Anatomic and Angiographic Study of the Vertebral- Basilar Arterial System in the Dog’

ERNEST0 D E LA TORRE: OLIVER CHARLES MITCHELL, AND

MARTIN G. NETSKY Department of Neurology and Section on Neurosurgery of the Bowman Gray School of Medicine of Wake Forest College, Winston-Salem, N . C .

An anatomic study of the intra- and extracranial circulations in the dog was presented by de la Torre, Netsky and Mes- chan (’59). The cerebral circulation was shown angiographically with radiopaque material injected into the internal caro- tid artery. Under normal conditions of cerebral circulation, however, contrast me- dium thus injected did not pass to the pos- terior communicating arteries. As a conse- quence, the vessels of the posterior portion of the circle of Willis were not seen in the living animal (fig. 1).

The territory supplied by the vertebral- basilar arterial system, under normal con- ditions of flow, is different from the terri- tory supplied by the internal carotid com- plex as was shown first by the distribution of colored dyes after perfusion experi- ments (Earner, ’12; Jewell and Verney, ’57). Comparable results were obtained by McDonald and Potter (’51) in the rab- bit; a similar separation is known to exist in most human brains. This concept of separate flow in two interconnected sys- tems, therefore, has long been known, but angiographic demonstration of these two major territories in the living dog has not been available.

This report deals with a study of the anatomy of the basilar and vertebral arte- ries, a physiologic method of visualizing these arteries, and an analysis of the re- sults.

MATERIAL AND METHODS

The cerebral vessels of 5 dogs were in- jected with methyl methacrylate monomer and then the brain was digested. The casts of the blood vessels were used for compari- son with angiograms, and allowed 3-di- mensional viewing. Further details of the

method and a study of parts of the circula- tion not seen angiographically will be re- ported separately (Netsky and Jackson). The branches of the vertebral artery in the neck were not contained in these plastic models, hence dissection was performed in three other animals to verify interpretation of these angiograms.

Vertebral angiography was done on 9 additional mongrel dogs, ranging in weight from 11.5 to 14 kilograms. Nembutal (R) was given as an intravenous anesthetic (30 mg per kilogram of body weight) and an endotracheal cannula was used to as- sure a patent airway throughout the ex- periments. In 5 of the 9 dogs, the wing of the atlas was removed to isolate the vertebral artery in the distal part of the neck. We refer to this approach hereafter as “high.” Four to 5 cm of the artery was exposed and cannulated with PE-50 polyethylene tubing, attached to a syringe for injection of the radiopaque medium. Ringer’s solution was used in a slow con- tinuous drip between injections.

In the other 4 animals, the vertebral artery was isolated at the base of the neck, between its origin from the subclavian artery and point of entrance into the ver- tebral canal. This approach is designated as “low.” The contrast medium then was injected either directly with needle and syringe or through a PE-50 polyethylene catheter.

The contrast media used were : Diodrast (R) 75% in one animal, Hypaque (R) 50 %in one animal, and Renographin 60 (R) in 7 animals. Only 1 ml of radiopaque

%This investigation was supported in part by re- search grants B-1088 and B-2417 from the National Institutes of Health, Public Health Service.

a Special Fellow (BT-685) from the Nahonal Insti- tutes of Health, Public Health Semce.

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188 ERNEST0 DE LA TORRE, OLIVER C. MITCHELL AND MARTIN G. NETSKY

External ophtholmic P .

ernol ophtholmic A.

Internal corotid A.

Fig. 1 Drawing of an angiogram obtained by direct injection of the internal carotid artery in the living dog. The posterior part of the cerebral circuIation is not seen despite forceful injection of 1 ml of contrast medium and filling of the extracranial circulation. Com- pare with figure 2.

material was injected into the vertebral artery in 4 to 5 seconds in the high ap- proach, and 2 ml was used during the same time in the low injections. Single roentgenographic exposures were obtained with standard 54 KV x-ray equipment. Ventrodorsal projections were taken rou- tinely because maximum information was obtained in this position.

