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Ruptured cerebral aneurysms associated with arterial occlusion
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Surg Neurol 1983;20:4-12
Ruptured Cerebral Aneurysms Associated with Arterial Occlusion Masayuki Matsuda, M.D., Jyoji Handa, M.D., Akira Saito, M.D., Isao Matsuda,* M.D., and Yoshinari Kamijyo,t M.D. Department of Neurosurgery, Shiga University of Medical Science, Seta, Ohtsu, Shiga-ken, Japan
Matsuda M, Handa J, Saito A, Matsuda I, Kamijyo Y. Ruptured cerebral aneurysms associated with arterial occlusion. Surg Neurol 1983;20:4-12.
Seven cases of ruptured cerebral aneurysm associated with an occlusion of a large cerebral artery are reported. All seven patients had never suffered from ischemic cerebrovascular disease before the aneurysmal rupture. All nine aneurysms, including the two unruptured ones, arose on the artery serving as an important collateral pathway, and eight of the nine were found in locations where saccular aneurysms are known to occur infrequently. The role of hemodynamic factors in the pathogenesis of these aneurysms is stressed. KEYWORDS: Arterial occlusion; Cerebral aneurysm; Cerebral artery; Collateral circulation; Hemodynamic factor; Pathogenesis
The pathogenesis of saccular aneurysm of the brain has been a controversial issue for the past several decades [1,2,6,24,28,37]. Glynn [8] reported the presence of medial defects in normal cerebral arteries, and he also showed that arteries with such medial defects did not necessarily yield to increased intraluminal pressure. Stehbens [32] also found medial defects in the bifurcation of normal cerebral arteries, but their anatomic distribution failed to conform to the sites of predilection of cerebral aneurysms. In autopsy specimens, C r o m p t o n [4] found that medial defects and changes of the internal elastic lamina in forks of the cerebral arteries were present even in neonates. Such changes, however, gradually increased in number, size, and severity with aging of the subject. H e further noted that sizable medial defects are Address reprint requests to: Masayuki' Matsuda, M.D., Department of Neurosurgery, Shiga University of Medical Science, Seta, Ohtsu, 520-21 Shiga-ken, Japan. *Present address: Department of Neurosurgery, Noe Saiseikai Hospital, Osaka, Japan. tPresent address: Department of Neurosurgery, Ohtsu Red Cross Hospital, Ohtsu, Japan.
© 1983 by Elsevier Science Publishing Co., Inc.
more numerous and structural changes in the intima and elastic tissue more marked in patients with cerebral aneurysms compared to control subjects without aneurysms. All of these reports seem to indicate that the presence of medial defects and changes of the elastic tissue are not sufficient conditions for the d e v e l o p m e n t of cerebral aneurysms, and an important role of hemodynamic forces has been stressed by Fergusson [5], Hassler [13], Shenkin et al [29], and others [3,7,9, 11,14,18,19,30,31,36]. In this paper, we report seven patients in whom hemodynamic factors are considered to have played an important role in the growth and rupture of an aneurysm, and probably in its formation as well.
Case Reports Clinical data on our patients are summarized in Table i. The main trunk of the middle cerebral artery was occluded in four patients. In one, the contralateral internal carotid artery was also occluded distal to the origin of the posterior communicating artery; in another, the middle cerebral arteries were occluded bilaterally. T h e internal carotid artery was occluded proximal to the carotid siphon in the remaining three patients. N o n e of these seven patients had experienced cerebral ischemic attacks before the aneurysmal rupture. At least five patients were known to be hypertensive. T w o patients (patients 5 and 6) were treated at an outside hospital, and their angiograms were made available to us for the preparation of this paper; the details of their clinical histories, however, remain obscure. The aneurysms were found on the posterior cerebral artery in all three patients with an internal carotid occlusion, whereas the sites of the aneurysms varied in patients with an occlusion of the middle cerebral artery. 0090-3019/83/$3.00
Aneurysm With Arterial Occlusion
A
F i g u r e 1. Patient 1. (A) Frontal projection of angiogram of the right carotid artery, showing a small aneurysm of the distal internal carotid artery (arrowhead). (B) Frontal and (C) lateral projection of angiogram of the left carotid artery, showing a total occlusion of the middle cerebral artery and an aneurysm arising from the anterior branch of the lateral posterior choroidal artery (arrowheads). (D) Frontal projection of angiogram of the left carotid artery 4 weeks later, showing an enlargement of the aneurysm (arrowhead).
Surg Neurol 1983;20:4-12
5
B
Table 1. Pertinent Clinical Data of Seven Patients Case
Age (yr)
Sex
1
51
F
Left MCA
2
54
F
Right MCA
55
F
Bilateral MCAs
47
M
Patient 1
3
A 51-year-old woman with a verified intraventricular hemorrhage was transferred to us 18 days after the onset of clinical symptoms. She had experienced severe headaches 15 years previously. A subarachnoid hemorrhage was suspected, but an angiographic study was not done at that time. She had been known to be hypertensive and had been receiving medication for it for the preceding 10 years. On admission the patient was disoriented, and a right hemiparesis, right homonymous hemianopia, and Gerstmann's syndrome were present. A computed tomography (CT) scan obtained on the day of onset showed
4
Site of occlusion
5 6
46
F
Right MCA and left ICA, distal Right ICA, proximal
66
F
Right ICA, proximal
7
53
F
Left ICA, proximal
Location of aneurysm Left lateral posterior choroidal artery, right I C A - A C A junction ~ Right MCA, cortical branch Right MCA, cortical branch ACoA Right P C A - P C o A junction Right P C A - P C o A junction Basilar bifurcation, left PCA, peduncular segment~
Abbreviations: yr = years; F = female; MCA = middle cerebral artery; ICA = internal carotid artery; ACA = anterior cerebral artery; M = male; ACoA = anterior communicating artery; PCA ~ posterior cerebral artery, PCoA = posterior communicating artery. *Unruptured aneurysm.
