Dominance of the Anterior Cerebral Artery as a Predictor of Vasospasm-Related Cerebral Infarction After Surgical Treatment of Ruptured Blood Blister-Like Aneurysm in the Internal Carotid Artery

Original Article

Dominance of the Anterior Cerebral Artery as a Predictor of Vasospasm-Related Cerebral Infarction After Surgical Treatment of Ruptured Blood Blister-Like Aneurysm in the Internal Carotid Artery Heui Seung Lee, Jae Sung Ahn, Jung Cheol Park, Seungjoo Lee, Moinay Kim, Wonhyoung Park

OBJECTIVE: Vasospasm (VSP)-related ischemic complications have been associated with poor outcomes in patients with subarachnoid hemorrhage due to ruptured blood blister-like aneurysms (BBAs) in the communicating segment of the internal carotid artery (ICA). The purpose of the present study was to investigate the incidence of, and factors related to, VSP-related cerebral infarction (VSP-CI) in patients with surgically treated BBAs in the communicating segment of the ICA.

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preoperative angiogram (P [ 0.023), with a hazard ratio of 14.14 (95% confidence interval, 1.57e127.68). CONCLUSIONS: The results of preoperative balloon test occlusion were less reliable for predicting postoperative ischemic complications of EC-IC bypass with trapping in patients with ruptured BBAs in the communicating segment of the ICA. However, anterior cerebral artery dominance ipsilateral to the ruptured aneurysm could be predictive for postoperative VSP-CI.

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METHODS: The medical records of 25 consecutive patients with surgically treated BBAs in the communicating segment of the ICA were reviewed. The preoperative angiographic findings, surgical methods, and patient outcomes, including VSP-CI, were evaluated.

INTRODUCTION

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RESULTS: Of the 25 patients, 10 had undergone extracranialeintracranial (EC-IC) bypass with trapping and 15 had undergone clipping surgery. VSP-CI occurred in the ipsilateral hemisphere to the aneurysm in 4 patients with EC-IC bypass with trapping and in 6 patients who had undergone received clipping. Positive balloon test occlusion findings did not affect the occurrence of VSP-CI in the ECIC bypass and trapping group. The occurrence of VSP-CI was significantly greater in the patients with a dominant anterior cerebral artery ipsilateral to the aneurysm on the

lood blister-like aneurysms (BBAs) at the nonbranching site of the communicating segment of the ICA account for 0.9%e6.6% of aneurysms of the internal carotid artery (ICA).1,2 Surgical treatment of ruptured BBAs at the nonbranching site of the communicating segment of the ICA has remained challenging, and ischemic complications from vasospasm (VSP) have been reported to be the major causes of postoperative morbidities and poor outcomes.3-5 Despite extracranialeintracranial (EC-IC) bypass for flow augmentation after trapping of the distal ICA, the rate of VSP-related cerebral infarction (VSP-CI) has been greater than that after distal ICA trapping in patients with

Key words Anterior cerebral artery - Blister-like aneurysm - Internal carotid artery - Infarction - Vasospasm

RA: Radial artery SAH: Subarachnoid hemorrhage STA: Superficial temporal artery TCD: Transcranial Doppler VSP: Vasospasm VSP-CI: Vasospasm-related cerebral infarction

Abbreviations and Acronyms ACA: Anterior cerebral artery AComA: Anterior communicating artery BBA: Blood blister-like aneurysm BTO: Balloon test occlusion CSF: Cerebrospinal fluid CT: Computed topography EC-IC: Extracranialeintracranial ICA: Internal carotid artery MCA: Middle cerebral artery mRS: Modified Rankin scale PcomA: Posterior communicating artery

Department of Neurosurgery, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea

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To whom correspondence should be addressed: Wonhyoung Park, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.143 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

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unruptured aneurysms in the distal ICA.5 This has been true regardless of cross-filling of the middle cerebral artery (MCA) on preoperative balloon test occlusion (BTO).6 However, information has been limited regarding the factors associated with delayed ischemic complications from VSP after surgical treatment of ruptured BBAs. No consensus has been reached regarding the strategies for the prevention of delayed infarction.7 In the present study, we investigated the potential factors associated with delayed infarction of the hemisphere ipsilateral to the aneurysm after surgical treatment of BBAs by evaluating the preoperative angiographic findings. METHODS Patient Inclusion Criteria and Data Collection An institutional database at our institute was searched from January 1999 to April 2018 to identify those patients who had presented with BBAs located in the nonbranching site of the communicating segment of the ICA in accordance with the classification of Bouthillier et al.8 Our institutional review board approved the present study before the data collection began. The patient medical records were reviewed to record the data regarding sex, age, underlying diseases, smoking status, interval from BBA onset to surgery, type of operation performed for each patient, occurrence of VSP, whether intra-arterial VSP therapy had been used, and the presence of symptomatic infarction of the hemisphere ipsilateral to the ruptured aneurysm. BBA was defined as a wide-necked aneurysmal dilatation originating from the communicating segment of the ICA without any relationship to an arterial branch. The presence of BBAs was confirmed using surgical microscopy. Surgical microscopy was used to identify the aneurysm rupture and characteristic blisterlike features, including thin vessel wall and purple and red coloring.9,10 If the aneurysm was not found during the initial angiographic study, the interval to the delayed detection was determined by the interval from the first onset of symptoms to the detection of a suspected aneurysm on a subsequent angiographic evaluation. Trauma-related ICA dissection or cases treated by endovascular intervention without confirmation by surgical inspection were excluded. Preoperative Assessment of Neuroimaging Studies BTO Findings. BTO was used to evaluate the degree of angiographic collateral blood flow after carotid occlusion. When performing BTO, either an Endeavor (Target Therapeutics, Boston Scientific, Fremont, California, USA) or a Hyperglide (Micro Therapeutics, Irvine, California, USA) nondetachable balloon was used to occlude the blood flow in the ICA. After the digital road map of the ICA under fluoroscopic guidance had been obtained to control balloon inflation, occlusion of ICA was confirmed by an angiographic series through the guiding catheter. Angiograms of the contralateral ICA and the dominant vertebral artery were obtained after balloon inflation. A total of 12 mL of iodinate contrast was injected at 5 mL/second for angiography of the ICA. A total of 10 mL of iodinate contrast at 5 mL/second was used for the vertebral artery. The BTO results were used to identify the presence or absence of MCA cross-filling. MCA cross-filling was defined as sufficient collateral blood flow to the ACA and MCA