RESULTS 1. Anatomic aspects. The vertebral ar-

tery has multiple branches during its course through the vertebral canal in the neck (fig. 2). These branches are seg- mental, arising in each case at the verte- bral interspace, then anastomosing freely with branches from the contralateral verte- bral artery and with the ventral spinal and cervical arteries. The vertebral artery per- forates the transverse foramen in the alar wing of the atlas, changing from a dorsal to a ventral position, and anastomoses with the inferior branch of the occipital

artery at the level of the upper margin of the wing of the atlas. The combined artery (occipito-vertebral) then courses medially to end in the cerebrospinal circle. The basilar artery originates from the rostal portion of this circle. The caudal end of the circle has ample connections with the ventral spinal artery or arteries.

The basilar artery courses ventrally to the brain stem, usually in a sinuous man- ner (figs. 2 , 3 ) . The largest branches of the basilar artery originate in the first 2 cm above the cerebrospinal circle and are cere- bellar arteries (fig. 3 ) . Two to 4 branches arise on each side, but with many varia- tions. These large vessels supply the anterior and inferior cerebellar surfaces and the medulla. The most rostral of these cerebellar arteries also sends small branches to the caudal portion of the pons. The final division of the basilar artery into the two posterior communicating ar- teries is at the level of the sulcus between the pons and the midbrain. The superior

VERTEBRAL-BASILAR ARTERIES IN DOG

Point of oncstomosis with internal carotid

Posterior comrnunica

Posterior cerebral A

Superior cerebellar A

Cerebrospinal circle

Occipito- vertebral A

Inferior branch of occipital A

Ventral spinal A

Fig. 2 Composite drawing of results of vertebral angiography. The needle and catheter are inserted as for high injection. Branches of the vertebral artery in the neck and their anastomoses are shown here for completeness, but are visible only with low injections. Com- pare with figure 1.

cerebellar and posterior cerebral arteries are the two major branches arising from each posterior communicating artery.

Although the blood supply of the pons is provided mainly by numerous minute branches arising directly from the basilar artery, the most rostra1 and ventral por- tions are nourished by branches coming from the posterior communicating arteries. The ventral surface of the midbrain is sup- plied by branches arising from the poste- rior communicating arteries and medial branches from the posterior cerebrals.

Both the posterior cerebral and the su- perior cerebellar arteries course in a paral- lel direction posteriorly and laterally to surround the cerebral peduncle and then turn medially on the dorsal aspect of the brain stem, thereby forming almost a com- plete circle. The posterior cerebral artery is then slightly cephalad, and surrounds

189

the most caudal portion of the thalamus and lateral geniculate body. It then passes directly back on the undersurface of the occipital lobe near the midline to irrigate the medial aspect and pole of this lobe.

2. Angiographic aspects. The details of the experiments are shown in table 1. With injections low in the neck, the intracranial portion of the vertebral-basilar arterial complex was not visualized in two of four dogs, even when larger amounts ( 4 ml) of contrast medium were injected. Anas- tomoses of the vertebral artery in the neck were seen only in dogs with low injections (fig. 4).

Visualization of the vertebral-basilar dis- tribution was satisfactory in all cases of the high approach (fig. 5). The posterior communicating, posterior cerebral, and superior cerebellar arteries were seen bi- laterally in each film. Some of the larger

190 ERNEST0 DE LA TORRE, OLIVER C. MITCHELL AND MARTIN G. NETSKY

TABLE 1 Results of injection of vertebral artery

Radiopaque Site of Visualization of Outcome after

anaomam Dog no. substance injection other arteries

233 2 ml Diodrast 75% (R) High Middle and anterior Died

238 1 ml Hypaque 50% (R) High - Normal

246 1 ml Renographin 60 (R) High - Normal

250 1 ml Renographin 60 (R) High Middle and anterior Died

253 1 ml Renographin 60 (R) High - Died

255 2 ml Renographin 60 (R) Low Ventral spinal and Normal

298 2 to 4 ml Renographin Low - Normal

309 2 to 4 ml Renographin Low - Normal

310 2 ml Renographin 60 ( R ) Low Ventral spinal and Normal

cerebral arteries

cerebral arteries

cervical anastomoses

60 (R)

60 (R)

cervical anastomoses

pontile and peduncular branches of the posterior communicating arteries were also visible.

