Endovascular treatment of ruptured posterior circulation aneurysms using electrolytically detachable...

12
Endovascular Treatment of Ruptured Posterior Circulation Cerebral Aneurysms Clinical and Angiographic Outcomes Todd E. Lempert, MD; Adel M. Malek, MD, PhD; Van V. Halbach, MD; Constantine C. Phatouros, MD; Philip M. Meyers, MD; Christopher F. Dowd, MD; Randall T. Higashida, MD Background and Purpose—We sought to describe the clinical outcome and angiographic results obtained in the endovascular therapy of ruptured posterior circulation cerebral aneurysms using Guglielmi detachable coils (GDC) over a 7-year period. Methods—A retrospective analysis was performed of 112 patients evaluated at the University of California at San Francisco Medical Center between June 1991 and August 1998. The Hunt-Hess grade at presentation of treated patients was I in 26 patients (24%), II in 24 (22%), III in 27 (25%), IV in 24 (22%), and V in 8 (7%). Clinical follow-up for the total population was achieved in 104 of 109 patients (96%), with a mean duration of 13.1 months. Angiographic follow-up for the subset excluding parent vessel occlusion cases was obtained in 93% of cases, with a mean duration of 7.2 months. Results—Technical success, defined as the ability to catheterize and embolize the aneurysm with GDC, was achieved in 109 of 112 of cases (97%). The mean angiographic occlusion rate, or projected area of the aneurysm occluded by the coils, for all 110 successfully treated aneurysms was 94.6%. At latest clinical follow-up, 81 of 109 patients (74%) achieved good recovery with Glasgow Outcome Scale (GOS) score of I, 10 of 109 (9%) were moderately (GOS II) and 5 of 109 (5%) were severely (GOS III) disabled, 1 of 109 (1%) remained in a vegetative state (GOS IV), and 12 of 109 (11%) were dead. Of the subset of 77 patients with Hunt-Hess grades I to III, 68 (88%) achieved a good clinical outcome (GOS I). A statistically significant correlation was demonstrated between Hunt-Hess grade at presentation and final GOS outcome score (x 2 541.4, P,0.0005). Procedure-related permanent morbidity was 2.8% (3/109 patients). Repeated hemorrhage was observed in a single patient (0.9%) with a partially treated aneurysm. Conclusions—The observed favorable outcome and low morbidity in this group of high-risk patients point to GDC embolization as an effective method for the endovascular management of patients with ruptured posterior circulation aneurysms. (Stroke. 2000;31:100-110.) Key Words: cerebral aneurysm n embolization, therapeutic n occlusion n outcome n subarachnoid hemorrhage T he management of patients with aneurysmal subarach- noid hemorrhage (SAH) caused by rupture of posterior circulation aneurysms presents a technically difficult prob- lem. 1 The surgical exposure needed for the clipping of aneurysms of the posterior circulation is considered compar- atively more challenging than in other locations. 2 The coin- cident presence of acute SAH with the associated cerebral edema and adhesion of aneurysm to the surrounding throm- bus further compounds the challenge of accessing aneurysms located near deep brain stem structures with interposed cranial nerves and perforator arteries. 3 The difficulty of treating these aneurysms in the acute phase of SAH is mirrored by the higher rate of complications and morbidity compared with lesions of the anterior circulation. 4 Endovas- cular treatment of difficult intracranial aneurysms in patients in poor clinical condition has had an increasingly important role in the management of ruptured aneurysms. The recent advent of the Guglielmi electrolytically detachable coil (GDC) has enabled a safer and more controlled form of endovascular therapy. 5 To describe the utility, safety, and intermediate-term efficacy of GDC therapy in a high-risk subset of patients, we report our experience in the endovas- cular treatment of ruptured posterior circulation aneurysms. Subjects and Methods From June 1991 to August 1998, 112 patients with acute or subacute SAH from ruptured posterior circulation aneurysms were evaluated Received June 22, 1999; final revision received October 6, 1999; accepted October 6, 1999. From the Departments of Radiology, Division of Interventional Neurovascular Radiology (T.E.L., A.M.M., V.V.H., C.C.P., P.M.M., C.F.D., R.T.H.) and Neurosurgery (V.V.H., C.F.D., R.T.H.), University of California at San Francisco. Correspondence to Adel M. Malek, MD, PhD, Division of Interventional Neurovascular Radiology, UCSF Medical Center, Room L-352, 505 Parnassus Ave, San Francisco, CA 94143. E-mail [email protected] © 2000 American Heart Association, Inc. Stroke is available at http://www.strokeaha.org 100 by guest on March 17, 2016 http://stroke.ahajournals.org/ Downloaded from

Transcript of Endovascular treatment of ruptured posterior circulation aneurysms using electrolytically detachable...

Endovascular Treatment of Ruptured PosteriorCirculation Cerebral Aneurysms

Clinical and Angiographic Outcomes

Todd E. Lempert, MD; Adel M. Malek, MD, PhD; Van V. Halbach, MD;Constantine C. Phatouros, MD; Philip M. Meyers, MD;Christopher F. Dowd, MD; Randall T. Higashida, MD

Background and Purpose—We sought to describe the clinical outcome and angiographic results obtained in theendovascular therapy of ruptured posterior circulation cerebral aneurysms using Guglielmi detachable coils (GDC) overa 7-year period.

Methods—A retrospective analysis was performed of 112 patients evaluated at the University of California at SanFrancisco Medical Center between June 1991 and August 1998. The Hunt-Hess grade at presentation of treated patientswas I in 26 patients (24%), II in 24 (22%), III in 27 (25%), IV in 24 (22%), and V in 8 (7%). Clinical follow-up forthe total population was achieved in 104 of 109 patients (96%), with a mean duration of 13.1 months. Angiographicfollow-up for the subset excluding parent vessel occlusion cases was obtained in 93% of cases, with a mean durationof 7.2 months.

Results—Technical success, defined as the ability to catheterize and embolize the aneurysm with GDC, was achieved in109 of 112 of cases (97%). The mean angiographic occlusion rate, or projected area of the aneurysm occluded by thecoils, for all 110 successfully treated aneurysms was 94.6%. At latest clinical follow-up, 81 of 109 patients (74%)achieved good recovery with Glasgow Outcome Scale (GOS) score of I, 10 of 109 (9%) were moderately (GOS II) and5 of 109 (5%) were severely (GOS III) disabled, 1 of 109 (1%) remained in a vegetative state (GOS IV), and 12 of 109(11%) were dead. Of the subset of 77 patients with Hunt-Hess grades I to III, 68 (88%) achieved a good clinical outcome(GOS I). A statistically significant correlation was demonstrated between Hunt-Hess grade at presentation and finalGOS outcome score (x2541.4,P,0.0005). Procedure-related permanent morbidity was 2.8% (3/109 patients). Repeatedhemorrhage was observed in a single patient (0.9%) with a partially treated aneurysm.

Conclusions—The observed favorable outcome and low morbidity in this group of high-risk patients point to GDCembolization as an effective method for the endovascular management of patients with ruptured posterior circulationaneurysms.(Stroke. 2000;31:100-110.)

