Endovascular therapy versus microsurgical clipping of unruptured wide-neck aneurysms: a prospective multicenter study with propensity score analysis

Justin R. Mascitelli Department of Neurosurgery, University of Texas Health Science Center, San Antonio, Texas;

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J Mocco Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Trevor Hardigan Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Benjamin K. Hendricks Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona; and

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James S. Yoon Department of Medicine, Yale School of Medicine, New Haven, Connecticut

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Kurt A. Yaeger Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Christopher P. Kellner Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Reade A. De Leacy Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Johanna T. Fifi Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Joshua B. Bederson Department of Neurosurgery, Icahn School of Medicine at Mount Sinai Hospital, Mount Sinai Health System, New York, New York;

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Felipe C. Albuquerque Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona; and

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Andrew F. Ducruet Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona; and

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Lee A. Birnbaum Department of Neurosurgery, University of Texas Health Science Center, San Antonio, Texas;

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Jean Louis R. Caron Department of Neurosurgery, University of Texas Health Science Center, San Antonio, Texas;

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Pavel Rodriguez Department of Neurosurgery, University of Texas Health Science Center, San Antonio, Texas;

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Michael T. Lawton Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona; and

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OBJECTIVE

Numerous techniques have been developed to treat wide-neck aneurysms (WNAs), each with different safety and efficacy profiles. Few studies have compared endovascular therapy (EVT) with microsurgery (MS). The authors’ objective was to perform a prospective multicenter study of a WNA registry using rigorous outcome assessments and to compare EVT and MS using propensity score analysis (PSA).

METHODS

Unruptured, saccular, not previously treated WNAs were included. WNA was defined as an aneurysm with a neck width ≥ 4 mm or a dome-to-neck ratio (DTNR) < 2. The primary outcome was modified Rankin Scale (mRS) score at 1 year after treatment (good outcome was defined as mRS score 0–2), as assessed by blinded research nurses and compared with PSA. Angiographic outcome was assessed using the Raymond scale with core laboratory review (adequate occlusion was defined as Raymond scale score 1–2).

RESULTS

The analysis included 224 unruptured aneurysms in the EVT cohort (n = 140) and MS cohort (n = 84). There were no differences in baseline demographic characteristics, such as proportion of patients with good baseline mRS score (94.3% of the EVT cohort vs 94.0% of the MS cohort, p = 0.941). WNA inclusion criteria were similar between cohorts, with the most common being both neck width ≥ 4 mm and DTNR < 2 (50.7% of the EVT cohort vs 50.0% of the MS cohort, p = 0.228). More paraclinoid (32.1% vs 9.5%) and basilar tip (7.1% vs 3.6%) aneurysms were treated with EVT, whereas more middle cerebral artery (13.6% vs 42.9%) and pericallosal (1.4% vs 4.8%) aneurysms were treated with MS (p < 0.001). EVT aneurysms were slightly larger (p = 0.040), and MS aneurysms had a slightly lower mean DTNR (1.4 for the EVT cohort vs 1.3 for the MS cohort, p = 0.010). Within the EVT cohort, 9.3% of patients underwent stand-alone coiling, 17.1% balloon-assisted coiling, 34.3% stent-assisted coiling, 37.1% flow diversion, and 2.1% PulseRider-assisted coiling. Neurological morbidity secondary to a procedural complication was more common in the MS cohort (10.3% vs 1.4%, p = 0.003). One-year mRS scores were assessed for 218 patients (97.3%), and no significantly increased risk of poor clinical outcome was found for the MS cohort (OR 2.17, 95% CI 0.84–5.60, p = 0.110). In an unadjusted direct comparison, more patients in the EVT cohort achieved a good clinical outcome at 1 year (93.4% vs 84.1%, p = 0.048). Final adequate angiographic outcome was superior in the MS cohort (97.6% of the MS cohort vs 86.5% of the EVT cohort, p = 0.007).

CONCLUSIONS

Although the treatments for unruptured WNA had similar clinical outcomes according to PSA, there were fewer complications and superior clinical outcome in the EVT cohort and superior angiographic outcomes in the MS cohort according to the unadjusted analysis. These results may be considered when selecting treatment modalities for patients with unruptured WNAs.

ABBREVIATIONS

ACA = anterior cerebral artery; AComm = anterior communicating artery; BAC = balloon-assisted coiling; CTA = computed tomography angiography; DTNR = dome-to-neck ratio; DSA = digital subtraction angiography; EDH = epidural hemorrhage; EVT = endovascular therapy; FD = flow diversion; fPCA = fetal posterior cerebral artery; ICA = internal carotid artery; MCA = middle cerebral artery; mRS = modified Rankin Scale; MS = microsurgery; PComm = posterior communicating artery; PSA = propensity score analysis; SAC = stent-assisted coiling; SDH = subdural hemorrhage; WNA = wide-neck aneurysm; WNBA = wide-neck bifurcation aneurysm.

OBJECTIVE

Numerous techniques have been developed to treat wide-neck aneurysms (WNAs), each with different safety and efficacy profiles. Few studies have compared endovascular therapy (EVT) with microsurgery (MS). The authors’ objective was to perform a prospective multicenter study of a WNA registry using rigorous outcome assessments and to compare EVT and MS using propensity score analysis (PSA).

METHODS

Unruptured, saccular, not previously treated WNAs were included. WNA was defined as an aneurysm with a neck width ≥ 4 mm or a dome-to-neck ratio (DTNR) < 2. The primary outcome was modified Rankin Scale (mRS) score at 1 year after treatment (good outcome was defined as mRS score 0–2), as assessed by blinded research nurses and compared with PSA. Angiographic outcome was assessed using the Raymond scale with core laboratory review (adequate occlusion was defined as Raymond scale score 1–2).