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Surg Neurol 1983;20:4-12
C
an intraventricular hemorrhage, m o r e marked in the left lateral ventricle. Angiography of the carotid artery showed an occlusion at the origin of the left middle cerebral artery. Distal branches of the left middle cerebral artery were filled with contrast medium via fine vascular networks, and an aneurysm was found in the anterior branch of the left lateral posterior choroidal artery. This aneurysm was thought to be the source of the bleeding. T h e r e was no arterial occlusion in the right carotid system, but a small aneurysm was found on the medial side of the terminal portion of the right internal carotid artery, where the anterior cerebral artery originated (Figures 1A-C). Although the patient's neurological condition remained unchanged during the succeeding 4 weeks, the aneurysm of the left lateral posterior choroidal artery was found to have enlarged markedly (Figure 1D). The aneurysm was excised through a left temporal cortical incision, and an encephalomyosynangiosis [ 16] was performed in an attempt to improve the collateral blood flow to the ischemic left cerebral hemisphere. The aneurysm was found in the left temporal horn, partially e m b e d d e d in the choroid plexus. Histologically, it was
Matsuda et al
D
a true saccular aneurysm. The small aneurysm on the right side was left untouched. The patient was discharged with a residual right h o m o n y m o u s hemianopia and Gerstmann's syndrome.
Patient 2 A 54-year-old woman was admitted with the complaint of severe headaches and a left h o m o n y m o u s hemianopia. She had been treated for hypertension for the preceding 10 years. A C T scan obtained on admission disclosed a right occipital subcortical hematoma. Cerebral angiography showed an occlusion of the right middle cerebral artery at its origin. A small aneurysm was found in one of the small cortical branches of the right middle cerebral artery. The parent artery was filled with contrast m e d i u m from the posterior cerebral artery in a retrograde fashion (Figure 2). This aneurysm was considered to be the source of the hematoma. The hematoma was evacuated and the aneurysm was resected. The patient was discharged with a residual left h o m o n y m o u s hemianopia. Histologic examination of the excised aneurysm confirmed that it was a true saccular aneurysm. The d o m e
Aneurysm With Arterial Occlusion
Surg Neurol 1983;20:4-12
7
of the aneurysm pointed anteriorly; its neck was located more posteriorly. The direction of the aneurysm (from the neck toward the dome) was therefore opposite to the anatomic course of the parent artery; however, it was in keeping with the direction of the blood flow through the parent artery, as the direction of the blood flow had been reversed in this particular patient (Figure 3).
Patient 3
A
A 55-year-old woman with sudden onset of severe headaches was admitted. She had been treated for hypertension for 3 years. A C T scan showed a subarachnoid hemorrhage. Cerebral angiograms revealed an occlusion of the middle cerebral arteries immediately distal to the origin of the anterior temporal branch on each side. In addition an aneurysm was found arising from the anterior cerebral artery at the origin of the accessory middle cerebral artery. The aneurysm was successfully clipped. At operation, the right middle cerebral artery distal to the origin of the anterior temporal branch looked like a thin fibrous cord. The patient was discharged with no neurological deficit. This case has been reported elsewhere [10].
Patient 4
B
A 47-year-old man suddenly experienced severe headaches. Angiography of the right carotid artery disclosed an occlusion of the right middle cerebral artery distal to the origin of the anterior temporal branch, an aneurysm of the anterior communicating artery, contrast medium enhancement of both pericallosal arteries via a dominant right A1 segment, and enhancement of the left middle cerebral branches via the basal vascular networks without opacification of the left A1 segment. Angiography of the left carotid artery showed an occlusion of the left internal carotid artery immediately distal to the origin of the posterior communicating artery. The aneurysm was successfully clipped. The patient was discharged without neurological deficit. He had been known to be hypertensive for the preceding 5 years, but had received no medication for it.
Patient 5
Figure 2. Patient 2. (A) Lateral projection of angiogram of the right carotid artery, showing a total occlusion of the middle cerebral artery and a small peripheral aneurysm in the parietooccipital region. (B) Magnified view of (A). The cortical branch of the middle cerebral artery (small arrowheads) was filled with contrast medium from the posterior cerebral branch (large arrowhead) via a leptomeningeal anastomosis. The curved arrow indicates the direction of bloodflow through the parent artery.
A 46-year-old woman suddenly complained of severe headaches and lost consciousness. Cerebral angiography showed an occlusion of the extracranial portion of the right internal carotid artery and an aneurysm at the junction of the right posterior cerebral and posterior com-
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Figure 3. Photomicrograph of a longitudinal section of the aneurysm. P indicates the proximal side, D the distal side of the parent artery. The direction of bloodflow through this segment of the artery is reversed (from D to P, arrow), as the middle cerebral artery is occluded and the segment is supplied from the posterior cerebral branch via a leptomeningeal anastomosis. The direction of the aneurysm (from the neck toward the dome) i~ in keeping with the direction of bloodflou, (H & E).
municating arteries (Figure 4). The aneurysm was successfully clipped, but the patient died. Autopsy was not permitted.
Patient 6 A 66-year-old woman with sudden onset of severe headaches was admitted. Cerebral angiography showed an occlusion of the right internal carotid artery in its proximal portion and an aneurysm at the junction of the right posterior cerebral and posterior communicating arteries. She died ofrebleeding a few days later. Autopsy was not permitted.
Matsuda et al
Patient 7 A 53-year-old woman presented with sudden onset of severe headaches and disturbance of consciousness. A CT scan made on the day of onset showed a subarachnoid hemorrhage. At angiography the left internal carotid artery was not opacified from its origin up to the siphon. T h e terminal portion of the left internal carotid artery and its distal branches were filled with contrast medium from the vertebrobasilar system by way of an enlarged posterior communicating artery. The right carotid system was normal. Two aneurysms were found, one at the basilar bifurcation and the other at the peduncular segment of the left posterior cerebral artery (Figure 5). Both aneurysms were successfully clipped. At operation, the proximal portion of the left internal carotid artery was found to be fibrotic up to the origin of the posterior communicating artery. The aneurysm of the posterior cerebral artery was apparently unruptured. Postoperatively a left oculomotor palsy was noted, but it resolved in 2 months. The patient had been treated for hypertension for 10 years.
Aneurysm With Arterial Occlusion
A Figure 4. Patient 5. (A) Frontal and (B) lateral projection of right vertebral angiogram, showing an aneurysm of the right posterior cerebral artery at the junction with the posterior communicating artery (arrows).