Key Words: cerebral aneurysmn embolization, therapeuticn occlusionn outcomen subarachnoid hemorrhage

The management of patients with aneurysmal subarach-noid hemorrhage (SAH) caused by rupture of posterior

circulation aneurysms presents a technically difficult prob-lem.1 The surgical exposure needed for the clipping ofaneurysms of the posterior circulation is considered compar-atively more challenging than in other locations.2 The coin-cident presence of acute SAH with the associated cerebraledema and adhesion of aneurysm to the surrounding throm-bus further compounds the challenge of accessing aneurysmslocated near deep brain stem structures with interposedcranial nerves and perforator arteries.3 The difficulty oftreating these aneurysms in the acute phase of SAH ismirrored by the higher rate of complications and morbidity

compared with lesions of the anterior circulation.4 Endovas-cular treatment of difficult intracranial aneurysms in patientsin poor clinical condition has had an increasingly importantrole in the management of ruptured aneurysms. The recentadvent of the Guglielmi electrolytically detachable coil(GDC) has enabled a safer and more controlled form ofendovascular therapy.5 To describe the utility, safety, andintermediate-term efficacy of GDC therapy in a high-risksubset of patients, we report our experience in the endovas-cular treatment of ruptured posterior circulation aneurysms.

Subjects and MethodsFrom June 1991 to August 1998, 112 patients with acute or subacuteSAH from ruptured posterior circulation aneurysms were evaluated

Received June 22, 1999; final revision received October 6, 1999; accepted October 6, 1999.From the Departments of Radiology, Division of Interventional Neurovascular Radiology (T.E.L., A.M.M., V.V.H., C.C.P., P.M.M., C.F.D., R.T.H.)

and Neurosurgery (V.V.H., C.F.D., R.T.H.), University of California at San Francisco.Correspondence to Adel M. Malek, MD, PhD, Division of Interventional Neurovascular Radiology, UCSF Medical Center, Room L-352, 505 Parnassus

Ave, San Francisco, CA 94143. E-mail [email protected]© 2000 American Heart Association, Inc.

Stroke is available at http://www.strokeaha.org

100 by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

for endovascular treatment with the use of GDC (Target Therapeu-tics) at the University of California at San Francisco (UCSF) MedicalCenter. A retrospective analysis and review were undertaken of thehospital and outpatient charts, the operative report, and all angio-graphic, CT, and MR studies. This was supplemented by follow-upclinical examination and telephone interviews.

Angiographic AnalysisQuantitative measurement of aneurysm size was performed with theuse of digital subtraction angiographic projections obtained withexternally placed 1-cm reference washers to correct for geometricmagnification. Studies performed after 1996 used an on-boardangiographic digital computer (Toshiba Corporation) for measure-ment of aneurysm height, width, and neck size. The analysisincluded determination of aneurysm shape, degree of aneurysmocclusion, and extent of aneurysm recanalization. The angiographicprojections of the aneurysm used during initial treatment andsubsequent follow-up studies were separately analyzed by 2 neu-rointerventional radiologists to determine the rate of occlusion of theaneurysm, which is the proportion of the projected area of theaneurysm occluded by coil placement. A third independent neurora-diologist was called on for arbitration in cases of discrepancy. Onehundred percent occlusion was assigned only to aneurysms withdense packing and no contrast filling of the aneurysm fundus orneck. Aneurysm neck remnants were determined with respect to thetotal projected area of the aneurysm.

Clinical Outcome MeasuresClinical condition at the time of treatment was determined with theHunt-Hess grading scheme.3 Outcome was measured with theGlasgow Outcome Scale (GOS)6 (in which GOS I corresponds togood recovery and resumption of normal life despite minor deficits,GOS II to a moderately disabled but independent patient, GOS III toa severely disabled [but conscious] patient who is dependent onothers for daily support, GOS IV to a persistently vegetative state,and GOS V to death); the Quality of Life Outcome Scale (QOL)7 (inwhich QOL 1 corresponds to a patient with normal lifestyle, QOL 2to a patient with minor neurological dysfunction but who is able toperform activities of daily living without help, QOL 3 to a patientneeding assistance with daily activities, QOL 4 to one unable toperform activities of daily living and requiring full-time care, andQOL 5 to death); and the modified Rankin scale.8 Members of theUCSF neurovascular neurology team performed initial inpatientneurological examinations. Clinical data were obtained from neuro-logical examinations by UCSF neurovascular neurologists duringfollow-up angiographic studies, from examinations by patients’referring neurosurgeons and neurologists, and by telephone inter-views with a neurosciences clinical nurse specialist.

Clinical Management and Technical ComplicationsAdditional information included the interval between SAH andtreatment, dates of retreatment, medical history and complications,initial signs and symptoms and their progression or resolution,rebleeding, presence or absence of vasospasm, treatment of vaso-spasm, adverse events during diagnostic angiography, adverse eventsduring GDC embolization, and delayed complications. Adverseevents were categorized by type of adverse event, imaging charac-teristics, and adverse event outcome.

Statistical AnalysisClinical information, procedural information, follow-up, and angio-graphic data of all endovascular aneurysm treatments performed atUCSF since 1991 were maintained in a database, and statisticalanalysis was performed with the SAS Institute software package.ANOVA was used to compare outcome scores versus presentationand treatment characteristics, and the Tukey-Kramer honestly sig-nificant difference correction was used for comparison as appropri-ate. Additionally, Pearson’sx2 test was used to determine marginalhomogeneity among nominal variables. A value ofP#0.05 wasconsidered statistically significant.

Embolization TechniqueThe majority of cases used relied on general anesthesia by adedicated neuroanesthesiology team with neuromuscular blockade toprevent patient motion and improve control over patient hemody-namics in the case of an adverse event such as aneurysm perforation.A 6F or 7F vascular access sheath (Avanti, Cordis Endovascular)was inserted in the common femoral artery. Complete diagnosticangiography was performed through a 5F UCSF-II (Cordis) or 7FBerenstein (USCI-Bard) catheter with the use of biplane high-resolution digital subtraction angiography to evaluate the presenceand extent of vasospasm and other intracranial vascular anomalies.After the optimal orthogonal view for embolization was determined,a baseline activated clotting time was obtained, and the patient wasgiven a weight-based bolus of intravenous heparin (70 U/kg bodywt). A repeated activated clotting time was obtained after the initialbolus, and additional heparin was administered to achieve a valuebetween 250 and 300 seconds. Maintenance heparin was adminis-tered hourly at half the initial bolus dose. The heparin was reversedwith an appropriate dose of intravenous protamine sulfate at the endof the procedure. After therapeutic anticoagulation was confirmed, a6F (Envoy, Cordis) thin-walled, straight guide catheter was placedfor vascular access. With the use of magnified real-time fluoroscopyand digital road-mapping techniques, a microcatheter (0.010F to0.018F) was placed coaxially through the guide catheter and directedinto the aneurysm with the aid of a microguidewire (0.010F to0.016F). In cases of complex vascular anatomy, the microcatheterwas appropriately steam-shaped to accommodate complex curves.GDC embolization of aneurysms was performed with GDC T10(Target Therapeutics) electrolytically detachable coils. In cases ofsaccular aneurysms that had a definable neck, coils were used toobliterate the aneurysm fundus without impinging on the parentvessel. In fusiform ruptured aneurysms, the coils were used toocclude the aneurysmal segment of the parent vessel. Patients whounderwent intentional parent vessel occlusion did not routinelyundergo long-term follow-up surveillance angiography after deter-mination of satisfactory occlusion at the end of the initial study withdocumentation of complete flow arrest. This management protocolwas determined on the basis of the observation that a completelyoccluded parent artery does not undergo late recanalization9 (Figure1). After embolization, the patient was transferred to the neurologicalintensive care unit, under the joint care of members of the Depart-ment of Anesthesia and dedicated intensive care specialists from theneurovascular neurology team.