RESULTS

The analysis included 224 unruptured aneurysms in the EVT cohort (n = 140) and MS cohort (n = 84). There were no differences in baseline demographic characteristics, such as proportion of patients with good baseline mRS score (94.3% of the EVT cohort vs 94.0% of the MS cohort, p = 0.941). WNA inclusion criteria were similar between cohorts, with the most common being both neck width ≥ 4 mm and DTNR < 2 (50.7% of the EVT cohort vs 50.0% of the MS cohort, p = 0.228). More paraclinoid (32.1% vs 9.5%) and basilar tip (7.1% vs 3.6%) aneurysms were treated with EVT, whereas more middle cerebral artery (13.6% vs 42.9%) and pericallosal (1.4% vs 4.8%) aneurysms were treated with MS (p < 0.001). EVT aneurysms were slightly larger (p = 0.040), and MS aneurysms had a slightly lower mean DTNR (1.4 for the EVT cohort vs 1.3 for the MS cohort, p = 0.010). Within the EVT cohort, 9.3% of patients underwent stand-alone coiling, 17.1% balloon-assisted coiling, 34.3% stent-assisted coiling, 37.1% flow diversion, and 2.1% PulseRider-assisted coiling. Neurological morbidity secondary to a procedural complication was more common in the MS cohort (10.3% vs 1.4%, p = 0.003). One-year mRS scores were assessed for 218 patients (97.3%), and no significantly increased risk of poor clinical outcome was found for the MS cohort (OR 2.17, 95% CI 0.84–5.60, p = 0.110). In an unadjusted direct comparison, more patients in the EVT cohort achieved a good clinical outcome at 1 year (93.4% vs 84.1%, p = 0.048). Final adequate angiographic outcome was superior in the MS cohort (97.6% of the MS cohort vs 86.5% of the EVT cohort, p = 0.007).

CONCLUSIONS

Although the treatments for unruptured WNA had similar clinical outcomes according to PSA, there were fewer complications and superior clinical outcome in the EVT cohort and superior angiographic outcomes in the MS cohort according to the unadjusted analysis. These results may be considered when selecting treatment modalities for patients with unruptured WNAs.

In Brief

The authors' objective was to compare clinical and angiographic outcomes between endovascular therapy (EVT) and microsurgery (MS) for unruptured wide-neck aneurysms (WNAs). Although there was no difference in the primary clinical outcome, secondary clinical outcomes favored EVT and secondary angiographic outcomes favored MS. There are very few published studies that compare EVT and MS for unruptured WNAs, and this study helps fill that literature gap.

Wide-neck aneurysms (WNAs) are a subset of intracranial aneurysms that are of clinical interest because they are more challenging to treat and require more advanced endovascular therapy (EVT) and microsurgery (MS) techniques than narrow-neck aneurysms.1,2 From the EVT standpoint, adjunctive techniques such as use of balloon-assisted coiling (BAC),3 stent-assisted coiling (SAC),4 flow diversion (FD),5 intrasaccular devices,6 and novel neck-support devices7,8 have been developed specifically for the treatment of WNAs. From the MS standpoint, advanced clipping techniques (e.g., use of stacked clips, intersecting clips, and fenestrated tubes) and occasionally bypass surgery (in the case of very large/giant WNAs) are necessary to completely obliterate the aneurysm neck. Certainly, this subset of aneurysms draws more attention than narrow-neck aneurysms, for which more straightforward treatment options exist.

Although there is a surplus of studies in the literature that have evaluated various EVTs for WNAs, these are often retrospective and assess a single treatment type in isolation. There are fewer studies in the literature that have compared various treatments, especially EVT and MS.1,920,25 Studying the efficacy and safety of the various treatments for WNAs remains important. The purpose of this study was to perform a prospective multicenter analysis of a WNA registry by using rigorous blinded outcome assessments and then to compare EVT and MS. Our hypothesis was that there would be no difference in the primary outcome—modified Rankin Scale (mRS) score at 1 year after treatment—as analyzed using propensity score analysis (PSA).

Methods

This is a prospective multicenter analysis of a registry of patients with intracranial WNAs who were treated with both EVT and MS. Three high-volume academic institutions participated. Enrollment began in October 2017 and was completed in June 2019. Local IRB approval was obtained at all sites, and patients (or their appropriate surrogates) provided written informed consent to participate in this study. Consent was obtained from all patients included in this study. Although the registry was primarily designed to evaluate ruptured aneurysms, grant funding was available to collect data on both ruptured and unruptured aneurysms; therefore, a study of patients with ruptured aneurysms (n = 87) was performed and analyzed separately.25 The current study included only patients with unruptured aneurysms (n = 224).

Aneurysm treatment was determined at each treating center according to their standard practice. Practitioners at each site had variable experience, ranging from years to decades. We included patients with unruptured saccular WNAs (with a neck width ≥ 4 mm or dome-to-neck ratio [DTNR] < 2)21 who were 18–80 years of age. We excluded patients with narrow-neck aneurysms and atypical aneurysms (e.g., fusiform, dissecting, mycotic), as well as those who underwent previous aneurysm treatment.

If digital subtraction angiography (DSA) had been performed, the aneurysm was measured in the “working view” or using 3D reconstruction in the view that best demonstrated the aneurysm neck, as determined by the operator. If only computed tomography angiography (CTA) had been performed, then measurements were performed in the view (axial, sagittal, or coronal) that best demonstrated the aneurysm neck. Neck width, dome height, and dome width were measured in a single view (dome width 1), and dome width was measured again in the orthogonal view (dome width 2). Dome width 1 was used to calculate DTNR.

MS interventions included only clip reconstruction (not bypass). EVT interventions included stand-alone coiling, BAC, SAC, FD, and PulseRider-assisted coiling (Cerenovus). Inclusion of multiple WNAs from the same patient was permitted, whether these were treated in the same setting or separate settings. All data were reported per aneurysm (not per patient), except for complications data that were reported per procedure.

Baseline demographic information was collected, including age, sex, ethnicity, baseline mRS score for unruptured aneurysms, and method of presentation for unruptured aneurysms. Aneurysm characteristics were recorded, including aneurysm location, dome measurements (height, width 1, and width 2), neck width, DTNR, aneurysm type (side wall vs bifurcation aneurysm), and presence of a branch vessel and the location of that branch in relation to the aneurysm neck. Treatment characteristics included treatment type, and complications included those for both MS (intraoperative aneurysm rupture, vessel occlusion/injury, vessel stenosis, new cranial nerve injury, intracranial hemorrhage, operative subdural hemorrhage [SDH] or epidural hemorrhage [EDH], seizure, and wound infection/breakdown) and EVT (intraoperative aneurysm rupture, arterial dissection, and thromboembolic, device-related, and access site complications). Vessel stenosis was defined as radiographic stenosis without clinical sequelae, whereas vessel occlusion/injury was defined as a true ischemic complication with clinical sequelae. Every complication was reviewed and adjudicated. Complications that resulted in permanent morbidity or death at the last follow-up were reported.