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territories as visualized through the anterior communicating artery (AcomA).11 The absence of MCA cross-filling was defined as poor collateral blood flow to the ACA and MCA territories.11 During BTO, the presence of adequate angiographic collateral branches was defined by a venous phase delay of <2 seconds between the temporarily occluded hemisphere and the contrast-injected side.12 Determination of ACA Dominance. We determined the dominance of the ACA with the reference to the classification suggested by Tarulli and Fox,13 in which A1eA2 segment flow dominance was defined by maintenance of contrast in both A2 segments, with injection from only 1 side from the early to late dilution phases. To determine the dominance of the ACA, preoperative angiograms of each patient were independently evaluated by 3 readers, 2 of whom were dual-trained endovascular neurosurgeons and 1 of whom was a radiologist not involved in the present study. The initial categorization was determined by the vessel diameter. If an A1 segment appeared hypoplastic, the contralateral A1 segment side can be considered dominant (Figure 1J, K). If the A1 segments of both sides were not apparently different in size, ACA dominance was determined after evaluating the early and late arterial phases for the distal ACA, including the callosomarginal artery and cortical branches. If the cortical branches from the callosomarginal and pericallosal arteries were visualized on the contralateral side on the ipsilateral ICA angiogram, but those branches were not also observed with contrast injection during contralateral ICA angiography, the ipsilateral ACA was considered dominant (Figure 1AeC). If the cortical branches from the distal ACA were not visualized on the contralateral side throughout the arterial phases with contrast injection from the 1 side, the ACAs of both sides were considered to be symmetrical (Figure 1H, I). Surgical Treatment The operative records of all patients were reviewed in detail to identify the type of surgery performed, methods of ICA trapping and clipping used, and the occurrence of any unfavorable events during surgery, such as compromise of the ICA branches, including the posterior communicating artery (PcomA) and anterior choroidal artery, or intraoperative rupture of the aneurysm. In the case of severe brain swelling, intraoperative cerebrospinal fluid (CSF) drainage was performed after craniotomy. To avoid intraoperative aneurysm rupture from overdrainage of CSF, Paine’s point was used for intraoperative ventricular puncture to relieve brain swelling before arachnoid dissection, allowing for the regulation of the amount of CSF drainage during inspecting of the degree of brain swelling.14,15 EC-IC Bypass with Trapping. EC-IC bypass with trapping was used when the preoperative angiographic findings indicated that the BBA could not be obliterated by clipping. The procedure was also used when the aneurysmal neck had been identified as clippable on the preoperative angiogram but EC-IC bypass with trapping had been ultimately selected during surgery because the risk of postclipping rupture was expected to be high. For example, cases with a wide pathologic segment with a thin vessel wall continuous with the aneurysm neck, causing narrowing of the intraluminal

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Figure 1. Examples of ipsilateral, contralateral, and symmetrical dominance of the anterior cerebral artery (ACA) in the patients with the paraclinoid blister-like aneurysm in the right internal carotid artery (ICA). (AeC) Angiograms of both ICAs from the same patient showing ACA dominance ipsilateral (A,B) to the aneurysm side (B). (DeF) Angiograms showing more prominent pericallosal and cortical branches

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from the ACA of the contralateral side (F) to the aneurysm. (GeI) Examples of symmetrical ACA showing no prominent ACA branches to the contralateral side on both right and left ICA angiograms. (J,K) Contralateral ACA dominance with definite hypoplastic ipsilateral A1 on angiograms from a patient with the paraclinoid aneurysm in the right ICA.

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diameter of the ICA by >50% of the initial diameter, were treated with EC-IC bypass with trapping. As suggested by Yang et al.,11 we connected the stump of the superficial temporal artery (STA) to the M2 of the MCA bypass using a short interposition graft of the radial artery (RA) to augment perfusion of the ipsilateral hemisphere in all patients who had undergone trapping of the distal ICA. After the STA stumpeRA grafteM2 bypass was completed, the distal ICA segment affected by the ruptured aneurysm was trapped. Permanent clipping of both proximal and distal regions of the affected ICA, including the aneurysm, was the selected method for trapping of the distal ICA in all cases in the present series. The surgical procedures used for EC-IC bypass with trapping are shown in Figure 2. Aneurysm Clipping. The obliteration of the aneurysm by permanent clipping was selected when the aneurysmal sac was visible and aneurysmal neck clipping was considered feasible from the preoperative angiographic findings. For cases in which aneurysmal neck clipping had seemed possible on the angiogram but the thin-walled aneurysmal dome was found to have an increased risk of ICA dissection during surgery, the ICA was wrapped with a

Figure 2. Surgical procedures and intraoperative findings showing extracranialeintracranial bypass with surgical trapping. (A) A thin-walled blister-like aneurysm with an ill-defined aneurysmal neck (black arrowhead) was protruding from the right paraclinoid ICA (black arrow). (B) Trapping of the internal carotid artery using permanent clips was performed at the proximal and distal sides of the aneurysm without disturbing the