ResultsPatient Demographics and Clinical PresentationThe mean age was 52 years; age ranged from 18 to 79 years.There were 77 women (69%) and 35 men (31%). All patientsin this series had an acute or subacute SAH and wereclassified according to Hunt and Hess.3 The median time totreatment after initial SAH was 4 days. The stratification oftreated patients was as follows: grade I in 26 patients (24%),grade II in 24 patients (22%), grade III in 27 patients (25%),grade IV in 24 patients (22%), and grade V in 8 patients (7%).

Aneurysm Characteristics and MorphologyThe most prevalent location was at the basilar bifurcation in55 patients (49%) (Figure 2). Among treated aneurysms, 40(37%) were saccular in shape and had a narrow neck(,4 mm), 14 (13%) were saccular and harbored a wide neck(.4 mm), 25 (23%) were fusiform, 19 (18%) were irregularlyshaped or multilobed, and 8 (7%) were giant. Figure 3 showsa histogram distribution of the aneurysms by neck size(Figure 3A) and largest fundus dimension (Figure 3B).

Lempert et al Endovascular Treatment of Ruptured Posterior Circulation Aneurysms 101

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

Angiographic and Neurological Follow-UpAngiographic follow-up was obtained in 76 of 82 patients(93%) treated with preservation of the parent vessel, with amean angiographic follow-up of 7.2 months (range, 1 day to55 months). Clinical follow-up was achieved in 104 of the109 treated patients (95%). The mean duration of neurolog-ical follow-up was 13.1 months (median, 9.5 months; range,5.1 to 56 months).

Technical SuccessEndovascular treatment was successfully performed in 109 of112 patients (97%; Figure 4). In 3 patients (3%), the decisionto abort treatment was made after attempts to deploy the coilsin the aneurysm were not successful. In 1 case with a fusiformleft vertebral artery aneurysm and a contralateral right verte-bral artery occlusion, the coils could not be placed withoutcompromising flow in the parent vessel. In a second case ofa fusiform basilar artery aneurysm, coils could not be placedthat did not encroach on the parent vessel lumen. In the thirdcase of a basilar tip aneurysm that incorporated the posteriorcerebral arteries in the neck, no coil conformation could befound that did not encroach on the posterior cerebral arteries.

Angiographic OutcomeIn this series of 110 aneurysms, 82 aneurysms were treatedwith preservation of the parent vessel, and 76 of 82 (93%)underwent follow-up angiography; the distribution of dura-

Figure 1. A 53-year-old man suffered a Hunt-Hess grade IIISAH, as demonstrated by CT (A). Injection of the right vertebralartery outlines the fusiform aneurysm, which begins beyond theorigin of the posterior inferior cerebellar artery (B). The aneu-rysm was treated by parent vessel occlusion (PVO) with multipleelectrolytically delivered GDC (C). Follow-up angiography at 24hours after coil deployment into the fusiform aneurysm showsthat a right vertebral injection fills the posterior inferior cerebellarartery but not the distal right vertebral artery, confirming angio-graphic thrombosis of the aneurysm.

Figure 2. Anatomic location of ruptured posterior circulationaneurysms treated with GDC embolization. SCA indicates supe-rior cerebellar artery; PICA, posterior inferior cerebellar artery;and VB, vertebrobasilar.

Figure 3. Morphology and angiographic characteristics of rup-tured posterior circulation aneurysms. A, Largest angiographicaneurysm fundus dimension. B, Distribution of aneurysm neckdimensions.

Figure 4. A 38-year-old man suffered a Hunt-Hess grade I SAH.Angiography performed 9 days later identified an aneurysm atthe origin of the left posterior inferior cerebellar artery measuring4 mm with a 2-mm neck before (A) and after (B) embolizationwith GDC.

102 Stroke January 2000

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

tion between initial procedure and latest angiographicfollow-up is shown in Figure 5A. The initial mean angio-graphic occlusion rate for all 110 successfully treated poste-rior circulation aneurysms was 94.6%. The mean percentocclusion at final angiographic follow-up was 94.9%. Theinitial and final angiographic occlusion rates were determinedby aneurysm type for the subset of non–parent vessel occlu-sion aneurysms that underwent angiographic follow-up(n582) (Figure 6).

Aneurysms at the most common location, the basilarbifurcation (n553), showed an initial occlusion rate of 96.6%and final occlusion rate of 95.1%. The results indicateocclusion at latest follow-up of.90% in all locations exceptfor lesions of the basilar trunk, which were characterized bya wide neck and difficult morphology. Figure 7 illustrates acase of basilar tip aneurysm.

Overall, 54% of the non–parent vessel occlusion aneu-rysms were embolized to 99% to 100%, 40% were occludedto 90% to 99%, and 6% were incompletely occluded (#90%)after initial embolization. Aneurysm neck size was found tobe correlated with a lower final percent occlusion (Figure8A). The final occlusion rate in the subset of aneurysms withneck size,4 mm showed significantly higher final occlusioncompared with those with neck size of 4 to 6 mm (P,0.05)and those with neck size.8 mm (P,0.0001). Similarly, atrend was also identified between aneurysm fundus sizeand final extent of occlusion, with aneurysms with afundus.12 mm having a significantly lower rate of finalocclusion than those measuring 3 to 6 and 6 to 9 mm(P,0.002) (Figure 8B).

Recanalization After TreatmentOf the 76 aneurysms with angiographic follow-up, 77.6%(59/76) showed no evidence for recanalization, while

22.4% (17/76) did. Analysis of the aneurysms demonstrat-ing recanalization revealed that 88.2% (15/17) had either aneck size.4 mm (16 aneurysms) or were fusiform (1aneurysm). Two patients with initial 100% occlusionsshowed evidence of recanalization on follow-up angiogra-phy. The first showed 3% recanalization at 7 months andunderwent no further treatment. The second was a patient

Figure 6. Quantitative analysis of the extent of aneurysm occlu-sion assessed by angiographic contrast exclusion arranged byanatomic location at completion of the initial embolization pro-cedure and at latest angiographic follow-up (F/U). Abbreviationsare as defined in Figure 2 legend.

Figure 7. A 49-year-old woman suffered a Hunt-Hess grade I SAH.Angiography of the left vertebral artery injection reveals a basilar tipaneurysm measuring 6 mm and harboring a 4-mm neck (A, antero-posterior projection; B, lateral projection). The aneurysm wastreated with GDC, as shown by the posttreatment angiogram (C).Follow-up angiography at 9 months reveals persistent occlusionand stable appearance of the coil mass (D).

Figure 5. Duration between aneurysm embolization and latestneurological follow-up (F/U) in 104 of 109 treated patients (A)and duration between initial embolization and latest angio-graphic follow-up in 76 of the 82 aneurysms not treated by par-ent vessel occlusion (PVO) (x axis is on a logarithmic scale) (B).

Lempert et al Endovascular Treatment of Ruptured Posterior Circulation Aneurysms 103

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

with a basilar tip aneurysm initially showing 15% recan-alization at 28-month follow-up who underwent an unsuc-cessful attempt at retreatment. The patient returned 16months later with further recanalization to 25% andunderwent successful retreatment with occlusion of 99%.A follow-up angiogram 9 months later showed no changein aneurysm appearance.