The primary outcome was mRS score at 1 year after treatment, and the EVT and MS cohorts were compared using PSA. mRS score was assessed at 1 year after treatment by a research nurse, who was unfamiliar with the treatment received, in person or by telephone.22 Secondary outcomes included mRS score at discharge, retreatment rate, and angiographic outcome. Angiographic follow-up was determined by each treating center and was not standardized. DSA, CTA, and MR angiography were all accepted and recorded. Indocyanine green angiography was not used to evaluate any angiographic outcome measures. Angiographic outcomes included immediate aneurysm occlusion and follow-up angiographic occlusion, both assessed with the traditional Raymond scale.23 Angiographic outcome was assessed using core laboratory review by a blinded endovascular radiologist who did not participate in the treatment of any patient in the study. Final angiographic outcome was evaluated on the basis of the findings of the last posttreatment angiographic study for each aneurysm, which may have been an immediate (if only the immediate study was performed) or a delayed (if another was performed during follow-up) study.

Statistical Analysis

Patient demographic characteristics, aneurysm characteristics, procedural information, and outcomes were compared between the MS and EVT groups using the t-test for continuous variables and Pearson’s chi-square test or Fisher’s exact test for categorical variables, as appropriate.

PSA was performed to minimize treatment selection bias in the comparison of outcomes between the EVT and MS groups. Propensity scores for aneurysm treatment modality were created using a nonparsimonious logistic regression model with the following covariates: age, sex, ethnicity, preoperative mRS score, aneurysm location (internal carotid artery [ICA], middle cerebral artery [MCA], anterior cerebral artery [ACA], or posterior circulation), aneurysm width, aneurysm height, and aneurysm neck size. By using these predictors of treatment modality, we calculated a propensity score between 0 and 1 for each patient. Propensity scores were then included as covariates in the final multivariate logistic regression model with the primary outcome (1-year mRS score). Univariate logistic regression analysis was performed to explore unadjusted associations between independent variables and poor outcome at follow-up.

All statistical analyses were performed using Stata version 15 (StataCorp). The results are presented as mean ± SD unless noted otherwise, and statistical significance was defined as p < 0.05.

Results

Baseline Demographic Characteristics

In total, 224 aneurysms were included in this analysis. The average patient age was 60.9 years, and 78.6% of patients were female (Table 1). The majority of patients (94.1%) had good baseline clinical status (mRS score 0–2). There were no major differences between the EVT and MS cohorts in terms of the baseline demographic characteristics, including similar proportions of patients with good baseline mRS scores (94.3% of the EVT cohort vs 94.0% of the MS cohort, p = 0.941).

TABLE 1.

Baseline demographic information

CharacteristicEVT (n = 140)MS (n = 84)p Value
Age, yrs62.0 ± 11.860.3 ± 11.30.295
Sex0.161
 Female110 (78.6)59 (70.2)
 Male30 (21.4)25 (29.8)
Ethnicity0.173
 White83 (59.3)51 (60.7)
 Black13 (9.3)3 (3.6)
 Hispanic38 (27.1)29 (34.5)
 Other6 (4.3)1 (1.2)
Preop mRS score0.941
 0–2132 (94.3)79 (94.0)
 3–58 (5.7)5 (6.0)

Values are shown as number (%) or mean ± SD unless indicated otherwise.

Aneurysm Characteristics

The proportions of patients with each WNA subtype were similar between cohorts, and most patients had both neck width ≥ 4 mm and DTNR < 2 (50.7% of EVT cohort vs 50.0% of MS cohort, p = 0.228) (Table 2). There were significant differences in aneurysm location between the two cohorts (p < 0.001). More paraclinoid aneurysms (32.1% of the EVT cohort vs 9.5% of the MS cohort) and basilar tip aneurysms (7.1% vs 3.6%) were treated with EVT, whereas more MCA (13.6% vs 42.9%) and pericallosal (1.4% vs 4.8%) aneurysms were treated with MS (p < 0.001). The proportions of posterior communicating artery (PComm)/fetal posterior cerebral artery (fPCA) aneurysms (10.7% of the EVT cohort vs 7.1% of the MS cohort) and anterior communicating artery (AComm) aneurysms (14.3% vs 16.7%) were similar in both cohorts. Aneurysm domes were larger in the EVT cohort, with larger mean dome width (6.6 mm vs 5.7 mm, p = 0.040) and dome height (6.0 mm vs 5.2 mm, p = 0.038). Mean aneurysm neck width was similar between cohorts (4.6 mm in the EVT cohort vs 4.3 mm in the MS cohort, p = 0.161), but mean DTNR was lower in the MS cohort (1.3 vs 1.4, p = 0.010). More bifurcation aneurysms were included in the MS cohort (38.6% of the EVT cohort vs 59.5% of the MS cohort, p = 0.002). There were no differences in the presence or location of branch vessels between cohorts.

TABLE 2.

Aneurysm information

CharacteristicEVT (n = 140)MS (n = 84)p Value
Inclusion criteria0.228
 Neck ≥4 mm13 (9.3)3 (3.6)
 DTNR <256 (40.0)39 (46.4)
 Both71 (50.7)42 (50.0)
Location<0.001
 Anterior circulation
  ICA
   Ophthalmic32 (22.9)6 (7.1)
   SH9 (6.4)1 (1.2)
   Clinoidal4 (2.9)1 (1.2)
   Ventral wall1 (0.7)3 (3.6)
   Dorsal wall3 (2.1)1 (1.2)
   PComm/fPCA15 (10.7)6 (7.1)
   AChA1 (0.7)2 (2.4)
   Terminus6 (4.3)4 (4.8)
   Other7 (5.0) 0 (0.0)
  AComm20 (14.3)14 (16.7)
  Pericallosal2 (1.4)4 (4.8)
  Other ACA2 (1.4)0 (0.0)
  MCA19 (13.6)36 (42.9)
 Posterior circulation
  Vertebral2 (1.4)0 (0.0)
  PICA1 (0.7)1 (1.2)
  Basilar trunk1 (0.7) 0 (0.0)
  SCA3 (2.1)1 (1.2)
  PCA2 (1.4)1 (1.2)
  Basilar tip10 (7.1)3 (3.6)
Aneurysms size, mm
 Dome width6.6 ± 3.45.7 ± 3.20.040
 Dome height6.0 ± 2.75.2 ± 3.40.038
 Neck width4.6 ± 1.84.3 ± 1.70.161
 DTNR1.4 ± 0.51.3 ± 0.40.010
Aneurysm type0.002
 Bifurcation54 (38.6)50 (59.5)
 Side wall86 (61.4)34 (40.5)
Associated branch vessel62270.873
 Parent vessel35 (46.4)16 (59.3)
 Aneurysm neck22 (35.5)10 (37.0)
 Aneurysm dome5 (8.1)1 (3.7)

AChA = anterior choroidal artery; PCA = posterior cerebral artery; PICA = posterior inferior cerebellar artery; SCA = superior cerebellar artery; SH = superior hypophyseal.

