Abstract
Background
The Neuroform Atlas stent is thought to have features allowing for an improved stent delivery system. We aimed to provide a comparison of the Atlas and Neuroform EZ stents in patients treated with stent-assisted coiling.
Methods
Seventy-seven aneurysms treated with the Atlas stent and 77 aneurysms with similar characteristics treated with the EZ stent were retrospectively compared. Outcomes included angiographic occlusion per the Raymond–Roy (RR) scale, recanalization, retreatment and procedural complications.
Results
With the Atlas stent, technical success was 100% and immediate RR1 occlusion was 81.8%. Follow-up RR1 was achieved in 83.7%. The recanalization rate was 7% and the retreatment rate was 4.6%. The complication rate was 6.5% (new neurological deficit in 1.3%). With the EZ stent, technical success was 96%, immediate RR1 occlusion was 67.6% and follow-up RR1 was 67.6%. The recanalization rate was 12.7% and the retreatment rate was 14.1%. The complication rate was 10.4% (new neurological deficit in 2.6%). The rate of immediate RR1 occlusion was significantly higher with the Atlas stent (p = 0.03), and the rate of follow-up RR1 was nonsignificantly higher with the Atlas stent (p = 0.08). The retreatment rate was significantly lower with the Atlas stent (p = 0.009). There were no significant differences in the rates of recanalization (p = 0.5) and complications (p = 0.6).
Conclusions
Stent-assisted coiling with the Atlas stent is safe and effective and shows better immediate results as compared to the EZ stent, with improved overall follow-up outcomes.
Keywords: Atlas stent, EZ stent, endovascular treatment, intracranial aneurysms, stent-assisted coiling
Introduction
Wide-necked, complex aneurysms represent a more challenging subgroup of aneurysms that are occasionally difficult to treat with conventional endovascular techniques. 1 Patients harboring these aneurysms have been classically regarded as poor candidates for endovascular management given the technical challenges related to stabilization of the coil mass. Studies have shown lower occlusion rates and higher recanalization/retreatment rates for these aneurysms with standard coiling. 2 The introduction of stents designed for the intracranial circulation has changed the treatment paradigm for these aneurysms. 3 Stent-assisted coiling (SAC) now represents one of the most established techniques for endovascular management of large, wide-necked aneurysms.
The stents most commonly utilized in coil embolization of wide-necked intracranial aneurysms have been the Neuroform stent approved by the U.S. Food and Drug Administration (FDA) in 2002, and the Enterprise stent, approved in 2007. Recently, the Neuroform Atlas stent (Stryker, Kalamazoo, Michigan), a self-expandable nitinol stent, was developed with the intent of establishing an easy to use delivery system that would further advance the technology and improve patient outcomes. 4 The Atlas stent is thought to have enhanced stent conformability, a low-profile delivery system (through a 0.165-inch inner diameter microcatheter) and high deployment accuracy. 4 In 2019, the Neuroform Atlas stent was FDA approved for use with coiling in the anterior circulation in patients ≥18 years of age with saccular wide-necked cerebral aneurysms (neck width ≥4 mm or a dome-to-neck ratio <2), with a parent vessel diameter >2 mm and <4.5 mm.
Although the Atlas stent is thought to have features that improve stent delivery, no studies exist comparing outcomes of SAC using the Atlas stent to outcomes of SAC using prior generation stents. This study aimed to assess the safety and efficacy of SAC with the Neuroform Atlas stent and to compare this stent head-to-head with the Neuroform EZ stent (Stryker) in outcomes of SAC. We also aimed to evaluate factors associated with the outcomes of SAC.
Methods
Patient selection
The study protocol was approved by the Institutional Review Board. Consecutive patients with cerebral aneurysms treated with SAC between January 2015 and June 2019 at a single institution were retrospectively identified. Seventy-two patients with 77 aneurysms treated with SAC using the Neuroform Atlas stent were identified and 75 patients with 77 aneurysms treated with SAC using the Neuroform EZ stent were identified. Patient selection was blinded to outcome and in a 1-to-1 aneurysm ratio. We did not selectively match patients but rather included consecutive cases with overall similar characteristics. SAC treatment was offered for recurrent complex, wide-neck aneurysms, partially thrombosed aneurysms, and recurrent aneurysms treated unsuccessfully by conventional endovascular treatment. Baseline patient characteristics, aneurysm characteristics, and procedure characteristics were recorded.
