Similar anastomoses were not seen in the anterior portions of the middle meningeal branches.

Ewperimental alterations of flow Bouckaert and IIeymans (’35) suggested that the rate of

blood flow in the internal carotid artery of the dog was approximately 15 ml per minute. This contrasts with 120 ml per minute through the co’yIzmogz carotid artery reported by Jewel1 and Verney (’57). I n our experiments, although the force of injection was not measured, the time required to inject 1 ml of contrast medium into the internal carotid ranged from two to 4 seconds. The slower speed (1 ml in 4 seconds) therefore is similar to the estimated rate of normal flow.

The use of the Schonander rapid film changer allows the rapid consecutive exposure of multiple roentgen films, and proved ideal for the study of passage of contrast medium and blood through the cephalic circulation. Pulsatile flow in a given vessel, for example, was noted occasionally because this technique allowed visualization of vessels every 3 second. A vessel might be seen in one radiogram, disappear in the next, and reappear one-third of a second later. In addition, speed of blood flow with 1 ml of medium usually was so rapid that a time of one-half second might elapse between filling and emptying of the major cerebral vessels.

A striking difference in results was obtained with different rates of injection. When 1 ml of Diodrast (R) was injected into the internal carotid artery without clamping other vessels, and at physiologic rates of flow, the medium filled the internal carotid up to the junction of the anterior and middle cerebral before the maxillo-carotid anastomotic artery was seen (fig. 6). It is of interest that injections at normal rates would result in good filling of the opposite anterior cerebral artery, and occasionally in momentary visualization of the contra-lateral middle cerebral.


At rates of injection greater than normal flow, the internal carotid artery was distended; the medium passed back into the maxillo-carotid anastomotic artery which was seen before filling of the distal end of the internal carotid, and anterior and middle cerebral vessels (fig. 3). After the maxillo-carotid anastomotic artery was filled, secondary filling of the middle meningeal anastomosis was seen, and thereafter the internal maxillary artery. Thus, by altering the speed of injection, some of the arteries could be injected selectively. Normal rates filled the internal circulation exclusively (fig. 6). Greater rates of injection also filled the maxillo-carotid anastomotic artery (against the normal direction of flow), and thence of the external circulation (fig. 3).

Radiographic studies were made with various altered conditions of cerebral blood flow. Selected ipsi- and contra-lat- era1 blood vessels were clamped just prior to injection to obtain knowledge of the cerebral circulation under other conditions. Blood vessels and anastomotic connections other- wise obscured or not apparent in the usual angiograms were seen in some of these studies. Specific alterations were found constantly under given conditions. It was then possible to predict the part of the intra- and extra-cranial circulations which could be visualized.

Clamping of the common carotid artery on the same side as the injection of contrast medium, but below the site of insertion of the needle, resulted in good filling of the internal carotid up to the point where the maxillo-carotid anastomotic artery arose (fig. 7). The intracranial circulation was not seen beyond this point, unless the rate of injection was in- creased (fig. 8). The internal maxillary artery was then filled through the anastomosis, and the dye moved proximally through the external carotid, and distally into the orbital artery and its branches. The internal and external ethmoidal and ophthalmic arteries then were seen.

These results undoubtedly are related to lowered pressure in the external carotid circulation distal to the clamp. The


force of injection maintained pressure in the internal carotid but did not affect the external circulation.

When the common carotid artery was clamped on the side opposi te to the injection of dye, filling of the intracerebral circulation was enhanced (fig. 9). Not only were both anterior cerebral arteries seen well, but also both middle cere- brals. The posterior cerebral artery was not seen on either side. We believe these findings are caused by the drop in blood pressure on the side of the clamp. This maneuver, therefore, is recommended for simultaneous bilateral visualization of most of the interacerebral circulation.

When a clamp was applied to the external carotid artery on the same side as the injection of the internal carotid, the results were exactly the same as when the ipsilateral common carotid was clamped. Dye was not seen in the internal carotid artery distal to the origin of the maxillo-carotid anastomotic artery. The internal maxillary artery then was seen well.

