D ATA on blood flow or pressure measured. Exposure of the anterior part of the circle of Willis in the dog. Technical note

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1 Exposure of the anterior part of the circle of Willis in the dog Technical note SHIGEAKI HORI, M.D., AND W[LLIAMINA A. HIMWICH, PH.D. Thudichum Psychiatric Research Laboratory, Galesburg State Research Hospital, Galesburg, Illinois A technique for exposing the vessels in the anterior part of the circle of Willis in the dog is described. Some of the physiological and anatomical characteristics of the anterior communicating and the anterior cerebral arteries are discussed. KEY Worms anterior communicating artery anterior cerebral artery D ATA on blood flow or pressure measured directly in the major vessels of the base of the brain are indispensable for clarification of hemodynamics in the circle of Willis. However, few such studies have been reported in the literature. 4,~,6,8,1~ Of the major basal vessels in animals, the basilar artery has been a favored site of investigation, 3,4,10,19 while the vessels in the anterior part of the circle of Willis, particularly the anterior cerebral and anterior communicating arteries, have remained unchallenged probably because of their relative inaccessibility. Besides being of physiological interest, the anterior part of the circle of Willis is important from a clinical point of view, since most intracranial aneurysms occur in this vicinity2r To obtain data on flow and pressure in these arteries, we have exposed the anterior part of the circle of Willis in the dog through an anterior transsphenoidal approach. In this paper the technique of the exposure and some of the physiological and anatomical characteristics of the vessels in the anterior part of the circle of Willis will be described. Materials and Methods Eighty-two dogs, males or females weighing between 13.6 and 32.6 kg, were used. In the anterior cerebral or anterior communicating artery of 74 of the dogs, either blood flow was measured with an electromagnetic flowmeter or lateral pressure was ascertained using the method of external vertical cannulation described by Iwabuchi and Himwich. 7 These data will be the subject of a later communication. Photographic records were made of the operation in the other eight animals. After prernedication with 1 mg of atropine sulfate, anesthesia was induced by the intravenous injection of 30 mg/kg of sodium pentobarbital (Nembutal), which was administered as required. Spontaneous respira- J. Neurosurg. / Volume 41 / July, 1974 "107

2 S. Hori and W. A. Himwich tion was maintained with the aid of a tracheal tube; the systemic blood pressure was monitored by means of a cannula in the left femoral artery. During surgery an isotonic electrolyte-glucose solution was infused in the femoral vein, and temperature was maintained by a thermal blanket. After the buccal skin and mucosa were incised on both sides, the mouth was opened to its fullest possible extent by pulling the mandible, as well as the tongue, caudally. To facilitate opening the mouth and yet avoid compression of the carotid sinus by the angle of the mandible, the bone on both sides was either disarticulated at the mandibular joint or cut free at its angle. A U-shaped incision was made in the soft palate along the posterior border of the hard palate, and the soft palate was reflected posteriorly. The mucous membrane overlying the epipharynx was peeled off from the base of the skull and the medial pterygoid muscle was freed from the palatine and pterygoid bones on both sides. The basisphenoid, presphenoid, pterygoid, and parts of the vomer and palatine bones were rongeured out as widely as possible (Fig. 1 ) but with care taken not to injure the vessels and nerves of the optic canal, orbital fissure, and alar foramen as well as the internal carotid artery, which forms a loop around the external carotid foramen. As rongeuring progressed, the cavernous sinus appeared bilaterally. Unless bleeding from this sinus was profuse, it could be controlled by applying Gelfoam and cotton pledgets. However, in older dogs with tough adhesions between the skull and the wall of the sinus, the most meticulous handling was required during this part of the dissection. Rongeuring the bone around the optic foramen, tuberculum sellae, and anterior clinoid process was most tedious and timeconsuming, but the key of the surgery was to provide a sufficient working area around the target cerebral arteries. FIG. 1. Extent of rongeuring of the bones comprising the skull base for an anterior transsphenoidal approach. A = area rongeured for exposure of the anterior part of the circle of Willis; BS = basisphenoid; PS = presphenoid; PT = pterygoid; Pa = palatine; Vo = vomer; B = rongeuring extended to expose the basilar artery; Oc = occipital. ]08 J. Neurosurg. / Volume 41 / July, 1974