Stent-assisted coiling procedure
Patients were started on clopidogrel and aspirin at least 7 days prior to the intervention. VerifyNow™ assays (Instrumentation Laboratory, Bedford, MA) were performed to validate antiplatelet sensitivity several days prior to the procedure and on the day of the procedure. Additionally, Aspirin and Plavix assays were checked post-treatment during the inpatient stay as well as prior to clinical follow-up, to allow for possible modifications in dosing post-stenting. Patients were then maintained on dual antiplatelet therapy for 6 months following treatment. At 6 months, clopidogrel was stopped and patients were maintained on aspirin.
An angiographic evaluation assessed aneurysm dimensions, and precise measurements were obtained for stent placement. Treatment with SAC was performed with the patient under general anesthesia and neurophysiologic monitoring. Heparinization was carried out to maintain activated clotting time twice baseline. After embolization, an angiogram was immediately obtained, including high-magnification views and 3-dimensional rotational angiography. Patients were admitted to the neurointensive care unit and evaluated in the hospital for any complications. After discharge, patients were scheduled for clinical and angiographic follow-up. Patients continued on dual antiplatelet treatment for at least 6 months after the procedure.
Variables and outcomes
The independent variables evaluated in this study included the following: patient age, gender, aneurysm location, aneurysm size, rupture status, aneurysm shape, type of stent used, number of stents deployed, whether the procedure was staged, stent configuration, radiographic and clinical follow-up, and aspirin and Plavix function assays before the procedure and up to 72 hours following the procedure.
The outcomes of interest in this study were the following: 1) the efficacy of SAC as determined by the technical success of the procedure and angiographic occlusion per the Raymond-Roy (RR) grading system immediately following treatment and at the latest angiographic follow-up; 2) recanalization and retreatment following SAC; 3) the safety of the procedure as assessed by complications, morbidity, and mortality; and 4) a head-to-head comparison between SAC using the Atlas stent and SAC using the EZ stent.
Statistical analysis
Data are presented as mean and range for continuous variables and as frequency for categorical variables. Analysis was performed by using the unpaired t-test, Chi-square, and Fisher’s exact tests as appropriate. Univariate analysis was used to test covariates predictive of the following dependent outcomes: immediate RR grade 1 (RR1) occlusion, immediate RR1 and RR grade 2 (RR2) occlusion, follow-up RR1 occlusion, follow-up RR1 and RR2 occlusion, retreatment and complications. Factors predictive in univariate analysis (p < 0.10) were entered into a backwards multivariate logistic regression analysis. P values ≤0.05 were considered statistically significant. Statistical analysis was performed with STATA (StataCorp, College Station, Texas).
Results
Neuroform atlas stent group
Baseline and procedural characteristics
The mean patient age was 60.8 years (range 28–82) and the mean aneurysm size was 6.4 mm (range 3–13 mm). Two of the aneurysms (2.6%) were fusiform and 75 aneurysms (97.4%) were saccular, 4 of which (5.2%) were multilobed. Aneurysm locations were as follows: carotid ophthalmic (21), vertebro-basilar (15), supraclinoid ICA (8), anterior communicating artery (8), superior hypophyseal artery (7), posterior communicating artery (6), ICA terminus (5), anterior cerebral artery (4), middle cerebral artery (2) and anterior choroidal artery (1).
The median number of stents used was 1 (mean 1.1) with 5 cases (6.5%) requiring more than one stent placement. The stent-coiling procedure was staged in 6 cases (7.8%). There were 3 (3.9%) Y-stent coiling cases.
Outcomes
The procedure was technically successful in all cases (100%). Average angiographic follow-up was 8.7 months (6–13 months) and clinical follow-up was 6.1 months. On immediate angiographic analysis, RR1 aneurysm occlusion was obtained in 63 aneurysms (81.8%), while 14 aneurysms had a RR2 (18.2%) and no aneurysms had a RR grade 3 (RR3) (0%).
In 43 aneurysms that had angiographic follow-up (55.8%), RR1 was obtained in 36 aneurysms (83.7%), RR2 in 4 aneurysms (9.3%) and RR3 in 3 aneurysms (7%). The aneurysms with RR3 had all recanalized (7% of aneurysms with angiographic follow-up). Two of the recurrent aneurysms have been retreated with recoiling with RR1 occlusion on the latest follow-up (4.6% of aneurysms with angiographic follow-up) (Figure 1).
Figure 1.
A 62-year-old female presented with an unruptured carotid-ophthalmic aneurysm. (a) AP and (b) lateral right internal carotid artery injection demonstrates the 9.7 × 5.9 mm carotid-ophthalmic aneurysm with a 3.6 mm neck. She underwent stent-assisted coiling using the Atlas stent. Six-months follow-up angiogram with (c) AP and (d) lateral right internal carotid artery injection shows complete occlusion of the aneurysm.
