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Fusiform intracranial aneurysms. Clinicopathologic features
Surg Neurol 1988;29:263-70
263
Fusiform Intracranial Aneurysms Clinicopathologic Features M. Tayo Shokunbi, J.C.E. Kaufmann,
M . B . , B . S . , M . S c . , F . R . C . S . (C.), H . V . V i n t e r s , M . D . , F . R . C . P . ( C . ) , a n d M.B., Ch.B., F.R.C. Path.
Divisions of Neurosurgery and Neuropathology, Departments of Clinical Neurological Sciences and Pathology, University Hospital, London, Ontario, Canada
Shokunbi MT, Vinters HV, KaufmannJCE. Fusiform intracranial aneurysms. Clinicopathologicfeatures. Surg Neurol 1988;29: 263-70. Seven fusiform aneurysms were found at autopsy in five patients (two males and three females) over a 13-year period. The subjects were between 56 and 65 years of age. The basilar trunk was the most frequent site. Four aneurysms were of giant proportions and contained laminated thrombi. Subarachnoid hemorrhage occurred in four patients. Microscopic examination of the aneurysm walls revealed atheromatous degeneration, focal wall attenuation, mural hemorrhage, rupture, and acute and chronic inflammatory cell infiltration. These findings suggest that rupture is not rare and that atherosclerosis is but one mechanism in the pathogenesis of these lesions. KEYWORDS: Aneurysm; Fusiform; Atherosclerosis; Pathology
Fusiform intracranial aneurysms are infrequent vascular lesions [16]. Clinical reports have generally portrayed them as mass lesions with a propensity to produce ischemic neurological deficits. Several reports classify large fusiform aneurysms with saccular aneurysms of corresponding size as giant aneurysms, obscuring their clinical identity [1,13]. It is generally agreed that the vertebrobasilar trunk is the most frequent location of fusiform aneurysms [4,17]. The frequency with which they occur in the anterior portion of the circle of Willis is probably underestimated in autopsy series, reflecting the relatively benign clinical course of those aneurysms in this portion o f the cerebral circulation. Pathological studies are few and have been preoccupied with the atherosclerotic changes of the parent vessels. These changes have been regarded, perhaps erroneously, by Adress reprint requests to: Dr. M. Tayo Shokunbi, Neurosurgery Unit, Department of Surgery, University College Hospital, Ibadan, Nigeria. Received November 17, 1986; accepted October 20, 1987.
© 1988by ElsevierSciencePublishingCo., Inc.
some authors as the major pathogenetic mechanism of fusiform aneurysmal dilatation [8]. Although the pathological features of saccular intracranial aneurysms have been exhaustively investigated [3,6,24-26], the pathology of fusiform aneurysms has not been well documented. In particular, the microscopic features of these lesions have not been systematically studied. We report our experience with these lesions and describe the clinical, gross, and microscopic features of fusiform intracranial aneurysms encountered at autopsy. Materials and Methods Autopsy records between 1972 and 1985 of the University Hospital, London, Ontario, Canada, were reviewed. All subjects found to have fusiform intracranial aneurysms at autopsy were selected. The clinical records were analyzed with respect to medical and past neurological history, mode of final presentation to hospital (especially history of subarachnoid hemorrhage), and mode of death. The gross features of the aneurysms were reviewed and photographs taken at autopsy were examined. Random paraffin sections (8 /~m thick) stained with hematoxylin and eosin, Movat's pentachrome, and periodic acid-Schiff-alcian blue stains were carefully examined, and when necessary, additional sections were obtained and processed. An aneurysm was considered to be fusiform if the wall dilatation involved the entire circumference of the vessel and afferent and efferent vessels were identified.
Results Fusiform intracranial aneurysms were found at autopsy in five subjects that died between 1972 and 1985 (Table 1). During this period, 147 patients presented at necropsy with aneurysms of various types, saccular aneurysms being most frequent. The patients with fusiform aneurysms were between 56 and 65 years of age. There were two males and three females. Three patients had 0090-3019/88/$3.50
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Table 1. Clinical and Pathological Findings Case No.
