Neurosurg. Rev. 2i (1998)284-289
A giant dissecting aneurysm mimicking serpentine aneurysm angiographically Case report and review of the literature
Metin Tuna 1, A. lskender G/ifer 1, Siileyman OzeP, Hiiseyin Ba~dato~lu 1, Suzan Zorhidemir 2, and Sebahattin Haciyakupo~lu ~ Departments of ~Neurosurgery and 2Pathology, ~ukurova University School of Medicine, Adana, Turkey
Abstract
1 Introduction
Intracranial dissecting and giant serpentine aneurysms are rare vascular anomalies. Their precise cause has not yet been completely clarified, and the radiological appearance of such lesions can be different in each case according to the effect of hemodynamic stress on a pathologic vessel wall. For berry aneurysms, available evidence overwhelmingly favors their causation by hemodynamically induced degenerative vascular disease and there is an obvious need to determine the hemodynamic parameters most likely to induce the precursor atrophic lesions. In this study, a case of a giant dissecting aneurysm angiographically mimicking serpentine aneurysm of the right ophthalmic artery is reported and the relevant literature is reviewed to investigate the pathological characteristics and pathogenesis of this lesion. In the present case, radiological investigation of the lesion suggested a serpentine aneurysm, but the diagnosis was corrected to dissecting aneurysm subsequent to the pathological examination of the resected aneurysm.
Dissecting aneurysms of the intracranial arteries are rarely encountered in neurosurgical practice, although they have recently been recognized in the major trunks and proximal branches of the intracranial internal carotid artery [1, 3, 9,10,12,16, 22, 26, 39, 30, 34, 46]. Dissecting aneurysms are characterized angiographically by the so-called "string sign," "double lumen," "pearl and string" or a "pseudo-aneurysm" appearance in the affected arteries. However, angiographic diagnosis of these lesions might be difficult, even in histologically documented cases. Furthermore, little is known regarding the etiology of these lesions [3, 9,16,19, 29, 34, 44].
A giant dissecting aneurysm angiographically mimicking serpentine aneurysm and developing as the result of a circumferential dissection located between the internal elastic lamina and media is of particular interest when the etiology of these aneurysms is considered. To our knowledge this is the first report on intracranial dissecting aneurysm mimicking serpentine aneurysm angiographically. Our case illustrates the importance of careful serial section studies for a better understanding of the vascular pathology underlying the processes involved in intracranial serpentine aneurysms. We conclude that serpentine, dissecting and berry aneurysms may all arise by way of similar pathophysiological mechanisms.
Keywords: Angiography, Berry aneurysm, Dissecting aneurysm, Giant serpentine aneurysm.
© Springer-Verlag1998
Giant aneurysms that show sinusoid, tortuous "serpentine" vascular channels within partially thrombosed aneurysms in neuroradiological studies are referred to as giant serpentine aneurysms (GSAs) [2, 4, 11, 18, 21, 23, 25, 28, 43]. The case of a giant dissecting aneurysm angiographically mimicking the G S A appearance and arising from the ophthalmic branch of the right internal carotid artery is reported, and the literature is briefly discussed with reference to the etiology of this condition. To our knowledge this is the first report on intracranial dissecting aneurysm mimicking serpentine aneurysm angiographicaUy.
2 Case report A 3t-year-old woman complaining of a sudden onset of headache was admitted to the D e p a r t m e n t of Neurosurgery, Balcali hospital, on 24 July 1995. Her
Tuna et al., Giant dissectinganeurysm mimickingserpentine aneurysm
Figure L Plain CT scan showinghigh-densityareas in the aneurysm around the anterior communicatingartery and an extremely large irregular-shaped hyperdense mass within the right frontal region.
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Figure 3. Right carotid angiogram, anteroposterior view, showing a round ring-like blood channel connected to the right internal carotid artery. the anterior communicating artery and an extremely large, irregular-shaped hyperdense mass within the right frontal lobe were found on computed tomography (CT) scan (Figure 1). In addition to these lesions, magnetic resonance imaging (MRI) also showed reeanalization of the hematoma (pseudo-aneurysm) around the anterior communicating artery (Figure 2). For better confirmation of the underlying pathology, digital subtraction angiography (DSA) was performed on the following day: it showed a GSA arising from the right ophthalmic artery and having a round ring-like blood channel connected to the right internal carotid artery (Figure 3). The rest of the intracranial circulation was normal.