Discussion All seven patients reported herein had had no known cerebral ischemic events before the verified attack of an aneurysmal rupture, and the arterial occlusion was an unexpected finding at angiography. Exact time o f occurrence of the arterial occlusion remains unknown, and it might be argued that the association of an aneurysm and an arterial occlusion is nothing but a coincidence. For several reasons, however, we are more inclined to believe that hemodynamic changes secondary to arterial occlusion played an important role in the formation, further growth, and final rupture of the aneurysms in these patients. Three patients with an occlusion of the middle cerebral artery harbored four aneurysms, one each in the anterior branch o f the lateral posterior choroidal artery, at the junction of the internal carotid artery and the anterior cerebral artery, in the distal branch of the mid-
Surg Neurol 1983;20:4-12
9
B
die cerebral artery, and in the anterior cerebral artery at the origin of the accessory middle cerebral artery. In the fourth patient, in whom the middle cerebral artery and the contralateral distal internal carotid artery were occluded, an anterior communicating aneurysm was present. In the remaining three patients, the internal carotid artery was occluded and the aneurysm was found in the posterior circulation. In two of them an aneurysm was found at the junction of the posterior cerebral and posterior communicating arteries; the third had two aneurysms, one at the basilar bifurcation and the other in the proximal segment of the posterior cerebral artery. All three posterior cerebral aneurysms were found on the side of the carotid occlusion. It should be noted that all of the aneurysms in this series were found in sites at which saccular aneurysms generally develop infrequently [20,35], with the exception of the aneurysm of the anterior communicating artery in patient 4. The parent artery of each ruptured aneurysm had definitely served as an important collateral pathway. None of these patients had ever experienced any ischemic neurological attacks attributable to an arterial occlusion, indicating that the blood flow through the collateral routes
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Surg Neurol 1983;20:4-12
Matsuda et al
A
B
was adequate. Also, at least five of the seven patients were known to have been hypertensive for a long time. It seems plausible, therefore, that the parent vessels of these aneurysms had been exposed to significant hemodynamic stress. Pathologic findings on the aneurysm in patient 2 seem to substantiate further the importance of hemodynamic factors in its formation. The saccular aneurysm is generally known to point in the direction that the blood would flow through its parent artery; namely, its dome should point in the direction of the maximal hemodynamic thrust in the site of its parent artery with preaneurysmal change [25]. In patient 2, the direction of the blood flow through the parent artery had been reversed secondary to the proximal middle cerebral occlusion, and the aneurysm pointed exactly in the direction of the reversed flow via the leptomeningeal anastomosis between the posterior cerebral and middle cerebral arteries. Sayama et al [27] reported two similar cases. In their patients, multiple aneurysms were found in sites at which hemodynamic forces were presumed to be increased as a result of occlusion of the internal carotid artery. In each of their two patients, the initial symptoms were caused by a subarachnoid hemorrhage, and there was no previous history of cerebral ischemic attacks. The role of hemodynamic factors in the pathogenesis of cerebral aneurysms was suggested by Forbus as early as 1930 [6]. In 1961, Hassler [12] and Stehbens [33] suggested that the turbulence of blood flow at the major arterial forks was a likely cause of aneurysmal dilatation. Fergusson [5] negated the idea of turbulence at the apex
Figure 5. Patient 7. (A) Frontal and (B) lateral projection of left vetebral angiogram, showing two aneurysms, one at the basilar bifurcation (1) and the other at the peduncular segment of the left posterior cerebral artery (2). The proximal segment of the left internal carotid artery is occluded." the distal segment is filled with contrast medium from vertebral injection of the dye via the enlarged left posterior communicating artery. of the arterial forks. Based on extensive clinical and experimental studies, however, he stressed the importance of hemodynamically generated forces, such as shear stress, impulse, and pressure, as a cause of focal degeneration of the internal elastic lamina and enlargement of the medial defect at the apices of the major intracranial arterial forks on which the central bloodstream would impinge. According to Fergusson [5], the pulsatile impulse and the pressure head transmitted with each heartbeat would induce an aneurysmal outpouching at the apex with reduced resistance, and the vibration of the wall and the turbulence within the pouch would further promote the degeneration and weakening of the wall, eventually resulting in the growth of a frank saccular aneurysm. Recently, Hashimoto et al [11] demonstrated in rats that an aneurysm could be induced in the proximal segment of the posterior cerebral artery on the side of a ligation of the carotid artery, namely, in the artery with an apparent increase in hemodynamic stress. Patients 5, 6, and 7 in the present series are good clinical examples of these experimental results. Clinical evidence supporting the importance of hemodynamic factors in the development of cerebral aneurysms has been reported repeatedly. Salar and Mingrino [26] reported that 2 of 126 patients with carotid ligation developed a contralateral cerebral aneurysm.