Age (yr)
Sex
IHD
Hypertension
Presentation
Mode of death
F M F F M
Fatal myocardial infarction Angina None Previous myocardial infarction None
Absent Present Absent Present Present
SAH Brainstem compression SAH SAH SAH
Myocardial infarction Brainstem infarction SAH, vasospasm SAH, cerebral edema SAH, brainstem ischemia
Clinical Findings 1 2 3 4 5
59 61 63 65 56
Pathologicalfindings Gross Subarachnoid hemorrhage Atherosclerosis-circle of Willis Brainstem distortion and compression Intraaneurysmal thrombus Microscopic Subarachnoid hemorrhage Mural necrosis Inflammatory infiltrate Complicated atheroma Dissection Patchy disruption of internal elastic lamina Abbreviations: IHD, ischemic heart disease; SAH, subarachnoid hemorrhage.
previous histories of hypertension, but it was being controlled by medication at the time of death. Coronary atherosclerosis was evident at autopsy in four patients, had been symptomatic in three, and resulted in fatal myocardial infarction in one. In three patients, there was no antemortem ischemic cerebral/brainstem event. These individuals presented primarily with subarachnoid hemorrhage. One patient had three transient ischemic attacks (ocular, left and right hemispheric, successively). Another had experienced progressive hoarseness and dysphagia in the 12 years since his first subarachnoid hemorrhage. Brainstem infarction was the terminal event in the third patient. Subarachnoid hemorrhage occurred in four of the five patients, and was the first clinical manifestation o f an intracranial aneurysm in all four. It had occurred within 1 month of death in three of the four patients. Two patients had episodes resembling warning leaks prior to final presentation to the hospital. An antemortem angiographic diagnosis o f an intracranial aneurysm was made in four o f the five patients and the aneurysm was felt to be fusiform only in two of the four patients. The mode o f death was brainstem infarction in one patient, myocardial infarction in another, and subarachnoid hemorrhage in three.
Gross Findings at Autopsy There was a total o f seven fusiform aneurysms (Table 2). One patient with a fusiforrn basilar aneurysm had a
fusiform left middle cerebral artery aneurysm and another had bilateral fusiform internal carotid artery aneurysms. The basilar trunk was the favored site of such aneurysms in this series (Figure 1). However, this type of aneurysm occurred as frequently in the anterior circulation as it did in the posterior circulation. The aneurysms were spindle-shaped, with irregular bosselation o f their surfaces. They extended for variable distances along the length o f the parent vessel. The most extensive was a basilar trunk aneurysm measuring 5 cm long. The transverse diameter (as measured at the time of autopsy) was available for five aneurysms, two of which measured 1.5 cm each. The remainder exceeded 2.5 cm. Fresh subarachnoid hemorrhage was seen at autopsy in three patients, and in the fourth patient (no clinical indication o f subarachnoid hemorrhage), hemorrhage had occurred into the wall o f the aneurysm. The three aneurysms on the basilar trunk were partially embedded in the ventral brainstem, which showed considerable distortion and flattening (Figure 2A). Sectioning the aneurysms revealed extensive thrombosis in four. The
Table 2. Location of Fusiform Intracranial Aneurysms Anterior circulation Internal carotid artery Middle cerebral artery (left) Posterior circulation Basilar artery Vertebral artery (left)
2 1 3 l
Fusiform Intracranial Aneurysms
Figure 1. Basal view of the brain: giant fusiform aneurysm o f t & basilar trunk (white arrow) and ectatic atherosclerotic vertebral arteries (black arrows) are shown.
thrombus was laminated and the vessel lumen was reduced to small slits (Figure 2B). A rupture point was not identified at the time o f autopsy in any of the aneurysms. Generally, the vessels in the circle of Willis showed moderate-to-severe atherosclerosis (Figure 1) most marked in the parent vessel harboring the aneurysm. An anomalous circle of Willis was present in one o f the patients, in w h o m a persistent trigeminal artery connected the anterior circulation to the basilar trunk. Extracranial fusiform aneurysms were present in two patients: one had an abdominal aortic aneurysm and the other had two abdominal aortic aneurysms as well as an anterior spinal artery aneurysm.
Microscopic Features Without exception, the parent vessels contained atheromatous plaque (Figure 3) often complicated and associated with severe c o m p r o m i s e of the vessel lumen. Calcification was the most frequently seen complication of the plaque, although a few plaques were ulcerated. T h e r e was no microscopic evidence o f connective tissue deficiency or inflammatory arteritis. Surprisingly, atheromatous lesions were infrequent
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in the wall of the aneurysm itself, and were focal and patchy in contrast to the extent and severity of the lesions in the parent vessels. T h e wall was mostly fibrotic with markedly reduced muscularis. Elastica was absent in the majority of the sections examined; when present, it was severely attenuated and fragmented (Figure 4). This feature was present in all the autopsy cases and did not seem to vary in severity with the size of the aneurysm or the thickness of the aneurysm wall. The aneurysm wall was o f variable thickness. Some areas of the wall were extremely attenuated, the adventitial covering forming the major supporting element at these points (Figure 5). In the two cases in which rupture points were identified microscopically, these were located at zones of attenuation (Figure 5). In both cases the internal elastic lamina was absent at and adjacent to the rupture point. H e m o s i d e r i n and hematoidin pigments were extensively deposited in the aneurysm wall and the subarachnoid space in all cases. Microscopic evidence of recent extravasation into the vessel wall was seen in three aneurysms (including one with mural hemorrhage at the time o f autopsy). This included one of the two aneurysms in which a rupture point was evident histologically. The mural hemorrhages were multiple and occurred as small pools of blood within channels that were not lined by endothelium. Mononuclear inflammatory cell infiltration was a prominent feature in the aneurysm wall. T h e cells were sometimes clustered in relation to areas o f hemosiderin deposition. Acute (polymorphonuclear) inflammatory infiltration of the aneurysm wall was also seen in association with a peculiar alteration o f the wall, which was characterized by an eosinophilic hyaline change in the fibers comprising it (Figure 6). T h e p o l y m o r p h response was so intense in some areas that the entire thickness of the vessel in these areas was replaced by a basophilic dust of leukocyte nuclear debris.