There were 5 procedural complications (6.5%), one of which (1.3%) resulted in a new neurological deficit. Three were thromboembolic events and 2 were related to small aneurysm perforations. More specifically, in one case there was occlusion of a superior M2 segment branch that was not cannulated despite intravenous and intra-arterial antiplatelet agents with resultant infarct and new hemiparesis. In another case, there was a distal cervical ICA flow-limiting dissection associated with the MPC guide catheter, requiring further placement of additional stents and subsequent flow reconstitution. One patient had a non–flow limiting dissection without neurological deficits. One patient had a small aneurysm perforation that occurred during coiling and stopped with additional coiling; the patient woke up and remained without new neurological deficits. Another patient was noted to have minimal extravasation of contrast from the aneurysm after placement of the last coil; this was not appreciated on further angiographic runs; no additional coils were placed and the patient woke up and remained without new neurological deficits. There was one additional access-related complication (groin hematoma). The procedure-related mortality rate was 0%.
Neuroform EZ stent group
Baseline and procedural characteristics
The mean patient age was 56.1 years (range 24-88). The mean aneurysm size was 6.9 mm (range 3-24 mm). In this group, 3 ruptured aneurysms (3.9%) were stent-coiled acutely. Nine of the aneurysms (11.7%) were fusiform and 68 aneurysms (88.3%) were saccular, 2 of which (2.6%) were multilobed. Aneurysm locations were as follows: vertebro-basilar (22), carotid ophthalmic (13), supraclinoid ICA (11), anterior communicating artery (9), superior hypophyseal artery (8), posterior communicating artery (4), middle cerebral artery (3), ICA terminus (2), posterior inferior cerebellar artery (2), anterior cerebral artery (1), cavernous ICA (1) and anterior inferior cerebellar artery (1).
The median number of stents used was 1 (mean 1.2) with 12 cases (15.6%) requiring more than one stent placement. The stent-coiling procedure was staged in 8 cases (10.4%). There were 7 Y-stent coiling cases (9.1%). Mean angiographic follow-up was 25.1 months (6-54 months) and clinical follow-up was 23.8 months.
Outcomes
The procedure was technically successful in 74 cases (96%). In these cases, immediate RR1 aneurysm occlusion was achieved in 50 aneurysms (67.6%), while 16 aneurysms (21.6%) had a RR2 and 8 aneurysms (10.8%) had a RR3.
In 71 aneurysms that had angiographic follow-up (95.6%), RR1 occlusion was obtained in 48 aneurysms (67.6%), RR2 in 11 aneurysms (15.5%), and RR3 in 12 aneurysms (16.9%) (Figure 2). Nine aneurysms (12.7%) had recanalized, whereas 5 aneurysms had improved from RR3 to RR1 or RR2 on follow-up angiography. Ten of the recurrent aneurysms (14.1%) have been retreated with RR1 in 4 patients, RR2 in 3 patients, and RR3 in 3 patients at the latest follow-up. The 3 aneurysms that were not successfully stent-coiled were treated with other modalities.
Figure 2.
A 71-year-old female presented with an unruptured carotid-ophthalmic aneurysm. (a) AP and (b) lateral left internal carotid artery injection demonstrates the 15.5 × 10.7 mm carotid-ophthalmic aneurysm with a 4 mm neck. She underwent stent-assisted coiling using the Neuroform EZ stent. 6-months follow-up angiogram with (c) AP and (d) lateral left internal carotid artery injection shows persistent filling of the aneurysm.
There were 8 procedural complications (10.4%) in this group, two of which (2.6%) resulted in a new neurological deficit. Five were thromboembolic complications and 2 were aneurysm perforations. More specifically, one patient had a small thrombus that had formed on the stent involving the A1-A2 junction; this completely resolved after administration of intra-arterial Eptifibatide (patient had a poor neurological exam given presentation with high-grade subarachnoid hemorrhage, but presumably she did not have new neurological deficits from this event). Another patient developed a thrombus at the neck of the aneurysm within the left A2 segment during coiling, which was treated with intra-arterial Eptifibatide and resolved afterwards; patient did not have new neurological deficits. One patient developed a thrombus in the left anterior cerebral artery following stent placement. This was treated with intravenous abciximab with marked improvement in flow and resolution of the thrombus; patient woke up and remained without new neurological deficits. Another patient had an aneurysm perforation during coiling with a small amount of hemorrhage within the dependent portion of both occipital horns, which later increased on subsequent imaging; patient developed vasospasm during his hospital course, with new neurological deficits. One patient had premature coil detachment secondary to patient movement and device failure, with no new neurological deficits. Another patient had a non–flow limiting V2 segment dissection with transient neurological symptoms that resolved within a few days. One patient developed an in-stent thrombus near the completion of the procedure. This resolved after administration of IV abciximab; patient had no new neurological deficits. Another patient developed a vertebral artery dissection and resultant Wallenberg syndrome.