These studies demonstrate that the intracranial circulation is best studied by direct injection of the internal carotid artery. Clamping the common carotid artery on the opposite side promotes flow into both cerebral hemispheres. Clamping of the ipsilateral common or external carotid arteries allows filling of the maxillo-carotid anastomotic artery and promotes flow of blood externally.

DISCUSSION

The standard works on the anatomy of the dog (Sisson and Grossman ( '40), Bradley ( '48), and Miller ( '48) have a striking lack of information on the details of the cerebral circulation. The richness of anastomotic connections between internal and external circulations in the dog was known by Cooper as early as 1836, when he showed that survival might occur after ligation of both common carotid and both vertebral arteries. Andreyev ( '37) studied the collateral pathways enlarging after similar ligations were done in one or several


stages. The anastomoses were shown by post-mortem roentgenograms and dissection.

Lack of accurate information has impeded work on cere- brovascular problems in the dog. Halpern and Peyser ( ' 5 3 ) did angiographic studies using 12 ml of 35% Diodrast (R) injected "as rapidly as possible" to determine the effect of convulsions on the diameter of cranial vessels. This rate greatly exceeds normal flow, and the amount of Diodrast (R) damages the brain. The damage was shown in our experiments by passage of trypan blue into the brain with large amounts of Diodrast (R). Furthermore, extensive filling of the external circulation obscured clear visualization of the intracranial vessels.

A source of experimental error is the assumption that cerebral blood flow may be measured by study of flow in the common carotid after ligation of the external carotid artery. The angiograms demonstrate that this ligation enhances flow of blood from tlie internal to the external circulation through the various anatomoses. Thus, injection of contrast medium into the internal carotid artery after ligation of the external carotid causes return of the material to extracerebral circulation. Solid material may enter the cerebrum under these conditions as has been dcmonstrated with radiopayuc parti- cles in celloidin (Babcock and Netsky, '59), but entrance is less frequent.

TYe T ~ w . ? not able to see veins in any of the angiograms. This is probably because of the small amount of contrast riiediurri used, and dilution of it by Idood from the cxternal circulation. Margolis et al. ('57) used 30 ml in a single injection and were able to see spinal veins. I n addition to veins, the lnasilar artery systcni and the posterior part of the circle of TTillis were never seen in our carotid angiograms.

The anastomoses descrilwd in the dog have analogies in adult mail (Rlouiit and Taveras, '37). Tlie most important anastornotic connection in tlie cerebrum of tlie (log is thc maxillo-carotid anastornotic artery. The a~lgioprapliic studies show that the middle mcningcal artery, the internal ancl

360 ERNEST0 DF, LA TOILRE AND OTHERS

clxternal ophthalmic arteries, and the internal arid external cthnioidals - all have connections with tlie niasillo-carotid anastomotic artery which itself connects tlie internal niaxil- lary ivitli the internal carotid artery. In considering this important anastomosis, we s t u d i d successively its homology with the stapedial artery, tlic primitive niandibular (Vidian), and the primitive niasillary (liypopliyscal artery). W e con- cluded that tlie primitive rnasillary artery, later the liypo- pliyseal artery in both dog and inan, w a s tlie closest liomo- loguc of the rnaxillo-carotid anastoiiiotic artery. The details of our studies of homologics will be reported in a sepaixte ~)nhlication (de la Torre and Netsty, ’GO).