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temporalis muscle plug before permanent clipping to reinforce the wall of the ICA.16 Patient Follow-Up Postoperative Evaluation and Detection of Posthemorrhage VSP and VSP-CI. Postoperative computed tomography (CT) angiography and whole brain perfusion CT were used to calculate the mean transit time, time to peak, cerebral blood flow, and cerebral blood volume in all patients immediately after surgery. All the patients who had undergone EC-IC bypass with trapping or aneurysm clipping had undergone postoperative follow-up evaluations with cerebral angiography to verify bypass flow and obliteration of the aneurysmal segment between postoperative days 1 and 3. If increased intracranial pressure was identified by an intraoperative finding of brain swelling, the intracranial pressure was continuously monitored postoperatively using an extraventricular drainage catheter placed at Paine’s point during surgery. Transcranial Doppler (TCD) ultrasonography was performed daily at the patient’s bedside to detect VSP in the MCA of both ipsilateral and contralateral cerebral hemispheres. TCD grading criteria using the mean flow velocity and Lindegaard ratio were used to identify the presence and severity of VSP.17,18 When the mean velocity of the

blood clot covering the aneurysm. (C) Extracranialeintracranial bypass was established between the stump of the superficial temporal artery (white arrowhead) and M2 segment of the middle cerebral artery in an end-to-side fashion using a short interposition radial artery graft (white arrow). (D) Patency of the radial artery graft was confirmed with indocyanine green.

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MCA flow was 120e200 cm/second or the Lindegaard ratio was 3e6 for patients showing signs of neurological deterioration or when the mean MCA velocity was >200 cm/second or the Lindegaard ratio was >6, additional cerebral angiography was performed to confirm the presence of VSP. VSP-CI was defined as symptomatic cerebral infarction after the detection of VSP, in which the affected region was supplied by the artery affected by VSP. The presence of infarction was determined by the combination of radiological findings from diffusionweighted magnetic resonance imaging or CT studies and patient symptoms relevant to infarction. VSP Therapy. Intra-arterial angioplasty was performed immediately after cerebral angiography when radiologic VSP was confirmed to be severe or when the patient had experienced neurological deterioration that correlated with the VSP area of the cerebral hemisphere. Nimodipine was the agent of choice for chemical intra-arterial angioplasty. Intra-arterial angioplasty was performed through the ICA via arterial routes to the A1, AcomA, and MCA and the external carotid artery to reach the bypass graft of the STA in the cases in which EC-IC bypass with trapping had been performed. Balloon angioplasty was performed when the focal stenosis had been identified on the cerebral angiogram. Outpatient Follow-Up and Outcome Assessment. The outpatient follow-up protocol included a neurological examination and a review of the ischemic symptoms. The radiological follow-up evaluation included CT angiography to identify the development of hydrocephalus, aneurysm recurrence, and the occurrence of de novo aneurysms. All surviving patients had clinical and radiological follow-up data available for
6 months. The clinical outcomes were assessed using the modified Rankin scale (mRS) scores from the final follow-up evaluation. Patients with mRS scores of 3e6 were classified as having poor outcomes.19 The development of symptomatic posthemorrhagic hydrocephalus was defined as the necessity for ventriculoperitoneal shunt placement during the follow-up period.20 Statistical Analysis SPSS, version 22.0 (IBM Corp., Armonk, New York, USA), was used for statistical analysis. The normality of the data was tested using the Kolmogorov-Smirnov method. The Mann-Whitney U test was used to evaluate the statistically significant differences between the mean values of the continuous variables. The evaluated results of ACA dominance by the 3 different readers were analyzed using the k statistic to assess the interobserver concordance. A k value >0.75 indicated excellent agreement; <0.40, poor agreement; and 0.40e0.75, fair to good agreement. The c2 test was performed to compare the categorical variables. P values <0.05 were considered to indicate statistical significance. A Cox proportional hazards model was used to evaluate the association of the clinical variables with the occurrence of VSP-CI. RESULTS Patient Characteristics and Clinical Outcomes We identified 25 patients with subarachnoid hemorrhage (SAH) due to ruptured BBAs in the communicating segment of the ICA

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for the present study. The patient demographic data and preoperative and postoperative clinical data, including patient outcomes, are summarized in Table 1. The mean follow-up duration was 60.18  54.73 months (range, 6e187) for the 23 patients who had survived during the follow-up period. One patient had died of diffuse cerebral edema on postoperative day 5. The second patient, who had developed postoperative epidural hematoma, had died on postoperative day 7 of worsening of diffuse cerebral infarction in the MCA and ACA territories that had been compressed by hematoma, despite hematoma removal. Of the 25 patients, 10 (40%) had undergone EC-IC bypass with trapping and 15 (60%) had undergone surgical clipping. Of the 15 patients in the clipping group, wrapping of the aneurysmal segment of the ICA, followed by permanent clipping, was performed in 3, and 12 had undergone clipping only. For the patients who had undergone EC-IC bypass with trapping, postoperative 4vessel cerebral angiography was performed for all patients, and graft patency was confirmed to be intact in all cases. Either CT angiography or 4-vessel cerebral angiography was performed for patients in the clipping group to confirm obliteration of the aneurysm and patency of the ICA. Two cases of intraoperative rupture occurred in the clipping group. Of these 2 patients, 1 had died of severe brain swelling and the other patient had recovered with favorable outcomes. Blood flow to the PcomA or anterior choroidal artery was confirmed to be preserved without injury to the vessels in all 25 cases by intraoperative Doppler ultrasonography and postoperative angiographic evaluations. No significant differences were found between the EC-IC bypass with trapping and clipping groups in the preoperative clinical data, including the Fisher grade, apart from the interval to delayed detection of the aneurysm (P ¼ 0.04; Table 1). The interval to delayed detection of the aneurysm was significantly longer in the clipping group because of 1 case in which aneurysm detection had a 12-day delay. Of the 25 patients, 13 (52%) had unfavorable outcomes (mRS score
3) at the last follow-up evaluation. The occurrence of poor clinical outcomes according to the mRS score and the occurrence of postSAH hydrocephalus were not significantly different between the 2 groups (P > 0.99 and P ¼ 0.65, respectively; Table 1).