Clinical OutcomeClinical follow-up for .1 month was achieved in 104 of 109treated patients (95%; mean duration, 13.1 months) (Figure5B). At latest follow-up, 74% (81/109) of patients showedgood recovery (GOS I), 9% (10/109) had moderate disability(GOS II), 5% (5/109) were severely disabled (GOS III), 1%(1/109) were vegetative (GOS IV), and 11% (12/109) weredead (Figure 9A). Overall, 83% (91/109) of patients had goodrecovery or moderate disability (GOS I and II) at the time offinal follow-up. A statistically significant correlation betweenHunt-Hess grade at presentation and final GOS outcomescore was demonstrated (x2541.4, P,0.0005). All 26 pa-tients presenting in Hunt-Hess grade I had a final score ofGOS I. Of the 24 patients presenting in Hunt-Hess grade II,88% (21/24) improved to a final score of GOS I, 4% (1/24)had a final score of GOS III, and 8% (2/24) deteriorated tolower scores. Of 27 patients presenting in Hunt-Hess gradeIII, 78% (21/27) improved to GOS I, 15% (4/27) improved toGOS II, 4% (1/27) remained at GOS III, and 4% (1/27)

deteriorated to GOS V. Of the 24 patients presenting withHunt-Hess grade IV, 46% (11/24) recovered to GOS I, 21%(5/24) improved to GOS II, 8% recovered (2/24) to GOS III,1 recovered to GOS IV (4%), and 21% (5/24) deteriorated toGOS V status. Of the 8 patients with Hunt-Hess grade V atpresentation, 25% (2/8) improved to GOS I, 13% (1/8) toGOS II, 1 to GOS III, while 50% (4/8) deteriorated to GOSV. Overall, of the patients presenting in Hunt-Hess grades I toIII, 88% achieved a GOS I outcome score on final follow-up.

We used the QOL to assess the status of treated patients atfinal follow-up. A statistically significant relationship be-tween Hunt-Hess grade at presentation and final QOL scorewas demonstrated (x2554.6, P,0.00001) (Figure 9B). Asimilar analysis of the modified Rankin outcome at latestfollow-up established a significant correlation with Hunt-Hess grade at time of treatment (x2571.1, P,0.00001)(Figure 9C).

Other variables at presentation were analyzed for theirpotential contribution to patient outcomes. Specifically, thepresence of vasospasm was found to be inversely correlatedwith final clinical outcome as measured by GOS score(x2515.6, P,0.008). In contrast, patient age, sex, the pres-ence of recanalization, the need for subsequent retreatment,and the location of the aneurysm were not significantlycorrelated with patient clinical outcome.

Figure 8. Relationship between aneurysmal neck dimensions (A)and greatest aneurysmal dome dimension (B) and final angio-graphic occlusion rate in the subset of non–parent vessel occlu-sion aneurysms.

Figure 9. A, Final GOS score with respect to Hunt-Hess gradeat presentation for patients with ruptured posterior circulationaneurysms shows a statistically significant correlation by Pear-son’s test (x2541.4, P,0.0005). B, QOL index with respect toHunt-Hess grade at treatment indicates a statistically significantcorrelation (x2554.6, P,0.00001). C, Modified Rankin scoreindex at latest follow-up with respect to Hunt-Hess grade atpresentation (x2571.1, P,0.00001).

104 Stroke January 2000

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

TABLE 1. Technical Complications and Cases Leading to Morbidity

Age/Sex Aneurysm LocationSAH HHGrade Nature of Complication Symptoms Treatment Outcome

Complications associated with permanent morbidity or mortality

67/F Giant basilar trunkaneurysm

III Delayed rehemorrhage inrecanalized aneurysm (70%) 3 yafter treatmentVertebral artery dissection

ComaNone

MedicalNone

DeathAsymptomatic

52/F Superior cerebellaraneurysm

III Delayed PCA vasospasm/occlusion(day 9)

Blindness,Anton’s syndrome

Superselectivepapaverine andurokinaseinfusion

Partial recovery of leftvisual field

34/F Intracranial fusiformvertebral arteryaneurysm

III Ventromedullary infarct afterconsecutive craniotomy(unsuccessful) and embolization

Left hemiparesis Hypervolemia Improved to mildhemiparesis

67/F Superior cerebellaraneurysm

IV Pontine hemorrhage, not adjacentto aneurysm and without asubarachnoid component

Obtundation,hydrocephalus

Externalventriculardrain

Significantly improved

Complications without permanent morbidity or symptoms

44/M Basilar bifurcationaneurysm

II Intraprocedural aneurysmperforation

Hydrocephalus Reversal ofanticoagulant,completed coilembolization,ventriculardrain

No permanentmorbidity

45/F Vertebrobasilarjunction aneurysm

IV Distal branch occlusion Asymptomatic Heparin 24 h,follow-upangiography

Angiographicresolution, nopermanent morbidity

34/F Fusiform PCA(P2-segment)fetal-type PCA

III Retrograde thrombosis from PCAafter parent vessel occlusion of P2segment

Focal partial rightMCA thrombosis,hemisphericischemia

Superselectiveurokinaseinfusion

Successful completerecanalization withoutinfarct, no permanentmorbidity

47/F Superior cerebellaraneurysm

I Nonocclusive thrombus at coilinterface

Asymptomatic Heparin 24 h,follow-upangiography

Angiographicresolution, nopermanent morbidity

39/F Vertebrobasilarjunction

III Nonocclusive thrombus at coilinterface

Asymptomatic Heparin 24 h,follow-upangiography

Angiographicresolution, nopermanent morbidity

55/F Basilar bifurcationaneurysm

III Nonocclusive thrombus at coilinterface

Asymptomatic Systemicabciximab (GpIIb/IIIa)

Angiographicresolution, nopermanent morbidity

62/F Intracranialwide-neckedvertebral artery

III Coil encroachment on parentartery, leading to delayed vertebralartery occlusion

Asymptomatic No treatment No permanentmorbidity

57/F Basilar bifurcationaneurysm

II Coil encroachment on PCA Asymptomatic Heparin 24 h,follow-upangiography

Angiographicresolution, nopermanent morbidity

49/F Posterior inferiorcerebellar aneurysm

I Coil encroachment on PCACoil fracture during sameprocedure

AsymptomaticAsymptomatic

Heparin 24 h,follow-upangiographSnareredirection ofcoil end intoaneurysm

Angiographicresolution, nopermanent morbidityAngiographicresolution, nopermanent morbidity

34/F Wide-neckedmid-basilar

II Coil unraveling Asymptomatic Coilsuccessfullysnared

Angiographicresolution, nopermanent morbidity

64/F Basilar bifurcationaneurysm

III Coil unraveling Asymptomatic Coilsuccessfullysnared

Angiographicresolution, nopermanent morbidity

HH indicates Hunt-Hess; PCA, posterior cerebral artery; MCA, middle cerebral artery; and Gp, glycoprotein.

Lempert et al Endovascular Treatment of Ruptured Posterior Circulation Aneurysms 105

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

Complications Associated WithEndovascular Therapy

Aneurysm ReruptureOne patient suffered late rebleeding (0.9%, 1/109 patients).This patient was a Hunt-Hess grade III with a ruptured giantfusiform distal basilar artery aneurysm that was treated witha staged embolization. A 90% occlusion was achieved butwas complicated by an asymptomatic dissection of the leftvertebral artery that progressed to a complete occlusion.Despite a good neurological recovery, a follow-up angiogram21 months later showed 15% recanalization, but no furthertreatment was attempted because of inability to access theaneurysm. The patient suffered a recurrent SAH 3 years afterinitial treatment. An angiogram after the rehemorrhageshowed a stable 75% occlusion. The patient died fromcomplications related to recurrent hemorrhage.

