Hemodynamics in the Anterior Part of the Circle of Willis in Patients with Intracranial Aneurysms : A Study by Cerebral Angiography

Tohoku J. exp. Med., 1980, 132, 69-73 Hemodynamics in the Anterior Part of the Circle of Willis in Patients with Intracranial Aneurysms : A Study by Cerebral Angiography RYUNGCHAN KWAK, HIROSHI NIIZUMA and JIRO SUZUKI Division of Neurosurgery, Institute of Brain Diseases, Tohoku University School of Medicine, Sendai 980 KWAK, R., NIIZUMA, H. and SUZUKI, J. Hemodynamics in the Anterior Part of the Circle of Willis in Patients with Intracranial Aneurysms: A Study by Cerebral Angiography. Tohoku J. exp. Med., 1980, 132 (1), 69-73 - Cerebral angiography revealed that hypoplasia of the Al portion of the anterior cerebral artery is more frequent in patients with aneurysms of the anterior communicating artery than in those with aneurysms of other intracranial arteries. As for the hypoplasia of the Al, the angiographic findings corresponded to the surgical findings in 86.9% of all the patients. In patients with anterior communicating artery aneurysms, the incidence of hypoplasia of the A. portion was about 3 times higher on the right side than on the left side. intracranial aneurysms; hemodynamics; circle of Willis; cerebral angiography; hypoplasia of AI portion of anterior cerebral artery Most cerebral aneurysms occur in the circle of Willis. Furthermore, it is pointed out that such aneurysms often accompany anomalies or abnormal blood circulation in the circle of Willis (Busse 1921; Jacques 1926; Riggs and Rupp 1942; Kameyama 1961). We have already reported that an anomaly or abnormal blood circulation in the anterior part of the circle of Willis is observed in about 80% of patients with aneurysms of the anterior communicating artery, and that hypoplasia of the Al of the anterior cerebral artery is present on the right side in about 80% (Kwak and Suzuki 1974). We performed cerebral angiography on 1,000 patients to whom direct intracranial surgery had been done and found that abnormal blood circula tion in the anterior part of the circle of Willis is specifically frequent in patients with aneurysms of the anterior communicating artery. SUBJECTS AND METHODS Of 1,000 patients with direct intracranial surgery that we had carried out from June 1961 to September 1975, there were 485 subjects, 279 males and 206 females, in whom at Received for publication, July 16, 1979. Reprint Requests: Dr. Ryungchan Kwak, Department of Neurosurgery, Kanazawa Medical University, Uchinada-machi, Kahoku-gun, Ishikawa-ken 920-02. 69