Discussion The very low autopsy incidence o f fusiform intracranial aneurysms in this series confirms the experience of others [16,17]. W e have shown that the vertebrobasilar trunk is the most frequent site o f occurrence of such aneurysms. Several previously published reports of fusiform aneurysms at this location conveyed the impression that the posterior circulation is the favored site [4,8,15,21]. Despite the fact that this institution offers special expertise in the surgical management of posterior circulation aneurysms, autopsy data forming the basis of this study suggest that fusiform aneurysms occur equally as frequently in the anterior circulation. A
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A
B
Figure 2. (A) Transt,erse section of aneurysm and brainstem: extensire thrombosis within aneurysm, and set,ere compression and displacement of brainstem (arrows) are shown. (B) Transverse section of aneurysm." lamination of thrombns.
clinical series o f fusiform aneurysms of the anterior circulation has been reported by Little et al [12]. Consideration of possible pathogenetic mechanisms does not offer clues to support the observation that fusiform aneurysms occur preeminently in the posterior circulation. The distinction between a dolichoectatic intracranial artery and fusiform aneurysm o f the same may be difficult. Both are regarded by some as interchangeable entities [14,22]. Moreover, fusiform aneurysms may occur on a dolichoectactic artery. However, a dolichoectatic artery is characteristically elongated, tortuous, and dilated. T h e fusiform aneurysms considered in
this series were morphologically distinct and were not associated with significant elongation or tortuousity of nearby vessels, other than those resulting from displacement o f the aneurysms. Despite extensive thrombosis of the aneurysms, only two of our patients experienced ischemic neurological deficits, of whom one died of terminal brainstem infarction. Although the literature is replete with case reports o f fusiform intracranial aneurysms presenting with embolic ischemic phenomena [2,9,22], only 1 of 11 patients reported by Little et al [12] and 5 of 23 patients reported by Nijensohn et al [15] experienced ischemic neurologic deficits. The factors that determine the propensity o f massively thrombosed aneurysms to embolize are not completely understood. Massive fusiform aneurysms invariably encroached on adjacent brain and/or cranial nerves and could be recognized as space-occupying lesions on cranial computed tomography scans [27]. Dysphagia and hoarse-
Fusiform Intracranial Aneurysms
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267
Figure 3. Thin section of parent vessel: intimal fibromuscular hyperplasia and cholesterol clefts (hematoxylin and eosin, x 120~.
ness occurred in one o f the five patients, presumably as a result of compression of the glossopharyngeal and vagus nerves. That this has not occurred more frequently probably reflects slow aneurysmal enlargement allowing adjacent neural structures to accommodate to the space-occupying lesion. All three basilar aneurysms in this series compressed the brainstem. The latter structure, although severely distorted, still demonstrated neural constituents, albeit with mild demyelination of the long fiber tracts. T h e paucity of atherosclerotic plaques in the aneurysm walls was a surprising contrast to the severity of atherosclerotic change in the parent vessel. This raises doubts regarding the strength of the claims made for atheromatous degeneration as the m o d e of fusiform aneurysm formation [4,8,15,21]. Evidence in favor o f
atherosclerosis includes the following: the frequent finding o f significant atheromatous lesions in the aneurysm parent vessel and the rest of the circle of Willis; the occurrence of fusiform intracranial aneurysms at sites were atheroma is usually most severe; the occurrence of atherosclerosis in extracranial arteries, especially the coronary arteries and the abdominal aorta in the same patients; the existence of extracranial fusiform aneurysms presumed to be atherosclerotic in the same patient; and the occurrence of fusiform aneurysms in an age group in which atherosclerosis is prevalent. On the other hand, a fusiform aneurysm in a child and another in an adult have been reported [5,28]. In these cases, there were no histologic features of atheromatous degeneration or connective tissue disorder. It has been shown that atheroma occurs in a high proportion of
Figure 4. Thin section of aneurysm wall." marked reduction and fragmentation of elastica (arrows and attenuation of muscularis coat can be seen (hematoxylin and eosin, x 50).