(’cirtnin aiigiograpliic appearanccs are easily tliagnoscd because of constant aiid distinctive characteristics. The loop of the internal carotid artery is well visualized in ventro- dorsal (fig. 3), and oblique (fig. 5) projections. The maxillo- carotid anastoiiiotic artery (figs. 3, 4, 5, 7) is easily identified by its origin froin tlie internal carotid artery and by the “ S ” sliapcd coils at its distal eiid. -1 Iaiger “8” of a much thicker vessel is f‘ornicd by the internal niaxillury artery (figs. 7, 8). Tlic external etliriioidd aii t l t~xtcriial ophtlinlmic arteries cross cacli otlicr in an “ x ” seen in vcntro-dorsal vic\vs (fig. 3). In latcval proJ‘cctions the thick stump and tree-like branches of the orbital urtery are characteristic (fig. 4). A figure “ S ” is typically formed by the last wgnient of the internal carotid, arid tlie initial segniciits of the niaxillo-caro- tic1 anastoinotic and middle cerehral arteries (figs. 3, 51. Finally, two large sonicwliat circular sltado\vs are seen in ventro-dorsal pi*ojectioiis at tlie imjjor sites of anastomosis 1)etween external and intcimal c i imla tions ; these clusters of contrast medium arc found 011 the internal maxillary artcr*;v at the sites of insertion of the orbital and middle rricningeal arteries (figs. 3, S).

SUM1R7AlEY AND CONCLUSIONS

A detailed description is given of the extracranial and intracranial blood vessels in the dog. The anastomoses within

these systems are considered, both anatomically arld in ternis of fuiictional capacity. X technique is presented f o r the aiigiographic visualization of these vessels in the living ani- nial. Using this technique, cerebral blood flow has lwei1 studied under normal conditions, at different rates of injection of radiopaque media, and with clamping of vai-ious vessels in the neck. The radiographic anatomy of the cerc- bra1 blood vessels is prcscntcd. Clamping of various vessels allows the predictable visualizatioii of different portions of tlic cranial circulations. Direct injection into the internal carotid artery of 1 ml of contrast niedium a t plig’siolopic ratc of flow results in filling of tlic ipsilateral cerebral vessels. The posterior par t of the circulation was riot soen l)y this technique. Clamping the opposite coniirioii carotid artcry causes flow into most of the circlc of T;tTillis and most of tlic major iiitracerebral vessels on both sides of tlw braiii. Flov is diverted froiii the internal to the external circulation wheii the homolateral common carotid or external carotid artc3r.y is clamped.

LITERATUBE CITED .\NDBhYEV, I. h., 1935 Functional changes in the 1)iaiii of the dog aflrr i e

diietion of cerebral 1,loocl sopply. I. Ccrcbral cireulatioii aiicl the Clrvclopnieiit of an:istoniosis after ligation of the ar teiies. Arcli. Xeurol. I’\ycliiat., 3 / : 481-507.

1939 Respiiatorg and cardiovascular rc sponses t o cxperinicntal ccrcbrd emboli. ‘L’rans. Am. New. Assoc.,

On thc reflex regulation of the c c ~ cbbral I~ lood flow a n d the cercbrd vasomotor tone. J. Physiol., 84 : 3 ti 7-380.

I k U I L h Y , 0. c. 1928 ‘l-opogruphical Aiiatoiriy of the Dog. 5th cd. rev. 11r T. Gralianie. Oliver and Iioyii, Loiidoii.

COPPhR, A. 1836 Some experinicntz arid observatioris on tying the cai otid and ve1 tebral artcries and the pneumo gastric, phrenic, and sgnipathetic nerves. Guy’s Hospital Reports, 1: 457-475. 1836.

DE LA TORRE, E., AND M. G. NETSKY IIoniologies of human and canine eerebial circulation ( t o be pnblished).

IcLLENBERGFR, W., AND II., BAUN 1891 Rysteinntische und Topographisehe Anatomie des IIundcs. Paul Parev, Reilin.

HALPERN, L., AND E. PEYSER The cffrct of vatious convulsive procedurrs 011 the craiiial vcssels of the dog angiograpliically visualized. J . Neuropath. Exp. Neur., ZZ: 277-282.