3 Exposure of the anterior part of the circle of Willis After the anastomosis between the right and left ophthalamic veins had been obliterated by clipping or by coagulation with weak current, the dura mater was opened at the midline from the preoptic region to just before the intercavernous sinus, and retracted with thread. Removal of a small segment of both optic nerves was necessary to expose both anterior cerebral arteries. Gentle excision of the arachnoid covering the arteries completed the exposure of the anterior part of the circle of Willis. With this anterior transsphenoidal exposure both sides of the intracranial internal carotid arteries, the first portion of both sides of the middle cerebral arteries, both sides of the anterior cerebral arteries and their branches (i.e., the internal ophthalmic and internal ethmoidal arteries), and the anterior communicating artery and its small branches were clearly visible (Fig. 2). When the pituitary gland was pushed slightly aside, the bilateral posterior communicating arteries could also be seen. In three of the dogs, the basilar artery was also exposed by rongeuring caudally (Fig. 1) and splitting the intercavernous sinus. This part of the technique was essentially the same as that previously described by Iwabuchi and Himwich. 7 Fro. 2. Operative photograph of the anterior part of the circle of Willis exposed by an anterior transsphenoidal approach in the dog. Orientation diagram is below. J. Neurosurg. / Volume 41 / July, 1974 ]09

4 S. Hori and W. A. Himwich The exposure of the anterior part of the circle of Willis required from 4 to 5 hours. Monitoring of the systemic pressure was begun 45 to 90 min after the first injection of sodium pentobarbital when the dog s condition was judged to be stabilized, and was continued during the remaining surgical period. In 11 of the 82 dogs, decreases in the average mean systemic pressure from 137 to 120 mm Hg (-12%), in the average systemic pulse pressure from 51 to 49 mm Hg (-3%), and in the average pulse rate from 162 to 157/min (-3%) were noted over this period. Technical Comment In the majority of our dogs, the anterior communicating artery was a single longitudinal segment, 18 while a transverse bridgelike anterior communicating artery, which is common in man, was found in only five of the 82. Although this longitudinal segment, which had an outer diameter of 0.6 to 1.8 mm, was long enough (3 to 4 mm) so that a small pressure probe, or cannula, could be applied to it, in about one-fourth of the dogs a lack of space around the artery made it difficult to place even a miniaturized flow probe* on it. On the other hand, the anterior cerebral artery had a segment free of side branches between its branches, the internal ethmoid and perforating arteries, around which there was usually enough room to apply either a flow or a pressure probe. The outer diameter of this segment was about 0.5 to 1.2 mm. Attempts to measure either flow or pressure were unsuccessful in two of 74 dogs because the arteries were so tiny. It has been reported that in man one of the anterior cerebral arteries often has a greater diameter than the other, I~ particularly in patients with an aneurysm of the anterior communicating artery. TM The size of the anterior cerebral arteries was determined grossly immediately after their exposure in 61 of our dogs: in 33 there was no difference between the right and left, in 25 a *Model Ep-703 miniaturized flow probe manufactured by Electromagnetic Probe Company, 836 South Broad Street, Winston-Salem, North Carolina slight difference, and in three a distinct