Figure 5. Thin section of aneurysm wall near rupture site. Note variation in wall thickness, focal attenuation, and lack of elastica adjacent to rupture point (arrows).
Fusiform Intracranial Aneurysms
saccular intracranial aneurysms [3]. Moreover, animal studies have demonstrated changes similar to those of human atherosclerosis in experimental aneurysms of the aortic bifurcation [26]. The exact significance of atherosclerosis in fusiform intracranial aneurysms is therefore difficult to assess. Elucidation of a clear cause and effect relationship requires further studies. We favor the concept that fusiform aneurysms could result from poststenotic dilatation [18,23]. In this series, the severity of atherosclerotic narrowing of the parent vessel proximal to the aneurysm and the extent of loss o f elastica in the aneurysm wall are noteworthy and compatible with this concept. Turbulence distal to vascular stenosis vibrates the vessel wall, weakening its elastica, and permitting distensibility. Fusiform intracranial aneurysms have been reported to result from inflammatory vasculopathy [11] and to be associated with Marfan's syndrome [7] and pseudoxanthoma elasticum [20]. These entities were not present in any of the five patients described here. Attenuation of the wall of the aneurysm presumably results from a combination of loss of supporting elastica and degeneration of the muscularis. In accordance with Laplace's law, tension will mount on the vessel wall as the luminal diameter increases. This study has demon-
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Figure 6. Thin section of aneurysm wall." acute inflammatory cells infiltrate, with cells undergoing karyorrhexis (hematoxylin and eosin, × 320). strated that rupture occurred (in two cases) in association with focal areas o f severe mural attenuation and loss of elastica. The occurrence o f subarachnoid hemorrhage in four o f the patients is therefore not surprising. Equally compatible with these considerations was the observation of hemorrhage into the aneurysm wall. That some of these were subclinical is supported by the extensive deposition into the aneurysm wall of bloodderived pigment accompanied by a focal mononuclear inflammatory response. The polymorphonuclear response appears to be of a different significance. It is conceivable that this was a response to necrosis or damage o f the vessel wall component (collagen or muscle), but we are uncertain. If this is so, it will provide an alternative hypothetical mechanism of fusiform aneurysmal rupture. The authors thank Betty Gardiner for secretarial assistance. H.V. Vinters was supported by the Canadian Heart Foundation and the Heart and Stroke Foundation of Ontario, Mr. F.I. Nwankpa typed the final manuscript.
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References 1. Bull J. Massive aneurysms at the base of the brain. Brain 1969;92:535-70. 2. Cohen MM, Hemalatha CP, D'Addarid RT, Goldman HW. Embolization from a fusion middle cerebral artery aneurysm. Stroke 1980;11:158-61. 3. Compton MR. The pathogenesis of cerebral aneurysms. Brain 1966;89:797-814. 4. Corville CB. Arteriosclerotic aneurysms of the circle of Willis. Bull Los Angeles Neuro Soc 1962;27:1-13. 5. Esiri MM, Read D. Fusiform basilar artery aneurysm in a child. Neurology 1979;29:1045-9. 6. Ferguson GG. Turbulence in human intracranial saccular aneurysms. J Neurosurg 1970;33:485-97. 7. Finney HL, Roberts TS, Anderson RE. Giant intracranial aneurysm associated with Marfan's syndrome. Case report. J Neurosurg 1976;45:342-7. 8. Hayes WT, Bernhardt H, Young JM. Fusiform arteriosclerotic aneurysms of the basilar artery. Vasc Surg 1967;1:171-8. 9. Hirah LF, Gonzalez CF. Fusiform basilar aneurysm simulating carotid transient ischaemic attacks. Stroke 1979;10:598-601. 10. Jamieson KG. Aneurysms of the vertebrobasilar system. Surgical intervention in 19 cases. J Neurosurg 1964;21:781-97. 11. Johnson SD, Okamoto G, Koolker J. Fusiform basilar artery aneurysm in a child. Neurology 1977;27:334-6. 12. Little JR, St. Louis P, Weinstein M, Dohn DF. Giant fusiform aneurysm of the cerebral arteries. Stroke 1981;12:183-8. 13. Morley TF, Barr HWK. Giant intracranial aneurysms: diagnosis, course, and management. Clin Neurosurg 1969;16:73-94. 14. Moseley IF, Holland IM. Ectasia of the basilar artery: the breadth of the clinical spectrum and the diagnostic value of computed tomography. Neuroradiology 1979; 18:83-91.