Subgroup Analysis of Preoperative Angiographic Findings and VSP-CI Development The development of ipsilateral VSP was diagnosed using TCD ultrasonography or follow-up angiography in 19 of 25 patients (76%). Of the 19 patients with ipsilateral VSP, VSP in the contralateral MCA was identified in 6 patients, and VSP-CI was found in the ipsilateral hemisphere of 10 patients (52.6%; 4 patients from the EC-IC bypass with trapping group and 6 from the clipping group; Table 2 and Figure 3). The interobserver concordance of ipsilateral ACA dominance was excellent (interobserver correlation coefficient, 0.88; 95% confidence interval, 0.77e0.99). Ipsilateral ACA dominance was observed in 6 of 25 patients. No significant difference was found in the occurrence of ipsilateral VSP between the EC-IC bypass with trapping and clipping groups. Contralateral VSP and the development of ipsilateral VSP-CI were significantly more common in patients with ipsilateral ACA dominance than in patients with

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Table 1. Comparison of Clinical Characteristics and Postoperative Outcomes Total (n [ 25)

EC-IC Bypass with Trapping (n [ 10)

Surgical Clipping* (n [ 15)

P Value

47  9.9

48  9.29

46.4  10.56

0.7

Female

20

7

13

Male

5

3

2

7 (28)

2 (20)

5 (33.3)

Characteristic Age (years) Gender

0.36

Hypertension

0.66 >0.99

Fisher grade 1

2 (8)

0 (0)

2 (13.3)

2

4 (16)

2 (20)

2 (13.3)

3

11 (44)

5 (50)

6 (40)

4

8 (32)

3 (30)

5 (33.3)

11 (44)

4 (40)

7 (46.7)

3.45  3.42

1.25  0.5

4.71  3.77

1e12

1e2

1e12

Delayed detection of aneurysmy Interval to delayed detection (days)

>0.99 0.04

Mean  SD Range Intraoperative rupture

0

0

0

Compromise of distal ICA branch (PcomA or AChA)

0

0

0

19 (76)

7 (70)

12 (80)

0.65

Postoperative VSP

10 (40)

4 (40)

6 (40)

>0.99

9.7  4.16

9.25  4.57

10  4.29

0.8

VSP-CI Interval to VSP-CI from onset (days) Poor outcome (mRS score
3)

13 (52)

5 (50)

8 (53.3)

>0.99

Post-SAH hydrocephalus

6 (24)

3 (30)

3 (20)

0.65

Mortality

2 (8)

0 (0)

2 (13.3)

0.5

Data presented as mean  SD or n (%). EC-IC, extracranialeintracranial; SD, standard deviation; ICA, internal carotid artery; PcomA, posterior communicating artery; AChA, anterior choroidal artery; VSP, vasospasm; VSP-CI, vasospasm-related cerebral infarction; mRS, modified Rankin scale; SAH, subarachnoid hemorrhage. *Clipping only in 12 patients, and clipping with muscle wrapping in 3 patients. yCases in which aneurysms were not detected at the first angiographic evaluation using 4-vessel cerebral angiography but were identified by the subsequent angiographic evaluation.

symmetrical ACA or contralateral ACA dominance (P ¼ 0.001 and P ¼ 0.023, respectively; Table 2). Of the 10 patients in the EC-IC bypass with trapping group, 7 had developed VSP, including 4 who had developed VSP-CI. Four

patients in the EC-IC bypass with trapping group had ipsilateral ACA dominance, including three who had developed VSP-CI in the ipsilateral hemisphere. In contrast, 5 of the 6 patients without ipsilateral ACA dominance had recovered without developing VSP-CI.

Table 2. Occurrence of Vasospasm and Vasospasm-Related Cerebral Infarction Stratified by Anterior Cerebral Artery Dominance Ipsilateral ACA Dominance (n [ 6)

Symmetrical or Contralateral ACA Dominance (n [ 19)

P Value

Ipsilateral VSP

6 (100)

13 (68.4)

0.28

Contralateral VSP

5 (83.3)

1 (5.3)

0.001

Ipsilateral VSP-CI

5 (83.3)

5 (26.3)

0.023

Ipsilateral ACA infarction

3 (50)

2 (10.5)

0.07

Interval to VSP-CI (days)

9.4  3.36

10  5.24

0.92

Variable

Data presented as n (%) or mean  standard deviation. ACA, anterior cerebral artery; VSP, vasospasm; VSP-CI, vasospasm-related cerebral infarction.

