Recanalization and Rupture of Giant Vertebral Artery Aneurysm •« ro Recanalization and Rupture of a Giant Vertebral Artery Aneurysm after Hunterian Ligation: Case Report x Steven D. Chang, M.D., Michael P. Marks, M.D., 1 1 Cary K. Steinberg, M.D., Ph.D. ?! Departments of Neurosurgery (SDC, CKS) and Radiology (MPM) and the Stanford Stroke Center (SDC, MPM, GKS), Stanford University School of Medicine, Stanford, California ?r 1a 4 OBJECTIVE AND IMPORTANCE: Recanalization and subsequent rupture of giant aneurysms of the posterior circulation after Hunterian ligation is an S5 extremely rare event that has been noted to occur with basilar apex, basilar on trunk, and vertebrobasilar junction aneurysms. W e report the case of a giant, previously unruptured right vertebral artery aneurysm, which recanalized ;l from the contralateral vertebral artery and subsequently ruptured after previ­ ously performed angiography showed complete thrombosis of the aneurysm. a CLINICAL PRESENTATION: A 7 2 -y e a r-o ld w om an presented with h ead­ ib aches, ataxia, and low er extrem ity weakness. A giant 3-cm right vertebral i 1 artery aneurysm was found during the patient evaluation. si INTERVENTION: B ecau se o f th e size o f the aneurysm and the a b se n ce of a ni discrete neck, Hunterian ligation was performed. After treatm ent, angio­ al grams showed no filling o f the aneurysm from either the right or left if .0) 9 te vertebral artery. Nine days later, after the patient developed lethargy and nausea, repeat angiography show ed that a small portion of the aneurys­ mal base had recan alized . The next day, the patient had a massive subarachnoid h em o rrh ag e and subsequently died. I CONCLUSION: W e think that this is a previously undescribed complication associated with direct arterial ligation of giant vertebral artery aneurysms. I Patients with aneurysms treated using Hunterian ligation need to be followed sit up closely. Even aneurysms that have minimal recanalization are at risk for ii subarachnoid hemorrhage. (Neurosurgery 44:111 7 - 1 1 2 1 , 1999) h Key words: Aneurysm, Endovascular coiling, Hunterian ligation, R e c a n a liz a tio n (6 xmportant alternative treatment. Several T h e ideal treatment of intracranial a n ­ series have documented the results of eurysms is surgical clip ping of the such treatment for anterior circulation an­ uneurysmal neck, thereby preventing eurysms (4, 5, 13), and, more recently, n eruorrhage or further an eu rysm al enresults have been published regarding de­ a ar£ement while preserving the parent liberate basilar or vertebral artery occlu­ 5 e*ssel and other normal vessels of the sion (1, 8, 15, 17, 19, 20, 23). Other series !« ^ere ral circulation. H ow ever, som e aninclude results from treatment of both an­ i 0^ SrriS cann°t be successfully clipped terior and posterior circulation aneu­ \ r C^ ec* us*ng interventional techniques, rysms (2, 7, 9, 12, 14, 18, 21). 9 - Ular>y s°me giant, fusiform, or athStasis of contrast material within the ^ 1 ^ ° ^ aneurYsrns- Despite recent a n e u r y s m a l lu m e n a n d / o r p a r t ia l f (Fju ent acDances, proximal arterial throm bosis often occurs im m ediately af­ nterian) ligation has persisted as an Neurosurgery, Vol. 4 4 , No. , May 1999 5 1117 ter H unterian ligation, and com plete throm bosis is usually observed w ithin 1 month. In the absence of recanalization, a patient with com plete throm bosis is considered cured from the future risk of subarachnoid hem orrhage. W e report the case of a 72-year-old w om an w ho underw ent H unterian ligation of a gi­ ant, previously unruptured right verte­ bral artery aneurysm via endovascular sacrifice of the right vertebral artery. A f­ ter the procedure, angiograp hy show ed no filling of the aneurysm by either the right or left vertebral artery, with excel­ lent filling of the basilar artery from the left vertebral artery. The aneurysm later recanalized via contralateral flow from the left vertebral artery. The patient su b­ sequently bled from her aneurysm , re­ sulting in death. CASE REPORT The patient w as a 72-year-old w om an w ho presented with a 2-year history of progressively w orsening headaches and a 3-m onth history of progressive ataxia and right low er extrem ity w eakness. She was adm itted to an outside institu­ tion for initial evaluation, and m agnetic resonance im aging show ed a large m ass in the posterior fossa suspicious for an aneurysm (Fig IA). The patient