Values are shown as number, number (%), or mean ± SD unless indicated otherwise.

Treatment Characteristics

In total, 140 (62.5%) aneurysms were treated with EVT and 84 (37.5%) with MS (Table 3). Within the EVT cohort, 9.3% of aneurysms underwent stand-alone coiling, 17.1% BAC, 34.3% SAC, 37.1% FD, and 2.1% PulseRider-assisted coiling. One patient in the EVT cohort had a complication prior to FD placement and was not treated. All other patients completed treatment.

TABLE 3.

Procedural information and complications

CharacteristicEVT (n = 140)MS (n = 84)p Value
Treatment typeNA
 MS84 (100.0)
 EVT140 (100.0)
  Stand-alone coiling13 (9.3)
  BAC24 (17.1)
  SAC48 (34.3)
  FD52 (37.1)
  PulseRider3 (2.1)
Procedural complications15 (10.7)24 (28.6)<0.001
 MS
  Intraop aneurysm rupture0 (0.0)
  Vessel occlusion/injury8 (9.5)
  Vessel stenosis4 (4.8)
  New cranial nerve injury5 (6.0)
  Intracranial hemorrhage2 (2.4)
  Operative SDH/EDH0 (0.0)
  Seizure2 (2.4)
  Wound infection/breakdown2 (2.4)
 EVT
  Intraop aneurysm rupture1 (0.7)
  Thromboembolic complication9 (6.4)
  Device-related complication1 (0.7)
  Arterial injury2 (1.4)
  Access site2 (1.4)
Neurological morbidity secondary to complication2 (1.4)9 (10.3)0.003
Medical complication10 (7.1)13 (15.5)0.047

NA = not applicable.

Values are shown as number (%) unless indicated otherwise.

All patients in the MS cohort underwent surgical clipping. Procedural complications were more common in the MS cohort (28.6% of the MS cohort vs 10.7% of the EVT cohort, p < 0.001). The most frequent complications in the MS cohort were ischemic complication secondary to vessel occlusion/injury (9.5%) and new cranial nerve injury (6.0%). One patient returned to the operating room for clip repositioning. Neurological morbidity at the last follow-up secondary to the complication was more common in the MS cohort (10.3% vs 1.4%, p = 0.003). In the EVT cohort, 1 of the 2 patients (50%) with permanent neurological morbidity due to the complication had a poor outcome at 1 year. In the MS cohort, only 1 of the 9 patients (11.1%) with permanent neurological morbidity due to the complication had a poor outcome at 1 year. Medical complications were also more common in the MS cohort (15.5% vs 7.1%, p = 0.047).

Clinical and Angiographic Outcomes

The 1-year mRS scores were assessed in 218 patients (97.3%). The MS cohort did not demonstrate a significantly increased risk of poor clinical outcome (OR 2.17, 95% CI 0.84–5.60, p = 0.110) (Table 4). With regard to secondary outcomes, in an unadjusted direct comparison of the cohorts, more patients in the EVT cohort achieved a good clinical outcome at 1 year (93.4% vs 84.1%, p = 0.048) (Table 5). Additionally, more patients in the EVT cohort had a good clinical outcome at discharge (92.1% vs 66.7%, p < 0.001). Five patients in the MS cohort (6.0%) and 5 in the EVT cohort (3.6%) progressed from good clinical outcome at discharge to poor clinical outcome at 1 year.

TABLE 4.

Propensity score–adjusted association between treatment modality and poor clinical outcome*

TreatmentAdjusted OR (95% CI)p Value
EVTReference
MS2.17 (0.84–5.60)0.110

Defined as mRS score of 3–6 at 1 year.

OR was adjusted for age, sex, ethnicity, baseline mRS score, aneurysm location (ICA, MCA, ACA, or posterior circulation), aneurysm width, aneurysm height, aneurysm neck size, and medical complications using a multivariable logistic regression model with propensity score.

TABLE 5.

Secondary clinical and angiographic outcomes

CharacteristicEVT (n = 140)MS (n = 84)p Value
Immediate clinical outcome, mRS score at discharge14084<0.001
 0–2129 (92.1)56 (66.7)
 3–511 (7.9)28 (33.3)
 60 (0.0)0 (0.0)
Follow-up clinical outcome, mRS score at 1 yr136820.048
 0–2127 (93.4)69 (84.1)
 3–58 (5.9)9 (11.0)
 61 (0.7)4 (4.9)
Immediate angiographic outcome, RR grade14084<0.001
 0–284 (60.0)81 (96.4)
 356 (40.0)3 (3.6)
Final angiographic outcome 13383
 Follow-up, mos9.6 ± 4.94.0 ± 6.6<0.001
 Modality
  DSA105 (79.0)10 (12.0)<0.001
  CTA5 (3.7)68 (81.9)
  MRA23 (17.3)5 (6.0)
 Occlusion, RR grade0.007
  1–2115 (86.5)81 (97.6)
  318 (13.5)2 (2.4)
Retreatment5 (3.6)0 (0.0)0.160

RR = Raymond-Roy.

Values are shown as number, number (%), or mean ± SD unless indicated otherwise.

Immediate angiographic outcomes were superior in the MS cohort, with more aneurysms showing adequate occlusion (96.4% of the MS cohort vs 60.0% of the EVT cohort, p < 0.001). The EVT cohort had longer mean angiographic follow-up (9.6 months vs 4.0 months, p < 0.001). The EVT cohort primarily underwent DSA (79.0% of patients), whereas the MS cohort primarily underwent CTA (81.9%, p < 0.001). Final angiographic outcomes were superior in the MS cohort, with more aneurysms showing adequate occlusion (97.6% of the MS cohort vs 86.5% of the EVT cohort, p = 0.007). The retreatment rates were not statistically different, but no retreatments were reported in the MS cohort (3.6% of the EVT cohort vs 0.0% of the MS cohort, p = 0.160). There were no complications during aneurysm retreatment.