difference. No side preference was noted. Among the various types of dogs used in our experiments, the mesaticephalic, especially the beagle or basset hound, was felt to be preferable from the surgical point of view, because of its relatively wide skull base and soft bones. On the contrary, exposure was rather difficult and more timeconsuming in dogs of the collie type because of the narrow skull base and "crisp" bones. Special care was taken to avoid unnecessary mechanical stimulation of the arteries and to prevent contamination of the subarachnoid space with blood. With such precautions segmental vasoconstriction was not significant in any of the anterior communicating and anterior cerebral arteries exposed and observed throughout our experiments, although segmental vasodilatation was common among those arteries that were squeezed into an electromagnetic flow probe with a very small mouth. Discussion Reports dealing with exposure of the anterior part of the circle of Willis in experimental animals are difficult to find in the literature. The various approaches to the sellar region, such as fronto-ethmoid-sphenoidal, oronasal rhinoseptal, transethmoidsphenoidal or their many modifications, practiced in man have been recently reviewed by Decker and Malls. x The approach most frequently used is probably that of temporal craniotomy. In a preliminary study we used this approach in an attempt to expose the anterior cerebral and anterior communicating arteries. However, it was difficult to make enough room to apply either a flow or pressure probe to the arteries, particularly to the anterior communicating artery, unless the brain was subjected to extreme retraction. Ohta and Baldwin 14 exposed the anterior part of the circle of Willis in cats through an opening in the calvarium in order to stimulate the vessels. But even with their microtechnique the anterior part of the corpus callosum and caudate nucleus and adjacent brain substance had to be removed. Iwabuchi and Himwich 9 have described a technique to 1 0 J. Neurosurg. / Volume 41 / July, 1974

5 Exposure of the anterior part of the circle of Willis expose, in addition to the basilar artery, the entire circle of Willis in the dog by extending the rongeuring of the base of the skull anteriorly from the foramen magnum and splitting the intercavernous sinus. We adopted the technique described because it was mandatory in our experiments to provide an ample operative field in order to apply a flow or pressure probe to the arteries and to facilitate occlusive procedures on either side of the circle of Willis without distorting and pulling the arteries. The exposure described here does not require either splitting the intercavernous sinus, which can result in copious bleeding, or any retraction of the brain. Furthermore, if only the region in the vicinity of the anterior communicating artery is of interest, rongeuring of the base of the skull can be reduced to a small area around the tuberculum sellae, and the artery can be easily exposed by pushing aside the bilateral optic nerves instead of cutting them out. Freeing of the mandible can be eliminated, and the entire surgical procedure will be considerably shortened. The observation that no obvious segmental vasoconstriction was elicited in the anterior communicating or anterior cerebral arteries in our experiments is of interest in regard to the vasoreactivity of those vessels in the dog. It is well known that mechanical stimulation or contact with blood easily causes vasospasm in the basilar artery in the dog or cat. 8,4,~a However, the question of vasospasm in the anterior cerebral or anterior communicating arteries in the dog still seems debatable. It has been reported that the introduction of blood into the basal subarachnoid space in monkeys 2,2~ and dogs 2~ causes a rather diffuse spasm of the intradural arterial tree on angiograms. However, angiographical verification of spasm occurring exclusively in the anterior cerebral or anterior communicating arteries would be difficult, particularly when spasm was not segmental but diffuse, partly because if the major afferent arteries to the anterior circulation (mainly the internal carotid and basilar arteries) become spastic, diffuse reduction of the