Figure 2. MRI, coronal view, showing the large, partially thrombosed aneurysm at the anterior communicatingartery level. findings, including the results of laboratory and physical examination, were normal. Left hemiparesis and visual loss on the right eye were found on neurological examination. Subarachnoid hemorrhage, high-density areas in the aneurysm around Neurosurg.Re~21(1998)
Operation: After the right pterional craniotomy the dura was cut and tied up. The right frontal and temporal lobes were gently retracted after the arachnoidal opening, and the giant aneurysm was seen under the operating microscope. Following dissection of the aneurysm arising from the ophthalmic branch of the internal carotid, displacement of the internal carotid and the middle cerebral artery laterally, of the anterior cerebral artery inferoposteriorly, and of the optic nerve superomedially was also seen. Then, the involved ophthalmic arteriy just distal to the carotid-ophthalmic artery junction was clipped and the aneurysm was entirely excised.
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Postoperative course. There was no additional neurologic deficit, and the postoperative course was uneventful. The patient was discharged on the 8 postoperative day with left hemiparesis and right-sided loss of vision. Pathological examination. The surgical specimen was fixed in neutral buffered formalin, routinely processed, and paraffin-embedded. The sections were stained with hematoxylin-eosin, Van-Gieson and elastic Van-Gieson. The microscopic examination revealed a circumferential dissection located between the internal elastic lamina and media. The lumen and dissected space were filled with partially organized thrombus (Figures 4 and 5).
3 Discussion Intracranial arterial dissections occur in young adults (aged between their late twenties and early
forties). The patients are rarely hypertensive, and few have any history of atherosclerotic peripheral vascular disease or diabetes. The majority of dissecting intracranial aneurysms have no certain recognized cause, although isolated examples of intracranial dissections associated with atherosclerosis, arterial hypertension, tumor resection, aneurysm clipping, mucoid degeneration of the media, a congenital medial defect, fibrous or fibroelastic intimal thickening, fraying and splitting of the internal elastic lamina, surgery, syphilis, migraine, cystic, necrosis of the media, fibromuscular dysplasia, homocystinuria, strenuous physical exertion, Marfan's syndrome and head trauma have been reported [6, 7,10, 12, 14, 16, 17, 20, 22, 29, 32, 33, 35, 44, 45]. In the carotid system, dissection most commonly involves the middle cerebral or the supraclinoid carotid artery, usually extending into the proximal middle cerebral artery or, less often, into the ante-
Figure 4. Photomicrograph of the surgical specimen, showingthe separation of the internal elastic lamina (arrows) and the thrombus filling the dissected space (arrowheads). H & E, 100.
Figure 5. Photomicrograph of the surgical specimen, showing the dissected space (arrows) and the thrombus in the true lumen (arrowheads). H & E 100. Neurosurg.Rev.21(1998)
Tuna et al., Giant dissectinganeurysm mimickingserpentine aneurysm rior cerebral artery [12, 24, 29, 34]. The plane of dissection is generally restricted subintimally [12, 46]. Eskenasy et al. [9] reported that the dissected vessels showed the pathologic changes of characteristic segmental mediolytic "arteritis". The dissection between the internal elastic lamina and media usually results from diversion of the arterial stream into a weakened area of the arterial wall [8, 27]. The origin of GSAs has not yet been completely clarified. They can originate from fusiform or large saccular aneurysms [21]. Suzuki et al. [43] explained the pathogenesis of serpentine aneurysms as an elongation of the original lumen along with thrombosis caused by some anomalous congenital vascular conditions, such as an endothelial defect or the vulnerability of the wall. Horowitz et al. [18] reported that inflammatory lesions of the arterial wall and degenerative connective tissue discorders seem to predispose to giant serpentine fusiform aneurysms. Enlargement seems to be a consequence of arterial pulsations against a weakened vessel wall. Although the precise cause for GSAs remains uncertain, it is thought that tortuous vascular pathways are created within the aneurysm when blood flows to a giant aneurysm under conditions of a jet flow (the socalled Coanda effect) [25]. Most GSAs are localized in the middle cerebral artery [4, 11, 18, 21, 25, 43]. Previous reports have suggested that congenital vascular defects are worsened by atherosclerotic disease; however, the usual absence of other vascular lesions or atherosclerosis implies that this factor may be important in only a small number of cases. Fusiform, dolichoectatic and giant serpentine aneurysms may therefore present a spectrum of nonsaccular aneurysms that share a common gross and microscopic appearance, and these lesions may arise from the same pathophysiological mechanism: intimal disruption from dissection. The uniform presence of intimal defects, a thinned or absent smooth-muscle layer, the frequent absence of atherosclerosis, the occurrence in all age groups and the gross and MRI appearance of these lesions support this hypothesis [4]. Gull [13] explained berry aneurysm as a simple pouch with the sac wall as transparent and normal in appearance as the parent vessel, giving the impression of a pre-existing deformity. When early this century the etiology and pathogenesis of intracranial berry aneurysms were obscure, they were assumed to be congenital or the result of a congenital maldevNeurosurg. Rev. 21 (1998)
