Complex Intracranial Aneurysms: Combined Operative and Endovascular Approaches Lotfi Hacein-Bey, M.D., E. Sander Connolly, Jr., M.D., Stephan A. Mayer, M.D., William L. Young, M.D., John Pile-Spellman, M.D., Robert A. Solomon, M.D. Divisions of Interventional Neuroradiology, Departments of Radiology (LH-B, W LY, JP-S), Neurological Surgery (ESC, W LY, JP-S, RAS), Neurology (SAM), and Anesthesiology (WLY), College of Physicians and Surgeons, Columbia University, New York, New York O B J E C T IV E : E n d o v a s c u la r m a n age m e n t o f c o m p le x in tra c ra n ia l a n e u ry sm s is in c re a s in g ly b e in g co n sid e re d as an a lte rn a tiv e to sta n d a rd s u rg ic a l c lip p in g . H o w e v e r, little a tte n tio n has been p a id to the c o m p le m e n ta ry nature of su rg e ry an d e n d o v a s c u la r th e ra p y. M E T H O D S : B etw een Se p te m b e r 1 9 9 2 and M ay 1 9 9 7 , 12 p a tie n ts w ith c o m p le x in tra c ra n ia l a n e u ry sm s w ere treated w ith c o m b in e d o p e ra tiv e and e n d o v a s c u la r m e th o d s. Se ve n p a tie n ts d e m o n stra te d s u h a ra c h n o id hemorrhage (tw o o f G ra d e II, tw o o f G ra d e III, and th ree o f G ra d e IV ). Five p a tie n ts d e m o n stra te d u n ru p tu re d aneurysm s, i.e., th ree g ia n t a n e u ry sm s (o n e v e rte b ro b a sila r ju n c tio n a n e u ry sm , o n e m id d le c e re b ra l a rte ry b ifu rc a tio n aneurysm, and one in te rn a l c a ro tid a rte ry -o p h th a lm ic a rte ry a n e u ry sm ), o n e la rg e in te rn a l c a ro tid a rte ry -o p h th a lm ic artery a n e u ry sm , an d o n e m id d le ce re b ra l a rte ry se rp e n tin e a n e u ry sm . M a n a g e m e n t stra te g ie s in v o lv e d eith er surgery fo llo w e d by e n d o v a sc u la r th e ra p y (S-E ; n = 5) o r e n d o v a s c u la r th e ra p y fo llo w e d by s u rg e ry (E -S ; n = 7). S-E p a ra d ig m s in c lu d e d a n e u ry sm e x p lo ra tio n fo llo w e d by e n d o v a s c u la r tre a tm e n t (S -E 1 ; n = 3), p a rtia l aneurysm c lip p in g fo llo w e d by e n d o v a sc u la r a n e u rysm p a c k in g (S -E 2 ; n = 1), and e x tra c ra n ia l-to -in tra c ra n ia l bypass fo llo w e d by e n d o v a sc u la r p aren t vessel o c c lu s io n (S -E 3 ; n = 1). E-S p a ra d ig m s in c lu d e d su p e rse le c tiv e angiog­ ra p h y fo llo w e d by s u rg ic a l c lip p in g (E -S 1 ; n = 2 ), G u g lie lm i d e ta c h a b le c o il p a rtia l d o m e p a c k in g follow ed by d e la ye d s u rg ic a l c lip p in g (E -S 2 ; n = 2), p ro x im a l te m p o ra ry ve ssel b a llo o n o c c lu s io n fo llo w e d by aneurysm c lip p in g (E -S 3 ; n = 2), and p ro x im a l p e rm a n e n t vessel o c c lu s io n fo llo w e d by s u rg ic a l a n e u ry sm decom pression fo r m ass effect tre atm en t (E -S 4 ; n = 1). R E S U L T S : Ele ve n a n e u ry sm s ( 9 2 % ) w e re c o m p le te ly e lim in a te d . T h e re m a in in g a n e u ry sm w a s 9 0 % obliterated and re m a in e d q u ie sce n t at the 3 4 -m o n th fo llo w -u p e x a m in a tio n , d e sp ite p re se n tin g w ith s u b a ra c h n o id hemorrhage. N o p atie n t e x p e rie n c e d repeat b le e d in g (fo llo w -u p p e rio d , 23 ± 28 m o ). T h e re w e re no d e ath s. O n e patient a c h ie v e d a fa ir o u tco m e (G la s g o w O u tc o m e S c a le sc o re o f III) ; a ll o th e r p a tie n ts e x p e rie n c e d e xc e lle n t outcomes (G la s g o w O u tc o m e S c a le sc o re o f I). In a ll case s, the a n e u ry sm m a n a g e m e n t p a ra d ig m ch o se n had a positive effect on d e fin itiv e th e ra p y. C O N C L U S I O N : S e v e ra l fa cto rs ca n c o n trib u te to the c o m p le x ity o f in tra c ra n ia l a n e u ry sm s. M an age m en t strategies that c o m b in e o p e ra tiv e an d e n d o v a s c u la r te ch n iq u e s in a c o m p le m e n ta ry w a y , fo r the best p o ssib le outcom es for these p atie n ts, ca n be d e sig n e d a c c o r d in g ly . (Neurosurgery 43:1 304—131 3, 1998) Key words: Combined approach, Complex aneurysms, Endovascular treatment, Microneurosurgery omplex intracranial aneurysms are not uncommonly encountered in cerebrovascular practice (1, 6-8, 11, 13, 18, 19, 32, 40, 42). Often their complexity can render standard treatment (i.e., surgical clipping) either impossible or exceedingly hazardous (Tabic 1). Although endovascular C 1304 therapy is an available alternative to surgical clipping (2, 4,5, 9, 10, 14-16, 20-22, 29, 31, 33, 41), it is not without risks (2— 40In contrast, a combined approach that uses the strengths ot the two methods in a synergistic way may enhance the chances of success in these challenging situations. We report Neurosurgery, Vol. 4 1 No. 6, Dec ember 1448 Combined Treatment of Complex Aneurysms TABLE 1. Factors Contributing to a Com plex Aneurysm Aneurysm Anatomy Clinical Factors Size: large or giant, too small for a clip or a coil Shape: fusiform, serpentine Content: filled with fresh or laminated thrombus Neurological condition: poor grade at presentation Timing: vasospasm at time of presentation General: significant cardiovascular, pulmonary, renal, or endocrine comorbidity Age: advanced age Neck: difficult surgical access, broad, calcified, involves perforating arteries Perianeurysmal environment: aneurysm embedded in brain tissue, bone, edema, scar tissue from previous surgery our experience with 12 such cases and propose management paradigms. PATIENTS A N D M E T H O D S Between September 1992 and May 1997, 12 patients with complex aneurysms of the posterior (n = 5) or anterior (n = 7) circulation were treated in a combined manner by neurosur­ gical and endovascular methods. The average age was 50 years (range, 25-70 yr); five patients were male, and seven were female. Seven patients presented with subarachnoid hemorrhage (SAH) proven by computed tomographic scan­ ning, with two cases of Hunt and Hess Grade II, two of Grade III, and three of Grade IV. Five other patients presented with extraordinarily complex unruptured aneurysms, i.e., one gi­ ant distal