caliber of the anterior arterial tree will be clearly shown on angiograms. Pool, et al., ~5 reported spasm caused by mechanical stimulation of the intracranial internal carotid artery in dogs. Ohta and Baldwin 14 showed that, in cats, stroking the middle and anterior cerebral arteries close to the internal carotid produced local vasoconstriction when the stroke was parallel to the long axis of the vessel, and vasodilatation when it was at right angles to the vessel. Although the inevitable mechanical stimulation when the artery was put into either a flow or pressure probe consisted of forces both parallel and at right angles to the artery, neither the anterior communicating artery nor the segment of the anterior cerebral artery between the internal ethmoidal and the anterior communicating arteries showed vasoconstriction although they were under continuous observation. Suzuki s statement TM that he preferred to use cats rather than dogs in studying bloodinduced vasospasm because in dogs the spasm was elicited only in the basilar arteries may support our observation. Further studies on vasoreactivity in the anterior part of the circle of Willis, including observations under direct vision, will be necessary to elucidate this problem. References 1. Decker RE, Malis LI: Surgical approaches to midline lesions at the base of the skull: A review. Mount Sinai J Med (New York) 30:84-102, Echlin FA: Experimental vasospasm, acute and chronic, due to blood in the subarachnoid space. J Neurosurg 35: , Echlin FA: Spasm of basilar and vertebral arteries caused by experimental subarachnoid hemorrhage. J Neurosurg 23:1-11, Fukuyama GS, Hirnwich WA: Canine basilar arterial flow and effects of common carotid occlusion. Amer J Physiol 219: , Hirnwich WA, Clark ME: Cerebral blood flow comparisons between model and prototype. J Appl Physiol 31: , Himwich WA, Spurgeon HA: Pulse pressure contours in cerebral arteries. Acta Neurol Scand 44:43-56, Iwabuchi T, Himwich WA: External vertical cannulation of arteries without available side branches. J Appl Physiol 28: , Iwabuchi T, Himwich WA: Pressure in posterior communicating artery as influenced by carotid artery occlusion. Amer J Physiol 221: , Iwabuchi T, Himwich WA: Technique for exposure of the entire circle of Willis in the 1. Neurosurg. / Volume 41 / July, 1974 ] ] ]

6 S. Hori and W. A. Himwich dog, technical note. J Neurosurg 31: , Knapp FM, Mitchell WK, Himwich WA: Measurement of basilar and vertebral arterial pressures in the dog. Life Sei 4: , Krayenbiihl HA, Yasargil MG: Cerebral Angiography. Philadelphia, J. B. Lippincott Co., 1968, ed. 2, p Kwak R, Takahashi M, Suzuki J: (Anterior communicating artery aneurysm and the blood circulation at the anterior part of the circle of Willis and its vascular anomalies.) Brain Nerve (Tokyo) 22: , 1970 (Jap) 13. Miller ME, Christensen GC, Evans HE: Anatomy of the Dog. Philadelphia/London, W. B. Saunders Co., Obta T, Baldwin M: Experimental mechanical arterial stimulation at the vircle of Willis. J Neurosurg 28: , Pool JL, Jacobson S, Fletcher TA: Cerebral vasospasm--clinical and experimental evidence..iama 167: , Sahs AL, Perret GE, Locksley HB, et al (eds): Intraeranial Aneurysm and Subarachnoid Hemorrhage. Philadelphia/Toronto, J. B. Lippincott Co., 1969, p Suzuki J, Hori S, Sakurai Y: Intracranial aneurysms in the neurosurgical clinics in Japan. J Neurosurg 35:34-39, Suzuki S" Experimental study of cerebral vasospasm--vasospasm of the circle of Willis. Brain Nerve (Tokyo) 22: , 1970 (Jap) 19. Tanaka T: Cerebral angiospasm. An experimental study of the intracranial vertebrobasilar system. Advances Neurol Sei (Tokyo) 12: , Weir B, Erasmo R, Miller J, et al: Vasospasm in response to repeated subarachnoid hemorrhages in the monkey. J Neurosurg 33: , Wilkins RH, Levitt P: Intracranial arterial spasm in the dog. A chronic experimental model..l Neurosurg 33: , 1970 Present address for Dr. Hori: Division of Neurosurgery, Institute of Brain Diseases, Tc~hoku University, Nagamachi, Sendal, Kiyagi-ken, Japan. Address reprint requests to: Williamina A. Himwith, Ph.D., Nebraska Psychiatric Institute, University of Nebraska College of Medicine, 602 South 44th Avenue, Omaha, Nebraska ] ]2 J. Neurosurg. / Volume 41 / July, 1974