Because the posterior cerebral arteries almost completely surround the brain stem and turn back toward the midline, two vessels frequently were seen superimposed on the posterior portion of the circle of Willis. These vessels are the angiographic representation of the posterior cerebral arteries in their dorsal position and should not be confused with arteries arising di- rectly from the circle of Willis (fig. 5).

Contrast medium consistently was seen up to a point in the most anterior portion of the posterior communicating arteries at the site of junction with the internal caro- tids. The middle and anterior cerebral arteries were seen in only two cases (dogs 233 and 250). These dogs were apneic, in shock, and died as a result of the proce- dure. We consider the filling of the middle and anterior cerebral arteries in these ani- mals to be an abnormal finding because of alterations of flow occurring in shock.

DISCUSSION

The vertebral arteries in the dog, with multiple branches at each vertebral inter- space, are in striking contrast to adult man. The human vertebral artery, after

its origin from the subclavian artery, has no significant branches until it enters the skull.

The terminal portions of both vertebral arteries in man are the homologue of the rostral half of the cerebrospinal circle. The posterior inferior cerebellar artery, arising commonly in man from the vertebral ar- tery, comes off the basilar artery in the dog. The basilar artery is then relatively longer in the dog than in man, lying on the ven- tral surface of both medulla and pons. Furthermore, the posterior cerebral and the superior cerebellar arteries are branches of the basilar artery in man, but arise from the posterior communicating arteries in the dog.

Embryologically the posterior communi- cating vessels are direct continuations of the internal carotid arteries (Padget, '48). Carotid angiography in man results in fill- ing of the posterior cerebral arteries in about 34% of cases (Meschan, '59), but in the dog only one instance of ming of the posterior communicating arteries has been found by us in more than 100 carotid angiograms obtained in 50 animals. Ver- tebral angiography causes filling of the posterior communicating arteries consist- ently in the dog, but seldom in man.

VERTEBRAL-BASILAR ARTERIES IN DOG 191

Renographin 60 (R) was used predomi- nantly in this study because Tindall et al. ('58) demonstrated minimal toxicity to the central nervous system caused by methyl glucamine with sodium diatrizoate. Nevertheless, three of nine dogs died as a result of the angiography. This lethal effect is in striking contrast to internal carotid angiography with only one death in more than 50 animal studies performed by us. Other substances also may selectively af- fect different parts of the brain. Kramer ('12) noticed striking changes in respira- tion and blood pressure caused by small doses of alcohol or ether injected into the vertebral artery of the dog. These effects were negligible with similar doses in the carotid system.

Angiography with 1 ml of contrast me- dium injected in 4 seconds resulted in satisfactory visualization of the posterior portions of the circulation; other arteries were not clamped. We believe that greater amounts of medium or faster rates of in- jection are beyond the normal rate of blood flow. The diameter of the basilar artery is radiographically equal to the intracranial portion of the internal carotid, and the rate of flow in this last vessel has been calcu- lated to be in the range of 12 to 15 ml per minute (de la Torre, Netsky and Meschan, '59). The amount of contrast medium used in our low approach was increased because of the greater dilution and large number of branches to be filled, but nevertheless the low approach was less satisfactory for vertebr a1 angiograms.