vertebral artery aneurysm, one giant middle cere­ bral artery (MCA) aneurysm, one serpentine MCA aneurysm, and two carotid artery-ophthalmic artery aneurysms (Table 2). Factors contributing to and consistent with a complex an­ eurysm were identified for each patient. Three patients pre­ sented with a poor Hunt and Hess grade (Grade IV) after SAH. Associated problems, i.e., coronary artery disease (Pabent 1), severe vasospasm (Patients 1 and 8), and unfavorable aneurysm location (large midbasilar and low basilar locations m Patients 1 and 2, respectively), were present for these three patients. For the remaining nine patients, the complexity was mainly related to the aneurysm itself, i.e., restricted surgical access to the neck (Patients 3, 4, 5, and 9), embedding of the aneurysm in surrounding tissues (Patients 3, 4, 5, and 9), giant ^ize (Patients 7, 9, and 11), the presence of laminated throm­ bus (Patient 9), and broad neck (Patients 4, 6, 11, and 12). Treatment decisions for all 12 patients were made after Multidisciplinary consultation that involved neurosurgical, endovascular therapeutic, neurological, and anesthesiological ^ervices. The management strategy was either surgery fol°wed by endovascular therapy (S-E) (n = 5) or endovascular therapy followed by surgery (E-S) (n = 7) (Table 3). S"E paradigms included aneurysm exploration followed by end°vascular treatment (S-El; n = 3), partial aneurysm clipPln8 followed by endovascular aneurysm packing (S-E2; n = 1), j^nd extracranial-to-intracranial bypass followed by endovascuar parent vessel occlusion (S-E3; n = 1). E-S paradigms included N e u r o s u r g e r y , Vol. superselective angiography followed by surgical clipping (E-Sl; n = 2), partial dome packing with Guglielmi detachable coils (GDC) followed by delayed surgical clipping (E-S2; n = 2), proximal temporary vessel balloon occlusion followed by an­ eurysm clipping (E-S3; n = 2), and proximal vessel occlusion followed by surgical aneurysm decompression for mass effect treatment (E-S4; n = 1). Treatment was performed within 5 days after SAH for all seven patients who presented with bleeding. Patients with unruptured aneurysms were treated within 4 weeks of pre­ sentation. Heparin was administered intravenously to all pa­ tients during endovascular explorations (including superse­ lective angiography), embolization, or temporary arterial occlusion during surgical exploration. Also, patients who pre­ sented with SAH received heparin treatment for a few days after aneurysm obliteration. RESU LTS C lin ic a l o u tco m e s Eleven patients experienced excellent outcomes, defined as no neurological deficit at the time of the most recent follow-up examination (Glasgow Outcome Scale score of 1). One patient (Patient 2) experienced a fair outcome (Glasgow Outcome Scale score of 3 at a 2-yr follow-up examination), as a result of a thromboembolic complication (the only one in this series). After GDC packing of a large, recently ruptured, basilar apex aneurysm, this patient continued to receive heparin therapy to protect a large thalamo-perforating artery originating from the aneurysm base. Heparin administration was discontinued 4 hours later for the placement of a ventricular drain. A few hours later, the patient developed acute right third nerve palsy and left hemiparesis, and computed tomography dem­ onstrated an upper brain stem and right thalamic infarction. The patient eventually made a reasonable recovery, with moderate residual hemiparesis and diplopia. A n e u ry sm o b lite ra tio n All aneurysms were eventually eliminated, with the excep­ tion of one large midbasilar aneurysm (Patient 4). After SAH 43,No. December 1998 1305 1306 Hacein-Bey et al. T A B LE 2. D em ographic and C lin ic a l Data for 12 Patients with C o m p le x Cerebral Aneurysm s Complication Outcome Follow-up Period (mo) Excellent Fair 30 34 S-E1 None Midbrain infarction after embolization None Excellent 12 S-E1 None Excellent 34 S-E2 None Excellent 17 S-E1 None Excellent 35 E-S1 None Excellent 34 E-S1 None Excellent 56 E-S4 None Excellent 9 S-E3 None Excellent 12 E-S3 None Excellent 4 E-S3 None Excellent 2 Difficulty Factor Treatment Paradigm SAH/IV SAH/IV Poor grade after SAH Poor grade after SAH E-S2 E-S2 Large basilar apex SAH/II 38 Large midbasilar SAH/III M 42 Small anterior communicating SAH/II 6 F 52 SAH/III 7 M 25 8 F 50 9 M 70 Large ICAophthalmic Giant MCA bifu rcation Small anterior communicating Giant distal VA Difficult surgical access Broad neck, embedded in brain tissue Embedded in brain tissue, previous surgery Broad neck, embedded in bone Perforators near aneurysm neck Poor grade after SAH 10 M 47 11 F 66 12 F 42 Age Patient Gender (yr) Aneurysm/) 1 2 M F 65 33 Small mid-basilar Large basilar apex 3 F 69 4 F 5 Large serpentine MCA Giant ICAophthalmic Large ICAophthalmic Presentation/Grade Headaches SAH/IV X-XII cranial nerve compression Headaches, loss of consciousness Progressive vision loss Headaches Giant aneurysm with laminated thrombus Fusiform shape Broad neck, embedded in dura Broad neck, embedded in dura 7 MCA, middle cerebral artery; VA, vertebral artery; SAH, subarachnoid hemorrhage; E-S, endovascular therapy followed by surgery; S-E, surgery followed by endovascular therapy; ICA, internal carotid artery. h Aneurysm size: small, < 1 0 mm; large, 10 to 25 mm; giant, > 25 mm. TABLE 3. Management Paradigms for Com plex Aneurysms E-S Paradigms S-E Paradigms E-S1: superselective angiography —> surgical clipping E-S2: endovascular aneurysm dome packing —» surgica clipping E-S3: proximal temporary vessel balloon occlusion —» aneurysm clipping E-S4: endovascular proximal permanent occlusion —» surgica aneurysm decompression S-E1: surgical exploration —» endovascular treatment S-E2: partial surgical clipping -^endovascular aneurysm obliteration S-E3: EC-IC bypass —> endovascular parent vessel occlusion E-S, endovascular therapy followed by surgery; S-E, surgery followed by endovascular treatment; EC-IC, extracranial-to-intracranial. and unsuccessful GDC packing of the aneurysm dome, sur­ gical exploration revealed that the aneurysm was embedded