Procedure-Related Mortality and MorbidityThere were no cases of procedure-related mortality in theseries. Overall, there were 3 complications leading to perma-nent morbidity, for a rate of 2.8% (3/109 cases) (Table 1).Eight procedure-related complications were encountered thatdid not lead to a neurological deficit and were transient, for arate of 7.3% (8/109 cases). These included 1 case of aneu-rysmal rupture, 1 case of asymptomatic branch occlusionsuccessfully treated with superselective infusion of urokinase,

3 cases of transient nonocclusive thrombus, and 4 cases ofherniation of a portion of a GDC into the parent vessel. Weencountered technical problems during coil placement in 2patients that necessitated coil removal by use of a microsnaredevice (Microvena).

Medical ComplicationsPatients in this cohort suffered concurrent medical complica-tions, some of which were related to SAH. One patientsuffered a myocardial infarction and aspiration pneumoniaafter treatment. Another patient developed a pulmonaryembolus, which was treated to an uneventful recovery withanticoagulation. One patient with a Hunt-Hess grade V SAHsuffered a repeated hemorrhage before treatment and subse-quently developed severe vasospasm that was aggressivelytreated. The patient also developed pancreatitis, candidasinusitis, and severe fungemia. Three patients developedgastrointestinal bleeding, possibly due to stress ulcers.

MortalitySixteen treated patients died (16/109, 15%) during the courseof this study. Nine of the sixteen (56%) presented initially inHunt-Hess grade IV or V. This subset of patients had poorinitial neurological condition, refractory vasospasm withsubsequent infarction, and comorbid medical conditions(pneumonia, sepsis, congestive heart failure, and pulmonaryedema). None of these patients showed improvement in their

TABLE 2. Published Reports Describing Endovascular Therapy Using GDC

SERIES nCompletelyOccluded

#95%Occluded PC RC

Neck#4 mm

Size,15 mm

GradeI SAH

OverallOutcome

Excellent/Good

HH I/II

Excellent Good

UCSF 107 54%* 22% 100% 22.4% 37% N/A 24% 100% 83% 90% N/A

Pierot29 35 62% 38% 100% 14% N/A 91% 60% 91% 91% 91% N/A

Klein24 21 67% 33%† N/A 14% 57% 71% 14% 76% N/A 44% 25%

Leber25 106 66% 16% 26% 9% N/A N/A 38% 58% 75% 79.4% 12%

Eskridge14 150 75%‡ N/A 100% N/A N/A 72%§ 28% 49% 75% N/A N/A

Kuether13 77 40% 8% 47% 14% 53% 79%¶ 52%# 40% N/A 81% N/A

Vinuela5 403 50% N/A 57% N/A 53% 61% 20.30% 100% N/A N/A N/A

Cognard17 203 57% 37% 17% N/A N/A 100% 61% 72% N/A 79% 7.5%

Cognard20 56 73% 19% 45% 1% N/A 93% 49% 66% N/A N/A N/A

Debrun21 39 72% N/A N/A 18% .90%†† N/A 22% 100% N/A 79.5% N/A

Bavinzski19 45 54% 13% 100% N/A 40% 51% 13% 76% 69% 71% 21%

Vanninen33 52 50% 6% 11% N/A 73% 100% 60%‡‡ 100% 81% 90%§§ N/A

Gruber22 21 66%\\ 24% 100% 19% 23% 90% 36% 52% 90% N/A N/A

Raymond30 31 42% 6% 100% 23% 45% 58% 19% 74% 61% 100% 0%

PC indicates posterior circulation; RC, recanalization; and HH, Hunt-Hess grade.*99–100% occluded.†All wide-neck aneurysms.‡$90%.§Approximately.\57% of deaths in HH III/IV.¶Approximately.#HH I/II.**0% for completely occluded aneurysms.††6.2% had neck $5 mm.‡‡HH I/II.§§HH I/II.\\.95%.

106 Stroke January 2000

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

neurological examination or outcome scores after endovas-cular treatment and before death.

Four patients who initially presented with Hunt-Hess gradeII hemorrhages died. The first patient suffered from a rareanemia and developed a coagulopathy after a blood transfu-sion leading to a fatal hemorrhage from a previously unrup-tured pericallosal aneurysm. The second patient developed amassive gastrointestinal hemorrhage associated with severecirrhosis, which led to hypotensive shock. The third patientwith Wyburn-Mason’s syndrome with an arteriovenous mal-formation underwent successful coil therapy of a superiorcerebellar feeding artery aneurysm but suffered a massiveintracerebral hemorrhage from the arteriovenous malforma-tion and died 30 days later. The fourth patient died as a resultof overwhelming congestive heart failure, pulmonary edema,and pneumonia. Two patients died of myocardial infarctionsduring the follow-up period after discharge from the hospital.

DiscussionThe primary goal of endovascular therapy is the prevention ofrepeated hemorrhage and its devastating consequences.10 Theclinical experience from a series of ruptured aneurysmstreated conservatively has demonstrated a 37% risk of re-bleeding at 4 weeks and an overall mortality rate fromrepeated hemorrhage and its sequelae of 34% to 42%.11,12 Inthe context of this poor natural history, the results presentedhere for ruptured intracranial posterior circulation aneurysmsindicate that GDC embolization confers a protective effect.We encountered no recurrent SAH in the acute phase afterendovascular embolization. Furthermore, no aneurysm thatwas occluded to.75% by angiographic criteria rebled duringthe entire follow-up period.

The recurrent SAH rate and mortality from aneurysmrepeated rupture in this series are 0.92% (1/109 patients).This corresponds to a yearly rebleeding rate of 0.85%/y, a ratesimilar to those reported in other endovascular series (Table2), which range from 0%/y to 3%/y (Kuether et al,13 1.4%;

Eskridge et al,14 3%; Pierot et al,15 0%). Tsutsumi et al16

measured the rate of recurrent SAH at 1.4% to 1.8% in agroup of 220 patients treated with surgical clipping during afollow-up period ranging from 3 to 21 years. The cumulativerisk for recurrent SAH was estimated to be 0.5%, 2.2%, and5.5% at 5, 10, and 15 years postoperatively, respectively. Allthe aneurysms in the surgical series were thought to havebeen completely clipped at surgery, in distinction to ourseries, in which the aneurysm that rebled was known to havebeen incompletely treated from the outset.10–12,16

Clinical OutcomesThe initial clinical grade of the patient at presentationstrongly predicted patient outcome. In this series, 94% ofgood-grade patients (Hunt-Hess I or II) had good recoveryleading to a GOS I outcome at final follow-up.Intermediate-grade patients (Hunt-Hess III) predictablyhad a lower percentage of GOS I outcome (78%). Thisfinding is consistent with other series that have reportedlower percentages of good outcome for grade III patients:55%,17 57%,18 and 100%.13 In poor-grade patients (Hunt-Hess IV and V), fewer patients recovered to a good finaloutcome: only 46% of Hunt-Hess grade IV cases and only25% of Hunt-Hess grade V patients achieved GOS Ioutcomes. All measured indices, including GOS, modifiedRankin, and QOL, showed improved outcomes after GDCembolization when adjusted for the initial neurologicalcondition. Late deterioration resulted from medical prob-lems (7.3%, 8/109), vasospasm (8.3%, 9/109), and delayedcomplications (1.8%, 2/109). Our overall final excellent/good clinical outcome (GOS I/II) of 83% (91/109) iscomparable to the 69% to 91% (average of 77%) GOS I/IIoutcomes seen in other series (Table 2). In the currentsingle center study, 74% (81/109) of all treated patientsrecovered to a final GOS of I, compared with 69% of theruptured subset of the multicenter series of 150 basilarbifurcation aneurysms.14 Comparison with other publishedseries of endovascular treatment not limited to the subsetof ruptured posterior circulation lesions reveals compara-ble outcome statistics.5,13–15,17–33These series (Table 2)show GOS I outcome in 44% to 100% of good-gradepatients, with a mean of 79%.