S h o k u n b i et al
15. Nijensohn DE, Saez RJ, Reagan TJ. Clinical significance of basilar artery aneurysms. Neurology 1974;24:301-5. 16. Pia H. Classification of vertebro-basilar aneurysms. Acta Neurochir 1979;47:3-10. 17. Pool JL, Potts DG. Aneurysms and arteriovenous anomalies of the brain: diagnosis and treatment. New York: Hoeber Medical Division, 1965:46-53. 18. Roach MR. An experimental study of the production and time course of post-stenotic dilatation in the femoral and carotid arteries of adult dogs. Circ Res 1963;13:537-51. 19. Roach MR. Changes in arterial distensibility as a cause of post-stenotic dilatation. Am J Cardiol 1963;12:802-15. 20. Scheie HG, Hogan TF. Angioid streaks and generalized arterial disease. Arch Ophthalmol 1957;57:855-68. 21. Slade WR Jr. Massive basilar artery aneurysms. Vasc Surg 1974;8:74-81. 22. SteelJG, Thomas HA, Strollo PJ. Fusiform basilar aneurysm as a cause of embolic stroke. Stroke 1982;12:712-6. 23. Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. Arch Pathol 1963;75:45-64. 24. Stehbens WE. Histopathology of cerebral aneurysms. Arch Neurol 1963;8:272-85. 25. Stehbens WE. Pathology of cerebral blood vessels. St. Louis: CV Mosby, 1972. 26. Stehbens WE. Chronic vascular changes in the walls of experimental berry aneurysms of the aortic bifurcation in rabbits. Stroke 1981;12:643-7. 27. Thron A, Bockenheimer S. Giant aneurysms of the posterior fossa suspected as neoplasms on computed tomography. Neuroradiology 1979;18:93-7. 28. Tomasello F, Albanese V, Cioffi FA. Giant serpentine aneurysms: a separate entity. Surg Neurol 1979;12:429-32.
263
Fusiform Intracranial Aneurysms Clinicopathologic Features M. Tayo Shokunbi, J.C.E. Kaufmann,
M . B . , B . S . , M . S c . , F . R . C . S . (C.), H . V . V i n t e r s , M . D . , F . R . C . P . ( C . ) , a n d M.B., Ch.B., F.R.C. Path.
Divisions of Neurosurgery and Neuropathology, Departments of Clinical Neurological Sciences and Pathology, University Hospital, London, Ontario, Canada
Shokunbi MT, Vinters HV, KaufmannJCE. Fusiform intracranial aneurysms. Clinicopathologicfeatures. Surg Neurol 1988;29: 263-70. Seven fusiform aneurysms were found at autopsy in five patients (two males and three females) over a 13-year period. The subjects were between 56 and 65 years of age. The basilar trunk was the most frequent site. Four aneurysms were of giant proportions and contained laminated thrombi. Subarachnoid hemorrhage occurred in four patients. Microscopic examination of the aneurysm walls revealed atheromatous degeneration, focal wall attenuation, mural hemorrhage, rupture, and acute and chronic inflammatory cell infiltration. These findings suggest that rupture is not rare and that atherosclerosis is but one mechanism in the pathogenesis of these lesions. KEYWORDS: Aneurysm; Fusiform; Atherosclerosis; Pathology
Fusiform intracranial aneurysms are infrequent vascular lesions [16]. Clinical reports have generally portrayed them as mass lesions with a propensity to produce ischemic neurological deficits. Several reports classify large fusiform aneurysms with saccular aneurysms of corresponding size as giant aneurysms, obscuring their clinical identity [1,13]. It is generally agreed that the vertebrobasilar trunk is the most frequent location of fusiform aneurysms [4,17]. The frequency with which they occur in the anterior portion of the circle of Willis is probably underestimated in autopsy series, reflecting the relatively benign clinical course of those aneurysms in this portion o f the cerebral circulation. Pathological studies are few and have been preoccupied with the atherosclerotic changes of the parent vessels. These changes have been regarded, perhaps erroneously, by Adress reprint requests to: Dr. M. Tayo Shokunbi, Neurosurgery Unit, Department of Surgery, University College Hospital, Ibadan, Nigeria. Received November 17, 1986; accepted October 20, 1987.