u n d er­ w ent angiography of the carotid and vertebral arteries, w hich dem onstrated a giant 3.0-cm right vertebral artery an ­ eurysm located 1.5 cm proxim al to the vertebrobasilar junction. Angiography was complicated by an ischemic event, thought to be embolic in nature, consist­ ing of mental status changes and right upper extremity weakness, but these m in­ imal deficits resolved completely during the next several days. The patient was transferred to Stanford University M edi­ cal Center for treatment of her aneurysm. The patient underw ent repeat an giog­ raphy at Stanford, w hich confirm ed the presence of the giant right vertebral ar­ tery aneurysm (Fig. 1, B and C). The basilar artery was found to fill briskly from the larger contralateral left verte­ bral artery (Fig. ID). The right posteroinferior cerebellar artery and right a n ­ teroinferior cerebellar artery originated 1118 Chang et al. D NHw * ■ FIGURE 1. Axial magnetic resonance image showing the giant right vertebral artery aneurysm (A). Lateral ( B ) and anteropos terior (C) vertebral angiograms showing the giant right vertebral artery aneurysm. There is good filling of the basilar artery from the dominant left vertebral artery, as seen in the left vertebral injection ( D). The right posteroinferior cerebellar artery and anteroinferior cerebellar artery originate from a com m on trunk arising from the proximal basilar artery distal to the aneurysm (C, arrow ). from a com m on trunk at the base of the basilar artery distal to the aneurysm (Fig. 1C). Because of the size of the a n ­ eurysm and the absence of a discrete neck, it w as determ ined that direct proxim al arterial ligation w ould be the best treatm ent for this patient. After negative results of a clinical balloon oc­ clusion test of the right vertebral artery w ere obtained, a detachable balloon and several endovascular coils w ere used to occlude the right vertebral artery im m e­ diately proximal to the aneurysm . The patient tolerated the procedure well w ithout com plication. Post-treatm ent vertebral angiogram s showed no filling of the aneurysm from either the right or left vertebral artery, with excellent fill­ ing of the basilar artery from the left vertebral artery (Fig. 2). The patient was discharged hom e 2 days after u nd ergo­ ing the endovascular treatment. Nine days after the H unterian ligation was perform ed, the patient becam e in­ creasingly lethargic and developed n au ­ sea. She was transferred back to Stan ­ ford University Medical Center, w here com puted tom ography show ed throm ­ bus in the giant right vertebral an eu ­ rysm. However, repeat vertebral an gio­ grams showed that a small portion of the giant right vertebral aneurysmal base had recanalized and w as filling from the opposite left vertebral artery injection (Fig. 3A). T h e right vertebral artery re­ mained occluded. The basilar artery still filled well from the left vertebra) artery. The next day, the patient had a sudden cardiac arrest requiring intubation and becam e com atose. C om p u ted to m o g ra­ phy show ed m assive subarachnoid and intraventricular h em orrh ag e (Fig. 3B). No improvement was noted with ventric­ ulostomy placement. The patient subse­ quently developed cerebral vasospasm and brain stem infarction. The patient died 6 days after the onset of su b arach ­ noid hem orrhage. D ISC U SSIO N A lthough p erm an en t proxim al arte­ rial ligation is not the optim al treatm ent for aneurysm s and, in som e cases, leads to ischem ic com plications, results m ust be com pared with the natural history of untreated giant aneurysm s. A lthough there are a few reported cases of sp o n ­ taneous throm bosis of giant an eu rysm s (3, 16), the natural history of m ost u n ­ treated giant aneu rysm s is extrem ely poor. A pproxim ately 80% of patients with untreated anterior circulation a n ­ eurysm s becom e severely disabled or die secondary to hem orrhage, brain stem com pression, or throm bosis of crit­ ical arteries w ithin 5 years (2, 6, 11-13). The prognosis seem s to be even w orse for untreated posterior circulation giant aneurysm s, with an 80 to 100% rate of severe disability or death during a 5-year follow -up period (2, 4, 6, 11, 20). Partial throm bosis of an aneurysm , and/or stasis of contrast m aterial w ithin the sac, often occurs im m ediatelyJ after direct arterial ligation. In m ost cases, Neurosurgery, Vol. 4 4 , No. , May 5 1 9 9 9 com p lete throm