There was one additional access-related complication (femoral artery dissection with pseudoaneurysm formation). The procedure-related mortality rate was 0%.
Group comparison
The two populations were overall homogenous, with the exception of significant baseline differences in patient age (p = 0.02) and a significantly longer follow-up duration for patients treated with the Neuroform EZ stent (p < 0.001) (Table 1).
Table 1.
Baseline patient characteristics.
| Atlas stent(n = 77) | EZ stent(n = 77) | p-Value | |
|---|---|---|---|
| Mean patient age in years (range) | 60.8 (12.7) | 56.1 (12.7) | 0.02 |
| Gender (% male/female) | 16.9/83.1 | 33.8/66.2 | 0.2 |
| Mean aneurysm size in mm (range) | 6.4 (2.4) | 6.9 (3.6) | 0.3 |
| Ruptured aneurysm (%) | 0 | 3.9 | 0.2 |
| Aneurysm shape (% saccular/fusiform) | 97.4/2.6 | 88.3/11.7 | 0.06 |
| Multilobed aneurysm | 5.2 | 2.6 | 0.7 |
| Location (% anterior/posterior circulation) | 80.5/19.5 | 71.4/28.6 | 0.3 |
| Median number of stents deployed | 1 | 1 | 0.2 |
| Staged intervention (%) | 7.8 | 10.4 | 0.6 |
| Y-stenting (%) | 3.9 | 9.1 | 0.3 |
| Mean angiographic follow-up in months (range) | 8.7 (2.7) | 25.1 (11) | 0.0001 |
| Mean clinical follow-up in months (range) | 6.1 (4.1) | 23.8 (12.4) | 0.0001 |
| Mean pre-procedural aspirin assay level (range) | 444 (350–597) | 437 (350–584) | 0.49 |
| Mean pre-procedural plavix assay level (range) | 126 (30–247) | 149 (36–381) | 0.01 |
For the Atlas stent group, mean pre-procedural aspirin assay level was 444 (range 350-597) and mean pre-procedural Plavix assay level was 126 (range 30–247) vs. a mean pre-procedural aspirin assay level of 437 (range 350–584, p = 0.49) and a mean pre-procedural Plavix assay level of 149 for the EZ stent group (range 36–381, p = 0.01).
The rates of immediate RR1 occlusion (p = 0.03) and RR1 and RR2 occlusion (p < 0.001) were significantly higher in the Atlas stent group compared to the EZ stent group (Table 2). The rates of follow-up RR1 occlusion (p = 0.08) and RR1 and RR2 occlusion (p = 0.16) were nonsignificantly higher in the Atlas stent group than the EZ stent group. The recanalization rate was nonsignificantly higher with the EZ stent (p = 0.5). The retreatment rate was significantly higher in patients treated with the EZ stent (p = 0.009). There was no significant difference in the total complication rate between the two groups (p = 0.6). There were 3 thromboembolic complications with the Atlas stent (3.9%) vs. 5 thromboembolic complications with the EZ stent (6.5%, p = 0.7).
Table 2.
Outcomes following stent-assisted coiling.
| Atlas stent | EZ stent | p-Value | |
|---|---|---|---|
| Technical success (%) | 100 | 96 | 0.2 |
| Immediate RR1 occlusion (%) | 81.8 | 67.6 | 0.03 |
| Immediate RR2 occlusion (%) | 18.2 | 21.6 | 0.8 |
| Immediate RR3 occlusion (%) | 0 | 10.8 | 0.006 |
| Immediate RR1 and RR2 occlusion (%) | 100 | 89.2 | 0.0007 |
| Follow-up RR1 occlusion (%) | 83.7 | 67.6 | 0.08 |
| Follow-up RR2 occlusion (%) | 9.3 | 15.5 | 0.4 |
| Follow-up RR3 occlusion (%) | 7 | 16.9 | 0.16 |
| Follow-up RR1 and RR2 occlusion (%) | 93 | 83.1 | 0.16 |
| Recanalization (%) | 7 | 12.7 | 0.5 |
| Retreatment (%) | 4.6 | 14.1 | 0.009 |
| Thrombo-embolic complications (%) | 3.9 | 6.5 | 0.7 |
| Total complications (%) | 6.5 | 10.4 | 0.6 |
| Complication with new neurological deficit (%) | 1.3 | 2.6 | 1 |
RR: Raymond–Roy scale.