Aneurysm With Arterial Occlusion
Although these authors neglected to consider the influence of hemodynamic changes on aneurysmal development, it should be pointed out that the incidence of 1.6% (2 of 126) in their series might be higher than the estimated incidence of cerebral aneurysm in the general population (1%) [17]. Several other reports, by circumstantial evidence, seem to substantiate the hypothesis that cerebral aneurysms might develop after ligation or spontaneous occlusion of a carotid artery or other cerebral arteries [15,23,26-28,31]. Gurdjian et al [9] reported a 58-year-old woman in whom an internal carotid aneurysm developed 8 years after ligation of the contralateral carotid artery. German and Black [7] described two patients in whom the carotid artery had been ligated to treat an aneurysm of the internal carotid artery. One died of rupture of an aneurysm of the anterior communicating artery 15 years later; the other died of cerebral thrombosis 20 years later, and an unruptured aneurysm was found in the cavernous portion of the contralateral internal carotid artery. Somach and Shenkin [30] report a case in which an aneurysm developed at the junction of the right anterior cerebral and anterior communicating arteries 7 years after ligation of the left common carotid artery. Clark and Ray [3] also reported three cases in which an intracranial aneurysm appeared contralateral to a ligated carotid artery. In cerebral angiograms performed at the time of carotid ligation, no aneurysm other than that treated by the ligation was noted in any of these eight patients. Association of a cerebral aneurysm and a congenital anomaly of the cephalic arteries has also been well documented. Reviewing the literature, Waga et al [36] reported 16 cases, including their own, of intracranial aneurysm associated with absence of the internal carotid artery. Masuzawa et al [21] reported two cases of an intracranial aneurysm associated with a coarctation of the thoracic aorta. In one of them, a saccular aneurysm was found at the junction of the internal carotid and posterior communicating arteries, where no abnormalities had been found on angiography performed 3 years previously. They stressed the importance of abnormal hemodynamic stresses in the development of these aneurysms. According to Stehbens [34], the occurrence of cerebral aneurysms in patients with a coarctation of the aorta could be ascribed to the concomitant hypertension and resultant premature atherosclerosis of the cerebral arteries. McCormick and Schmalstieg [22] found no definitive correlation between hypertension and the development of cerebral aneurysms, and Hashimoto et al [11] demonstrated that hypertension alone failed to induce aneurysms in their experimental models in rats. However, Crompton [4] found that a greater number
Surg Neurol 1983;20:4-12
11
of large medial defects and more marked degenerative changes of the internal elastic lamina were found in the cerebral arteries of hypertensive patients than in those of normotensive control subjects. Therefore, hypertension may well contribute to the formation of cerebral aneurysms by accelerating structural changes and weakening of the arterial wall. Association of a cerebral aneurysm and a cerebral arteriovenous malformation (AVM) has also been described. Shenkin et al [29] reported a patient in whom the aneurysm of a major feeding artery regressed after removal of the AVM. Similar cases have been reported by others [14,19]. Collecting 74 cases of cerebral aneurysms associated with AVMs, Hayashi et al [14] found that 77% had developed in the arteries hemodynamically related to AVMs. All of these clinical reports also seem to lend further support to the hypothesis that the enhanced blood flow and pulsation may well contribute to the enlargement of medial defects and thus to the development and growth of the aneurysms [4]. In conclusion, an occlusion of a cerebral artery results in an alteration of hemodynamics in the remaining cerebral arteries. With the passage of time, the hemodynamically generated forces facilitate weakening of the arterial wall at the sites of structural defects of congenital and/or acquired origin by enlarging the medial defect and degenerating the internal elastic membrane, and lead to the formation and growth of a cerebral aneurysm and finally to its rupture.
References 1. Bremer JL. Congenital aneurysms of the cerebral arteries. Arch Pathol 1943;35:819-31. 2. Carmichael R. The pathogenesis of non-inflammatory cerebral aneurysms. J Pathol Bacteriol 1950;62:1-19 3. Clark WC, Ray MW. Contralateral intracranial aneurysm formation as a late complication of carotid ligation. Surg Neurol 1982;18:458-62. 4. Crompton MR. The pathogenesis of cerebral aneurysms. Brain 1966;89:797-814. 5. Fergusson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg 1972;37:666-77. 6. Forbus WD. On the origin of miliary aneurysms of the superficial cerebral arteries. Bull Johns Hopkins Hosp 1930;47:239-84. 7. German WJ, Black SPW. Cervical ligation for internal carotid aneurysms. An extended follow-up. J Neurosurg 1965;23:5727. 8, Glynn LE. Medial defects in the circle of Willis and their relation to aneurysm formation. J Pathol Bacteriol 1940;51:213-22. 9. Gurdjian ES, Lindner DW, Thomas LM. Experiences with ligation of the common carotid artery for treatment of aneurysms of the internal carotid artery. With particular reference to complications. J Neurosurg 1965;23:311-8. 10. Handa J, Matsuda M, Okamoto K, Kidooka K. Association be-
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tween accessory middle cerebral artery and cerebral aneurysm. Report of two cases. Acta Neurochir (Wien) 1982;64:151-'. 11. Hashimoto N, Handa H. Nagata 1, Hazama F. Experimentally induced cerebral aneurysms in rats: Part V. Relation of hemodynamics in the circle of Willis to formation of aneurysms. Surg Neurol 1980; 13:41-5. 12. Hassler O. Morphological studies on the large cerebral arteries. With reference to the aetiology of subarachnoid haemorrhage. Acta Psychiatr Neurol Stand 196l;36 (Suppl 1541:1-145. 13. Hassler O. Experimental carotid ligation followed by aneurysmal formation and other morphological changes in the circle of Willis. J Neurosurg 1963;20:1-7. 14. Hayashi S, Arimoto T, Itakura T, Fujii T, Nishiguchi T, Komai N. The association of intracranial aneurysms and arteriovenous malformation of the brain. Case report. J Neurosurg 1981;55:9715. 15. Jaffe ME, McHenry LC Jr. Cerebral aneurysm tollowing spontaneous carotid occlusion. Neurology (Minneap) 1968; 18:10124.
16. Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y, Ohnishi H, Taki W. A surgical treatment of "moyamoya" disease. "Encephalo-myo-synangiosis".Neurol Med Chir {Tokyo) 197v; 1v(Pt I/:27-37. 17. Kazmeier F, Voigt HJ. Nervenarzt 1956;27:345. Cited by Heidrich R. Subarachnoid haemorrhage. In: Vinken PJ, Bruyn GW, eds. Handbook of clinical neurology. Vol 12. Vascular diseases of the nervous system, Pt II. Amsterdam: North-Holland, 1972:68204. 18. Klemme WM. Hemorrhage from a previously undemonstrated intracranial aneurysm as a late complication of carotid artery ligation. Case report. J Neurosurg 1977;46:654-8. 19. Koulouris S, Rizzoli HV. Coexisting intracranial aneurysm and arteriovenous malformation. Case report. Neurosurgery 1981;8:219-22. 20. Locksley HB. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section V, Part 1. Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the cooperative study. J Neurosurg 1966;25:219-39. 21. Masuzawa T, Shimabukuro H, Sato F, Furuse M, Fukushima K. The development of intracranial aneurysms associated with pulseless disease. Surg Neurol 1982;17:132-6.