bosis occurs within 1 m onth. W ith anterior circulation aneu­ rysm s, throm bosis is more likely to oc­ cur after intracranial, compared with ex­ tracranial, H unterian ligation. Proximal internal carotid artery (ICA) occlusion (in the neck) results in poor rates of throm bosis for supraclinoid ICA aneu­ rysm s (13). Steinberg et al. (20) showed, in their series of 201 posterior circula­ tion an eu ry sm s (87% giant), that 70% of the an eu ry sm s had completely or virtu­ ally com p letely thrombosed within the 1st m onth. W hen analyzed by site, 66% of the patients with basilar bifurcation giant an eu ry sm s had complete throm­ bosis after upper basilar artery occlu­ sion, whereas 34% had incomplete throm­ bosis. Ninety percent of the basilar trunk aneurysm s had complete thrombosis after lower basilar artery occlusion; 10% had incomplete thrombosis. Vertebrobasilar junction giant aneurysms had a 78 to 84 > rate of complete thrombosis and a 16 to 22% rate of incomplete thrombosis, de pending on whether one or both of the vertebral arteries were ligated. Vertebra artery giant aneurysms had an 87% com plete and a 13% incomplete rate of throm bosis after ipsilateral vertebral artery os elusion. O f the incompletely thromboses posterior circulation aneurysms docu mented at 1 month (60 aneurysms, 30 " an additional one-fourth (17) thromboses within a period of 3 months to 1 year None of the thrombosed aneurysn* this series subsequently bled or had ss umented recanalization. Comply Recanalization and Rupture of Giant Vertebral Artery Aneurysm i n 1* B * m * FIGURE 3. A, left vertebral angiogram, obtained 9 days after Hunterian ligation, showing recanalization of a small portion of the base of the right giant vertebral artery aneu ­ rysm (c u rv ed arrow ) filling from the contralateral left verte bral artery via retrograde flow through the right vertebral artery (straight arrow ). B, computed tom ographic scan IGURE 2. Immediate post-Hunterian ligation angiograms lowing no filling of the giant right vertebral artery aneurysm om either the right vertebral artery (A) or contralaterally om the left vertebral artery ( B ). showine the subarachnoid hemorrhage. near complete thrombosis is essential for neurological protection; 67% of the pa­ tients with incomplete thrombosis suf­ fered neurological complications, 86% of which were fatal (20). Aneurysms at the vertebrobasilar junction, basilar trunk, or basilar apex are at some risk for aneurysm al recan a­ lization and rupture because of excellent collateral flow (from the posterior co m ­ municating arteries in the cases of b a si­ lar apex or trunk or from the basilar artery or contralateral vertebral artery in cases of vertebrobasilar junction a n e u ­ rysm) (20). The only previously reported case of subarachnoid hem orrhage occur­ ring after deliberate proximal artery oc­ clusion for treatment of a vertebral artery aneurysm was that described in the series presented by Steinberg et al. (20) of Hunt­ erian ligation for posterior fossa aneu­ rysms. Of their 37 cases of vertebral artery aneurysms, only one subsequently re­ sulted in subarachnoid hemorrhage, and this was an aneurysm known to have inc°mplete thrombosis based on a postHunterian ligation angiogram. None of the completely thrombosed aneurysms in * i s series subsequently bled. Aneurysms of the proximal vertebral artery should have minimal recanalizan once the parent vessel is sacrificed, , Particularly if there is no arterial outflow .* Prorriote blood flow. In this case, both ately after Hunterian ligation should be the ipsilateral posteroinferior cerebellar artery and anteroinferior cerebellar artery emerged from the basilar trunk distal to the aneurysm. Arterial occlusion of the right vertebral artery proximal to the an­ eurysm should have resulted in complete stasis within the vertebral artery from the site of occlusion to the right vertebrobasi­ lar junction because there were no large collateral vessels over this segment. To date, only two cases of recanaliza­ tion of a previously unruptured throm­ bosed giant aneurysm have been re­ p orted . S w e a rin g e n and H ero s (22) reported a patient with sym ptom s of brain stem com pression from a giant basilar apex aneurysm that w as throm ­ bosed as revealed by angiography. Four m onths later, the patient had a fatal su b ­ arachnoid hem orrhage. M atsuda et al. (10) reported the case o f a 51-year-old w om an with an unruptured giant