Factors associated with outcomes
Immediate RR1 occlusion
In univariate analysis, factors associated with immediate RR1 occlusion included a smaller aneurysm size (odds ratio (OR) 1.3, 95% CI 1.10–1.46, p = 0.001), saccular aneurysm shape (versus fusiform, OR 6.8, 95% CI 1.6–28, p = 0.009) and use of the Atlas stent (OR 2.12, 95% CI 1.004–4.5, p = 0.05). In multivariate analysis, only smaller aneurysm size was associated with immediate RR1 occlusion (OR 1.23, 95% CI 1.06–1.42, p = 0.005). The use of the Atlas stent approached significance in multivariate analysis when accounting for aneurysm size and shape (OR 2.02, 95% CI 0.92–4.44, p = 0.08).
Immediate RR1 and RR2 occlusion
Similarly, in univariate analysis, factors associated with immediate RR1 and RR2 occlusion included a smaller aneurysm size (OR 1.5, 95% CI 1.18–1.9, p = 0.001), saccular aneurysm shape (versus fusiform, OR 13.7, 95% CI 2.6–71, p = 0.002) and use of the Atlas stent (perfectly predicted RR1 and RR2 occlusion, since there were no cases with RR3 occlusion). In multivariate analysis, smaller aneurysm size (OR 1.29, 95% CI 1.03–1.61, p = 0.005) and use of the Atlas stent (predicted outcome perfectly) were associated with immediate RR1 and RR2 occlusion.
Follow-up RR1 occlusion
In univariate analysis, factors associated with follow-up RR1 occlusion included a smaller aneurysm size (OR 1.5, 95% CI 1.22–1.76, p < 0.001) and shorter follow-up duration (OR 1.06, 95% CI 1.02–1.1, p = 0.002). The use of the Atlas stent (OR 2.44, 95% CI 0.94–6.34, p = 0.06) approached significance. In multivariate analysis, only smaller aneurysm size was associated with follow-up RR1 occlusion (OR 1.47, 95% CI 1.17–1.85, p = 0.001).
Follow-up RR1 and RR2 occlusion
Similarly, in univariate analysis, factors associated with follow-up RR1 and RR2 occlusion included a smaller aneurysm size (OR 1.48, 95% CI 1.21–1.81, p < 0.001), saccular aneurysm shape (versus fusiform, OR 5.36, 95% CI 1.01–27, p = 0.04) and shorter follow-up duration (OR 1.06, 95% CI 1.01–1.1, p = 0.01). In multivariate analysis, only smaller aneurysm size was associated with follow-up RR1 and RR2 occlusion (OR 1.4, 95% CI 1.19–1.74, p = 0.003).
Retreatment
In univariate analysis, factors associated with aneurysm retreatment included the use of the Neuroform EZ stent (OR 6.9, 95% CI 1.5–32.1, p = 0.01), a larger aneurysm size (OR 1.4, 95% CI 1.16–1.69, p < 0.001), fusiform aneurysm shape (OR 7.6, 95% CI 1.89–30.4, p = 0.004) and longer follow-up duration (OR 1.05, 95% CI 1.005–1.10, p = 0.03). In multivariate analysis, only larger aneurysm size was associated with aneurysm retreatment (OR 1.36, 95% CI 1.08–1.70, p = 0.007).
Complications
In univariate (OR 3.78, 95% CI 1.4–10.1, p = 0.008) and multivariate (OR 3.49, 95% CI 1.33–9.19, p = 0.01) analyses, the only factor associated with complications was the use of multiple stents.