BLIKOCK, 11. II., AND 11. G. NETSHY

81: 85-88. Coircf \ I ic~~, J. J., AM) C. IIEIIILNS 1933

1960

1933


HARRISON, C. R., AND C. LUTTRELL 1953 Persistent carotid-basilar anastomosis. Three arteriographically demonstrated eases with one anatomical specimen. J. Neurosurg., 10: 205-215.

1952 The anastomoses between interual and external carotid circulations in the dog. J. Anat., 86: 83-94.

1957 An experimental attempt to determine the site of the ncurohypophysial osmoreceptors, in the dog. Phil. Trans. Roy. Soc. Lond. Ser., E, 240: 197-324.

MARGOLIS, G., A. T. GRIFFIN, P. D. KENAN, G . TINDALL, E. H. LAUGHLIN AND

R. L. PHILLIPS Temporal phases of the blood flow measured by fluorescein and serioroentgenographic methods. J. Neurosurg., 74: 506- 514.

MILLER, M. E. 1948 Guide to the Dissection of the Dog. Ithaca, lithoprinted by Edwards Brothers, Ann Arbor, Michigan.

MOUNT, 1,. A., AND J. M. TAVERAS 1957 Arteriograpliic demonstration of the collateral circulation of the cerebral hemispheres. A.M.A. Arch. New. Psychint., 78: 235-253.

1948 The developmcnt of the cranial arteries in the embryo. Contr. Enibryol. Carneg. Inst., No. 212, 9,?: 205-261.

JEWELL, P. A.

JEWELL, P. A., AND E. B. VERNEY

1957

PADGET, D. H.

PIERSOL, G . A . 1923 Human Anatomy, 8th cd., Lippincott, Philadelphia. SCHNIDT, C. F. 1950 The Cerebral Circulation in Health and Disease. Thomas,

Springfield. SISSON, s., AND J. D. GROSSMAN Thc Ariatomy of the Domestic Animals,

3rd ed. Saunders, Philadrlphia. TANDLEE, J. 1899 Zur vergleithertden Anatomie der Kopfartcrien bci den

Mammalin. Denkschr. Akad. TViss. Wien, 67 : G77-784.

1940

Abbreviations irsed in figures

A.C., anterior cerebral artery $.Ch., anterior choroidal artery A.Co., anterior communicating artery A.P., ascending pharyngeal artery A.W., alar wing of atlas B., basilar artery C.1,2,3, cervical vertebrae C.C., common carotid artery Csp.C., cerebrospinal circle E.C., external carotid artery E.E., external ethnioidal artery E.O., external ophthalmic artery H.N., hypoglossal nerve LC., internal carotid artery I.E., internal ethmoidal artery I.M., internal maxillary nrtcry 1.0.. internal ophthalmic artery I.Oc., inferior branch of occipital artery I.Or., infraorbital artery

M.C., middle cerebral artery M.C.A., maxillo-carotid anastornotic

M.M., middle meningeal artery M.M.A., middle meingeal anastornotic

Oe., occipital artery Or., orbital artery O.V., occipito-vertebral artery P.C., posterior cerebral artery P.Co,, posterior Communicating artery P.M., posterior menigeal artery S.Ce., superior cerebellar artcry S.Oc., superior branch of occipital V., vertebral artery Va., vagus nerve V.Sp., ventral spinal artery Z., zygomatic arch

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PLATE 2

EXPLANATION OF FIGURE

2 Composite drawing to demonstrate the relation of the intraeranial and extracranial circulations to the bony landmarks of skull and upper vertebrae. The assending pharyngeal artery is not shown. The occipito-vertebral artery (O.V.) is shown on the right as arising from the inferior branch of the occipital artery (O.C.), and on the left as arising the vertebral artery (V.).

366

CRANIAL CIRCULATION I N DOQ E. DE LA TORRE. M. G . NETSKY AND 1. MEICHAN

I

1.

A. C A.

I?