in the pons and therefore unclippable. During the subsequent 1 month, the patient developed progressive left-sided facial weakness, diplopia, and hemisensory loss in the trigeminal distribution. Repeat angiography revealed that the aneurysm had grown, and repeat magnetic resonance imaging sug­ gested that a short circumferential, brain stem perforator had been occluded. GDC packing of the aneurysm fundus was then performed, with little effect on subsequent aneurysm growth. Finally, staged bilateral vertebral artery balloon oc­ clusion was performed, with evidence of gradual aneurysm obliteration to approximately 90% in follow-up angiograms. IL L U S T R A T IV E C A S E S Patient 1 w as a 65-year-old m ale patient with hypertension and coronary artery disease, for w hich he had recently undergone a coronary artery b y p ass graft. H e presented with Hunt and Hess G rad e IV. An initial an giog ram yielded norm al findings; a second angiogram revealed a sm all m id basilar aneu rysm {Fig. 1 A). The pa­ tient w as initially treated with partial (95%) aneurysm coil packing {Fig. IB ), to allow him to be treated in the intensive care unit during the critical vasosp asm / rep eat h em orrh age period. Although the clin­ ical cou rse for this patient w as initially com plicated by sepsis, hydro cephalus requiring a ventriculoperitoneal shunt, and deep venous throm bosis requiring placem ent of a Greenfield filter, the patient eventually m ad e a good recovery. Delayed surgical clipping of the Neurosurgery , Vol. 41, No. 6, Hoc ember 1948 Combined Treatment of Complex Aneurysms n o 7 V ' ■ ■* A FIG U R E 1. A to C, Patient 1, a 65-year-old male patient with hypertension and coronary artery disease who presented in Hunt and Hess Grade IV condition. % A small basilar aneurysm ^ (A, arrowhead) was initially treated with partial (9 5 % ) aneurysm coil packing ( B, arrowhead) to allow management in the intensive care unit during the critical period. Delayed aneurysm clipping was performed uneventfully, after repeat angiography showed a patent neck (C, arrowhead). L eurysm w as eventually p erform ed uneventfully, after repeat an )graphy showed a p aten t n e c k <• whQ suffered a G ra d e 11 Patient 5 was a 43-year-old m a p anterior com m unicatiH from a broad-necked, upw ard v Poin ; ' hnicany difficult, in /r• 9 a \ Qnr{?0 rv w as tecnn j artery aneurysm (Fig. I M - =>u r & .v placed across rt because of n u m ero u s p erforators, w o treated in the intene aneurysm neck. T h e p atien t w as s u c c e s s f u l y r e a p e d ^ re care unit for v asosp asm . R ep eat a W ™ ™ ^ du ced the n eck 2 0 confirmed eurysm was patent, although partia c ippi -e presence I * < Fof» n* u »• m erou s p erfora f “ k i " 8 as possible (Fig. 2D). Patient 9 was a 70-year-old e m p lo y e usi perienced a 3-m onth history o f in creasin g ^vprutive w h o had jUent d j ZZiness, d w eight lo ss. it ataxia, and loss o f appetite, resu ltin g m a eaj ed a partially 'aluation by m agnetic reso n an ce rombosed giant an eu ry sm co m p res ography suggested that the ;ht vertebral artery (Fig. 3B). D esp m edulla (Fig. 3A). An-nate(j from the distal g an R e g r e s s i v e presigm oid found to b e unclip- aniectomy for exploration, the ane^ sn\ ible. Three m onths later, h y d ro cep a peritoneal shunt was placed. The patien wa eloped and a ventricurppxamined 3 m onths orns^ jncluding ter because of further p ro g ression o Q:i.aHn a a w alker), and urseness of voice, w o rsen in g ataxia n eces ^ ovascu j ar balloon piration pneum onia. A t that p oin t, an as placed across the an eu ry sm n eck in 6 ig. 3C), after successful tem p orary test occ ^ e aneurysm w as found to b e fully t co mpression (Fig. 3D ), the sig n s o f m edulh y vertebral artery ^ ^eW Weeks later, ^ su rgical deession quickly solvedV, erienced a generalized Patient 1 0 was driving his car w h en e exP g e n e t i c resonance nic-clonic seizure, w ith loss o f co n scio u sn es M C A aneurysm 'aging showed a 2 -cm , partially throm bosed , FIG U R E 2. A to D, Patient 5, a 43-year-old male patient who suffered a Grade II SAH from a broad-necked, upwardly pointing, anterior com m unicating artery aneurysm (A). Sur­ gery was technically difficult, in part because of numerous perforators; two clips were placed across the aneurysm neck. Repeat angiograms showed that the aneurysm remained patent, with partial neck clipping (B, arrowhead). Superse­ lective angiography confirmed the presence of numerous perforators (C ). Total G D C aneurysm packing was possible (D , arrowhead). (Fig. 4A ). A ngiography revealed a serpentine aneu rysm , with two posterior parietal branches arising from its distal part (Fig. 4B). S u r­ gical exploration confirm ed the fusiform nature of the lesion, and a graft w as perform ed that connected the superficial tem poral artery to the M CA distal to the aneurysm . The follow ing day, bypass patency w as confirm ed (Fig. 4C ) and the M C A branch afferent to the a n e u ­ rysm w as occluded for 2 0 m inutes with a platinum coil. The patient passed the test, and the vessel w as perm anently occluded, resulting in aneurysm exclusion (Fig. 4D ). D IS C U S S IO N Direct clipping of intracranial aneurysms is currently the standard of care whenever possible with acceptable operative risks (1, 2, 5-9, 11, 13, 15, 18-20, 29, 31-33, 40, 41). Endovas­ cular management (usually GDC packing) is generally re­ served for patients for whom the risk/benefit ratio for direct surgery is considered greater than that for endovascular treat­ ment (1, 6-8, 11, 13, 18-20, 29, 31, 32, 40, 42). The estimated risk/benefit ratio for each treatment method is highly variable among operators (with varying experience levels and philos­ ophies). As a result, different institutions may elect to treat similarly complex lesions in different ways, based on both anatomic factors (aneurysm size, shape, content, and neck configuration and perianeurysmal reaction) and clinical fac­ tors (neurological grade, timing of presentation, presence of N e u r o s u r g e r y , Vol. 43 , No. 6, December 1998 1308 Hacein-Bey et al »I rM p r f r * r -i A FIG U R E 3. A to D, Patient 9, a 70-year-old male patient with a 3-month history of increasing intermittent dizziness, gait ataxia, and loss of appetite, resulting in a 30-pound weight loss. Magnetic resonance imaging revealed a partially thrombosed giant aneurysm compressing the medulla (A, arrowheads). Angiographic results suggested that the aneurysm originated from the distal right vertebral artery (B, arrowhead). Endovascular balloon occlusion across the aneurysm neck in the distal vertebral artery was performed (C, arrowhead) after successful temporary test occlusion. A few weeks later, the aneurysm was found to be fully thrombosed; after surgical decompression (D , arrowhead ), the signs of m edullary compression quickly resolved. vasospasm, general medical condition, and patient age) (Table 1). Although several reports have attempted to delineate the supe­ riority of one method or the other in certain settings, the advan­ tages of a multidisciplinary team approach to aneurysm treat­ ment have not been well documented. Although neurosurgical rescue for coil migration, endovascular vessel rupture, or clip­ ping of coil-treated aneurysm remnants (2, 5, 15, 41) and endo­ vascular packing of partially clipped aneurysms (Patient 5) have been reported (10), combined management paradigms that em­ brace proactive team evaluation to optimally use the strengths of these divergent techniques to treat difficult conditions have not been highlighted. The advantages of such a combined philoso­ phy can be represented as management paradigms (Tabic 3). S u p e rse le c tiv e a n g io g ra p h y b efo re su rg e ry Aneurysm anatomy is often difficult to completely delin­ eate during routine preoperative angiography. Certain fac­ tors, including unstable patient condition, moderate experi­ ence of the angiographer, limitations in contrast medium resulting from systemic patient disease, the presence of vaso­ FIG U R E 4. A to D, Patient 10, a 47-year-old male patient who was driving his car when he experienced a generalized tonic-clonic seizure, with loss of consciousness. Magnetic resonance im aging showed a 2-cm , partially thrombosed, M CA aneurysm (A). Angiography (postbypass study shown) revealed a serpentine aneurysm, with two posterior parietal branches arising from its distal part ( B ). Surgical exploration confirm ed the fusiform nature of the lesion, and a superficial temporal artery-distal M CA bypass graft was performed. The follow ing day, bypass patency was confirm ed (C ), and the M CA branch afferent to the aneurysm was occluded with a platinum coil (D , arrowhead). spasm or intra-aneurysmal thrombus, and the presence of nu­ merous overlying vessels, may contribute to suboptimal assess­ ment of neck and perforator anatomic features. Superselective angiographic aneurysm exploration before surgery may prove useful in selected cases, especially when information on the anatomic features and number of neighboring perforators is crucial. With experienced investigators, this should outw eigh the potential risks of superselective aneurysm angiography (throm­ bus migration and perforation). For Patient 7, information re­ garding the exact location of the M2-MCA branches associated with the neck of the giant MCA bifurcation aneurysm not only was helpful in guiding eventual clip placement but also influ­ enced the decision to pursue clipping, rather than proximal occlusion after distal bypass. Another advantage of preoperative superselective aneu­ rysm neck exploration for broad-neck aneurysms neighboring arterial bifurcations, such as the MCA bifurcation, lies in the precise identification of branches involved in the aneurvsm neck, for which a distal bypass is necessary for clipping to bt most effective. Such information should help avoid the de\ astating effect of bypassing the noninvolved branch. Neurosurgery, Vol. 43, No. (•>, December 1998 Combined Treatment of Complex Aneurysms Temporary e n d o v a sc u la r p ro te c tio n fo r p atien ts w ith SAH who are at h igh risk Although the effect of poor neurological grade at presen­ tation on the outcomes for surgically treated patients is well documented (32), it has also been demonstrated that, with aggressive surgical clipping, favorable outcomes could be obtained for patients with poor Hunt and Hess grades. This was the case for 55% of patients of Grade IV condition and 25% of those of Grade V condition in a recent study (25, 26). Also, in the same study, intraoperative complications (failure to occlude the aneurysm, intraoperative rupture, and cerebral contusion) were no greater among patients of poor-grade condition undergoing early surgery than among those of good-grade condition, at least for anterior circulation aneu­ rysms (25, 26). In addition, age alone has been reported not to be associated with markedly increased surgical complication rates (11). Nonetheless, in clinical practice, early surgery for patients of poor-grade condition (Grades IV and V) with difficult aneurysms is not advocated (41). It is also widely thought that older patients, who are more likely than younger patients to present with a poorer clinical status at admission, a larger amount of subarachnoid blood, higher incidences of hydrocephalus and intraventricular hemorrhage, more preex­ isting medical conditions, and a greater incidence of symp­ tomatic vasospasm because of diminished cerebrovascular reserve (23), should be more strongly considered for endovas­ cular therapy whenever possible (5, 14, 29, 33, 41, 43). Several groups have demonstrated the effectiveness of en­ dovascular GDC aneurysm treatment in protecting patients at high risk from subsequent bleeding (5, 14, 29, 33, 43). How­ ever, procedural morbidity (9-31%) and mortality (2-9%) rates were highly variable among groups (5, 14, 29, 33, 43). Although troubling, these values can be compared with those of generally accepted surgical results, namely 14% overall morbidity and 27% mortality rates in a largely quoted series °f 153 patients (37). Perhaps somewhat more disappointing are the reported short-term angiographic follow-up