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elopment, but such assumptions were based on lowquality evidence and inadequate statistical analyses [37, 38]. Examination of infants' cerebral arteries failed to reveal berry aneurysms in neonates [36-38]. Years later, proponents of the congenital theory accepted that these aneurysms are absent at birth and rarely occur during childhood [41]. A review of reported cases in infancy provides good reason for doubting their validity in support of this theory, as most of the aneurysms were inflammatory or traumatic [15, 31, 38, 40]. Some workers have suggested that the cause of saccular aneurysms in infancy differs from that of berry aneurysms in adults [5]. However, it has been conceded that berry aneurysms are acquired; most specimens encountered clinicallyor at autopsy are in individuals between 40 and 70 years of age, the mean age being approximately 50 years [38, 39] - only 6 years younger than the subjects in an autopsy study of primary intracerebral hemorrhage [37]. Berry aneurysms characteristically arise from the forks and adj acent walls of bifurcations of large cerebral arteries, which have high flow rates, and less frequently from the bifurcations of splanchnic arteris. They also occur on enlarged collateral spinal arteries in aortic coarctation or associated with spinal arteriovenous aneurysms, suggesting that the high blood velocityis a factor in their development. This cerebral preponderance is also believed to be due to architectural peculiarities of cerebral and spinal arteries namely, the thin media and adventitia). Most of the elastin is in the internal elastic lamina, with only a few fibrils in the adventitia and less in the media [38]. Arterial walls are not homogeneous structures but consist of a heterogeneous mix of connective-tissure fibrous proteins, cells, proteoglycans, glycoproteins, glycolipids, adhesion molecules, etc., all of which contribute to the overall cohesion and physical and functional integrity of the wall. Inherited defects of any one of these components are likely to interfere with the function, viscoelastic properties, fatigue resistance, and mural integrity as a whole, and as such they constitute predisposing factors to aneurysm formation. A high rate of familial occurrence may be due to an inherited factor of any one mural constituent, but the aneurysmal dilatation itself is not inherited. In genuine instances of familial aneurysms, very early development of aneurysms, or extreme multiplicity,it is appropriate to seek a possible inherited defect of a mural constituent, and not of berry aneurysms per se. [42].
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Stehbens concludes that berry aneurysms are not congenital and are not due to hypothetical developmental errors. Available evidence overwhelmingly favors their causation by hemodynamicatly induced degenerative vascular disease. There is probably a predisposition to aneurysm formation in cases of hypertension and connective tissue disorders im which mural fragility develops. Furthermore, arterial occlusive lesions may also predispose to aneurysm formation postnatally at specific arterial forks affected by secondary imbalance of blood flow. There is an obvious m e e d to determine the hemodynamic parameters most likely to induce the precursor atrophic lesions [41]. In the fight of the G S A findings in our case, the preoperative diagnosis was a giant serpentine aneurysm of the right ophthalmic artery with ay round ring-like blood channel connected to the right internal carotid artery, which is angiographically a pathognomonic feature for GSA. However, microscopic examination of the resected aneurysm re-
vealed a circumferential dissection located between the internal elastic lamina and media. The lumen and dissected space were filled with partially organized thrombus. Therefore, these findings are in favor of dissecting aneurysm. In conclusion, as the differential diagnosis of dissecting and serpentine aneurysms can easily be confused when lesions are examined angiographically, it is concluded that dissecting, serpentine and berry aneurysms may also arise as the results of similar pathophysiological mechanism and that their angiographic appearances depend on the effect of hemodynamic stress on a pathologic vessel wall. Appropriate hemodynamic conditions suitable for the Coanda effect might occur in a giant saccular aneurysm and can cause intimal disruption and dissection between the elastic lamina and tunica media. Our case illustrates the importance of careful serial section studies for better understanding of the vascular pathology underlying the processes involved in intracranial serpentine aneurysms.