Angiographic OutcomeSmall aneurysms with narrow necks and saccular shapedemonstrated excellent initial and final occlusion rates. Over-all, 88% of the treated non–parent vessel occlusion aneu-rysms were occluded in the 90% to 100% range, while allparent vessel occlusion–treated aneurysms (n528) showedcomplete angiographic occlusion at the end of the treatment.In comparison, the multicenter study of 150 basilar apexaneurysms14 noted 75% of aneurysms at 90% to 100%occlusion after GDC embolization. Other series of posteriorcirculation aneurysms treated with GDC embolization (Table2) report complete and near-complete (99% to 100%) angio-graphic occlusion in a mean of 62% of patients (range, 42%to 85%), compared with 54% in our series. In surgical series,Peerless et al35 reported an 87.4% rate of total occlusion byclipping, with a neck remnant seen in 5.8% and residual

TABLE 2. Continued

HH III/IV(Excellent)

IndirectMortality

DirectMortality Morbidity Rebleed

59% 15% 0% 2.80% 0.92%

100% 8.8% 2.9% 3% 0%

N/A 5% N/A 5% 0%

39% 6.6% N/A N/A 0%

N/A 23%\ 2.7% 5% 3.30%

N/A 19.4% 6.4% 9.10% 2.9%**

N/A 8.9% 1.7% N/A 2.20%

N/A 11% 3% 2% 0.70%

N/A N/A N/A N/A N/A

N/A 3% 1.8% 3.60% N/A

60% 18% 2.2% 4.4% 2.2%

N/A N/A 2% 6% %

N/A N/A 0% 9.5% 0%

69% N/A 3% 3% 0%

Lempert et al Endovascular Treatment of Ruptured Posterior Circulation Aneurysms 107

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

aneurysm body or fundus in 6.8%. Recently, the series ofSamson et al34 reported residual aneurysm after surgicalclipping in 6% of cases by postoperative angiography. Com-plex aneurysm geometry was responsible for less than com-plete occlusion in almost all cases. In the present series, fully39% of treated aneurysms harbored a wide neck (.4 mm),and 38% measured.10 mm in largest diameter. The diffi-culty in attaining complete obliteration of these complexaneurysms is shared with surgical series, which have simi-larly reported greater difficulty in complete occlusion byclipping in this group.34,35Incomplete aneurysm occlusion byendovascular coil placement may still offer a measure ofprotection from rehemorrhage, as shown by the low repeatedrupture rate in this and other series, although the threshold ofocclusion needed to achieve such protection is unclear.Histopathological examination of human aneurysms treatedwith GDC has shown that incompletely treated aneurysmsdevelop an organized thrombus along the periphery of theaneurysm, possibly reinforcing the wall.36,37 Frank recanali-zation and aneurysm growth were noted in some wide-neckedaneurysms with poor initial occlusion, a phenomenon similarto that recently reported by Mericle et al.38 Recent experi-mental modifications of the GDC, such as ion implantationand surface coating39 with collagen or growth factors,40 haveled to improved endothelial proliferation on the coil surfaceand better aneurysm occlusion in animal studies. The possiblefuture incorporation of these advances may eventually yieldbetter intermediate and long-term angiographic occlusion inwide-necked and large aneurysms treated from an endovas-cular route.

ComplicationsThere were no cases of procedure-related mortality in ourseries, compared with rates ranging from 0% to 6.4% in otherendovascular series. The permanent morbidity rate of 2.8%compares favorably with other series ranging from 2% to 5%(Table 2). The permanent combined morbidity and mortalityin our series was 3.7% (morbidity, mortality, and death fromrepeated hemorrhage). Other endovascular series havereported combined morbidity and mortality rates between5% and 16.9%. A recent meta-analysis41 of 48 eligibleendovascular studies totaling 1383 patients reported per-manent complications in 46 of 1256 patients (3.7%; 95%CI, 2.7% to 4.9%).

Comparison With Surgical andEndovascular SeriesRecent reports have compared endovascular and surgicaltreatment. Gruber et al22 performed a retrospective study of41 patients with basilar apex aneurysms. Of the 11 whounderwent GDC embolization after SAH, 91% had a GOSscore of I or II compared with 73% for the 15 patients whounderwent surgery in the same setting. Overall, patients whounderwent GDC embolization had significantly better out-come (P,0.001) than patients who underwent surgery, evenwhen poor-grade patients were excluded in that report. Thesecond study by Vanninen et al33 described a prospectiverandomized trial of surgery versus endovascular therapy in109 patients. Clinical outcome at 3 months showed 83% of

coil-treated patients with posterior circulation aneurysm withGOS I and II scores compared with 60% of surgical patients.This study, which is limited by the small number of cases,failed to detect a statistically significant difference in finaloutcome. Leber et al25 performed a retrospective studycomparing endovascular and surgical treatment of 248 aneu-rysms and concluded that the clinical outcomes showed nosignificant difference between the 2 methods in terms ofsafety and efficacy. This series analyzed 297 aneurysms, 162treated surgically and 134 treated by endovascular tech-niques. Although these 3 studies have significant limitations,they suggest that short-term clinical outcome of patientstreated with GDC embolization are at least equivalent tosurgery. In the present study, restricted to posterior circula-tion aneurysms that in most surgical series have fewerfavorable outcomes, we were able to demonstrate goodoutcomes (GOS I or II) in 94% of good-grade patients(Hunt-Hess I and II). This is comparable to the clinicaloutcome of similar cohorts in these 3 surgical/endovascularstudies (Table 2) (GOS scores of 91%, 83%, and 91%,respectively). The 3 studies also reported the morbidity/mortality rates of the surgical versus endovascular ap-proaches. Leber et al25 demonstrated a 6.2% mortality rateafter surgery and 4.5% after endovascular treatment. Gruberet al22 reported a 50% morbidity/mortality rate in the surgicalgroup compared with 10% in the endovascular group. Van-ninen et al33 reported an equal 6% morbidity/mortality in bothsurgical and endovascular arms of their study, althoughposterior circulation aneurysms constituted only 11% of casesin that series (Table 2). Importantly, Leber et al25 found nosignificant difference in morbidity between anterior versusposterior circulation aneurysms treated with the endovascularapproach. In contrast, surgical clipping is associated with asignificantly higher morbidity and mortality in posteriorcompared with anterior circulation aneurysms.42

The surgical management of posterior circulation aneu-rysms has evolved significantly over the past 30 years.2,35,43,44