results; although 20-70% of aneurysms underwent initially total oblit­ eration (5, 14, 29, 33, 43), 15-30% recanalization was reported at 12 months (5-33). Furthermore, delayed bleeding at 6 months (29), symptomatic regrowth requiring retreatment in nearly one-third of the patients at the 3-year follow-up exam­ inations (33), and no overall improvements in outcomes and mortality rates for patients of poor-grade status, especially those with basilar aneurysms (29, 33), were all reported in initial studies. Fortunately, in a large, more recent, multicenter study (43) of 403 patients, the overall morbidity rate lvas °nly 8.9% and the mortality rate was only 6.2%. Although these values compare favorably with reported neurosurgical results, it is not unreasonable to expect significantly better results in an established practice, because two important char­ acteristics of the study were a patient selection bias toward Patients at high risk, who were considered poor surgical Candidates, and wide variations in operator skills (during the lrhtial learning period for some). F°r these reasons, partial endovascular aneurysm packing, 0 °btain temporary protection without compromising future 1309 surgical management, has been advocated (2, 5, 15, 21, 22, 41, 43). This is not always possible or easy, because of the mul­ tiplicity of aneurysm configurations; future clipping can be rendered extremely difficult, often requiring prolonged tem­ porary occlusion and aneurysm opening for coil extraction before final clip placement (2, 41). However, such a sequential approach was successful for Patients 1 and 2 in this series, for whom the crucial protective effect of partial endovascular aneurysm packing was compatible with delayed permanent surgical clipping. The authors think that, whenever techni­ cally and logistically possible, patients with complex aneu­ rysms at high risk should be treated with temporary partial endovascular occlusion, followed by surgical clipping. It has also been suggested that ruptured giant or broad-necked an­ eurysms should undergo partial GDC packing followed by further embolization or surgical clipping (43), although these types of aneurysms may be treated with surgical clipping during temporary balloon occlusion of the parent vessel (39) or, in selected cases, with permanent occlusion of the parent vessel, if tolerated (1, 6, 8, 9). Intraop erative tem porary b alloo n o cclu sio n for clip p in g Large aneurysms of the ophthalmic segment can be diffi­ cult to treat. Recent improvements in microsurgical tech­ niques, such as complete removal of the posterior orbit, optic strut, and superior orbital fissure, have contributed to making many of these aneurysms clippable. Also, suction decompres­ sion techniques have been shown to be of help. All of these maneuvers require proximal control of the extracranial inter­ nal carotid artery (ICA), which is most commonly obtained by surgical exposure of the cervical carotid artery. Also, certain posterior circulation aneurysms, such as large posteroinferior cerebellar artery or basilar apex aneurysms, greatly benefit from proximal control of the vertebral artery. Intraoperative endovascular techniques are well suited for proximal control of cervical arteries and decompression (39). One factor that might explain the lack of popularity of intraoperative endo­ vascular techniques, in addition to the need for specialized equipment and excellent team coordination, is the require­ ment for heparin treatment. Indeed, with extensive bone ma­ nipulation, heparin treatment can potentially aggravate blood loss. However, we and others (39) have found that rapid technique, timely coordination among operators, and experi­ ence with the procedures allow the use of minimal amounts of heparin. Other advantages to this approach include the ability to extemporaneously confirm angiographically determined optimal clip placement, postclipping documentation of aneu­ rysm obliteration, and obviation of the need for surgical ex­ posure of the carotid artery in the neck. E n d o v a sc u la r a rte ria l o c c lu s io n fo r a n e u rysm d e co m p re ssio n Aneurysms can present with mass effects that are alleviated by decompression, either by aneurysm sac packing or by parent vessel occlusion (16). In the anterior circulation, the currently preferred treatment for cavernous ICA aneurysms and certain complex posterior ICA aneurysms involves ICA N e u r o s u r g e r y , Vol. 43, No. 6, December / 998 1310 Hacein-Bey et al occlusion. The effectiveness of hunterian ligation is greatest when the aneurysm neck is occluded, and it decreases grad­ ually as the occlusion is more remote from the neck. Endo­ vascular balloon occlusion provides the ability to occlude the vessel close to the aneurysm, which also reduces the likeli­ hood of "stump emboli" (9). For vertebrobasilar aneurysms originating just distal to the posteroinferior cerebellar artery and midbasilar aneurysms originating just distal to critical midbrain perforators, as demonstrated by superselective an­ giography, proximal ligation or trapping via direct clipping is the recommended treatment, because balloons may occlude the origins of critical vessels. More proximal balloon occlu­ sion, which is slightly less effective but safer, was performed for Patient 4, with a basilar bifurcation aneurysm that could not be treated by clipping or coil placement. Vertebral artery balloon occlusion across the neck of a giant distal vertebral aneurysm allowed thrombosis of the lesion before successful surgical debulking for mass effect treatment for Patient 9. E x p lo ra to ry su rg e ry b e fo re e n d o v a sc u la r tre atm e n t In some circumstances, only exploratory craniotomy con­ firms, for a surgeon, that a complex aneurysm is unclippable. Also, total aneurysm neck clipping is not always possible, for a variety of reasons (presence of perforators, lack of adequate exposure, lack of an adequate clip, calcification in the neck region of the aneurysm, and partial intracavemous location). However, exploratory or incomplete surgery should not be viewed as a failure, because