PLATE 2

367

PLATE 3

EXPLANATTION OF FlQUIlE

3 Cerebral arterial aiigiogram iu vcvtrodorsal projection. Iiijectiou w t greater rate tLa pliysiologic flow hncr ctlosecl filling of internal aud portions of ex- teriid systtenis. AII “ 8” is Poriiicd by the iiiteriid carotid (I.C.), middle cerebral (M.C.) md n scgment of mtudlloctlrotid amstornotic (M.C.A.), artcricci. The “necordioii” loops of tho latter vcsvol are shown, as well as the ‘‘P” formed by the csteriial opthtilmic (E.O.) and extariia1 etlimoiclal (E.E.) arteries. Note tlic origins of the two aiiastoiuoses arising from the interim1 uinsillary artery (1.M.).

368

CRANIAL CIRCULATION IN DOG 1. DE LA TORRE. M. G. NETSKY AND 1. MESCHAN

PLATE 4


4 Cerebral arterial angiogram in lateral projection. Two milliliters of contrast medium were injected a t greater rate than normal flow. The origin and branches of the orbital artery (Or.) are readily seen. Note the caudal direction of the maxillo-carotid anastomotic artery (M.C.A.). The loop of the internal carotid artery (I.C.) after entering the skull has been retouched in the roentgenogram. The ventral spinal artery (V.Sp.) and basilar artery system have been added to the inset for completeness.

370


PLATE 4

371

PLATK .5

ESPLANATION OF FIQllBE

6 Cercbrul urteriiil a.ngiogrrun in oblique projection, tlic contrast niedium injected at ratc greater than physiologic flow. The loop formed by the internal carotid (I.C.) with the middle cerebral artery is more prominent than in the ventral view. The middlo niaiiiigwl aiiastomot.ie (N .Y.A.) and maxillo- carotid mastoniotio (M.C.A.) arteries are seen best in this projectiou.

372

PLATE 5

373


PLATE 6


6 Cerebral arterial angiograni in veritrodorsal projection, injection a t normal rate of flow. Only the intrrnal carotid arterial bystem has filled. The com- plete intraeraiiial course of tho internal carotid artery (I.C.) is well demonstrated. The proxi~nal portioiis of the anterior (A.C.) and middle cerebral (h1.C.) arteries are seen. Only a small portion of the niasillo raroticl nnas- tomotic artery (M.C.A.) is fillerl.

374

C R ~ U I A L CIRCULATION IN noa E UL I \ TORRC, iV U . h E T S K I AND 1. M h S C H 4 N

PLATE 7


i Cerebral artcrial aiiiogrant in veittrodorsal projection, iiijcetioii a t normal ratc. The ipxilateral coiiiiiioii carotid. aitery 1,elom the site of injection has been clamped. The internal carotid artery (I.C.) filled slightly beyond thc junetioii with the iiiaxillo-carotid aiinstomotic artery ( X.CA4.). Thereafter, only the crternnl circulation filled. Note the orbital arterj- (Or.). The effect was sirniIar when the ipsilntwal external carotid zrtcry was elamped.

3iG

377


PLATE 8

GSPLAWATION OF FIGURE

8 Tho eoiiditioiis of tlic cxperiiuait wcre tlie ~aiiic as in figurc 7, but the es- ternd carotid artery (E.O.) was ela.iiiped, and the rate of iujection was in- erenwd. Morc of the iirtcriiol circu1:utou is iillod than in figure 7. Kote thc miastonosis of crtcriiril (E.O.) tiiitl iiitcriial oylithtilmic, (1.0.) arteries.

37n

9 Ceiebrd aitciial niiiogrnin i i i rcwtiot ioiwl ino jwt in i i , iiijectiori a t phj siologic rate. Thc coiitiulntcinl c'oniiiioii rniotiil :irtery n : i s clniiiped. Kote bilnteinl filling of anterior (A.C.) nud middle corcbinl ( J I V.) nrtciies. Tlierc is no radiopaque medium i n tlic cx-tc~m:il circulation.

380

381


intracranial and extracranial circulations in the dog: anatomic and angiographic studies

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