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Figure 3. Flow diagram of the clinical course after extracranialeintracranial (EC-IC) bypass with trapping or clipping. Each circle represents a patient (red circles indicate patients with ipsilateral anterior cerebral artery [ACA] dominance; blue circles, patients with symmetrical ACA or contralateral ACA dominance). Vasospasm-related cerebral infarction (VSP-CI) developed in 4 of 10 patients who had undergone

In 15 patients in the clipping group, 12 developed VSP, including 6 who had developed VSP-CI. Ipsilateral ACA dominance was observed in 2 patients in the clipping group, and VSP-CI had developed in these 2 patients. In contrast, 4 of 13 patients with contralateral ACA dominance had developed VSP-CI (Figure 3). Although no statistically significant difference (P ¼ 0.18) was found, the occurrence of VSP contralateral to the ruptured aneurysm was more frequent in patients with VSP-CI than in those who had recovered without VSP-CI (4 of 10 with ipsilateral VSP-CI vs. 2 of 15 patients who had recovered without VSP-CI; Table 3). Four patients had undergone intra-arterial VSP therapy for ischemic symptoms. Of these 4 patients, 3 with ipsilateral ACA dominance had developed VSP-CI during the postoperative course. In contrast, the 1 patient with contralateral ACA dominance did not develop VSP-CI. MCA cross-filling was not observed in 2 of 10 patients who had undergone BTO before EC-IC bypass with trapping. However,

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EC-IC bypass with trapping and in 6 of 15 patients who had undergone clipping. Of the 6 patients with ipsilateral ACA dominance, 5 developed VSP-CI. In contrast, VSP-CI developed in 5 of 19 patients with symmetrical ACA or contralateral ACA dominance. Of the 25 patients, 14 had recovered without VSP-CI, and 2 in the clipping group had died of diffuse VSP-CI (n ¼ 1) and progression of cerebral edema (n ¼ 1).

these 2 patients recovered without the development of VSP-CI during the postoperative follow-up period. MCA cross-filling was observed during the preoperative BTO in all 4 patients who had developed VSP-CI after EC-IC bypass with trapping. No significant association was found between a venous delay of >3 seconds during the BTO and the development of ipsilateral VSP-CI (P ¼ 0.076; Table 3). A venous delay of >3 seconds was observed in 4 patients during the BTO before EC-IC bypass with trapping; none of these patients developed VSP-CI. The log-rank test of cumulative VSP-CIefree survival showed that patients with ipsilateral ACA dominance had a significantly greater probability of developing VSP-CI compared with those patients who had symmetrical or contralateral ACA dominance (P ¼ 0.006; Figure 4). The Cox proportional hazard model identified ipsilateral ACA dominance as a significant predictor of VSP-CI, with the hazard ratio of 14.14 (95% confidence interval, 1.57e127.68; Table 3).

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Table 3. Univariate and Cox Regression Analysis Results Stratified by Vasospasm-Related Cerebral Infarction Development

Variable EC-IC bypass with trapping/clipping

Ipsilateral VSP-CI (n [ 10)

Recovery without VSP-CI (n [ 15)

P Value

Univariate Analysis (OR; 95% CI)

4/6

6/9

>0.99

1 (0.19e5.12)

Cox Regression Analysis (HR; 95% CI)

46.5  11.92

47.4  8.74

0.83

NA

NA

Postoperative VSP

10 (100)

9 (60)

0.051

Infinite

NA

Contralateral VSP

4 (40)

2 (13.3)

0.18

4.3 (0.61e30.57)

0.29 (0.33e2.49)

Age (years)

Ipsilateral A1 dominance

5 (50)

1 (6.7)

0.023

14 (1.3e150.9)

14.14 (1.57e127.68)

Symmetric A1 or ipsilateral A1 nondominance

5 (50)

14 (93.3)

0.023

NA

NA

NA

NA

Absence of MCA cross-filling

0/10 (0)

2/10 (20)

0.47

Venous delay
3 seconds

0/10 (0)

4/10 (66.7)

0.076

Carotid test compression*

VSP-CI, vasospasm-related cerebral infarction; OR, odds ratio; CI, confidence interval; HR, hazard ratio; EC-IC, extracranialeintracranial; NA, not applicable; VSP, vasospasm; MCA, middle cerebral artery. *Number of patients/EC-IC bypass with trapping patients.

DISCUSSION Although clipping on wrapping material by applying the clip blades parallel to the ICA has been suggested by some as the choice for surgical treatment of ruptured BBAs in the ICA,21-23 EC-IC bypass followed by trapping of the affected segment of the distal ICA has been suggested to be the most durable surgical treatment for BBAs with ill-defined aneurysmal necks.3,6 However, poor outcomes resulting from delayed cerebral ischemic complications of VSP after ICA trapping are a concern because VSP is known to affect the arteries in regions near ruptured aneurysms.2,3,24,25 VSP-related ischemic complications have been reported even in cases with adequate collateral cerebral blood flow identified using preoperative BTO.2 Therefore, the protective role of EC-IC bypass to the MCA before the onset of symptomatic VSP has been emphasized.2,6,25 Previous studies have emphasized that the necessity of EC-IC bypass should be determined from the preoperative carotid test occlusion results when ICA trapping has been planned.26-28 In the present study, neither MCA cross-filling nor a venous delay of
3 seconds during BTO were significantly associated with the occurrence of VSP-CI after EC-IC bypass with trapping. Even when MCA cross-filling has been identified during carotid test occlusion, flow through the AcomA from the contralateral side after ICA trapping might not be sufficient for the ipsilateral cerebral hemisphere when the intracranial pressure has increased and VSP is present. Moreover, it has been suggested that heparin use or the fluctuation in intraluminal pressure of the ICA during preoperative BTO at the ipsilateral ICA that includes the ruptured BBA will increase the risk of repeat bleeding.29 Considering the potential risks of preoperative BTO with the findings we have reported, this procedure might not determine the postoperative tolerance of ICA trapping and, thus, could be omitted in patients with acute SAH.25 Among the patients who had undergone underwent ICA trapping, permanent surgical clipping was performed to isolate the