© 1988by ElsevierSciencePublishingCo., Inc.
some authors as the major pathogenetic mechanism of fusiform aneurysmal dilatation [8]. Although the pathological features of saccular intracranial aneurysms have been exhaustively investigated [3,6,24-26], the pathology of fusiform aneurysms has not been well documented. In particular, the microscopic features of these lesions have not been systematically studied. We report our experience with these lesions and describe the clinical, gross, and microscopic features of fusiform intracranial aneurysms encountered at autopsy. Materials and Methods Autopsy records between 1972 and 1985 of the University Hospital, London, Ontario, Canada, were reviewed. All subjects found to have fusiform intracranial aneurysms at autopsy were selected. The clinical records were analyzed with respect to medical and past neurological history, mode of final presentation to hospital (especially history of subarachnoid hemorrhage), and mode of death. The gross features of the aneurysms were reviewed and photographs taken at autopsy were examined. Random paraffin sections (8 /~m thick) stained with hematoxylin and eosin, Movat's pentachrome, and periodic acid-Schiff-alcian blue stains were carefully examined, and when necessary, additional sections were obtained and processed. An aneurysm was considered to be fusiform if the wall dilatation involved the entire circumference of the vessel and afferent and efferent vessels were identified.
Results Fusiform intracranial aneurysms were found at autopsy in five subjects that died between 1972 and 1985 (Table 1). During this period, 147 patients presented at necropsy with aneurysms of various types, saccular aneurysms being most frequent. The patients with fusiform aneurysms were between 56 and 65 years of age. There were two males and three females. Three patients had 0090-3019/88/$3.50
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Table 1. Clinical and Pathological Findings Case No.
Age (yr)
Sex
IHD
Hypertension
Presentation
Mode of death
F M F F M
Fatal myocardial infarction Angina None Previous myocardial infarction None
Absent Present Absent Present Present
SAH Brainstem compression SAH SAH SAH
Myocardial infarction Brainstem infarction SAH, vasospasm SAH, cerebral edema SAH, brainstem ischemia
Clinical Findings 1 2 3 4 5
59 61 63 65 56
Pathologicalfindings Gross Subarachnoid hemorrhage Atherosclerosis-circle of Willis Brainstem distortion and compression Intraaneurysmal thrombus Microscopic Subarachnoid hemorrhage Mural necrosis Inflammatory infiltrate Complicated atheroma Dissection Patchy disruption of internal elastic lamina Abbreviations: IHD, ischemic heart disease; SAH, subarachnoid hemorrhage.
previous histories of hypertension, but it was being controlled by medication at the time of death. Coronary atherosclerosis was evident at autopsy in four patients, had been symptomatic in three, and resulted in fatal myocardial infarction in one. In three patients, there was no antemortem ischemic cerebral/brainstem event. These individuals presented primarily with subarachnoid hemorrhage. One patient had three transient ischemic attacks (ocular, left and right hemispheric, successively). Another had experienced progressive hoarseness and dysphagia in the 12 years since his first subarachnoid hemorrhage. Brainstem infarction was the terminal event in the third patient. Subarachnoid hemorrhage occurred in four of the five patients, and was the first clinical manifestation o f an intracranial aneurysm in all four. It had occurred within 1 month of death in three of the four patients. Two patients had episodes resembling warning leaks prior to final presentation to the hospital. An antemortem angiographic diagnosis o f an intracranial aneurysm was made in four o f the five patients and the aneurysm was felt to be fusiform only in two of the four patients. The mode o f death was brainstem infarction in one patient, myocardial infarction in another, and subarachnoid hemorrhage in three.
Gross Findings at Autopsy There was a total o f seven fusiform aneurysms (Table 2). One patient with a fusiforrn basilar aneurysm had a
fusiform left middle cerebral artery aneurysm and another had bilateral fusiform internal carotid artery aneurysms. The basilar trunk was the favored site of such aneurysms in this series (Figure 1). However, this type of aneurysm occurred as frequently in the anterior circulation as it did in the posterior circulation. The aneurysms were spindle-shaped, with irregular bosselation o f their surfaces. They extended for variable distances along the length o f the parent vessel. The most extensive was a basilar trunk aneurysm measuring 5 cm long. The transverse diameter (as measured at the time of autopsy) was available for five aneurysms, two of which measured 1.5 cm each. The remainder exceeded 2.5 cm. Fresh subarachnoid hemorrhage was seen at autopsy in three patients, and in the fourth patient (no clinical indication o f subarachnoid hemorrhage), hemorrhage had occurred into the wall o f the aneurysm. The three aneurysms on the basilar trunk were partially embedded in the ventral brainstem, which showed considerable distortion and flattening (Figure 2A). Sectioning the aneurysms revealed extensive thrombosis in four. The
Table 2. Location of Fusiform Intracranial Aneurysms Anterior circulation Internal carotid artery Middle cerebral artery (left) Posterior circulation Basilar artery Vertebral artery (left)
2 1 3 l
Fusiform Intracranial Aneurysms
Figure 1. Basal view of the brain: giant fusiform aneurysm o f t & basilar trunk (white arrow) and ectatic atherosclerotic vertebral arteries (black arrows) are shown.