Discussion
The recently approved Neuroform Atlas stent represents a new tool in the endovascular armamentarium that is beneficial in the treatment of complex and wide-neck aneurysms. Technical success was achieved in 100% of SAC cases with the Atlas stent (versus 96% with the EZ stent), matching recent reports of 93-100% technical success using the Atlas stent.4–12 The Atlas stent was designed with enhanced stent conformability and a low-profile delivery system, and it has been shown to have high deployment accuracy with less foreshortening than braided stents, making this system easier to use than prior devices.4,5 Furthermore, its compatibility with a 0.165-inch inner diameter microcatheter makes this stent very versatile; the ability to treat aneurysms in more difficult and distal locations as well as more tortuous vascular segments is a major improvement over previous stents. 4 The Atlas stent has an open-cell body, which results in a higher radial force and improved stability.6,7 Although this also limits the ability to resheath the stent, 4 the need for stent adjustment after initial deployment is likely lower, with careful planning, than for previous devices. Furthermore, a lead wire is not necessary thus reducing the risk of inadvertent distal vessel injury. 13
Our experience has demonstrated that stent-assisted coiling with the Atlas stent is safe and effective for cerebral aneurysms. This head-to-head comparison also reports superior immediate results and overall better follow-up angiographic occlusion with the Atlas stent compared to the EZ stent. There was a statistically significant difference in immediate aneurysm occlusion between the Atlas and EZ stents (RR1 occlusion of 81.8% versus 67.6%, respectively, p = 0.03). Follow-up angiographic occlusion rates, however, were non-significantly higher using the Atlas stent (RR1 occlusion in 83.7% and RR1 and RR2 in 93% versus, respectively, 67.6% and 83.1% for the EZ stent group). The loss of a significant difference on follow-up could be related to the significant number of Atlas stent patients who lacked angiographic follow-up, which limits the power of the analysis. This could also be attributable to similar recanalization rates for the Atlas and EZ stents—7% and 12.7%, respectively (p = 0.5).
A few studies have reported on outcomes with the Neuroform Atlas stent (Table 3). Jankowitz et al. 4 conducted a prospective, multicenter, single-arm trial involving 30 patients with unruptured wide-necked aneurysms treated with Atlas stent-assisted coiling and reported RR1 angiographic occlusion (without target aneurysm retreatment or significant parent artery stenosis) in 86.7% of patients at 6 months and 92.6% of patients with 12-month angiographic follow-up. 4 Ten Brinck et al. 5 retrospectively evaluated 27 patients treated with SAC with the Atlas stent and reported a successful aneurysm occlusion rate (RR1 and RR2) of 69.2% at 6-month follow-up. Cay et al. 8 evaluated 55 aneurysms treated with Atlas stent-assisted coiling and reported a RR1 or 2 aneurysm occlusion in 94.1% of patients with a mean follow-up duration of 8 months. Tsai et al. 6 retrospectively analyzed 58 patients treated with SAC using the Atlas stent and reported immediate RR1 occlusion in 70.7% of patients. Quintana et al. 7 reported immediate RR1 and RR2 occlusion in 29 of 30 aneurysms, and RR1 occlusion in 18 of 30 aneurysms at 1-year follow-up; all 30 patients were clinically stable.
Table 3.
Review of studies on stent-assisted coiling with the Neuroform Atlas stent.
| Study | Study design | No. of aneurysms | Technical success | Immediate aneurysm occlusion rate | Follow-up aneurysm occlusion rate | Complication rate | Mean follow-up period (months) |
|---|---|---|---|---|---|---|---|
| Caragliano et al. 2 | Retrospective, multi-center | 113 | 100% | RR1 in 88%, RR2 in 9% | RR1 in 82%, RR2 in 13% | 6.2% | 12 |
| Cay et al. 3 | Retrospective, single center | 55 | 100% | – | RR1 and RR2 in 94.1% | One minor stroke, with no permanent deficits | 7.9 |
| Goertz et al. 8 | Retrospective, multi-center | 37 | 100% | RR1 in 83.8%, RR2 in 16.2% | RR1 in 80.8%, RR2 in 11.5% | 2.7% (major stroke) | 6 |
| Gross et al. 9 | Retrospective, single center | 37 | 97% | RR1 in 57%, RR2 in 24% | RR1 in 92%, RR2 in 8% | 3% (one patient with major stroke) | 12.1 |
| Jankowitz et al. 10 | Multi-center single-arm trial | 30 | 100% | 60% | 6 months follow up: 86.7%; 12 months follow up: 92.6% | 3.3% with no permanent deficits | 12 |
| Quintana et al. 13 | Retrospective, single center | 30 | 96.7% | RR1 in 56.6%, RR2 in 40% | RR1 in 60% | 3.3%, with no permanent deficits | 12 |
| ten Brinck et al. 14 | Retrospective, single center | 27 | 100% | RR1 in 63%, RR2 in 11.1% | RR1 and RR2 in 69.2% | Intraoperative thromboembolic complications in 14.8% and ischemic stroke in 15.4%, with no permanent deficits | 7.9 |
| Tsai et al. 15 | Retrospective, single center | 58 | 100% | RR1 in 70.7%, RR2 in 20.7% | – | Transient thrombosis in 5.2% and aneurysm rupture in 1.7% | – |
| Ulfert et al. 16 | Retrospective, multi-center | 37 | 100% | RR1 in 84%, RR2 in 17% | RR1 in 93%, RR2 in 7% | 3%, with no permanent deficits | 6.1 |
| Sweid et al. 18 | Retrospective, multi-center | 69 | 95.7% | RR1 and RR2 in 87% | RR1 and RR2 in 97.7% | No symptomatic major complications (0%). Asymptomatic major complications in 10.1% | 4 |