an eu ­ rysm of the ICA treated with gradual occlusion of the proxim al ICA and ex­ tracranial to intracranial bypass. C o m ­ plete throm bosis of the aneurysm was confirm ed by angiography, but the p a­ tient had a fatal subarachnoid h em or­ rhage 34 days later. This case report and the two cases re­ ported by Swearingen and Heros (22) and Matsuda et al. (10) demonstrate that even those patients with complete absence of aneurysm filling on angiograms immedi­ Neurosurgery, Vol. 4 4 , No. 5, May 1 9 9 9 followed up closely, especially in regions such as the basilar apex and distal verte­ bral artery where recanalization is more likely to occur from luxuriant collateral flow. Noninvasive imaging using m ag­ netic resonance angiography or com ­ puted tomographic angiography might be the best method of evaluating these patients for at least 6 months after H unt­ erian ligation and apparent complete an­ eurysm thrombosis. New or recurrent symptoms should be aggressively evalu­ ated using angiography, and recanalized aneurysms should be treated. As this case showed, even aneurysms that have mini­ mal recanalization are at risk for sub­ arachnoid hemorrhage. ACKNOW LEDGMENTS This work was supported in part by funding from Ronni and Bernard Lacroute and the William Randolph Hearst Founda­ tion (to GKS). R e c e iv e d , S e p te m b e r 8, 1998. A c c e p te d , O c to b e r 28, 1998 R e p rin t re q u e sts: G a ry K. S te in b e rg , M .D ., P h.D ., P rofessor a n d C h a irm a n , D e p a rtm e n t o f N e u ro s u rg e ry , S ta n fo rd U n iv e rs ity M e d ic a l C e n te r, 300 P asteur D riv e , R o o m R-281, S tan­ fo rd , C A 94305. 1120 Chang et al REFERENCES 1. Aymard A, Gobin YP, Hodes JE, Bien S, Rufenacht D, Reizine D, George B, Merland JJ: Endovascular occlusion of vertebral arteries in the treatment of unclippable vertebrobasilar an­ eurysms. J Neurosurg 74:393-398, 1991. 2. Bull J: Massive aneurysms at the base of the brain. Brain 92:535-570, 1969. 3. Carlson DH, Thomson D: Spontaneous throm­ bosis of a giant cerebral aneurysm in five days: Report of a case. Neurology 26:334-336, 1976. 4. Drake CG: Giant intracranial aneurysms: Expe­ rience with surgical treatment in 174 patients. Clin Neurosurg 26:12-95, 1979. 5. Drake CG, Peerless SJ, Ferguson GG: Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. ] Neurosurg 81:656665, 1994. 6. Duvoisin RC, Yahr MD: Posterior fossa aneu­ rysms. Neurology 15:231-241, 1965. 7. Handa H, Hashimoto N, Yonekawa Y: Surgical treatment of giant aneurysms. Neurosurg Rev 5:169-172, 1982. 8. Hopkins LN, Budny JL, Castellani D: Extracranialintracranial arterial bypass and basilar artery liga­ tion in the treatment of giant basilar artery aneu­ rysms. Neurosurgery 13:189-194, 1983. 9. Hosobuchi Y: Direct surgical treatment of giant intracranial aneurysms. J Neurosurg 51:743-756, 1979. 10. Matsuda M, Shiino A, Handa J: Rupture of pre­ viously unruptured giant carotid aneurysm af­ ter superficial temporal-middle cerebral artery bypass and internal carotid occlusion. Neuro­ surgery 16:177-184, 1985. 11. Michael WF: Posterior fossa aneurysms simu­ lating tumours. J Neurol Neurosurg Psychiatry 37:218-223, 1974. 12. Morley TP, Barr HW: Giant intracranial aneu­ rysms: Diagnosis, course, and management. Clin Neurosurg 16:73-94, 1969. 13. Ojemann RG, Ogilvy CS, Crowell RM, Heros RC, eds: Surgical M anagement o f Cerebrovascular Disease. Baltimore, William & Wilkins, ed 3, 1995. 14. Onuma T, Suzuki J: Surgical treatment of giant in­ tracranial aneurysms. J Neurosurg 51:33-36, 1979. 15. Rozario RA, Stein BM: Ligation of the basilar artery as the definitive treatment for a giant aneurysm of the basilar artery apex: Case re­ port. Neurosurgery 6:87-91, 1980. 16. Scott RM, Ballantine HT Jr: Spontaneous throm­ bosis in a giant middle cerebral artery aneurysm: Case report. J Neurosurg 37:361-363, 1972. 17. Shintani A, Zervas NT: Consequence of ligation of the vertebral artery. J Neurosurg 36:447-450, 1972. 18. Sonntag VK, Yuan RH, Stein BM: Giant intra­ cranial aneurysms: A review of 13 cases. Surg Neurol 8:81-84, 1977. 19. Spetzler RF, Carter LP: Revascularization and aneurysm surgery: Current status. Neurosurgery 16:111-116, 1985. 20. Steinberg GK, Drake CG, Peerless SJ: Deliberate basilar or vertebral artery occlusion in the treat­ ment of intracranial aneurysms: Immediate re­ sults and long-term outcome in 201 patients. J Neurosurg 79:161-173, 1993. 