70 R. Kwak et al. least bilateral carotid angiography had been done and data had been preserved completely. 162 patients with multiple aneurysms were excluded from this study. Patients aged between thirties and sixties occupied about 95% of all the patients. The youngest patient was 18 years old, and the oldest one was 72 years old. Sites of the aneurysms were the anterior communicating artery in 213 patients, the internal carotid artery in 134 patients, the middle cerebral artery in 97 patients, the anterior cerebral artery in 28 patients and the vertebro-basilar artery in 13 patients. Control subjects were 76 patients who visited our Department from 1970 to the end of 1975 and who had had bilateral carotid angiography. These patients included 66 with epilepsy and 10 with hysteria which had been finally diagnosed. Patients with intracranial space-occupying lesions were excluded from this study. The control patients consisted of 51 males and 25 females, who were younger in general than patients with cerebral aneurysms, that is, the youngest was 4 years old, and the oldest was 57 years old. In all patients studied, contrast medium was injected neither into the intramural region nor into the extravasal space. All the angiograms were well visualized from the internal carotid artery to the intracranial peripheral vessels. x-ray films having different magnifica tions were adjusted to a given magnification for observation. From cerebral angiographic and surgical findings, more than two times difference in the diameter between the left and right A, portions of the anterior communicating artery was regarded as hypoplasia of a unilateral Al. Based upon the method described in the previous paper, the vascular narrowing due to hypoplasia of the A, was distin guished from that due to arteriosclerosis or that due to cerebral vasospasm. That is, in patients with hypoplasia of the A the Al was constantly narrow from the origin to the anterior communicating artery. In patients with vasospasm, the vascular diameter was unequal. In patients with arteriosclerosis, moth-eaten narrowing was observed. In the patients with hypoplasia of the Al or arteriosclerosis, the status of angiograms taken at various times was the same. However, the status of angiograms was various from time to time in patients with vasospasm. Patients in whom evaluation was impossible by this method were ruled out from this study. RESULTS Cerebral angiographic findings of hypoplasia of the A, of the anterior cerebral artery Cerebral angiography revealed that the hypoplasia of a unilateral Al was present in 145 of 213 patients with aneurysms of the anterior communicating artery (68.1%), in 39 of 134 patients with aneurysms of the internal carotid artery (29.1%), in 33 of 97 patients with aneurysms of the middle cerebral artery (34.0%), in 13 of 28 patients with aneurysms of the anterior cerebral artery (46.4%), in 1 of 13 patients with aneurysms of the vertebro-basilar artery (7.7%), and in 22 of 76 control patients (28.9%) (Table 1). The difference between patients with aneurysms of the anterior communicating artery and those with aneurysms of the anterior cerebral artery was statistically significant (p<0.05), and furthermore, the difference between patients with aneurysms of the anterior communicating artery and those with aneurysms of other intracranial arteries or control patients was highly significant (p<0.005). The incidence of hypoplasia of the right Al was compared with that of hypoplasia of the left A1 in patients with cerebral aneurysms in various sites by cerebral angiography. In all patients, the hypoplasia of the A1 was more frequent on the right side than on the left side. The ratio of hypoplasia of the left Al to

Hemodynamics in Intracranial Aneurysms 71 TABLE 1. Incidence of angiographic hypoplasiaa of the A, portion ACom, anterior communicating artery; IC, internal carotid artery; MC, middle cerebral artery; AC, anterior cerebral artery; V-B, vertebro-basilar artery. that of the right Al was 1:3.0 in patients with aneurysms of the anterior com municating artery, 1:1.6 in patients with aneurysms of the internal carotid artery, 1:2.0 in patients with aneurysms of the middle cerebral artery, and 1:5.5 in patients with aneurysms of the anterior cerebral artery. In patients with aneurysms of the vertebro-basilar artery, the case of hypoplasia of the left A, was none and that of the right Al was one. In control patients, it was 1:1.2. From the statistical point of view, hypoplasia not only in the right A, but also in the left A, was also much more frequent in patients with aneurysms of the anterior communicating artery than in those with aneurysms of other intracranial arteries and than in control patients, except in those with aneurysms of the anterior cerebral artery. Difference in the hypoplasia of the A, of the anterior cerebral artery between cerebral angiographic and surgical findings In 191 patients with aneurysms of the anterior communicating artery in whom the bilateral A, portions of the anterior cerebral artery was confirmed and the diameter could be compared at the time of surgery, a comparative study was made on differences in the hypoplasia of the Al between cerebral angiographic and surgical findings. TABLE 2. Angiographic and surgical findings of hypoplasiaa of A, portion in patients with aneurysm of the anterior communicating artery * The agreement between angiographic and operative findings is 166/191 (86.9%).