thrombus was laminated and the vessel lumen was reduced to small slits (Figure 2B). A rupture point was not identified at the time o f autopsy in any of the aneurysms. Generally, the vessels in the circle of Willis showed moderate-to-severe atherosclerosis (Figure 1) most marked in the parent vessel harboring the aneurysm. An anomalous circle of Willis was present in one o f the patients, in w h o m a persistent trigeminal artery connected the anterior circulation to the basilar trunk. Extracranial fusiform aneurysms were present in two patients: one had an abdominal aortic aneurysm and the other had two abdominal aortic aneurysms as well as an anterior spinal artery aneurysm.
Microscopic Features Without exception, the parent vessels contained atheromatous plaque (Figure 3) often complicated and associated with severe c o m p r o m i s e of the vessel lumen. Calcification was the most frequently seen complication of the plaque, although a few plaques were ulcerated. T h e r e was no microscopic evidence o f connective tissue deficiency or inflammatory arteritis. Surprisingly, atheromatous lesions were infrequent
Surg Neurol 1988;29:263-70
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in the wall of the aneurysm itself, and were focal and patchy in contrast to the extent and severity of the lesions in the parent vessels. T h e wall was mostly fibrotic with markedly reduced muscularis. Elastica was absent in the majority of the sections examined; when present, it was severely attenuated and fragmented (Figure 4). This feature was present in all the autopsy cases and did not seem to vary in severity with the size of the aneurysm or the thickness of the aneurysm wall. The aneurysm wall was o f variable thickness. Some areas of the wall were extremely attenuated, the adventitial covering forming the major supporting element at these points (Figure 5). In the two cases in which rupture points were identified microscopically, these were located at zones of attenuation (Figure 5). In both cases the internal elastic lamina was absent at and adjacent to the rupture point. H e m o s i d e r i n and hematoidin pigments were extensively deposited in the aneurysm wall and the subarachnoid space in all cases. Microscopic evidence of recent extravasation into the vessel wall was seen in three aneurysms (including one with mural hemorrhage at the time o f autopsy). This included one of the two aneurysms in which a rupture point was evident histologically. The mural hemorrhages were multiple and occurred as small pools of blood within channels that were not lined by endothelium. Mononuclear inflammatory cell infiltration was a prominent feature in the aneurysm wall. T h e cells were sometimes clustered in relation to areas o f hemosiderin deposition. Acute (polymorphonuclear) inflammatory infiltration of the aneurysm wall was also seen in association with a peculiar alteration o f the wall, which was characterized by an eosinophilic hyaline change in the fibers comprising it (Figure 6). T h e p o l y m o r p h response was so intense in some areas that the entire thickness of the vessel in these areas was replaced by a basophilic dust of leukocyte nuclear debris.
Discussion The very low autopsy incidence o f fusiform intracranial aneurysms in this series confirms the experience of others [16,17]. W e have shown that the vertebrobasilar trunk is the most frequent site o f occurrence of such aneurysms. Several previously published reports of fusiform aneurysms at this location conveyed the impression that the posterior circulation is the favored site [4,8,15,21]. Despite the fact that this institution offers special expertise in the surgical management of posterior circulation aneurysms, autopsy data forming the basis of this study suggest that fusiform aneurysms occur equally as frequently in the anterior circulation. A
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A
B
Figure 2. (A) Transt,erse section of aneurysm and brainstem: extensire thrombosis within aneurysm, and set,ere compression and displacement of brainstem (arrows) are shown. (B) Transverse section of aneurysm." lamination of thrombns.
clinical series o f fusiform aneurysms of the anterior circulation has been reported by Little et al [12]. Consideration of possible pathogenetic mechanisms does not offer clues to support the observation that fusiform aneurysms occur preeminently in the posterior circulation. The distinction between a dolichoectatic intracranial artery and fusiform aneurysm o f the same may be difficult. Both are regarded by some as interchangeable entities [14,22]. Moreover, fusiform aneurysms may occur on a dolichoectactic artery. However, a dolichoectatic artery is characteristically elongated, tortuous, and dilated. T h e fusiform aneurysms considered in
this series were morphologically distinct and were not associated with significant elongation or tortuousity of nearby vessels, other than those resulting from displacement o f the aneurysms. Despite extensive thrombosis of the aneurysms, only two of our patients experienced ischemic neurological deficits, of whom one died of terminal brainstem infarction. Although the literature is replete with case reports o f fusiform intracranial aneurysms presenting with embolic ischemic phenomena [2,9,22], only 1 of 11 patients reported by Little et al [12] and 5 of 23 patients reported by Nijensohn et al [15] experienced ischemic neurologic deficits. The factors that determine the propensity o f massively thrombosed aneurysms to embolize are not completely understood. Massive fusiform aneurysms invariably encroached on adjacent brain and/or cranial nerves and could be recognized as space-occupying lesions on cranial computed tomography scans [27]. Dysphagia and hoarse-
Fusiform Intracranial Aneurysms
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Figure 3. Thin section of parent vessel: intimal fibromuscular hyperplasia and cholesterol clefts (hematoxylin and eosin, x 120~.