The international cooperative study described by Kassel etal45,46 included 266 patients treated for vertebrobasilar aneu-rysms. This series reported an overall death rate of 31.2%,good recovery in 52.6%, and a 7.9% incidence of severelydisabled/vegetative outcome. Other surgical clipping se-ries2,35,43,44report mortality of 6% to 11% and morbidity of10%. The most recent published surgical series by Samson etal34 describes the results of 303 aneurysms of the basilar apex,one third of which were unruptured. At 6-month follow-up,81% of patients were judged to be neurologically intact or tohave mild nonlimiting deficits (GOS I and II). Residualaneurysm was identified by follow-up angiography in 6% ofpatients. No patient suffered recurrent SAH during a meanfollow-up of approximately 8 years. Other large series haveshown similar outcome data, with GOS I and II outcomeranging from 82% to 85%.43,44,47–49Any direct retrospectivecomparison of endovascular and surgical results is greatlyhampered by differences in clinical condition at presentation,proportion of ruptured aneurysms, and acuity of treatmentafter SAH, since a longer wait before treatment selectsbetter-grade patients). For example, our study had a higher

108 Stroke January 2000

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

proportion of poor-grade patients compared with that ofSamson et al34 (29% Hunt-Hess IV and V versus 13%).

The dependence of risk and complications on aneurysmlocation in surgical clipping and relative independence inendovascular treatment limits any direct comparison of re-sults obtained with surgical and endovascular therapy. Thecriteria for difficulty and associated risk in treatment of ananeurysm are different. Whereas anatomic location and therequired surgical exploration and exposure contribute to themorbidity of clipping, the angiographic determinants, such asneck size and aneurysm morphology, primarily affect the riskof endovascular therapy. The present study is probablycharacterized by a referral bias since a significant proportionof patients in the early phases of the study period werereferred for coil therapy either because they were believed tobe poor candidates for or had failed open surgical clipping.This partly accounts for the high proportion of fusiformaneurysms treated by parent vessel occlusion.

Despite the inherent limitations in comparing surgical andendovascular studies, the retrospective nature of this study,and potential selection and referral bias, our results of 0%direct mortality, 2.8% overall mortality, and 83% overallexcellent/good outcome (GOS I and II) compare favorablywith published surgical results of ruptured posterior circula-tion aneurysms.1,2,21,25,34,35,43,45–47Our findings confirm thatGDC embolization is effective in preventing repeated hem-orrhage of ruptured posterior circulation aneurysms, and theyalso highlight the need for surveillance angiography inpartially treated lesions. Future studies will be needed todetermine the extended long-term outcome and efficacy ofthis endovascular therapy.

AcknowledgmentsWe are thankful for the assistance of Drs D.R. Gress, W.S. Smith,and C. Johnston.

References1. Drake CG, Peerless S, Hernesniemi J.Surgery of Vertebrobasilar Aneu-

rysms. New York, NY: Springer-Verlag; 1996.2. Batjer HH, Samson DS. Causes of morbidity and mortality from surgery

of aneurysms of the distal basilar artery.Neurosurgery. 1989;25:904–915; comment 915–916.

3. Hunt WE, Hess RM. Surgical risks as related to time of intervention in therepair of intracranial aneurysms.J Neurosurg. 1968;28:14–20.

4. Hillman J, Saveland H, Jakobsson KE, Edner G, Zygmunt S, FridrikssonS, Brandt L. Overall management outcome of ruptured posterior fossaaneurysms.J Neurosurg. 1996;85:33–38.

5. Vinuela F, Duckwiler G, Mawad M. Guglielmi detachable coil emboli-zation of acute intracranial aneurysm: perioperative anatomical andclinical outcome in 403 patients.J Neurosurg. 1997;86:475–482.

6. Jennett B, Bond M. Assessment of outcome after severe brain damage.Lancet. 1975;1:480–484.

7. Stachniak JB, Layon AJ, Day AL, Gallagher TJ. Craniotomy for intra-cranial aneurysm and subarachnoid hemorrhage: is course, cost, oroutcome affected by age?Stroke. 1996;27:276–281.

8. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Inter-observer agreement for the assessment of handicap in stroke patients.Stroke. 1988;19:604–607.

9. Lempert TE, Halbach VV, Higashida RT, Dowd CF, Urwin RW,Balousek PA, Hieshima GB. Endovascular treatment of pseudoaneurysmswith electrolytically detachable coils.AJNR Am J Neuroradiol. 1998;19:907–911.

10. Schievink WI, Wijdicks EF, Piepgras DG, Chu CP, O’Fallon WM,Whisnant JP. The poor prognosis of ruptured intracranial aneurysms ofthe posterior circulation.J Neurosurg. 1995;82:791–795.

11. Nishioka H, Torner JC, Graf CJ, Kassell NF, Sahs AL, Goettler LC.Cooperative study of intracranial aneurysms and subarachnoid hemor-rhage: a long-term prognostic study, III: subarachnoid hemorrhage ofundetermined etiology.Arch Neurol. 1984;41:1147–1151.

12. Nishioka H, Torner JC, Graf CJ, Kassell NF, Sahs AL, Goettler LC.Cooperative study of intracranial aneurysms and subarachnoid hemor-rhage: a long-term prognostic study, II: ruptured intracranial aneurysmsmanaged conservatively.Arch Neurol. 1984;41:1142–1146.

13. Kuether TA, Nesbit GM, Barnwell SL. Clinical and angiographicoutcomes, with treatment data, for patients with cerebral aneurysmstreated with Guglielmi detachable coils: a single-center experience.Neu-rosurgery. 1998;43:1016–1025.

14. Eskridge JM, Song JK. Endovascular embolization of 150 basilar tipaneurysms with Guglielmi detachable coils: results of the Food and DrugAdministration multicenter clinical trial.J Neurosurg. 1998;89:81–86.

15. Pierot L, Boulin A, Castaings L, Rey A, Moret J. The endovascularapproach in the management of patients with multiple intracranial aneu-rysms.Neuroradiology. 1997;39:361–366.

16. Tsutsumi K, Ueki K, Usui M, Kwak S, Kirino T. Risk of recurrentsubarachnoid hemorrhage after complete obliteration of cerebral aneu-rysms.Stroke. 1998;29:2511–2513.

17. Cognard C, Weill A, Castaings L, Rey A, Moret J. Intracranial berryaneurysms: angiographic and clinical results after endovascular treatment.Radiology. 1998;206:499–510.

18. Malisch TW, Guglielmi G, Vinuela F, Duckwiler G, Gobin YP, MartinNA, Frazee JG. Intracranial aneurysms treated with the Guglielmidetachable coil: midterm clinical results in a consecutive series of 100patients.J Neurosurg. 1997;87:176–183.

19. Bavinzski G, Richling B, Gruber A, Killer M, Levy D. Endosaccularocclusion of basilar artery bifurcation aneurysms using electricallydetachable coils.Acta Neurochir (Wien). 1995;134:184–189.

20. Cognard C, Pierot L, Boulin A, Weill A, Tovi M, Castaings L, Rey A,Moret J, Toevi M. Intracranial aneurysms: endovascular treatment withmechanical detachable spirals in 60 aneurysms.Radiology. 1997;202:783–792.

21. Debrun GM, Aletich VA, Kehrli P, Misra M, Ausman JI, Charbel F.Selection of cerebral aneurysms for treatment using Guglielmi detachablecoils: the preliminary University of Illinois at Chicago experience.Neu-rosurgery. 1998;43:1281–1295; comment 1296–1297.