Multiple factors were evaluated with univariate logistic regression analysis to determine their associations with poor outcome (Table 6), including age, sex, aneurysm location (anterior vs posterior circulation), WNA criteria, aneurysm type (bifurcation vs side wall), treatment modality (EVT vs MS), procedural complications, and neurological morbidity from complications. However, the only factor that was associated with poor outcome was MS treatment modality (OR 2.65, 95% CI 1.08–6.53, p = 0.033).

TABLE 6.

Unadjusted bivariate associations between demographic, aneurysm, procedural, and clinical characteristics and poor outcome at 1 year (MRS score 3–6)

VariableUnivariate
OR (95% CI)p Value
Age*1.09 (0.75–1.59)0.656
Sex
 FemaleReference
 Male1.22 (0.45–3.31)0.692
Race
 WhiteReference
 Other1.03 (0.42–2.51)0.956
Aneurysm location
 Posterior circulationReference
 Anterior circulation2.93 (0.38–22.79)0.304
WNA criteria
 BothReference
 Neck ≥4 mm1.85 (0.72–4.73)0.201
 DTNR <21.94 (0.37–10.15)0.431
Aneurysm type
 BifurcationReference
 Side wall0.87 (0.36–2.09)0.750
Treatment modality
 EVTReference
 MS2.65 (1.08–6.53)0.033
Procedural complications2.48 (0.94–6.59)0.068
Neurological morbidity secondary to complication2.08 (0.42–10.29)0.370
Medical complications1.47 (0.40–5.43)0.563

Evaluated at 10-year intervals.

Defined as both neck width ≥ 4 mm and DTNR < 2.

Discussion

Main Findings

At 1 year after treatment, there was no difference in clinical outcome between the EVT and MS cohorts according to PSA. EVT had superior 1-year clinical outcomes compared with MS according to an unadjusted direct comparison and multivariate analysis. There was a higher complication rate (both procedural and medical) in the MS cohort, and procedural complications more frequently led to neurological morbidity by the last follow-up. The most frequent procedural complications in the MS cohort were ischemic complications secondary to vessel occlusion or injury and new cranial nerve injury. The complication rate in the MS cohort was higher than expected and should be noted. With that said, procedural complications overwhelmingly did not lead to poor clinical outcome at 1 year.

There were superior angiographic outcomes in the MS cohort compared with those of the EVT cohort. Additionally, there was a trend toward more retreatments in the EVT cohort and no retreatments in the MS cohort. The cohorts were well matched except for aneurysm location, with more paraclinoid and basilar apex aneurysms in the EVT cohort and more MCA and pericallosal aneurysms in the MS cohort. There were more bifurcation aneurysms in the MS cohort.

Previously Published Studies in the Literature

Although a great deal of work has compared EVT with MS for the treatment of intracranial aneurysms, there is a paucity of studies in the literature that compared these two modalities for the treatment of WNAs.1,14,1820 Studies frequently focus on the safety and efficacy of one treatment type in isolation, especially EVTs. Many studies also compared different endovascular approaches (e.g., BAC vs stand-alone coiling or FD vs SAC).913,1517 However, few studies compared EVT with MS. A post hoc analysis of the Barrow Ruptured Aneurysm Trial (BRAT) demonstrated similar clinical outcomes between EVT and MS for ruptured WNAs.14 Similarly, the Endovascular Therapy Versus Microsurgical Clipping of Ruptured Wide Neck Aneurysms (EVERRUN) Registry (the ruptured cohort of our study that was published separately25) demonstrated similar outcomes between EVT and MS. These studies are less applicable to the present analysis, however, because both evaluated only ruptured aneurysms.

Fiorella et al.1 performed a meta-analysis of traditional therapies, including coiling, SAC, and MS, for wide-neck bifurcation aneurysms (WNBAs). The authors had a unique method for measuring angiographic outcome and excluded 12% of studies because of non–core laboratory adjudication. Forty-three (2794 aneurysms) and 65 (5366 patients) studies were included for evaluation of efficacy and safety, respectively. The rates of adequate occlusion were 43.8% and 69.7% for EVT and MS, respectively. The rates of occurrence of adverse events were 21.1% and 24.3% for EVT and MS, respectively. The study did not report clinical outcome. The authors concluded that conventional therapies for WNBA were associated with low rates of complete occlusion and that complications were not infrequent. In comparison, we achieved better occlusion rates and lower complication rates in the EVT cohort of our study. Certainly, WNBAs present greater challenges than WNAs, and this may partially account for the differences. It should be noted that there were more WNBAs in our MS cohort, and this may have impacted the outcome of the study.

Won et al. reported a stand-alone analysis of microsurgical treatment of WNAs, both ruptured and unruptured.24 They reported that 90.2% of patients in the unruptured cohort (n = 148) had good clinical outcome at follow-up, 95.9% had adequate occlusion, and 8.1% had complications, all of which are relatively consistent with our data. However, this was not a comparative analysis with EVT. Goertz et al. recently published a PSA that compared MS with the WEB Embolization System (MicroVention) for the treatment of anterior circulation WNAs.19 Complications were more frequent in the clipping group (13% vs 6% of patients) and good angiographic outcome was superior in the clipping group (94% vs 75%), which are consistent with the findings of our study. However, the proportions of patients with good clinical outcome were similar between cohorts (99% of the MS cohort vs 98% of the WEB cohort), which is inconsistent with the results of our study when considering the unadjusted univariate outcomes. The study by Goertz et al. was performed retrospectively without blinded outcome measures, which may account for this difference.

MCA location, a traditional surgical location, has been the subject of a few recent comparative analyses of EVT versus MS. Pflaeging et al. published a retrospective review of clipping and EVT for 160 unruptured MCA aneurysms and found that patients who underwent clipping had a superior occlusion rate (89% vs 76%) and similar rates of complications (17% vs 20%) and good functional outcome (99% vs 95%).18 A meta-analysis of clipping versus EVT for unruptured MCA aneurysm was reported by Toccaceli et al. and included 29 studies and 1552 patients. Again, the clipping cohort had superior adequate angiographic outcomes (96% vs 78%) but worse good clinical outcome (84% vs 97%), both of which mimicked our results. Additionally, a greater proportion of patients in the EVT cohort had complications (5.6% vs 2.9%).20

In all, there are very few studies that compared EVT and MS, which highlights the value of our analysis. Our results, though not completely consistent, generally align with the findings in the literature and show that patients who underwent EVT had superior clinical outcomes and inferior angiographic outcomes compared with those who underwent MS. The rate of complications of the MS cohort was higher than expected in our study, and the rate of complications of the EVT cohort was lower than expected. Certainly, the risks of cranial nerve palsy and ischemic complications should be considered when selecting MS for patients with unruptured aneurysms. Treatment decisions are becoming increasingly more complicated as more and more novel EVT devices are released, such as the WEB Embolization System,6 PulseRider,7 Comaneci (Rapid Medical),8 and many others. Some of these devices offer the advantage of mono antiplatelet therapy rather than dual antiplatelet therapy.