it may provide important infor­ mation to the interventional neuroradiologist. Observations regarding the thinnest part of an aneurysm wall or, even better, muslin wrapping of the thin aneurysm wall contrib­ utes to the safety of subsequent endovascular treatment, by helping avoid dome perforation by a catheter or coils. boembolism, with resultant ischemic stroke, were not uncom­ mon. Furthermore, antegrade flow was not always completely obliterated, especially in the case of carotid artery bifurcation or basilar apex lesions, which often continued to fill via fetal posterior communicating arteries. Balloon test occlusion has allowed functional evaluation in conscious patients, thereby greatly improving patient selec­ tion. This test has become even more effective with the advent of additional pharmacological challenges. When test occlu­ sion is tolerated, subsequent occlusion with complete hepa­ rinization decreases thromboembolic complications; as a re­ sult, this approach has become the treatment of choice for certain aneurysms, such as giant proximal intradural carotid artery aneurysms. For patients who do not tolerate test occlu­ sion, a preliminary extracranial-to-intracranial bypass (either superficial temporal artery-MCA or external carotid arteryMCA, with reversed saphenous vein) is performed. These bypasses can, in some cases, result in such profound flow alteration that aneurysm thrombosis is promoted before final parent vessel occlusion, as was the case for Patient 10 in our series. O b s ta c le s There are several potential obstacles to the development of a completely integrated approach to aneurysm management, such as differences in perceived roles among various specialty teams, geographic separation of operating rooms and endo­ vascular suites within health facilities, and the current lack of guidelines for the training of interventionalists. In addition, the lack of unbiased outcome data for either management strategy may contribute to creating distrust among participants in the two groups. However, increased communication between groups is the best approach to transcend these barriers. P a rtia l s u rg ic a l c lip p in g fo llo w e d by e n d o v a sc u la r a n e u rysm o b lite ra tio n Completion of aneurysm obliteration by endovascular means after partial clipping has been reported (10). Partial clipping also reduces the size of the neck, making compaction of the coil mass less technically challenging and safer. Other advantages to this approach involve the information provided by the surgeon regarding the perianeurysmal environment, such as the presence of perforators, and the possibility of further protecting the aneurysm by wrapping it with muslin. E n d o v a sc u la r a rte ria l o c c lu s io n after b yp ass Hunterian or proximal ligation of parent arteries has long been used for the treatment of both anterior and posterior circulation aneurysms (1, 6-9, 11, 13, 18-20, 29, 31, 32, 40, 42). Traditionally, ICA ligation was performed extracranially by surgical ligation, and posterior fossa aneurysms were treated either by direct vertebral artery sacrifice distal to the postero­ inferior cerebellar artery or by basilar occlusion between the superior cerebellar artery and the posterior cerebral artery segments. Because of the lack of preoperative functional test­ ing and postoperative heparinization, flow failure and throm­ C O N C L U S IO N S Not infrequently, the therapeutic difficulties presented by complex cerebral aneurysms are not appreciated prospectively, for a variety of reasons, including the severity of the disease and the need to provide protection from s u b s e q u e n t hemorrhaging. Treating physicians, whether neurosurgeons or interventional neuroradiologists, may find themselves pressed to exceed the limits of their techniques. However, the availability of other options and their judicious integration in patient care may have a positive effect on outcomes. Temporary endovascu­ lar protection of aneurysms before clipping, endovascular d e l i n ­ eation of perforator anatomic features before surgery, comple­ tion of aneurysm packing after partial clipping, intraoperative temporary balloon occlusion of the parent vessel to assist s u r g i ­ cal clipping, and bypass surgery before endovascular occlusion are all possible using combined surgical/endovascular manage­ ment strategies. When used rationally, this approach emphasizes the complementary nature of these techniques and offers the — best chance for reducing treatment morbidity and improving long-term outcomes in the most difficult cases. Neurosurgery , Vol. 43 , No. 6, December 1998 • Combined Treatment of Complex Aneurysms Received, January 23, 1998. Accepted, July 31, 1998. 17. Heros RC: T h rom boem b olic com plications after com bined inter­ Reprint requests: Lotfi H acein-Bey, M.D., D iagnostic and Interven­ tional Neuroradiology Section, D ep artm ent of Radiology, University of Vermont College of M edicine, 1 1 1 C olchester A venue, Burlington, VT 05401. nal carotid ligation and extracranial to intracranial bypass. Su rg N eurol 2 1 :7 5 -7 9 , 1984. 18. Heros RC, Nelson PB, O jem ann RG, Crow ell RM, Debrun G: Large and giant paraclinoid aneurysm s: Surgical techniques, c o m ­ plications and results. N eu rosu rgery 12:153-163, 1983. 19. H igashida RT, Halbach VV, Hieshim a GB, W einstein PR, Hoyt REFERENCES WF: Treatm ent of a giant carotid op hthalm ic artery aneurysm by . Barnett DW, Barrow DL, Josep h GJ: C om bined extracranialintracranial bypass and intraoperative balloon occlusion for the 1 1311 intravascular balloon em bolization therapy. S u rg N eurol 3 0 :3 8 2 386, 1988. treatment of intracavernou s and proxim al carotid artery an eu ­ rysms. Neurosurgery 3 5 :9 2 -9 8 , 1994. 20. H igashida RT, Hieshim a GB, Halbach VV, G oto K: Cervical ca­ 2. Batjer HH: A neurysm clipping after end ovascu lar treatment with coils: A report of eight patients. Neurosurgery 38 :960 -961 , 1996 (comment). loon em bolization therapy. Acta R adiol S u p p l 3 6 9 :5 9 1 -5 9 3 , 1986. 