References [1] ADAMSHP Jr, CA ASCHENBRENER,NF KASSEL,L ANSBACHER,SH CORNELL:Intracranial hemorrhage produced by spontaneous dissecting intracranial aneurysm. Arch Neuro139 (1982) 773-776 [2] ALETICHVA, GM DEBRUN,LH MONSEIN,HJ NAUTA, RF SPETZLER:Giant serpentine aneurysms: a review and presentation of five cases. AJNR Am J Neuroradio116 (1995) 1061-1072 [3] ANSONJ, RM CROWELL:Cervicocranial arterial dissection. Neurosurgery 29 (1991) 89-96 [4] ANSONJA, MT LAWTON,RF SPETZLER:Characteristics and surgical treatment of dolichocctatic and fusiform aneurysms. J Neurosurg 84 (1996) 185-193 [5] BECKERDH, GD SILVERBERG,DH NELSON,JW HANBERY:Saccular aneurysm of infancy and early childhood. Neurosurgery 2 (1978) 1-7 [6] BERGERMS, CB WILSON:Intracranial dissecting aneurysms of the posterior circulation. J Neurosurg 61 (1984) 882-894 [7] BIGELOWNH: Intracranial dissecting aneurysms. An analysis of their significance. Arch Pathol 60 (1955) 271-275 [8] ENDO S, M NISHIJMA, H NOMURA,A TAKAKU,E OKADA:A pathological study of intracranial posterior circulation dissecting aneurysms with subarachnoid hemorrhage: Report of three autopsied cases and Review of the literature. Neurosurgery 33 (1993) 732-738 [9] ESKENASY-COTTIERAC, HJ LEU, C BASSETTI,J BOGOUSSLAVSKY,F REGLI,R e JANZER:A case of dissec-
[10] [11]
[12]
[13] [14]
[15]
[16] [17]
tion of intracranial cerebral arteries with segmental mediolytic "arteritis". Clin Neuropathol 13 (1994) 329-337 FRIEDMANAH, CG DRAKE: Subarachnoid hemorrhage from intracranial dissecting aneurysm. J Neurosurg 60 (1984) 325-334 GREENEKA, JA ANSON,RF SPETZLER:Giant serpentine middle cerebral artery aneurysm treated by extracranial-intracranial bypass. Case report. J Neurosure 78 (1993) 974-978 GROSMANH, VL FORNASIER,D BONDER,KE LIVINGSTON,ME PLATIS:Dissecting aneurysms of the cerebral arteries. Case report J Neurosurg 53 (1980) 693-697 GULL,WM: Cases of aneurysm of the cerebral vessels. Guys Hosp Rep 5 (1859) 281-304 GURmIJ, J GALLEGO,F MONZON,F AGUILERA:Intracerebral hemorrhage caused by transmural dissection of the anterior cerebral artery. Stroke 24 (1993) 1400-1402 GUTIERREZFA, J BAILES,DG McLONE: Intracranial aneurysm and pseudo-aneurysm occuring during infancy and childhood: diagnosis and surgical results. Concepts Pediatr Neurosurg 7 (1987) 153-168 HARTRG, JD EASTON:Dissections of cervical and cerebral arteries. Neurol Clin 1 (1983) 155-182 HEYEN, JR IGLESIAS,H HENKES,R FERZST,K MAIERHAUFF: Dissecting aneurysm of middle cerebral artery following resection of meningioma (letter). J Neurol Neurosttrg Psychiatry 52 (1989) 683 Neurosurg. Rev.21 (1998)
Tuna et al., Giant dissecting aneurysm mimicking serpentine aneurysm [18] HOROWlTZ MB, H YONAS, C JUNGREIS, TK HUNG: Management of a giant middle cerebral artery fusiform serpentine aneurysm with distal clip application and retrograde thrombosis-case report and review of the literature. Surg Neuro141 (1994) 221-225 [19] HOUSEROW, B MOKRLTM SUNDT Jr, HL BAKERJr, DF REESE: Spontaneous cervical cephalic arterial dissection and its residuum: Angiographic spectrum. AJNR A m J Neuroradiol 5 (1984) 27-34 [20] ISHIKAWAR, S SUNAGAWA,I ITOH,K IWASHITA:A n experience of dissecting cerebral aneurysm of the anterior cerebral artery. No Shinkei Gekay 21 (1993) 355-359 [21] ISLAA, F ALVAREZ,JM RODA,J MUI~OZ,C MORALES, MG BLAZQUEZ:Serpentine aneurysm: Regrowth after a superficial temporal artery-middle cerebral artery bypass and internal carotid artery ligation: case report. Neurosurgery 34 (1994) 1072-1074 [22] JOHNSON HRM, JR SOUTH: Traumatic dissecting aneurysm of the middle cerebral artery. Surg Neuro114 (1980) 224-226 [23] KHAN MT, CS McKINSTRY,KE BELL,TF FANNIN,DP B YRNES,R VASISHTA:Serpentine aneurysm of the posterior circulation: report of two cases Br J Neurosurg 4 (1990) 217-223 [24] KITANIR, T ITOUJI,Y NODA, M KIMURA,S UCHIDA: Dissecting aneurysms of the anterior circle of Willis arteries. Report of two cases. J Neurosurg 67 (1987) 296-300 [25] KUMABET, U KANEKO,T ISHIBASHI, K KANEKO, S UCHIGASAKI:Two cases of giant serpentine aneurysm. Neurosurgery 26 (1990) 1027-1033 [26] KUNZE ST, W SCHIEFER:Angiographic demonstration of a dissecting aneurysm of the middle cerebral artery. Neuroradiology 2 (1971) 201-206 [27] MANZ JU, AJ LUESSENHOP:Dissecting aneurysm of intracranial vertebral artery: case report and review of the literature. J Neuro1230 (1983) 25-35 [28] MAWADME, RP KLUCZNIK: Giant serpentine aneurysms; radiographic features and endovascular treatment. AJNR A m J Neuroradiol 16 (1995) 1053-1060 [29] MIZUTANIT: Middle cerebral artery dissecting aneurysm with persistent patent pseudolumen. Case report. J Neurosurg 84 (1996) 267-268 [30] NAKAZAWAT, A SAITO,K WATANABE,M MATSUDA,J HANDA: Dissecting aneurysm of the anterior cerebral artery: report of a case. No Shinkei Geka 12 (1984) 1211-1216 [31] NAKSTADP, H NORNES,FIN HAUGE: Traumatic aneurysms of the pericallosal arteries. Neuroradiology 28 (1986) 335-338 [32] O'CONNELL BK, J TOWFIGHI,RW BRENNAN,W TYLER, M MATHEWS,WA WEIDNER,RF SAUL:Dissecting aneurysms of head and neck. Neurology 35 (1985) 993-997
Neurosurg. Rev.21 (1998)
289
[33] PIEPGRASDG, KM MCGRAIL, HD TAZELAAR:Intra-
[34] [35]
[36]
[37] [38] [39] [40] [41] [42]
[43]
[44]
[45]
[46]
cranial dissection of the distal middle cerebral artery as an uncommon cause of distal cerebral artery aneurysm. Case report. J Neurosurg 80 (1994) 90%913 SASAKIO, T KOIKE,S TAKEUCHI,R TANAKA:Serial angiography in a spontaneous dissecting anterior cerebral artery aneurysm. Surg Neuro136 (1991) 49-53 SATO O, JF BASCOM,J LOGOTHETIS: Intracranial dissecting aneurysm. Case report. J Neurosurg 35 (1971) 483-487 SMITH DE, RB WINDSOR: Embryologic and pathogenic aspects of the development of cerebral saccular aneurysms. In: Fields WS (ed): Pathogenesis and treatment of cerebrovascular disease. Charles C Tomas, Springfield, 1961 STEHBENSWE: Aneurysms and anatomical variation of cerebral arteries. Arch Patho175 (1963) 45-64 STEHBENSWE: Pathology of the cerebral blood vessels. Mosby, St Louis, 1972 STEHRENSWE: Etiology of cerebral aneurysms. Lancet (1981) 524-525 STEHBENSWE: Intracranial berry aneurysms in infancy. Surg Neuro118 (1982) 58-60 STEHBENSWE: Etiology of intracranial berry aneurysms. J Neurosurg 70 (1989) 823-831 STEHSENSWE: Heredity and the etiology of intracranial berry aneurysms (letter). Stroke 27 (1996) 2338-2339 SuzuKI S, T TAKAHASHI,H OHKUMA,T SHIMIZU,S FuJITA:Management of giant serpentine aneurysms of the middle cerebral artery. Review of the literature and report of a case successfully treated by STA-MCA anastomosis only. Acta Neurochir (Wien) 117 (1992) 23-29 YAMASHITAM, K TANAKA,T MATSUO,K YOKOYAMA,T FUHI, H SAKAMOTO:Cerebral dissecting aneurysms in patients with moyamoya disease. Report of two cases. J Neurosurg 58 (1983) 120-125 YANOH, M SAWADA,J SHINODA,T FUNAKOSHI:Ruptured dissecting aneurysm of the peripheral anterior cerebral artery. A case report. Neurol Med Chir Tokyo 35 (1995) 45O-453 YONAS,H, DAGAMANOLIS,YTAKAOKA,RJWHITE: Dissecting intracranial aneurysms. Surg Neurol 8 (1977) 407-415 Submitted May 2,1997. Revised November 14,1997. Accepted August 19,1998. Metin Tuna, M. D. Department of Neurosurgery ~ukurova University School of Medicine Balcali, Adana, 01330 Turkey