ness occurred in one o f the five patients, presumably as a result of compression of the glossopharyngeal and vagus nerves. That this has not occurred more frequently probably reflects slow aneurysmal enlargement allowing adjacent neural structures to accommodate to the space-occupying lesion. All three basilar aneurysms in this series compressed the brainstem. The latter structure, although severely distorted, still demonstrated neural constituents, albeit with mild demyelination of the long fiber tracts. T h e paucity of atherosclerotic plaques in the aneurysm walls was a surprising contrast to the severity of atherosclerotic change in the parent vessel. This raises doubts regarding the strength of the claims made for atheromatous degeneration as the m o d e of fusiform aneurysm formation [4,8,15,21]. Evidence in favor o f
atherosclerosis includes the following: the frequent finding o f significant atheromatous lesions in the aneurysm parent vessel and the rest of the circle of Willis; the occurrence of fusiform intracranial aneurysms at sites were atheroma is usually most severe; the occurrence of atherosclerosis in extracranial arteries, especially the coronary arteries and the abdominal aorta in the same patients; the existence of extracranial fusiform aneurysms presumed to be atherosclerotic in the same patient; and the occurrence of fusiform aneurysms in an age group in which atherosclerosis is prevalent. On the other hand, a fusiform aneurysm in a child and another in an adult have been reported [5,28]. In these cases, there were no histologic features of atheromatous degeneration or connective tissue disorder. It has been shown that atheroma occurs in a high proportion of
Figure 4. Thin section of aneurysm wall." marked reduction and fragmentation of elastica (arrows and attenuation of muscularis coat can be seen (hematoxylin and eosin, x 50).
Figure 5. Thin section of aneurysm wall near rupture site. Note variation in wall thickness, focal attenuation, and lack of elastica adjacent to rupture point (arrows).
Fusiform Intracranial Aneurysms
saccular intracranial aneurysms [3]. Moreover, animal studies have demonstrated changes similar to those of human atherosclerosis in experimental aneurysms of the aortic bifurcation [26]. The exact significance of atherosclerosis in fusiform intracranial aneurysms is therefore difficult to assess. Elucidation of a clear cause and effect relationship requires further studies. We favor the concept that fusiform aneurysms could result from poststenotic dilatation [18,23]. In this series, the severity of atherosclerotic narrowing of the parent vessel proximal to the aneurysm and the extent of loss o f elastica in the aneurysm wall are noteworthy and compatible with this concept. Turbulence distal to vascular stenosis vibrates the vessel wall, weakening its elastica, and permitting distensibility. Fusiform intracranial aneurysms have been reported to result from inflammatory vasculopathy [11] and to be associated with Marfan's syndrome [7] and pseudoxanthoma elasticum [20]. These entities were not present in any of the five patients described here. Attenuation of the wall of the aneurysm presumably results from a combination of loss of supporting elastica and degeneration of the muscularis. In accordance with Laplace's law, tension will mount on the vessel wall as the luminal diameter increases. This study has demon-
Surg Neurol 1988;29:263-70
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Figure 6. Thin section of aneurysm wall." acute inflammatory cells infiltrate, with cells undergoing karyorrhexis (hematoxylin and eosin, × 320). strated that rupture occurred (in two cases) in association with focal areas o f severe mural attenuation and loss of elastica. The occurrence o f subarachnoid hemorrhage in four o f the patients is therefore not surprising. Equally compatible with these considerations was the observation of hemorrhage into the aneurysm wall. That some of these were subclinical is supported by the extensive deposition into the aneurysm wall of bloodderived pigment accompanied by a focal mononuclear inflammatory response. The polymorphonuclear response appears to be of a different significance. It is conceivable that this was a response to necrosis or damage o f the vessel wall component (collagen or muscle), but we are uncertain. If this is so, it will provide an alternative hypothetical mechanism of fusiform aneurysmal rupture. The authors thank Betty Gardiner for secretarial assistance. H.V. Vinters was supported by the Canadian Heart Foundation and the Heart and Stroke Foundation of Ontario, Mr. F.I. Nwankpa typed the final manuscript.
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