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22. McCormick WF, Schmalstieg EJ. The relationship of arterial hypertension to intracranial aneurysms. Arch Neurol 1977;34:285Z
23. NofzingerJD, Britt LG, Murphey F, PateJW. Unusual treatment of an intracranial aneurysm contralateral to a previous common carotid ligation. A case report. J Neurosurg 1965;22:182-4. 24. Padget DH. The circle of Willis, its embryology and anatomy. In: Dandy WE, ed. lntracranial arterial aneurysms. New York: Comstock, 1944. Cited by Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. Arch Pathol 1963;v5:45 6L 25. Rhoton AL Jr, Fujii K, Saeki N, Perlmutter D, Zeal A. Microsurgical anatomy ofintracranial aneurysms. Pt 1. In: Hopkins LN, Long DM, eds. Clinical management of intracranial aneurysms. New York: Raven Press, 1982:201-43. 26. Salar G, Mingrino S. Development of intracranial saccular aneurvsms. Report of two cases. Neurosurgery 1981 ;8:462-5. 2 ~. Sayama 1, lto Z, Nakajima K, Ohta H, Suzuki A, Kobayashi T. Two cases with multiple aneurysms accompanied by unilateral internal carotid occlusion. Problems in surgical treatment. No Shinkei Geka 1979;7:797-804 (Engl abstr). 28. Sekhar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms. A review. Neurosurgery 1981;8:248-60. 29. Shenkin HA, Jenkins F, Kim K. Arteriovenous anomaly of the brain associated with cerebral aneurysm. Case report.J Neurosurg 19 ~1;34:225-8. ~,0. Somach FM, Shenkin HA. Angiographic end-results of carotid ligation in the treatment of carotid aneurysms. J Neurosurg 1966;2.4:966-34. ~,l. Spalhme A, Cantore G. The role of extracranial carotid abnormalities in the genesis of cerebral aneurysms. J Neurosurg 1981 ;55:693-700. ~,2. Stehbens WE. Medial defects of the cerebral arteries of man. J Pathol Bacteriol 1959;78:1 v9-85. ~ . Stehbens WE. Discussion on vascular flow and turbulence. Neurology (Minneap) 1961 : 1 1:66-7. ~4. Stehbens WE. Cerebral aneurysms and congenital abnormalities. Australas Ann Med 1962~11:11/2-12. ~,5. Suzuki J, Hori S, Sakurai Y. lntracranial aneurysms in the neurosurgical clinics in Japan. J Neurosurg 1971 ;35:34-9. "]6. Waga S, Okada M, Kojima T. Saccular aneurysm associated with absence of the left cervical carotid arteries. Neurosurgery 1978;~ :2//8-12. {-. Walker AE, Allegre GW. The pathology and pathogenesis of cerebral aneurysms.J Neuropathol Exp Neurol 1954; 13:248-59.
Surg Neurol 1983;20:4-12
Ruptured Cerebral Aneurysms Associated with Arterial Occlusion Masayuki Matsuda, M.D., Jyoji Handa, M.D., Akira Saito, M.D., Isao Matsuda,* M.D., and Yoshinari Kamijyo,t M.D. Department of Neurosurgery, Shiga University of Medical Science, Seta, Ohtsu, Shiga-ken, Japan
Matsuda M, Handa J, Saito A, Matsuda I, Kamijyo Y. Ruptured cerebral aneurysms associated with arterial occlusion. Surg Neurol 1983;20:4-12.
Seven cases of ruptured cerebral aneurysm associated with an occlusion of a large cerebral artery are reported. All seven patients had never suffered from ischemic cerebrovascular disease before the aneurysmal rupture. All nine aneurysms, including the two unruptured ones, arose on the artery serving as an important collateral pathway, and eight of the nine were found in locations where saccular aneurysms are known to occur infrequently. The role of hemodynamic factors in the pathogenesis of these aneurysms is stressed. KEYWORDS: Arterial occlusion; Cerebral aneurysm; Cerebral artery; Collateral circulation; Hemodynamic factor; Pathogenesis
The pathogenesis of saccular aneurysm of the brain has been a controversial issue for the past several decades [1,2,6,24,28,37]. Glynn [8] reported the presence of medial defects in normal cerebral arteries, and he also showed that arteries with such medial defects did not necessarily yield to increased intraluminal pressure. Stehbens [32] also found medial defects in the bifurcation of normal cerebral arteries, but their anatomic distribution failed to conform to the sites of predilection of cerebral aneurysms. In autopsy specimens, C r o m p t o n [4] found that medial defects and changes of the internal elastic lamina in forks of the cerebral arteries were present even in neonates. Such changes, however, gradually increased in number, size, and severity with aging of the subject. H e further noted that sizable medial defects are Address reprint requests to: Masayuki' Matsuda, M.D., Department of Neurosurgery, Shiga University of Medical Science, Seta, Ohtsu, 520-21 Shiga-ken, Japan. *Present address: Department of Neurosurgery, Noe Saiseikai Hospital, Osaka, Japan. tPresent address: Department of Neurosurgery, Ohtsu Red Cross Hospital, Ohtsu, Japan.
© 1983 by Elsevier Science Publishing Co., Inc.
more numerous and structural changes in the intima and elastic tissue more marked in patients with cerebral aneurysms compared to control subjects without aneurysms. All of these reports seem to indicate that the presence of medial defects and changes of the elastic tissue are not sufficient conditions for the d e v e l o p m e n t of cerebral aneurysms, and an important role of hemodynamic forces has been stressed by Fergusson [5], Hassler [13], Shenkin et al [29], and others [3,7,9, 11,14,18,19,30,31,36]. In this paper, we report seven patients in whom hemodynamic factors are considered to have played an important role in the growth and rupture of an aneurysm, and probably in its formation as well.