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affected area of the ICA. Because of the fragile and thin vessel wall, some have advocated for endovascular trapping of BBAs.30,31 Kim et al.30 suggested that endovascular ICA trapping was effective, reporting only 1 case of perfusion decrease in 11 patients. However, they also reported 1 case of coil recanalization and 4 cases of PcomA occlusion in their series.30 We have found that temporary clamping of the ICA allows for exploration and trapping of the affected segment of the ICA when treating BBAs using permanent clipping, which can be achieved without disturbing the firm clot covering the ruptured portion of the aneurysm. Thus, we have advocated for surgical ICA trapping by permanent clipping, which could be more durable and effective in avoiding PcomA compromise by direct surgical inspection of the vessels. In general, it has been reported that w70% of patients with aneurysmal SAH will have angiographic evidence of VSP, 40% will have symptomatic VSP, and w30% will have delayed ischemic complications from VSP.24,32,33 In our study, 19 of our 25 patients (76%) with ruptured BBAs in the communicating segment of the ICA developed VSP, and the incidence of VSP-CI was 40%, slightly greater than what has been reported in the general population with aneurysmal SAH.24,33-35 The evidence for the use of the STAeRA grafteM2 bypass instead of high-flow bypass using a saphenous vein graft has been insufficient for ICA trapping with VSP present.36 However, we used an RA graft owing to the risk of perioperative and longterm occlusion of the saphenous vein graft.37-39 Yu et al.40 reported that the flow velocity for the internal maxillary arteryeRA grafteMCA was >60 mL/min, which was significantly greater than that of the STAeMCA bypass.40 Yang et al.11 suggested the usefulness of a short interposition using an RA graft to connect the proximal STA and M2 segment of the MCA in the treatment of complex intracranial aneurysms. Moreover, adaptive enlargement of the STA stump to meet the flow demand after STA stumpeRA grafteM2 bypass with ICA

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Figure 4. (A) The estimated rate of vasospasm-related cerebral infarction (VSP-CI) at 20 days from onset was 83.3% in the ipsilateral ACA dominant group and 26. 3% in the contralateral ACA dominant or symmetrical

trapping has been reported in previous studies.11,41,42 We selected the STA stumpeRA grafteM2 bypass as the method for EC-IC bypass owing to the additional advantage of shorter procedure times.11,43 Based on our findings that the occurrence of VSP-CI was similar between the EC-IC bypass with trapping group and the clipping

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ACA group. (B) Kaplan-Meier curves stratified by anterior cerebral artery (ACA) dominance. Ipsilateral ACA dominance was associated with a significantly greater probability of developing VSP-CI.

group, we have assumed that the blood flow from the STA stump through the short interposition of the RA graft can be equivalent to the flow through the ICA that involves the segment of the clipped aneurysm. Therefore, we believe that an RA graft as a short interposition can be used as a substitute for the distal ICA after trapping of the affected segment when treating ruptured

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BBAs. However, the 40% occurrence of VSP-CI despite the use of EC-IC bypass in our series was greater than that reported in the general population with aneurysmal SAH and remains a problem to overcome.24,33-35 Previous studies have suggested postoperative approaches for the prevention of ischemic complications such as high levels of intensive care, the evaluation of cerebral blood flow by perfusion CT, and the addition of antiplatelet and anticoagulation therapy.3,44 However, no data have been reported concerning the predictive factors of cerebral infarction in the presence of VSP. To the best of our knowledge, our study is the first to demonstrate the importance of ACA dominance in the prediction of VSP-CI of the hemisphere ipsilateral to ruptured BBAs in the communicating segment of the ICA. We hypothesized that the territory covered by the blood flow from the ICA would be related to the flow burden of the ICA and that the risk of VSP-CI would increase with the flow burden of the ICA on the aneurysm side. Therefore, if the flow burden of the ICA is reflected in the RA graft after EC-IC bypass with trapping, the risk of VSP-CI would increase with the preoperative flow burden of the ICA, despite flow from the RA graft. Among the 10 patients who had undergone ECIC bypass with trapping, the 3 who had experienced neither VSP nor VSP-CI during the postoperative course did not have ipsilateral ACA dominance on the preoperative angiogram. Also, 2 patients in the clipping group had not experienced either VSP or VSP-CI, and ACA dominance was observed on the contralateral side in both patients. According to 1 anatomical study, the distal ACA of 1 hemisphere will branch to the contralateral hemisphere in 64% of brains.45 In addition, the anastomosis between the distal branches of the ACA and the distal segments of the MCA will allow for partial maintenance of blood flow and resistance to cerebral ischemia.46 The ICA flow burden can be larger when the ipsilateral ACA is dominant and distributes its distal flow to the contralateral hemisphere. Therefore, in the development of VSP, the extent of the anastomosis between the distal ACA and MCA could be smaller in cases of ipsilateral ACA dominance than in those of symmetrical ACA or contralateral ACA dominance. On the same principle, the greater rates of VSP-CI after EC-IC bypass with trapping in the case of ipsilateral ACA dominance can be explained by the flow burden through the RA graft after EC-IC bypass. Therefore, our findings suggest that VSP therapy should be considered, with a lower threshold for VSP progression, for the patients with ACA dominance on the ipsilateral side of the ruptured aneurysm. Furthermore, we should consider postoperative evaluations of the cerebral blood flow, in addition to the high level of intensive care, for patients in whom ACA dominance of the ipsilateral side might be a predictor of VSP-CI.

REFERENCES 1. Kim JH, Kwon TH, Kim JH, Park YK, Chung HS. Internal carotid artery dorsal wall aneurysm with configurational change: are they all false aneurysms? Surg Neurol. 2006;66:441-443 [discussion: 443].