| Present series | Retrospective, single center | 77 | 100% | RR1 in 81.8%, RR2 in 18.2% | RR1 in 83.7%, RR2 in 9.3% | 6.5%, with new neurological deficits in 1.3% | 8.7 |
In comparison to studies reporting on SAC using the Neuroform and Enterprise stents, our results are in accord with prior studies, with both immediate and follow-up RR1 occlusion in 67.6% with the Neuroform EZ stent. Fargen et al. 14 evaluated 229 aneurysms and reported a near-complete aneurysm occlusion rate of 81%, and complete occlusion in 59%. In a meta-analysis that included 2,698 aneurysms treated with SAC, the pooled immediate occlusion rate was 57.7% and the follow-up occlusion rate was 87.6%. 15 The reported recanalization and retreatment rates following SAC are approximately 12% and 6%, respectively. 16 In our study, the retreatment rate was significantly higher in the EZ stent group (12.7% recanalization and 14.1% retreatment rates versus 7% recanalization and 4.6% retreatment rates with the Atlas stent). This difference could be attributable to more stability and durability of treatment with the Atlas stent but again may be confounded by the longer follow-up period for the EZ stent group. Studies with long-term follow-up are needed to further establish the recanalization/retreatment rates after SAC with the Atlas stent.
The complication rate was non-significantly lower with the Atlas stent. SAC is reported to be associated with a thromboembolic complication rate ranging from 4.2% to 17%, an ischemic stroke rate ranging from 3.4% to 8.8% and a hemorrhagic complication rate ranging from 1.2% to 8%.5,17 In the Jankowitz et al. trial, 4 the primary safety endpoint of stroke occurred in one patient (3.3%), who made a complete clinical recovery at discharge. Cay et al. 8 encountered one (1.8%) minor stroke in a patient who had discontinued antiplatelet therapy after SAC but no permanent neurological deficits and similarly Sweid et al reported no major symptomatic procedural complications. 18 Tsai et al. 6 reported procedural complications in 5.2% of patients and aneurysm rupture in one patient (1.7%) and no permanent neurological deficits. 6 Overall, the complication rate with SAC is low and experience with the Atlas stent has shown similar or improved safety endpoints with no prominent safety concerns. The Atlas stent is thought to have a low thrombogenic profile and fewer technical issues associated with implantation, possibly improving the overall safety of SAC. 7 We routinely perform aspirin and Plavix function assays before and after the procedure and attempt to optimize these assays. 19 In the present report, however, neither pre- nor post-procedural aspirin or Plavix function assays were associated with the occurrence of complications.
Other factors were noted to be associated with outcomes in our study. As noted in previous reports, larger aneurysm size and fusiform shape were associated with a lower chance of aneurysm occlusion. 16 Most patients in our series had a single stent deployed in the parent vessel. A small number of patients were treated with Y-stenting for wide neck bifurcation aneurysms (primarily basilar apex). Although the placement of multiple stents was noted to be associated with higher odds of complications, these were not related to Y-stenting. In fact, no complications were encountered in these cases and we noted good stent stability without significant foreshortening during delivery of the second stent during Y-stenting procedures. The association of multiple stents with complications in the present study is likely related to additional stents being placed to manage procedural complications (i.e., dissections).
Limitations
This study is limited by its retrospective design, the chart review process, the inherent selection bias for SAC versus another intervention and the nonrandomized treatment with the EZ stent versus the Atlas stent. This study is a single-institutional series, which could affect the generalizability of the results. It is a head-to-head evaluation of stents in consecutive patients. The study groups were not matched, but baseline characteristics were overall similar with a significant difference in age and more importantly follow-up duration, with lack of angiographic follow-up in the Atlas stent group. The Atlas stent is a newer technology and long-term results are scarce. The advent of this technology has changed our clinical practice with preference for its use for the appropriate indications. As the Atlas stent gains more use and popularity, prior stent generations such as the Neuroform EZ stent are being used less commonly. An understanding of how the Atlas stent compares to prior generations has not been previously assessed and that’s how this manuscript adds to the existing body of literature. Studies reporting on long-term outcomes, however, are still needed. One study that compared 37 patients treated with SAC using the Atlas stent to 27 patients treated with the LVIS Jr stent reported a higher initial RR1 and follow-up RR1 and RR2 occlusion with the Atlas stent (57% vs. 41%, p = 0.03, and 100% vs. 81%, p = 0.04, respectively). 10 Given that there are no trials evaluating different stent designs, and the difficulties with conducting such studies, further comparative case series are needed.