Cerebral angiograms in the dog obtained by others for the most part have been made under what we consider to be non- physiologic conditions. Halpern and Pey- ser ( '53) and James and Hoerlein ('60) performed angiography by injecting force- fully more than 10 ml of contrast medium into the common carotid artery of dogs. Filling was obtained of the anterior and posterior circulations, as well as of the external circulation, with this method. Himwich et al. ('60) obtained angiograms after surgically produced anastomoses in the carotid and vertebral arterial com- plexes, but they recognize that blood flow was altered by these anastomoses. When alteration of normal flow occurs after ex-

perimental procedures, in shock or after death, with increased intracranial pres- sure, or as a result of forceful injections, contrast medium injected into one system may pass through the circle of Willis to the other. In the healthy animal, under physiologic conditions, each of these two large systems (vertebral-basilar and caro- tid) is exclusively supplied by its own ar- teries.

SUMMARY

A technique is described for angio- graphic demonstration of the vertebral- basilar circulation in the dog, and the anatomy of the vertebral-basilar arterial system is correlated with the angiographic appearance. The vertebral-basilar and carotid systems are physiologically inde- pendent. Intermixing occurs only in patho- logic conditions. High morbidity and mor- tality rates occur in vertebral as compared with carotid angiograms.

ACKNOWLEDGMENT

Renographin 60 ( R ) was provided by E. R. Squibb and Sons.

LITERATURE CITED de la Torre, E., M. G. Netsky and I. Meschan

1959 Intracranial and extracranial circula- tions in the dog: anatomic and angiographic studies. Am. J. Anat., 105: 343-382.

de la Torre, E., and M. G. Netsky 1960 Study of persistent primitive maxillary artery in hu- man fetus; some homologies of cranial arteries in man and dog. Ibid., 106: 185-195.

Halpern, L., and E. Peyser 1953 The effect of various convulsive procedures on the cranial vessels of the dog angiograpically visualized. J. Neuropath. Exp. Neurol., 12: 277-282.

Himwich, W. A., E. Costa, R. G. Canham and S. L. Goldstein 1960 Isolation and injection of selected arterial areas in the brain. J. Appl. Physiol., 15: 303-306.

James, C. W., and B. F. Hoerlein 1960 Cerebral angiography in the dog. Vet. Med., 55: 45-56.

Jewell, P. A., and F. V. Verney 1957 A n ex- perimental attempt to determine the site of the neurohypophysial osmoreceptors in the dog. Phil. Trans. Roy. SOC. London, Ser. E., 240:

Kramer, S. P. 1912 On the function of the cir- cle of Willis. Exp. Med., 15: 348-364.

McDonald, D. A., and J. M. Potter 1951 The distribution of blood to the brain. J. Physiol.,

Meschan, I. 1959 A n Atlas of Normal Radio- graphic Anatomy. Saunders, Philadelphia.

197-332.

114: 356-371.

192 ERNEST0 DE LA TORRE, OLIVER C. MITCHELL AND MARTIN G. NETSKY

Netsky, M. G., and F. Jackson Further studies of Tindall, G. T., P. D. Kenan, R. L. Phillips, G. Mar- the canine cerebral circulation. (To be pub- golis and K. S. Grimson 1958 Evaluation of lished. ) roentgen contrast agents used in cerebral ar-

Padget, D. H. 1948 The development of the teriography. 11. Application of a new method. cranial arteries in the embryo. Contrib. Em- J. Neurosurg., 15: 37-44. bryol. Carneg. Inst., No. 212, 32: 205-261.

PLATE 3

EXPLANATION OF FIGURE

3 Photograph of ventral surface of brain digested after in- jecting blood vessels with methyl methacrylate monomer. The upper part of the cerebrospinal circle is seen at the bottom of the photograph. The dye in the sinuous basilar artery is unevenly distributed. All major vessels are filled because the injection was done after death.

VERTEBRAL-BASILAR ARTERIES IN DOG Ernest0 de la Torre

PLATE 1

193

PLATE 2

EXPLANATION O F FIGURE

4 Roentgenogram after injection of contrast medium in a living animal. The low approach was used. The seg- mental arteries in the neck can be seen.

194

VERTEBRAL-BASILAR ARTERIES IN DOG Emesto de la Tome

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