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Study Limitations The present study was limited by its retrospective nature and the small number of included patients. Although the present study identified a potential relationship between VSP-CI with ipsilateral ACA dominance in patients who had undergone EC-IC bypass with trapping, the findings might be inconclusive for the patients who had undergone clipping owing to the small sample size. Moreover, the reason for the development of VSP-CI in 5 of 19 patients with symmetrical or contralateral ACA dominance was not determined. Also, the factors associated with anastomoses between the distal MCA branches were not analyzed in the present study. The present study was also confined to BBAs of the nonbranching site of the ICA. In the preliminary investigation, non-BBAs in the nonbranching site of the ICA that had ruptured were large to giant aneurysms, which have high risk of perforator injury during surgical manipulation. To exclude an outcome bias from perforator injury in the assessment of surgical outcomes, we excluded ruptured large to giant aneurysms that had been surgically treated by trapping with bypass or suction decompression. Furthermore, by excluding branching site aneurysms, we intended to maximally investigate the ischemic complications from VSP of the major arteries, including the ICA. To the best of our knowledge, the present study was the first to evaluate the association of the preoperative radiological findings with the occurrence of postoperative ischemic complications from VSP. A larger study with more patients with ruptured paraclinoid BBAs with and without ischemic complications from VSP is necessary to identify the preventable and modifiable risk factors and to better understand the optimal timing of interventional VSP therapy. Considering the rarity of the disease, it is also necessary to recruit more patients in a multicenter retrospective study or meta-analysis to better understand the risk factors associated with VSP-CI development. In conclusion, the results of preoperative BTO were less reliable for predicting postoperative ischemic complications after EC-IC bypass and trapping in patients with ruptured BBA in the communicating segment of the ICA. However, ACA dominance ipsilateral to the ruptured aneurysm can be used as a predictive factor for the development of VSP-CI for both patients undergoing EC-IC bypass with trapping and those undergoing clipping to manage with postoperative VSP. Therefore, more aggressive management of VSP could be necessary for patients with ACA dominance on the ipsilateral side to the ICA with a ruptured BBA. ACKNOWLEDGMENTS The authors are thankful to all staff members of the neurosurgical department and the patients in the study groups, whose contributions made this work possible.

2. Meling TR, Sorteberg A, Bakke SJ, Slettebo H, Hernesniemi J, Sorteberg W. Blood blister-like aneurysms of the internal carotid artery trunk causing subarachnoid hemorrhage: treatment and outcome. J Neurosurg. 2008;108:662-671. 3. Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. Ischemic complications

after radial artery grafting and aneurysmal trapping for ruptured internal carotid artery anterior wall aneurysm. World Neurosurg. 2012;77:166-171.

4. Regelsberger J, Matschke J, Grzyska U, et al. Blister-like aneurysms—a diagnostic and therapeutic challenge. Neurosurg Rev. 2011;34:409-416.

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VSP-CI IN RUPTURED BBA IN THE ICA

diagnosis by means of angiography and blood velocity measurements. Acta Neurochir (Wien). 1989;100:12-24.

5. McLaughlin N, Laroche M, Bojanowski MW. Blister-like aneurysms of the internal carotid artery—management considerations. Neurochirurgie. 2012;58:170-186. 6. Kazumata K, Nakayama N, Nakamura T, Kamiyama H, Terasaka S, Houkin K. Changing treatment strategy from clipping to radial artery graft bypass and parent artery sacrifice in patients with ruptured blister-like internal carotid artery aneurysms. Neurosurgery. 2014;10(suppl 1):66-72 [discussion: 73]. 7. Sanelli PC, Kishore S, Gupta A, et al. Delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: proposal of an evidence-based combined clinical and imaging reference standard. AJNR Am J Neuroradiol. 2014;35: 2209-2214. 8. Bouthillier A, van Loveren HR, Keller JT. Segments of the internal carotid artery: a new classification. Neurosurgery. 1996;38:425-432 [discussion: 432, 423]. 9. Horiuchi T, Kusano Y, Yako T, Murata T, Kakizawa Y, Hongo K. Ruptured anterior paraclinoid aneurysms. Neurosurg Rev. 2011;34:49-55. 10. Liu Z, Zhang S, Wang S, Chen Q. Management of blood blister-like aneurysms of the internal carotid artery: lessons learned from direct clipping in 22 cases. World Neurosurg. 2017;108: 618-626. 11. Yang K, Ahn JS, Park JC, Kwon DH, Kwun BD, Kim CJ. The efficacy of bypass surgery using a short interposition graft for the treatment of intracranial complex aneurysm. World Neurosurg. 2015;83:197-202. 12. Abud DG, Spelle L, Piotin M, Mounayer C, Vanzin JR, Moret J. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. AJNR Am J Neuroradiol. 2005;26:2602-2609.

19. Powers WJ, Derdeyn CP, Biller J, et al. 2015 American Heart Association/American Stroke Association focused update of the 2013 guidelines for the early management of patients with acute ischemic stroke regarding endovascular treatment: a guideline for healthcare professionals from the American Heart Association/ American Stroke Association. Stroke. 2015;46: 3020-3035. 20. O’Kelly CJ, Kulkarni AV, Austin PC, Urbach D, Wallace MC. Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: incidence, predictors, and revision rates. Clinical article. J Neurosurg. 2009;111:1029-1035. 21. Kubo Y, Ogasawara K, Tomitsuka N, Otawara Y, Watanabe M, Ogawa A. Wrap-clipping with polytetrafluoroethylene for ruptured blisterlike aneurysms of the internal carotid artery. Technical note. J Neurosurg. 2006;105:785-787. 22. McLaughlin N, Laroche M, Bojanowski MW. Surgical management of blood blister-like aneurysms of the internal carotid artery. World Neurosurg. 2010;74:483-493. 23. Owen CM, Montemurro N, Lawton MT. Blister aneurysms of the internal carotid artery: microsurgical results and management strategy. Neurosurgery. 2017;80:235-247. 24. Dabus G, Nogueira RG. Current options for the management of aneurysmal subarachnoid hemorrhage-induced cerebral vasospasm: a comprehensive review of the literature. Interv Neurol. 2013;2:30-51. 25. Meling TR. What are the treatment options for blister-like aneurysms? Neurosurg Rev. 2017;40: 587-593.