Case Reports Clinical data on our patients are summarized in Table i. The main trunk of the middle cerebral artery was occluded in four patients. In one, the contralateral internal carotid artery was also occluded distal to the origin of the posterior communicating artery; in another, the middle cerebral arteries were occluded bilaterally. T h e internal carotid artery was occluded proximal to the carotid siphon in the remaining three patients. N o n e of these seven patients had experienced cerebral ischemic attacks before the aneurysmal rupture. At least five patients were known to be hypertensive. T w o patients (patients 5 and 6) were treated at an outside hospital, and their angiograms were made available to us for the preparation of this paper; the details of their clinical histories, however, remain obscure. The aneurysms were found on the posterior cerebral artery in all three patients with an internal carotid occlusion, whereas the sites of the aneurysms varied in patients with an occlusion of the middle cerebral artery. 0090-3019/83/$3.00
Aneurysm With Arterial Occlusion
A
F i g u r e 1. Patient 1. (A) Frontal projection of angiogram of the right carotid artery, showing a small aneurysm of the distal internal carotid artery (arrowhead). (B) Frontal and (C) lateral projection of angiogram of the left carotid artery, showing a total occlusion of the middle cerebral artery and an aneurysm arising from the anterior branch of the lateral posterior choroidal artery (arrowheads). (D) Frontal projection of angiogram of the left carotid artery 4 weeks later, showing an enlargement of the aneurysm (arrowhead).
Surg Neurol 1983;20:4-12
5
B
Table 1. Pertinent Clinical Data of Seven Patients Case
Age (yr)
Sex
1
51
F
Left MCA
2
54
F
Right MCA
55
F
Bilateral MCAs
47
M
Patient 1
3
A 51-year-old woman with a verified intraventricular hemorrhage was transferred to us 18 days after the onset of clinical symptoms. She had experienced severe headaches 15 years previously. A subarachnoid hemorrhage was suspected, but an angiographic study was not done at that time. She had been known to be hypertensive and had been receiving medication for it for the preceding 10 years. On admission the patient was disoriented, and a right hemiparesis, right homonymous hemianopia, and Gerstmann's syndrome were present. A computed tomography (CT) scan obtained on the day of onset showed
4
Site of occlusion
5 6
46
F
Right MCA and left ICA, distal Right ICA, proximal
66
F
Right ICA, proximal
7
53
F
Left ICA, proximal
Location of aneurysm Left lateral posterior choroidal artery, right I C A - A C A junction ~ Right MCA, cortical branch Right MCA, cortical branch ACoA Right P C A - P C o A junction Right P C A - P C o A junction Basilar bifurcation, left PCA, peduncular segment~
Abbreviations: yr = years; F = female; MCA = middle cerebral artery; ICA = internal carotid artery; ACA = anterior cerebral artery; M = male; ACoA = anterior communicating artery; PCA ~ posterior cerebral artery, PCoA = posterior communicating artery. *Unruptured aneurysm.
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C
an intraventricular hemorrhage, m o r e marked in the left lateral ventricle. Angiography of the carotid artery showed an occlusion at the origin of the left middle cerebral artery. Distal branches of the left middle cerebral artery were filled with contrast medium via fine vascular networks, and an aneurysm was found in the anterior branch of the left lateral posterior choroidal artery. This aneurysm was thought to be the source of the bleeding. T h e r e was no arterial occlusion in the right carotid system, but a small aneurysm was found on the medial side of the terminal portion of the right internal carotid artery, where the anterior cerebral artery originated (Figures 1A-C). Although the patient's neurological condition remained unchanged during the succeeding 4 weeks, the aneurysm of the left lateral posterior choroidal artery was found to have enlarged markedly (Figure 1D). The aneurysm was excised through a left temporal cortical incision, and an encephalomyosynangiosis [ 16] was performed in an attempt to improve the collateral blood flow to the ischemic left cerebral hemisphere. The aneurysm was found in the left temporal horn, partially e m b e d d e d in the choroid plexus. Histologically, it was
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D
a true saccular aneurysm. The small aneurysm on the right side was left untouched. The patient was discharged with a residual right h o m o n y m o u s hemianopia and Gerstmann's syndrome.
Patient 2 A 54-year-old woman was admitted with the complaint of severe headaches and a left h o m o n y m o u s hemianopia. She had been treated for hypertension for the preceding 10 years. A C T scan obtained on admission disclosed a right occipital subcortical hematoma. Cerebral angiography showed an occlusion of the right middle cerebral artery at its origin. A small aneurysm was found in one of the small cortical branches of the right middle cerebral artery. The parent artery was filled with contrast m e d i u m from the posterior cerebral artery in a retrograde fashion (Figure 2). This aneurysm was considered to be the source of the hematoma. The hematoma was evacuated and the aneurysm was resected. The patient was discharged with a residual left h o m o n y m o u s hemianopia. Histologic examination of the excised aneurysm confirmed that it was a true saccular aneurysm. The d o m e
Aneurysm With Arterial Occlusion
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7
of the aneurysm pointed anteriorly; its neck was located more posteriorly. The direction of the aneurysm (from the neck toward the dome) was therefore opposite to the anatomic course of the parent artery; however, it was in keeping with the direction of the blood flow through the parent artery, as the direction of the blood flow had been reversed in this particular patient (Figure 3).
Patient 3
A
A 55-year-old woman with sudden onset of severe headaches was admitted. She had been treated for hypertension for 3 years. A C T scan showed a subarachnoid hemorrhage. Cerebral angiograms revealed an occlusion of the middle cerebral arteries immediately distal to the origin of the anterior temporal branch on each side. In addition an aneurysm was found arising from the anterior cerebral artery at the origin of the accessory middle cerebral artery. The aneurysm was successfully clipped. At operation, the right middle cerebral artery distal to the origin of the anterior temporal branch looked like a thin fibrous cord. The patient was discharged with no neurological deficit. This case has been reported elsewhere [10].
Patient 4
B
A 47-year-old man suddenly experienced severe headaches. Angiography of the right carotid artery disclosed an occlusion of the right middle cerebral artery distal to the origin of the anterior temporal branch, an aneurysm of the anterior communicating artery, contrast medium enhancement of both pericallosal arteries via a dominant right A1 segment, and enhancement of the left middle cerebral branches via the basal vascular networks without opacification of the left A1 segment. Angiography of the left carotid artery showed an occlusion of the left internal carotid artery immediately distal to the origin of the posterior communicating artery. The aneurysm was successfully clipped. The patient was discharged without neurological deficit. He had been known to be hypertensive for the preceding 5 years, but had received no medication for it.