22. Gruber DP, Zimmerman GA, Tomsick TA, van Loveren HR, Link MJ,Tew JM Jr. A comparison between endovascular and surgical man-agement of basilar artery apex aneurysms.J Neurosurg. 1999;90:868–874.

23. Horowitz M, Purdy P, Kopitnik T, Dutton K, Samson D. Aneurysmretreatment after Guglielmi detachable coil and nondetachable coil embo-lization: report of nine cases and review of the literature.Neurosurgery.1999;44:712–719; comment 719–720.

24. Klein GE, Szolar DH, Leber KA, Karaic R, Hausegger KA. Basilar tipaneurysm: endovascular treatment with Guglielmi detachable coils:midterm results.Radiology. 1997;205:191–196.

25. Leber KA, Klein GE, Trummer M, Eder HG. Intracranial aneurysms: areview of endovascular and surgical treatment in 248 patients.MinimInvasive Neurosurg. 1998;41:81–85.

26. McDougall CG, Halbach VV, Dowd CF, Higashida RT, Larsen DW,Hieshima GB. Endovascular treatment of basilar tip aneurysms usingelectrolytically detachable coils.J Neurosurg. 1996;84:393–399.

27. Nichols DA, Brown RD Jr, Thielen KR, Meyer FB, Atkinson JL, PiepgrasDG. Endovascular treatment of ruptured posterior circulation aneurysmsusing electrolytically detachable coils.J Neurosurg. 1997;87:374–380.

28. Picard L, Bracard S, Lehericy S, Anxionnat R, Miyachi S, Prada E, PerA, Burdin D, Auque J, Marchal JC. Endovascular occlusion of intra-cranial aneurysms of the posterior circulation: comparison of balloons,free coils and detachable coils in 38 patients.Neuroradiology. 1996;38(suppl 1):S133–S141.

29. Pierot L, Boulin A, Castaings L, Rey A, Moret J. Selective occlusion ofbasilar artery aneurysms using controlled detachable coils: report of 35cases.Neurosurgery. 1996;38:948–953.

30. Raymond J, Roy D. Safety and efficacy of endovascular treatment ofacutely ruptured aneurysms.Neurosurgery. 1997;41:1235–1245.

31. Raymond J, Roy D, Bojanowski M, Moumdjian R, L’Esperance G.Endovascular treatment of acutely ruptured and unruptured aneurysms ofthe basilar bifurcation.J Neurosurg. 1997;86:211–219.

32. Rowe JG, Molyneux AJ, Byrne JV, Renowden S, Aziz TZ. Endovasculartreatment of intracranial aneurysms: a minimally invasive approach withadvantages for elderly patients.Age Ageing. 1996;25:372–376.

Lempert et al Endovascular Treatment of Ruptured Posterior Circulation Aneurysms 109

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

33. Vanninen R, Koivisto T, Saari T, Hernesniemi J, Vapalahti M. Rupturedintracranial aneurysms: acute endovascular treatment with electrolyticallydetachable coils: a prospective randomized study.Radiology. 1999;211:325–336.

34. Samson D, Batjer HH, Kopitnik TA Jr. Current results of the surgicalmanagement of aneurysms of the basilar apex.Neurosurgery. 1999;44:697–702; comment 702–704.

35. Peerless SJ, Hernesniemi JA, Gutman FB, Drake CG. Early surgery forruptured vertebrobasilar aneurysms.J Neurosurg. 1994;80:643–649.

36. Shimizu S, Kurata A, Takano M, Takagi H, Yamazaki H, Miyasaka Y,Kiyotata F. Tissue response of a small saccular aneurysm after incompleteocclusion with a Guglielmi detachable coil.AJNR Am J Neuroradiol.1999;20:546–548.

37. Castro E, Fortea F, Villoria F, Lacruz C, Ferreras B, Carrillo R.Long-term histopathologic findings in two cerebral aneurysms embolizedwith Guglielmi detachable coils.AJNR Am J Neuroradiol. 1999;20:549–552.

38. Mericle RA, Wakhloo AK, Lopes DK, Lanzino G, Guterman LR,Hopkins LN. Delayed aneurysm regrowth and recanalization afterGuglielmi detachable coil treatment: case report.J Neurosurg. 1998;89:142–145.

39. Murayama Y, Vinuela F, Suzuki Y, Do HM, Massoud TF, Guglielmi G,Ji C, Iwaki M, Kusakabe M, Kamio M, Abe T. Ion implantation andprotein coating of detachable coils for endovascular treatment of cerebralaneurysms: concepts and preliminary results in swine models.Neuro-surgery. 1997;40:1233–1243.

40. Kallmes DF, Williams AD, Cloft HJ, Lopes MB, Hankins GR, Helm GA.Platinum coil-mediated implantation of growth factor-secreting endo-vascular tissue grafts: an in vivo study.Radiology. 1998;207:519–523.

41. Brilstra EH, Rinkel GJ, van der Graaf Y, van Rooij WJ, Algra A.Treatment of intracranial aneurysms by embolization with coils: a sys-tematic review.Stroke. 1999;30:470–476.

42. Drake CG. The treatment of aneurysms of the posterior circulation.ClinNeurosurg. 1979;26:96–144.

43. Yacargil MG. Vertebrobasilar aneurysms. In:Microneurosurgery. NewYork, NY: Georg Thieme Verlag; 1984:232–295.

44. Sugita K, Kobayashi S, Shintani A, Mutsuga N. Microneurosurgery foraneurysms of the basilar artery.J Neurosurg. 1979;51:615–620.

45. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL.The International Cooperative Study on the Timing of Aneurysm Surgery,part 1: overall management results.J Neurosurg. 1990;73:18–36.

46. Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP. The Interna-tional Cooperative Study on the Timing of Aneurysm Surgery, part 2:surgical results.J Neurosurg. 1990;73:37–47.

47. Solomon RA, Stein BM. Surgical approaches to aneurysms of the ver-tebral and basilar arteries.Neurosurgery. 1988;23:203–208.

48. Hernesniemi JVM, Niskanen M, Kari A. Management outcome for ver-tebrobasilar artery aneurysms by early surgery.Neurosurgery. 1992;31:857–862.

49. Ojemann RG, Crowell R.Surgical Management of CerebrovascularDisease. Baltimore, Md: Williams & Wilkins; 1988.

110 Stroke January 2000

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from

Meyers, Christopher F. Dowd and Randall T. HigashidaTodd E. Lempert, Adel M. Malek, Van V. Halbach, Constantine C. Phatouros, Philip M.

and Angiographic OutcomesEndovascular Treatment of Ruptured Posterior Circulation Cerebral Aneurysms: Clinical

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 2000 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/01.STR.31.1.100

2000;31:100-110Stroke. 

http://stroke.ahajournals.org/content/31/1/100World Wide Web at:

The online version of this article, along with updated information and services, is located on the

  http://stroke.ahajournals.org//subscriptions/

is online at: Stroke Information about subscribing to Subscriptions: 

http://www.lww.com/reprints Information about reprints can be found online at: Reprints:

  document. Permissions and Rights Question and Answer process is available in the

Request Permissions in the middle column of the Web page under Services. Further information about thisOnce the online version of the published article for which permission is being requested is located, click

can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office.Strokein Requests for permissions to reproduce figures, tables, or portions of articles originally publishedPermissions:

by guest on March 17, 2016http://stroke.ahajournals.org/Downloaded from