3. Casasco AE, A ym ard A, G obin YP, H oudart E, Rogopoulos A, George B, Hodes JE, C o p h ig n o n J, M erland JJ: Selective en d ov as­ cular treatment of 71 intracranial an eu rysm s with platinum coils. J Neurosurg 7 9 :3 -1 0 , 1993. 4. Chavis TD, H opkins LN: Early treatm ent of ruptured aneurysm s with Guglielmi d etachable coils: Effect on subsequent bleeding. Neurosurgery 3 7 :6 4 7 -6 4 8 , 1995 (com m ent). 5. Civit T, Auque J, M archal JC , Bracard S, Picard L, H epner H: Aneurysm clipping after en d o v ascu lar treatm ent with coils: A report of eight patients. N eurosurgery 3 8 :9 5 5 -9 6 1 , 1996. 6 . Debrun G, Fox A, D rake C, Peerless S, G irvin J, Ferguson G: Giant unclippable aneurysm s: T reatm en t with detachable balloons. AJNR Am J Neuroradiol 2 :1 6 7 -1 7 3 , 1981. 7. Drake CG: Giant intracranial aneurysm s: Experience with surgi­ cal treatment in 174 patients. Clin Neurosurg 26:12-9 5, 1979. 8 . Drake CG, Peerless SJ, Ferguson G G : H unterian proxim al arterial occlusion for giant an eu ry sm s of the carotid circulation. J Neuro­ surg 81:656-665, 1994. 9. Fox AJ, Vinuela F, Pelz DM , Peerless SJ, Ferguson G G , Drake CG, Debrun G: Use of d etachable balloons for proxim al artery occlu­ sion in the treatm ent of un clip pable cerebral aneurysm s. J Neuro­ rotid artery aneu rysm s and pseud oaneurysm s: Treatm ent by b al­ 21. Kurokaw a Y, Abiko S, O kam u ra T, W atanabe K: Direct surgery for giant aneurysm exhibiting progressive enlargem ent after intraaneurysm al balloon em bolization. Su rg N eurol 3 8 :1 9 -2 5 , 1992. 22. Ladouceur DL: Transcranial clipping of recurrent cerebral an eu ­ rysm s after endovascular treatment. S tro k e 2 4 :1 0 8 7 -1 0 8 9 , 1993. 23. Lanzino G, Kassell NF, G erm anson TP, K ongable G L, Truskow ski LL, Tom er JC, Jane JA: Age and outcome after aneurysmal subarach­ noid hemorrhage: W hy do older patients fare worse? J Neurosurg 85:410-418, 1996. 24. Larson JJ, Tew JM Jr, T om sick TA, van Loveren HR: T reatm ent of aneurysm s of the internal carotid artery by intravascular balloon occlusion: Long-term follow -up of 58 patients. N eu ro su rg ery 36: 2 6 -3 0 , 1995. 25. LeRoux PD, Elliott JP, N ew ell DW , G rad y MS, W inn HR: The incidence of surgical com plications is sim ilar in good and poor grade patients undergoing repair of ruptured anterior circulation aneurysm s: A retrospective review of 355 patients. N eu rosu rg ery 38:887 -895 , 1996. 26. LeRoux PD, Elliott JP, N ew ell DW , G rad y MS, W inn HR: Predict­ ing outcom e in poor-grade patients with subarachnoid h em o r­ rhage: A retrospective review of 159 aggressively m anaged cases. J N eu rosu rg 8 5:3 9 -4 9 , 1996. 27. Linskey ME, Sekhar LN, Horton JA, Hirsch W L Jr, Y onas H: surg 66:40-46, 1987. 10. Fraser KW, Halbach VV, T eitelbau m GP, Sm ith TP, H igashida RT, Dowd CF, W ilson CB, H ieshim a GB: Endovascular platinum coil A neurysm s of the intracavernous carotid artery: A m ultidisci­ embolization of incom pletely surgically clipped cerebral an eu ­ 28. M atas R: Testing the efficiency of the collateral circulation as a rysms. Surg Neurol 4 1 :4 -8 , 1994. 11. Fridriksson SM , H illm an J, Saveland H, Brandt L: Intracranial prelim inary to the occlusion of the great surgical arteries. A n n aneurysm surgery in the 8 th and 9th decades of life: Im pact on population-based m an ag em en t outcom e. Neurosurgery 3 7 :6 2 7 632, 1995. 29. M cD ougall CG , Halbach VV, Dowd CF, H igashida RT, Larsen 12. Gilbasch GM, H arders AG: M orbidity and m ortality after early 1 1 plinary approach to treatment. J N eu rosu rg 75:525-534, 1991. Su rg 5 3 :1 -4 3 , 1911. DW, H ieshim a GB: Endovascular treatm ent of basilar tip a n e u ­ rysm s using electrolytically detachable coils. J N eu rosu rg 8 4 :3 9 3 399, 1996. aneurysm surgery: A p rospective study with nim odipine p reven ­ 30. M cGrail KM , Heros RC, D ebrun G, Beyerl BD: A n eu rysm of the tion. Acta Neurochir (Wien) 9 6 :1 -7 , 1989. Gobin YP, Vinuela F, G u rian G H , G uglielm i G, D uckw iler GR, Massoud TF, M artin N A : T reatm en t of large and giant fusiform ICA petrous segm ent treated by balloon entrapm ent after EC-IC intracranial aneurysm s with G uglielm i detachable coils. J Neuro­ surg 84:55-62, 1996. 14’ Graves VB, Strother C M , D uff TA , Perl J II: Early treatment of ruptured aneurysm s with G u glielm i detachable coils: Effect on subsequent bleeding. N eurosurgery 3 7 :6 4 0 -6 4 8 , 1995. 15- Gurian JH, Martin N A, K ing W A , D uckw iler GR, G uglielm i G, Vinuela F: N eurosurgical m an ag em en t of cerebral aneurysm s following unsuccessful or incom plete end ovascu lar em bolization. I Neurosurg 8 3:8 4 3 -8 5 3 , 1995. 6- Halbach VV, H igashida RT, Dowd CF, Barnwell SL, Fraser KW , Smith TP, Teitelbaum G P, H ieshim a GB: The efficacy of endosaccular aneurysm occlusion in alleviating neurological deficits pro­ duced by mass effect. J N eurosurg 8 0 :6 5 9 -6 6 6 , 1994. N e u ro su rg e ry , bypass: Case report. J N eu rosu rg 65 :24 9-25 2, 1986. 31. M olyneux AJ: Giant carotid aneurysm s: Treatm ent by detachable balloons. Acta R ad iol S u p p l 369:59 7-599 , 1986. 32. Peerless SJ, H ernesniem i JA, G utm an FB, D rake CG: Early surgery for ruptured vertebrobasilar aneurysm s. J N eu rosu rg 8 0:6 43-6 49, 1994. 33. Raym ond J, Roy D, Bojanow ski M, M oum djian R, L 'E sp eran ce G: Endovascular treatm ent of acutely ruptured and unruptured a n ­ eurysm s of the basilar bifurcation. J N eu rosu rg 86 :2 1 1 -2 1 9 , 1997. 34. Roski RA, Spetzler RF, Nulsen FE: Late com plications of carotid ligation in the treatm ent of intracranial aneurysm s. J N eu rosu rg 54:583-587, 1981. 35. Schievink WI: M edical progress: Intracranial aneurysm s. N Engl J M ed 3 36 :28 -40, 1997. Vol. 43, No. 6, December 1998 1312 Hacein-Bey et al. 36. Schm idt JH III, W itsberger TA: Treatm ent of giant intracranial aneurysm with carotid ligation, sap henous vein bypass graft. W V Med ] 8 8:3 4 6 -3 4 7 , 1992. 37. Seiler RW , Reulen HJ, H uber P, G rolim und P, Ebeling U, Steiger HJ: O u tcom e of aneurysm al subarachnoid hem orrhage in a hos­ pital population: A prospective study including early operation, intravenous nim odipine, and transcranial D oppler ultrasound. Neurosurgery 2 3 :5 9 8 -6 0 4 , 1988. 