Patient 5
Figure 2. Patient 2. (A) Lateral projection of angiogram of the right carotid artery, showing a total occlusion of the middle cerebral artery and a small peripheral aneurysm in the parietooccipital region. (B) Magnified view of (A). The cortical branch of the middle cerebral artery (small arrowheads) was filled with contrast medium from the posterior cerebral branch (large arrowhead) via a leptomeningeal anastomosis. The curved arrow indicates the direction of bloodflow through the parent artery.
A 46-year-old woman suddenly complained of severe headaches and lost consciousness. Cerebral angiography showed an occlusion of the extracranial portion of the right internal carotid artery and an aneurysm at the junction of the right posterior cerebral and posterior com-
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Figure 3. Photomicrograph of a longitudinal section of the aneurysm. P indicates the proximal side, D the distal side of the parent artery. The direction of bloodflow through this segment of the artery is reversed (from D to P, arrow), as the middle cerebral artery is occluded and the segment is supplied from the posterior cerebral branch via a leptomeningeal anastomosis. The direction of the aneurysm (from the neck toward the dome) i~ in keeping with the direction of bloodflou, (H & E).
municating arteries (Figure 4). The aneurysm was successfully clipped, but the patient died. Autopsy was not permitted.
Patient 6 A 66-year-old woman with sudden onset of severe headaches was admitted. Cerebral angiography showed an occlusion of the right internal carotid artery in its proximal portion and an aneurysm at the junction of the right posterior cerebral and posterior communicating arteries. She died ofrebleeding a few days later. Autopsy was not permitted.
Matsuda et al
Patient 7 A 53-year-old woman presented with sudden onset of severe headaches and disturbance of consciousness. A CT scan made on the day of onset showed a subarachnoid hemorrhage. At angiography the left internal carotid artery was not opacified from its origin up to the siphon. T h e terminal portion of the left internal carotid artery and its distal branches were filled with contrast medium from the vertebrobasilar system by way of an enlarged posterior communicating artery. The right carotid system was normal. Two aneurysms were found, one at the basilar bifurcation and the other at the peduncular segment of the left posterior cerebral artery (Figure 5). Both aneurysms were successfully clipped. At operation, the proximal portion of the left internal carotid artery was found to be fibrotic up to the origin of the posterior communicating artery. The aneurysm of the posterior cerebral artery was apparently unruptured. Postoperatively a left oculomotor palsy was noted, but it resolved in 2 months. The patient had been treated for hypertension for 10 years.
Aneurysm With Arterial Occlusion
A Figure 4. Patient 5. (A) Frontal and (B) lateral projection of right vertebral angiogram, showing an aneurysm of the right posterior cerebral artery at the junction with the posterior communicating artery (arrows).
Discussion All seven patients reported herein had had no known cerebral ischemic events before the verified attack of an aneurysmal rupture, and the arterial occlusion was an unexpected finding at angiography. Exact time o f occurrence of the arterial occlusion remains unknown, and it might be argued that the association of an aneurysm and an arterial occlusion is nothing but a coincidence. For several reasons, however, we are more inclined to believe that hemodynamic changes secondary to arterial occlusion played an important role in the formation, further growth, and final rupture of the aneurysms in these patients. Three patients with an occlusion of the middle cerebral artery harbored four aneurysms, one each in the anterior branch o f the lateral posterior choroidal artery, at the junction of the internal carotid artery and the anterior cerebral artery, in the distal branch of the mid-
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9
B
die cerebral artery, and in the anterior cerebral artery at the origin of the accessory middle cerebral artery. In the fourth patient, in whom the middle cerebral artery and the contralateral distal internal carotid artery were occluded, an anterior communicating aneurysm was present. In the remaining three patients, the internal carotid artery was occluded and the aneurysm was found in the posterior circulation. In two of them an aneurysm was found at the junction of the posterior cerebral and posterior communicating arteries; the third had two aneurysms, one at the basilar bifurcation and the other in the proximal segment of the posterior cerebral artery. All three posterior cerebral aneurysms were found on the side of the carotid occlusion. It should be noted that all of the aneurysms in this series were found in sites at which saccular aneurysms generally develop infrequently [20,35], with the exception of the aneurysm of the anterior communicating artery in patient 4. The parent artery of each ruptured aneurysm had definitely served as an important collateral pathway. None of these patients had ever experienced any ischemic neurological attacks attributable to an arterial occlusion, indicating that the blood flow through the collateral routes
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A
B
was adequate. Also, at least five of the seven patients were known to have been hypertensive for a long time. It seems plausible, therefore, that the parent vessels of these aneurysms had been exposed to significant hemodynamic stress. Pathologic findings on the aneurysm in patient 2 seem to substantiate further the importance of hemodynamic factors in its formation. The saccular aneurysm is generally known to point in the direction that the blood would flow through its parent artery; namely, its dome should point in the direction of the maximal hemodynamic thrust in the site of its parent artery with preaneurysmal change [25]. In patient 2, the direction of the blood flow through the parent artery had been reversed secondary to the proximal middle cerebral occlusion, and the aneurysm pointed exactly in the direction of the reversed flow via the leptomeningeal anastomosis between the posterior cerebral and middle cerebral arteries. Sayama et al [27] reported two similar cases. In their patients, multiple aneurysms were found in sites at which hemodynamic forces were presumed to be increased as a result of occlusion of the internal carotid artery. In each of their two patients, the initial symptoms were caused by a subarachnoid hemorrhage, and there was no previous history of cerebral ischemic attacks. The role of hemodynamic factors in the pathogenesis of cerebral aneurysms was suggested by Forbus as early as 1930 [6]. In 1961, Hassler [12] and Stehbens [33] suggested that the turbulence of blood flow at the major arterial forks was a likely cause of aneurysmal dilatation. Fergusson [5] negated the idea of turbulence at the apex
Figure 5. Patient 7. (A) Frontal and (B) lateral projection of left vetebral angiogram, showing two aneurysms, one at the basilar bifurcation (1) and the other at the peduncular segment of the left posterior cerebral artery (2). The proximal segment of the left internal carotid artery is occluded." the distal segment is filled with contrast medium from vertebral injection of the dye via the enlarged left posterior communicating artery. of the arterial forks. Based on extensive clinical and experimental studies, however, he stressed the importance of hemodynamically generated forces, such as shear stress, impulse, and pressure, as a cause of focal degeneration of the internal elastic lamina and enlargement of the medial defect at the apices of the major intracranial arterial forks on which the central bloodstream would impinge. According to Fergusson [5], the pulsatile impulse and the pressure head transmitted with each heartbeat would induce an aneurysmal outpouching at the apex with reduced resistance, and the vibration of the wall and the turbulence within the pouch would further promote the degeneration and weakening of the wall, eventually resulting in the growth of a frank saccular aneurysm. Recently, Hashimoto et al [11] demonstrated in rats that an aneurysm could be induced in the proximal segment of the posterior cerebral artery on the side of a ligation of the carotid artery, namely, in the artery with an apparent increase in hemodynamic stress. Patients 5, 6, and 7 in the present series are good clinical examples of these experimental results. Clinical evidence supporting the importance of hemodynamic factors in the development of cerebral aneurysms has been reported repeatedly. Salar and Mingrino [26] reported that 2 of 126 patients with carotid ligation developed a contralateral cerebral aneurysm.