Limitations

This study has limitations. The data were generated across three large-volume centers, and the findings may not be widely generalizable. As is the case for any multicenter study, each institution had its own treatment biases and clinical/angiographic outcomes, which may not be completely consistent and may have impacted the results. Similarly, the practitioners at each institution had variable levels of experience, which also may have impacted the results. The registry format resulted in nonequivalent treatment cohorts, with individual and institutional biases determining how each individual WNA was treated, especially with regard to aneurysm location. PSA was used to correct for this limitation, but it should still be kept in mind when interpreting the results. Given the discrepancy in aneurysm location, the two modalities may be considered complementary approaches that could be used to achieve similar outcomes for different aneurysms. The study was powered to detect only a large difference between treatment cohorts. Angiographic follow-up was not standardized: more follow-up studies were performed in the EVT cohort, and a greater proportion of patients in the EVT cohort underwent DSA than CTA. Certainly, a neck remnant (and possibly even a small aneurysm remnant) can be overlooked on CTA. Nonuniform angiographic follow-up should be kept in mind when interpreting the angiographic results. Finally, this analysis did not include more novel EVT treatments, such as the WEB or Comaneci device.

Strengths

The registry format allowed for more patients to participate or enroll in a randomized clinical trial. All patients were treated at high-volume tertiary academic centers by multidisciplinary cerebrovascular teams. All data were collected prospectively. Clinical outcomes were obtained rigorously in a prospective fashion by unbiased blinded research nurses. The primary outcome was assessed in 97.3% of patients. Likewise, angiographic outcomes were analyzed rigorously using core laboratory review by a neurointerventional radiologist who did not participate in the treatment of any patient included in this study and was blinded to both patient information and the treating center during angiographic review. Core laboratory review has been shown to be more reliable than self-reported results.2 Finally, there are very few studies in the literature that compare EVT and MS, and our analysis contributes greatly to this literature gap.

Conclusions

Although the treatments for unruptured WNA had similar clinical outcomes according to the PSA, there were fewer complications and superior clinical outcomes in the EVT cohort according to the unadjusted analysis, a trend toward superior clinical outcomes in the EVT cohort according to the PSA, and superior angiographic outcomes in the MS cohort. These results may be considered when selecting treatment modalities for patients with unruptured WNAs. Treatment decisions are becoming increasingly more complicated as more and more novel EVT devices are released, and it is important to evaluate and compare these treatment options.

Acknowledgments

This study was graciously supported by the 2017 The Bee Foundation Preventative Brain Aneurysm Research Grant.

Disclosures

Dr. Mascitelli is a consultant for Stryker. Dr. Mocco is a principal investigator for research trials funded by Stryker Neurovascular, MicroVention, and Penumbra; is an investor in Cerebrotech, Imperative Care, EndoStream, Viseon, BlinkTBI, Myra Medical, Serenity, Vastrax, NTI, RIST, Viz.ai, Synchron, Radical, and Truvic; and is a consultant for or was a consultant for Cerebrotech, Viseon, EndoStream, Vastrax, RIST, Synchron, Viz.ai, Perflow, and CVAid. Dr. Hendricks is a consultant for Medtronic and holds patents with Medtronic. Dr. Kellner receives research grant support from Penumbra, Siemens, and Viz.ai. Dr. De Leacy receives grant support from Asahi Intec and Medtronic; serves on the advisory board of Cerenovus; owns stock in Spartan Micro, Q’Apel, Synchron, and EndoStream; and is a consultant for Siemens, Cerenovus, Stryker Neurovascular, Penumbra, and Imperative Care. Dr. Fifi receives grant support from Stryker and Penumbra; is a consultant for Stryker, MicroVention, Penumbra, and Cerenovus; and owns stock in EndoStream. Dr. Bederson has received financial compensation from Brainlab, Carl Zeiss Meditec, Inc., and Surgical Theater; and holds equity with NeuroTechnologies Investors and Surgical Theater. Dr. Ducruet is a consultant for Cerenovus, Stryker, Medtronic, Koswire, Oculus, and Penumbra. Dr. Lawton is a consultant for Zeiss and Aesculap and receives royalties from Mizuho.

Author Contributions

Conception and design: Mascitelli, Mocco, Hendricks, Albuquerque. Acquisition of data: Mascitelli, Mocco, Hardigan, Hendricks, Yaeger, Kellner, De Leacy, Fifi, Bederson, Albuquerque, Ducruet, Birnbaum, Caron, Rodriguez, Lawton. Analysis and interpretation of data: Mascitelli, Mocco, Hardigan, Hendricks, Yoon, Yaeger, Kellner, Fifi, Bederson, Albuquerque, Ducruet, Birnbaum, Caron, Lawton. Drafting the article: Mascitelli, Mocco, Hardigan, Hendricks, Yoon, Yaeger. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Mascitelli. Statistical analysis: Mascitelli, Hardigan, Yoon. Administrative/technical/material support: Mascitelli, Mocco, Bederson, Albuquerque. Study supervision: Mascitelli, Mocco.

References

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  • 2

    De Leacy RA, Fargen KM, Mascitelli JR, Fifi J, Turkheimer L, Zhang X, et al. Wide-neck bifurcation aneurysms of the middle cerebral artery and basilar apex treated by endovascular techniques: a multicentre, core lab adjudicated study evaluating safety and durability of occlusion (BRANCH). J Neurointerv Surg. 2019;11(1):3136.

    • Crossref
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  • 3

    Shapiro M, Babb J, Becske T, Nelson PK. Safety and efficacy of adjunctive balloon remodeling during endovascular treatment of intracranial aneurysms: a literature review. AJNR Am J Neuroradiol. 2008;29(9):17771781.

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    Mocco J, Snyder KV, Albuquerque FC, Bendok BR, Alan S B, Carpenter JS, et al. Treatment of intracranial aneurysms with the Enterprise stent: a multicenter registry. J Neurosurg. 2009;110(1):3539.