31. Matsubara N, Miyachi S, Tsukamoto N, et al. Endovascular coil embolization for saccularshaped blood blister-like aneurysms of the internal carotid artery. Acta Neurochir (Wien). 2011;153: 287-294. 32. Hui C, Lau KP. Efficacy of intra-arterial nimodipine in the treatment of cerebral vasospasm complicating subarachnoid haemorrhage. Clin Radiol. 2005;60:1030-1036. 33. Reilly C, Amidei C, Tolentino J, Jahromi BS, Macdonald RL. Clot volume and clearance rate as independent predictors of vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2004;101:255-261. 34. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1-9. 35. Vergouwen MD. Participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage. Vasospasm versus delayed cerebral ischemia as an outcome event in clinical trials and observational studies. Neurocrit Care. 2011;15: 308-311. 36. Alaraj A, Ashley WW Jr, Charbel FT, AminHanjani S. The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus. 2008;24: E7. 37. Regli L, Piepgras DG, Hansen KK. Late patency of long saphenous vein bypass grafts to the anterior and posterior cerebral circulation. J Neurosurg. 1995;83:806-811. 38. Maselli G, Tommasi CD, Ricci A, Gallucci M, Galzio RJ. Endovascular stenting of an extracranial-intracranial saphenous vein high-flow bypass graft: technical case report. Surg Neurol Int. 2011;2:46.

13. Tarulli E, Fox AJ. Potent risk factor for aneurysm formation: termination aneurysms of the anterior communicating artery and detection of A1 vessel asymmetry by flow dilution. AJNR Am J Neuroradiol. 2010;31:1186-1191.

26. Barnett DW, Barrow DL, Joseph GJ. Combined extracranial-intracranial bypass and intraoperative balloon occlusion for the treatment of intracavernous and proximal carotid artery aneurysms. Neurosurgery. 1994;35:92-97 [discussion: 97-98].

39. Goldman S, Zadina K, Moritz T, et al. Long-term patency of saphenous vein and left internal mammary artery grafts after coronary artery bypass surgery: results from a Department of Veterans Affairs Cooperative Study. J Am Coll Cardiol. 2004;44:2149-2156.

14. Hyun SJ, Suk JS, Kwon JT, Kim YB. Novel entry point for intraoperative ventricular puncture during the transsylvian approach. Acta Neurochir (Wien). 2007;149:1049-1051 [discussion: 1051].

27. Kai Y, Hamada J, Morioka M, et al. Treatment strategy for giant aneurysms in the cavernous portion of the internal carotid artery. Surg Neurol. 2007;67:148-155 [discussion: 155].

15. Matsuzaki H, Otsuka T, Uekawa K, Nakagawa T, Tsubota N. Use of Paine’s technique: projecting puncture point to the skull and skin. World Neurosurg. 2017;104:45-47.

28. Shimizu H, Matsumoto Y, Tominaga T. Parent artery occlusion with bypass surgery for the treatment of internal carotid artery aneurysms: clinical and hemodynamic results. Clin Neurol Neurosurg. 2010;112:32-39.

40. Yu Z, Yang Y, Shi X, Qian H, Liu F. A comparison of haemodynamics between subcranialintracranial bypass and the traditional extracranial-intracranial bypass. Br J Neurosurg. 2017;31:668-671.

16. Shin HS, Kim TH, Hwang YS, Park SK. Circumferential wrapping and clipping with temporalis fascia for treatment of unclippable intracranial aneurysms. Yonsei Med J. 2003;44:210-214. 17. Kumar G, Alexandrov AV. Vasospasm surveillance with transcranial Doppler sonography in subarachnoid hemorrhage. J Ultrasound Med. 2015;34: 1345-1350. 18. Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm

29. Kikkawa Y, Ikeda T, Takeda R, et al. Results of early high-flow bypass and trapping for ruptured blood blister-like aneurysms of the internal carotid artery. World Neurosurg. 2017; 105:470-477. 30. Kim BC, Kwon OK, Oh CW, et al. Endovascular internal carotid artery trapping for ruptured blood blister-like aneurysms: long-term results from a single centre. Neuroradiology. 2014;56: 211-217.

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41. Deshmukh VR, Porter RW, Spetzler RF. Use of “bonnet” bypass with radial artery interposition graft in a patient with recurrent cranial base carcinoma: technical report of two cases and review of the literature. Neurosurgery. 2005;56:E202 [discussion: E202]. 42. Iwata Y, Mizuta T, Takemoto O, Shimizu K, Nakatani S. An interposed superficial temporal artery graft bypass for anterior cerebral artery ischemia. Microsurgery. 1988;9:14-17. 43. Ishikawa T, Mutoh T, Nakayama N, et al. Universal external carotid artery to proximal middle cerebral artery bypass with interposed radial artery graft prior to approaching ruptured blood blister-

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like aneurysm of the internal carotid artery. Neurol Med Chir (Tokyo). 2009;49:553-558. 44. Mohit AA, Sekhar LN, Natarajan SK, Britz GW, Ghodke B. High-flow bypass grafts in the management of complex intracranial aneurysms. Neurosurgery. 2007;60:ONS105-ONS122 [discussion: ONS122, ONS103]. 45. Perlmutter D, Rhoton AL Jr. Microsurgical anatomy of the distal anterior cerebral artery. J Neurosurg. 1978;49:204-228.

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46. Winship IR. Cerebral collaterals and collateral therapeutics for acute ischemic stroke. Microcirculation. 2015;22:228-236.

Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.06.143 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com

Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.

Received 18 February 2019; accepted 19 June 2019

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