Aneurysm With Arterial Occlusion
Although these authors neglected to consider the influence of hemodynamic changes on aneurysmal development, it should be pointed out that the incidence of 1.6% (2 of 126) in their series might be higher than the estimated incidence of cerebral aneurysm in the general population (1%) [17]. Several other reports, by circumstantial evidence, seem to substantiate the hypothesis that cerebral aneurysms might develop after ligation or spontaneous occlusion of a carotid artery or other cerebral arteries [15,23,26-28,31]. Gurdjian et al [9] reported a 58-year-old woman in whom an internal carotid aneurysm developed 8 years after ligation of the contralateral carotid artery. German and Black [7] described two patients in whom the carotid artery had been ligated to treat an aneurysm of the internal carotid artery. One died of rupture of an aneurysm of the anterior communicating artery 15 years later; the other died of cerebral thrombosis 20 years later, and an unruptured aneurysm was found in the cavernous portion of the contralateral internal carotid artery. Somach and Shenkin [30] report a case in which an aneurysm developed at the junction of the right anterior cerebral and anterior communicating arteries 7 years after ligation of the left common carotid artery. Clark and Ray [3] also reported three cases in which an intracranial aneurysm appeared contralateral to a ligated carotid artery. In cerebral angiograms performed at the time of carotid ligation, no aneurysm other than that treated by the ligation was noted in any of these eight patients. Association of a cerebral aneurysm and a congenital anomaly of the cephalic arteries has also been well documented. Reviewing the literature, Waga et al [36] reported 16 cases, including their own, of intracranial aneurysm associated with absence of the internal carotid artery. Masuzawa et al [21] reported two cases of an intracranial aneurysm associated with a coarctation of the thoracic aorta. In one of them, a saccular aneurysm was found at the junction of the internal carotid and posterior communicating arteries, where no abnormalities had been found on angiography performed 3 years previously. They stressed the importance of abnormal hemodynamic stresses in the development of these aneurysms. According to Stehbens [34], the occurrence of cerebral aneurysms in patients with a coarctation of the aorta could be ascribed to the concomitant hypertension and resultant premature atherosclerosis of the cerebral arteries. McCormick and Schmalstieg [22] found no definitive correlation between hypertension and the development of cerebral aneurysms, and Hashimoto et al [11] demonstrated that hypertension alone failed to induce aneurysms in their experimental models in rats. However, Crompton [4] found that a greater number
Surg Neurol 1983;20:4-12
11
of large medial defects and more marked degenerative changes of the internal elastic lamina were found in the cerebral arteries of hypertensive patients than in those of normotensive control subjects. Therefore, hypertension may well contribute to the formation of cerebral aneurysms by accelerating structural changes and weakening of the arterial wall. Association of a cerebral aneurysm and a cerebral arteriovenous malformation (AVM) has also been described. Shenkin et al [29] reported a patient in whom the aneurysm of a major feeding artery regressed after removal of the AVM. Similar cases have been reported by others [14,19]. Collecting 74 cases of cerebral aneurysms associated with AVMs, Hayashi et al [14] found that 77% had developed in the arteries hemodynamically related to AVMs. All of these clinical reports also seem to lend further support to the hypothesis that the enhanced blood flow and pulsation may well contribute to the enlargement of medial defects and thus to the development and growth of the aneurysms [4]. In conclusion, an occlusion of a cerebral artery results in an alteration of hemodynamics in the remaining cerebral arteries. With the passage of time, the hemodynamically generated forces facilitate weakening of the arterial wall at the sites of structural defects of congenital and/or acquired origin by enlarging the medial defect and degenerating the internal elastic membrane, and lead to the formation and growth of a cerebral aneurysm and finally to its rupture.
References 1. Bremer JL. Congenital aneurysms of the cerebral arteries. Arch Pathol 1943;35:819-31. 2. Carmichael R. The pathogenesis of non-inflammatory cerebral aneurysms. J Pathol Bacteriol 1950;62:1-19 3. Clark WC, Ray MW. Contralateral intracranial aneurysm formation as a late complication of carotid ligation. Surg Neurol 1982;18:458-62. 4. Crompton MR. The pathogenesis of cerebral aneurysms. Brain 1966;89:797-814. 5. Fergusson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg 1972;37:666-77. 6. Forbus WD. On the origin of miliary aneurysms of the superficial cerebral arteries. Bull Johns Hopkins Hosp 1930;47:239-84. 7. German WJ, Black SPW. Cervical ligation for internal carotid aneurysms. An extended follow-up. J Neurosurg 1965;23:5727. 8, Glynn LE. Medial defects in the circle of Willis and their relation to aneurysm formation. J Pathol Bacteriol 1940;51:213-22. 9. Gurdjian ES, Lindner DW, Thomas LM. Experiences with ligation of the common carotid artery for treatment of aneurysms of the internal carotid artery. With particular reference to complications. J Neurosurg 1965;23:311-8. 10. Handa J, Matsuda M, Okamoto K, Kidooka K. Association be-
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