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  • 5

    Becske T, Brinjikji W, Potts MB, Kallmes DF, Shapiro M, Moran CJ, et al. Long-term clinical and angiographic outcomes following Pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the Pipeline for Uncoilable or Failed Aneurysms Trial. Neurosurgery. 2017;80(1):4048.

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    Pierot L, Costalat V, Moret J, Szikora I, Klisch J, Herbreteau D, et al. Safety and efficacy of aneurysm treatment with WEB: results of the WEBCAST study. J Neurosurg. 2016;124(5):12501256.

    • Crossref
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    Srinivasan VM, Srivatsan A, Spiotta AM, Hendricks BK, Ducruet AF, Albuquerque FC, et al. Early postmarket results with PulseRider for treatment of wide-necked intracranial aneurysms: a multicenter experience. J Neurosurg. 2020;133(6):17561765.

    • Crossref
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    • Search Google Scholar
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  • 8

    Taqi MA, Raz E, Vechera A, Shapiro M, Gupta R, Haynes J, et al. Early Experience with Comaneci, a newly FDA-approved controllable assist device for wide-necked intracranial aneurysm coiling. Cerebrovasc Dis. 2021;50(4):464471.

    • Crossref
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    • Search Google Scholar
    • Export Citation
  • 9

    Pierot L, Cognard C, Anxionnat R, Ricolfi F. Remodeling technique for endovascular treatment of ruptured intracranial aneurysms had a higher rate of adequate postoperative occlusion than did conventional coil embolization with comparable safety. Radiology. 2011;258(2):546553.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Hetts SW, Turk A, English JD, Dowd CF, Mocco J, Prestigiacomo C, et al. Stent-assisted coiling versus coiling alone in unruptured intracranial aneurysms in the matrix and platinum science trial: safety, efficacy, and mid-term outcomes. AJNR Am J Neuroradiol. 2014;35(4):698705.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Fan L, Tan X, Xiong Y, Zheng K, Li Z, Liu D, et al. Stent-assisted coiling versus coiling alone of ruptured anterior communicating artery aneurysms: a single-center experience. Clin Neurol Neurosurg. 2016;144:96100.

    • Crossref
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    • Search Google Scholar
    • Export Citation
  • 12

    Cai K, Zhang Y, Shen L, Ni Y, Ji Q. Comparison of stent-assisted coiling and balloon-assisted coiling in the treatment of ruptured wide-necked intracranial aneurysms in the acute period. World Neurosurg. 2016;96:316321.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Consoli A, Vignoli C, Renieri L, Rosi A, Chiarotti I, Nappini S, et al. Assisted coiling of saccular wide-necked unruptured intracranial aneurysms: stent versus balloon. J Neurointerv Surg. 2016;8(1):5257.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Mascitelli JR, Lawton MT, Hendricks BK, Nakaji P, Zabramski JM, Spetzler RF. Analysis of wide-neck aneurysms in the Barrow Ruptured Aneurysm Trial. Neurosurgery. 2019;85(5):622631.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Malhotra A, Wu X, Brinjikji W, Miller T, Matouk CC, Sanelli P, Gandhi D. Pipeline endovascular device vs stent-assisted coiling in small unruptured aneurysms: a cost-effectiveness analysis. Neurosurgery. 2019;85(6):E1010E1019.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Salem MM, Ravindran K, Enriquez-Marulanda A, Ascanio LC, Jordan N, Gomez-Paz S, et al. Pipeline embolization device versus stent-assisted coiling for intracranial aneurysm treatment: a retrospective propensity score-matched study. Neurosurgery. 2020;87(3):516522.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Limbucci N, Cirelli C, Valente I, Nappini S, Renieri L, Laiso A, et al. Y-stenting versus PulseRider-assisted coiling in the treatment of wide-neck bifurcation aneurysms: role of anatomical features on midterm results. Neurosurgery. 2020;87(2):329337.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Pflaeging M, Kabbasch C, Schlamann M, Pennig L, Juenger ST, Grunz JP, et al. Microsurgical clipping versus advanced endovascular treatment of unruptured middle cerebral artery bifurcation aneurysms after a "coil-first" policy. World Neurosurg. 2021;149:e336e344.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Goertz L, Liebig T, Siebert E, Pennig L, Laukamp KR, Celik E, et al. Woven Endobridge Embolization versus microsurgical clipping for unruptured anterior circulation aneurysms: a propensity score analysis. Neurosurgery. 2021;88(4):779784.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Toccaceli G, Diana F, Cagnazzo F, Cannizzaro D, Lanzino G, Barbagallo GMV, et al. Microsurgical clipping compared with new and most advanced endovascular techniques in the treatment of unruptured middle cerebral artery aneurysms: a meta-analysis in the modern Era. World Neurosurg. 2020;137:451464.e1.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Hendricks BK, Yoon JS, Yaeger K, Kellner CP, Mocco J, De Leacy RA, et al. Wide-neck aneurysms: systematic review of the neurosurgical literature with a focus on definition and clinical implications. J Neurosurg. 2020;133(1):159165.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Janssen PM, Visser NA, Dorhout Mees SM, Klijn CJ, Algra A, Rinkel GJ. Comparison of telephone and face-to-face assessment of the modified Rankin Scale. Cerebrovasc Dis. 2010;29(2):137139.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32(9):19982004.

  • 24

    Won SY, Seifert V, Dubinski D, Kashefiolasl S, Dinc N, Bruder M, Konczalla J. Short- and midterm outcome of ruptured and unruptured intracerebral wide-necked aneurysms with microsurgical treatment. Sci Rep. 2021;11(1):4982.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Mascitelli JR, Lawton MT, Hendricks BK, et al. Endovascular Therapy Versus Microsurgical Clipping of Ruptured Wide Neck Aneurysms (EVERRUN Registry): a multicenter, prospective propensity score analysis. J Neurosurg. Published online November 5, 2021.doi: 10.3171/2021.7.JNS211323

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Images from Minchev et al. (pp 479–488).