38. Sekhar LN, Patel SJ: Perm anent occlusion of the internal carotid artery during skull-base and vascular surgery: Is it really safe? Am J Otol 14:421-422, 1993 (com m ent). 39. Shucart W A , K w an ES, H eilm an CB: T em p orary balloon o cclu ­ sion of a proxim al vessel as an aid to clipping an eu rysm s of the basilar and paraclinoid internal carotid arteries: Technical note. Neurosurgery 27 :11 6-11 9, 1990. 40. Sinson G, Philips MF, Flamm ES: Intraoperative end ovascu lar surgery for cerebral aneurysm s. J Neurosurg 8 4 :6 3 -7 0 , 1996. 41. Solom on RA: A neurysm clipping after end ovascu lar treatm ent with coils: A report of eight patients. Neurosurgery 38:961, 1996 (com m ent). 42. Taki W, Nishi S, Y am ashita K, Sadatoh A, N akahara I, Kikuchi H, Iwata H: Selection and com bination of various end ovascu lar tech­ niques in the treatm ent of giant aneurysm s. J Neurosurg 77:37-4 2, 1992. 43. Vinuela F, D uckw iler G, M aw ad M: G uglielm i detachable coil em bolization of acute intracranial aneurysm : Perioperative a n a ­ tomical and clinical ou tcom e in 403 patients. J Neurosurg 8 6 :4 7 5 482, 1997. CO M M EN TS Hacein-Bey et al. describe their experience with 12 patients with complex intracranial aneurysms who were treated with combined operative and endovascular methods. Although these approaches have been reported in simple case reports from other institutions, the authors have systematically sum­ marized the options from both the endovascular and surgical perspectives. In Table 3, the authors discuss the management paradigms for complex aneurysms and, in the category of endovascular followed by surgical treatment, they indicate that supraselective angiography might lead to surgical clip­ ping because of a large neck or perforator involvement, which would preclude endovascular therapy. Our experience with computed tomographic angiography has demonstrated that supraselective angiography is often not necessary to delineate these features, but computed tomographic angiography is extremely useful in assessing not only neck size but also the presence of critical perforators in areas that could only be treated surgically and that would be at high risk from endo­ vascular occlusion. In addition, endovascular dome packing followed by surgical clipping has not actually been shown to reduce repeat bleeding, although the authors observed no repeat hemorrhaging in this small group of patients. We also have provided aneurysm protection by incomplete endovas­ cular obliteration, but our approach has been to treat the entire lesion with coils, if at all possible. If a delayed recur­ rence occurs, then certainly these patients can be treated with definitive surgical therapy; proximal temporary balloon oc­ clusion and suction decompression have been found to be extremely useful in the treatment of giant paraclinoid aneu­ rysms and aneurysms of the posterior circulation. These tech­ niques provide excellent decompression of the sac and are easily performed intraoperatively from a transfemoral route. It has not been our experience that the heparin infusion asso­ ciated with this technique leads to increased blood loss. There is no question that partial surgical clipping of large complex aneurysms may lead to successful endovascular obliteration, by transforming large-necked aneurysms into small-necked aneurysms, allowing safe coil placement within the aneurysms without fear of parent vessel occlusion, and providing better long-lasting obliteration rates by controlling the inflow zone. Obviously, this finding must be investigated in a larger study. Most importantly, the authors, from a very experienced neurovascular center, emphasize that a multidis­ ciplinary approach is essential for the best patient care and we should put aside differences in perceived roles among various specialty teams. It is hoped that, in the future, the approach to such complex aneurysms will be multidisciplinary. Robert H . Rosenwasser Philadelphia, Pennsylvania The authors report the management outcomes for 12 pa­ tients with complex intracranial aneurysmal disease. This re­ port emphasizes the necessity for a collaborative and multi­ disciplinary approach to these difficult problems. The authors draw our attention to several specific aspects of the diagnos­ tic, therapeutic, and postoperative periods for which the com­ bination of intravascular and extravascular approaches is sen­ sible. Clinicians can evaluate each case in terms of the assets and liabilities of each specific therapeutic alternative and can develop well-considered strategies onlv by working as a co­ hesive team. As the authors have illustrated, unexpected events during the course of treatment mandate a flexible approach, with reconsideration of alternatives to the origi­ nally planned strategy. It is becoming clearer that certain lesions are best treated by microsurgery and other lesions are best treated by endovas­ cular techniques. However, there is an increasing percentage of lesions for which the best treatment is not obvious. It is these lesions that the authors have discussed in the context of a true multidisciplinary approach. It is important to remem­ ber that the advent of microsurgery was originally thought to have solved the problem of simple and complex intracranial aneurysms. The development of endovascular techniques was similarly thought, several years ago, to provide the definitive solution. Time has clarified this issue and has confirmed that we do not now have the means to manage the most complex forms of this condition. The dysplastic vasculature leading to complex large and giant aneurysms defies straightforward treatment. Regardless of the strategies applied, it is critical that long-term follow-up monitoring (for many years) be used for these patients. Despite comments to the contrary, recur­ rence remains a lifetime risk, regardless of treatment strategy, for patients with complex aneurysms. Neurosurgery, Vol. 43, No. 6, December 1C)C)8 H. H unt B atjer C h ic a g o , Illinois