72 R. Kwak et al. Of 96 patients with angiographic findings of hypoplasia of the right Al, surgical findings also showed it in 80 patients (83%), but did not show it in the remaining 16 patients (17%). On the other hand, of 34 patients with angiographic findings of hypoplasia of the left Al, surgical findings also showed it in 26 patients (77%), but did not show it in the remaining 8 patients (24%). Of 61 patients without angiographic finding of hypoplasia of Al, surgical findings showed it in only one patient (2%), but did not show it in the other 60 patients (98%). To sum up, angiographic findings were in accordance with surgical findings in 166 of the 191 patients (87%) (Table 2). DISCUSSION There are various theories concerning the cause of cerebral aneurysm; aplasia of the media (Forbus 1930; Suzuki and Ohara 1978), residual blood vessels at the fetal period (Bremer 1943), abnormal genesis of the blood vessels (Dandy 1944; Padget 1944; Walton 1956), and degeneration of the vascular walls (Walker and Allergre 1954). As already pointed out (Kwak and Suzuki 1974), it seems that an abnormal blood circulation or an abnormality in the anterior part of the circle of Willis is often associated in patients with aneurysms of the anterior communicating artery. In addition, cerebral aneurysms seem to occur by a constant action of higher blood pressure at the bifurcation of the blood vessels, where the aplasia of the media is present, than at its surrounding blood vessels. From this aspect, the fact that aneurysms of the anterior communicating artery often accompany the abnormal blood circulation in the anterior part of the circle of Willis is con sidered to be very important. Cerebral angiography evidently revealed that hypoplasia of a unilateral Al is much more frequent in patients with aneurysms of the anterior communicating artery than in those with aneurysms of other in tracranial arteries and in control patients. These findings almost correspond to those on 96 patients with aneurysms of the anterior communicating artery (Kwak and Suzuki 1974). The incidence of abnormal blood circulation in the anterior part of the circle of Willis is significantly higher on the right side than on the left side. The cause has yet been unsolved. However, this fact suggests that the left carotid angiography with a higher frequency of discovery of aneurysm should first be undertaken in patients with subarachnoid hemorrhage, especially in patients who are suspected of having aneurysms of the anterior communicating artery. As already reported (Endo et al. 1973), the above findings are important for diagnosis of aneurysm of the anterior communicating artery which is not visualized by angiography. In addition, those findings are also considered to be important for surgical approach to aneurysm of the anterior communicating artery. That is, the interruption of the cerebral blood flow on the side of the dominant unilateral A l i s important for the procedure of the neck of aneurysm, in order to prolong the interruption and to prevent the rupture of the aneurysm.

Hemodynamics in Intracranial Aneurysms 73 References 1) Bremer, J.L. (1943) Congenital aneurysms of the cerebral arteries. An embryologic study. Arch. Path., 35, 819-831. 2) Busse, 0. (1921) Aneurysmen and Bildungsfehler der Arteria commuincans anterior. Virchows Arch., 229, 178-206. 3) Dandy, W.E. (1944) Intracranial Arterial Aneurysms. N.Y. Comstock Publishing Co., Ithaca. 4) Endo, S., Kwak, R. & Suzuki, J. (1973) Non-filling ruptured aneurysm of anterior communicating artery: Report of two operated cases. Brain Nerve, 25, 905-909. (Japanese) 5) Forbus, W.D. (1930) On the origin of miliary aneurysm of the superficial cerebral arteries. Bull. Johns Hopkins Hosp., 47, 239-284. 6) Jacques, J. (1926) Aneurysm and anomaly of the circle of Willis. Arch. Path., 1, 213-220. 7) Kameyama, M. (1961) Clinico-pathological meaning of the variation of arteries in base of brain. Advanc. neural. Sci., 5, 758-767. (Japanese) 8) Kwak, R. & Suzuki, J. (1974) Correlation of anterior communicating artery aneurysm with blood circulation at the anterior part of the circle of Willis and its vascular anomalies. Phronesis, 11, 407-417. 9) Padget, D.H. (1944) The circle of Willis, its embryology and anatomy. In: Intracranial Aneurysms, edited by W.E. Dandy, N.Y. Comstock Publishing Co., Ithaca. 10) Riggs, H.E. & Rupp, C. (1942) Miliary aneurysms: Relation of anomalies of the circle of Willis to aneurysm formation. J. Neuropath. exp. Neurol., 1, 442. 11) Suzuki, J. & Ohara, H. (1978) Clinicopathological study of cerebral aneurysms. J. Neurosurg., 48, 505-514. 12) Walker, A.E. & Allergre, G.W. (1954) The pathology and pathogenesis of cerebral aneurysms. J. Neuropath. exp. Neurol., 13, 248-259. 13) Walton, J.N. (1956) Subarachnoid Haemorrhage. Livingstone, London.