21. Sundt TM Jr, Piepgras DG: Surgical approach to giant intracranial aneurysms: Operative experi­ ence with 80 cases. J Neurosurg 51:731-742, 1979. 22. Swearingen B, Heros RC: Fatal rupture of a thrombosed giant basilar artery aneurysm. Surg Neurol 23:299-302, 1985. 23. Yamada K, Hayakawa T, Ushio Y, Iwata Y, Koshino K, Bitoh S, Takimoto N: Therapeutic occlusion of the vertebral artery for unclippable vertebral aneurysm: Relationship between site of occlusion and clinical outcome. Neurosurgery 15:834-838, 1984. imal flow arrest would avoid distal coil embolization after detachment. Coils could then be stacked across the aneu­ rysm neck, in the aneurysm, and into the proximal vertebral artery. Alternatively because the authors knew that the patient would tolerate vertebral sacrifice, thev J might have been able to embolize the an­ eurysm fundus with large diameter nonGuglielmi detachable coils (i.e., vein of Galen coils). Because of their size, these coils would be unlikely to embolize out of the aneurysm neck and into the basilar C O M M EN TS The authors have provided an excel­ lent exam p le of the failure of H unterian ligation to provide end uring protection against subarachnoid h em orrhag e from intracranial aneurysm s. W e have had a J sim ilar case in the past of a w om an with a giant vertebral aneurysm w ho w as treated with end ovascu lar H unterian li­ gation. The patient initially did well, with docum ented aneurysm throm bosis or at least lack of aneurysm op acifica­ tion revealed by follow -up im aging. She returned several years later with sy m p ­ tomatic brain stem com p ression and was found to have both partial recana­ lization and aneurysm grow th. C o m ­ plete trapping and an eu rysm o rrh ap h v were perform ed. A side from transient lower cranial nerve neu ropathy, the p a ­ tient ultim ately did well. Despite numerous reports of successes with proximal feeding vessel ligation, we have tended to favor complete aneurysm trapping, either surgically or endovascularly, in cases such as that reported herein by Chang et al. Although it m akes intui­ tive sense that Hunterian ligation will promote thrombosis up to the next arte­ rial branch point (in this case, the verte­ bral con fl uens), we do not feel secure until the lesion is anatomically disconnected from the native circulation. This treatment holds true for congenital and acquired an­ eurysms and intracranial vessel dissections. O ur approach to the case described would have been focused on com p lete trapping. Interventionally, this could pos­ sibly have been achieved by using a d ou ­ ble lumen balloon catheter placed in the proximal right vertebral artery for antero­ grade flow arrest. Guglielmi detachable coils could then be advanced and depos­ ited fairly accurately distal to the lesion and proximal to the confluens. The prox­ Neurosurgery, Vol. 4 4 , No. 5 , May 1 4 4 4 artery, especially considering that the au­ thors determined that the distal neck was 1.5 cm proximal to the confluens. Finally, the authors might have obliterated the proximal right vertebral artery with coils and balloons, as they demonstrated, and then catheterized the right vertebral ar­ tery distal to the aneurysm via the left vertebral arterv J and confluens. Distal sacrifice could be achieved with Guglielmi detachable coils or balloons. If en d o v ascu lar trapping could not be achieved, w e w ould have considered surgical trapping and aneurysm evacu­ ation. A lthough the risks of lower cra­ nial nerve paresis with simple trapping of this large m ass are probably at least 60% , w e have found that the majority of patients recover with only mild subjec­ tive dysphagia. All o f our patients with posteroinferior cerebellar artery (PICA) an eu ry sm s that required tracheostomy and G -tu b e for dysphagia and aspira­ tion after surgery w ere decannulated b\ 6 m onths. In su m m ary , w e find th e a u th o rs case to be sobering, and despite n u m e r o u s reports of th e relative success of H unt­ e r ia n ligation f o r posterior c i r c u l a t i o n an eu ry sm s, we continue to favor either endovascular or surgical trapping with or without bvpass for those cases t h a t c a n n o t be primarily clipped or embolized. M ichael B. Horowitz D u k e Samson Dallas , Texas This is a case report of a giant verfc bral artery aneurysm that was t r e a t s by ipsilateral vertebral ligation with re suiting com p lete thrombosis of tlhe < eurvsm as dem onstrated angiognH