  • 1

    Fiorella D, Arthur AS, Chiacchierini R, Emery E, Molyneux A, Pierot L. How safe and effective are existing treatments for wide-necked bifurcation aneurysms? Literature-based objective performance criteria for safety and effectiveness. J Neurointerv Surg. 2017;9(12):11971201.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    De Leacy RA, Fargen KM, Mascitelli JR, Fifi J, Turkheimer L, Zhang X, et al. Wide-neck bifurcation aneurysms of the middle cerebral artery and basilar apex treated by endovascular techniques: a multicentre, core lab adjudicated study evaluating safety and durability of occlusion (BRANCH). J Neurointerv Surg. 2019;11(1):3136.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Shapiro M, Babb J, Becske T, Nelson PK. Safety and efficacy of adjunctive balloon remodeling during endovascular treatment of intracranial aneurysms: a literature review. AJNR Am J Neuroradiol. 2008;29(9):17771781.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Mocco J, Snyder KV, Albuquerque FC, Bendok BR, Alan S B, Carpenter JS, et al. Treatment of intracranial aneurysms with the Enterprise stent: a multicenter registry. J Neurosurg. 2009;110(1):3539.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Becske T, Brinjikji W, Potts MB, Kallmes DF, Shapiro M, Moran CJ, et al. Long-term clinical and angiographic outcomes following Pipeline embolization device treatment of complex internal carotid artery aneurysms: five-year results of the Pipeline for Uncoilable or Failed Aneurysms Trial. Neurosurgery. 2017;80(1):4048.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Pierot L, Costalat V, Moret J, Szikora I, Klisch J, Herbreteau D, et al. Safety and efficacy of aneurysm treatment with WEB: results of the WEBCAST study. J Neurosurg. 2016;124(5):12501256.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Srinivasan VM, Srivatsan A, Spiotta AM, Hendricks BK, Ducruet AF, Albuquerque FC, et al. Early postmarket results with PulseRider for treatment of wide-necked intracranial aneurysms: a multicenter experience. J Neurosurg. 2020;133(6):17561765.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Taqi MA, Raz E, Vechera A, Shapiro M, Gupta R, Haynes J, et al. Early Experience with Comaneci, a newly FDA-approved controllable assist device for wide-necked intracranial aneurysm coiling. Cerebrovasc Dis. 2021;50(4):464471.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Pierot L, Cognard C, Anxionnat R, Ricolfi F. Remodeling technique for endovascular treatment of ruptured intracranial aneurysms had a higher rate of adequate postoperative occlusion than did conventional coil embolization with comparable safety. Radiology. 2011;258(2):546553.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Hetts SW, Turk A, English JD, Dowd CF, Mocco J, Prestigiacomo C, et al. Stent-assisted coiling versus coiling alone in unruptured intracranial aneurysms in the matrix and platinum science trial: safety, efficacy, and mid-term outcomes. AJNR Am J Neuroradiol. 2014;35(4):698705.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Fan L, Tan X, Xiong Y, Zheng K, Li Z, Liu D, et al. Stent-assisted coiling versus coiling alone of ruptured anterior communicating artery aneurysms: a single-center experience. Clin Neurol Neurosurg. 2016;144:96100.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Cai K, Zhang Y, Shen L, Ni Y, Ji Q. Comparison of stent-assisted coiling and balloon-assisted coiling in the treatment of ruptured wide-necked intracranial aneurysms in the acute period. World Neurosurg. 2016;96:316321.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Consoli A, Vignoli C, Renieri L, Rosi A, Chiarotti I, Nappini S, et al. Assisted coiling of saccular wide-necked unruptured intracranial aneurysms: stent versus balloon. J Neurointerv Surg. 2016;8(1):5257.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Mascitelli JR, Lawton MT, Hendricks BK, Nakaji P, Zabramski JM, Spetzler RF. Analysis of wide-neck aneurysms in the Barrow Ruptured Aneurysm Trial. Neurosurgery. 2019;85(5):622631.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Malhotra A, Wu X, Brinjikji W, Miller T, Matouk CC, Sanelli P, Gandhi D. Pipeline endovascular device vs stent-assisted coiling in small unruptured aneurysms: a cost-effectiveness analysis. Neurosurgery. 2019;85(6):E1010E1019.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Salem MM, Ravindran K, Enriquez-Marulanda A, Ascanio LC, Jordan N, Gomez-Paz S, et al. Pipeline embolization device versus stent-assisted coiling for intracranial aneurysm treatment: a retrospective propensity score-matched study. Neurosurgery. 2020;87(3):516522.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Limbucci N, Cirelli C, Valente I, Nappini S, Renieri L, Laiso A, et al. Y-stenting versus PulseRider-assisted coiling in the treatment of wide-neck bifurcation aneurysms: role of anatomical features on midterm results. Neurosurgery. 2020;87(2):329337.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Pflaeging M, Kabbasch C, Schlamann M, Pennig L, Juenger ST, Grunz JP, et al. Microsurgical clipping versus advanced endovascular treatment of unruptured middle cerebral artery bifurcation aneurysms after a "coil-first" policy. World Neurosurg. 2021;149:e336e344.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Goertz L, Liebig T, Siebert E, Pennig L, Laukamp KR, Celik E, et al. Woven Endobridge Embolization versus microsurgical clipping for unruptured anterior circulation aneurysms: a propensity score analysis. Neurosurgery. 2021;88(4):779784.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Toccaceli G, Diana F, Cagnazzo F, Cannizzaro D, Lanzino G, Barbagallo GMV, et al. Microsurgical clipping compared with new and most advanced endovascular techniques in the treatment of unruptured middle cerebral artery aneurysms: a meta-analysis in the modern Era. World Neurosurg. 2020;137:451464.e1.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Hendricks BK, Yoon JS, Yaeger K, Kellner CP, Mocco J, De Leacy RA, et al. Wide-neck aneurysms: systematic review of the neurosurgical literature with a focus on definition and clinical implications. J Neurosurg. 2020;133(1):159165.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Janssen PM, Visser NA, Dorhout Mees SM, Klijn CJ, Algra A, Rinkel GJ. Comparison of telephone and face-to-face assessment of the modified Rankin Scale. Cerebrovasc Dis. 2010;29(2):137139.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32(9):19982004.

  • 24

    Won SY, Seifert V, Dubinski D, Kashefiolasl S, Dinc N, Bruder M, Konczalla J. Short- and midterm outcome of ruptured and unruptured intracerebral wide-necked aneurysms with microsurgical treatment. Sci Rep. 2021;11(1):4982.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Mascitelli JR, Lawton MT, Hendricks BK, et al. Endovascular Therapy Versus Microsurgical Clipping of Ruptured Wide Neck Aneurysms (EVERRUN Registry): a multicenter, prospective propensity score analysis. J Neurosurg. Published online November 5, 2021.doi: 10.3171/2021.7.JNS211323

    • PubMed
    • Search Google Scholar
    • Export Citation

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