Conclusion
The use of the Neuroform Atlas stent in SAC is safe and effective, as demonstrated in this large single-institution series. Initial occlusion rates were higher with the Atlas stent as compared to the Neuroform EZ stent, and follow-up outcomes were overall non-significantly superior to the EZ stent.
Footnotes
Declaration of conflicting interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iDs: Badih J Daou https://orcid.org/0000-0001-6712-2641
Aditya S Pandey https://orcid.org/0000-0003-0789-4273
Ethical approval statement/IRB approval
Study approved by the University of Michigan IRB – HUM00067645.
References
- 1.Zhao B, Yin R, Lanzino G, et al. Endovascular coiling of wide-neck and wide-neck bifurcation aneurysms: a systematic review and meta-analysis. Am J Neuroradiol 2016; 37: 1700–1705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Pierot L, Spelle L, Leclerc X, et al. Endovascular treatment of unruptured intracranial aneurysms: comparison of safety of remodeling technique and standard treatment with coils. Radiology 2009; 251: 846–855. [DOI] [PubMed] [Google Scholar]
- 3.Benitez RP, Silva MT, Klem J, et al. Endovascular occlusion of wide-necked aneurysms with a new intracranial microstent (Neuroform) and detachable coils. Neurosurgery 2004; 54: 1359–1367. [DOI] [PubMed] [Google Scholar]
- 4.Jankowitz BT, Hanel R, Jadhav AP, et al. Neuroform Atlas Stent System for the treatment of intracranial aneurysm: primary results of the Atlas Humanitarian Device Exemption cohort. J Neurointerv Surg 2019; 11: 801–806. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.ten Brinck MFM, de Vries J, Bartels RHMA, et al. NeuroForm Atlas stent-assisted coiling: preliminary results. Neurosurgery 2019; 84: 179–189. [DOI] [PubMed] [Google Scholar]
- 6.Tsai JP, Hardman J, Moore NZ, et al. Early post-Humanitarian Device Exemption experience with the Neuroform Atlas stent. J Neurointerv Surg 2019. DOI: 10.1136/neurintsurg-2019-014874. [DOI] [PubMed] [Google Scholar]
- 7.Quintana EM, Valdes PV, Deza EM, et al. Initial experience and one-year follow-up with Neuroform Atlas Stent System for the treatment of brain aneurysms. Interv Neuroradiol 2019; 25: 521–529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Cay F, Peker A, Arat A. Stent-assisted coiling of cerebral aneurysms with the Neuroform Atlas stent. Interv Neuroradiol 2018; 24: 263–269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Ulfert C, Pham M, Sonnberger M, et al. The Neuroform Atlas stent to assist coil embolization of intracranial aneurysms: a multicentre experience. J Neurointerv Surg 2018; 10: 1192–1196. [DOI] [PubMed] [Google Scholar]
- 10.Gross BA, Ares WJ, Ducruet AF, et al. A clinical comparison of Atlas and LVIS Jr stent-assisted aneurysm coiling. J Neurointerv Surg 2019; 11: 171–174. [DOI] [PubMed] [Google Scholar]
- 11.Goertz L, Dorn F, Siebert E, et al. Safety and efficacy of the Neuroform Atlas for stent-assisted coiling of intracranial aneurysms: a multicenter experience. J Clin Neurosci 2019; 68: 86–91. [DOI] [PubMed] [Google Scholar]
- 12.Caragliano AA, Papa R, Pitrone A, et al. The low-profile Neuroform Atlas stent in the treatment of wide-necked intracranial aneurysms - immediate and midterm results: an Italian multicenter registry. J Neuroradiol 2019. DOI: 10.1016/j.neurad.2019.03.005. [DOI] [PubMed] [Google Scholar]
- 13.Koduri S, Daou BJ, Pandey AS. Arly multicenter experience with the Neuroform Atlas stent: feasibility, safety, and efficacy. Neurosurgery 2020; 87: E336–E337. [DOI] [PubMed] [Google Scholar]
- 14.Fargen KM, Hoh BL, Welch BG, et al. Long-term results of enterprise stent-assisted coiling of cerebral aneurysms. Neurosurgery 2012; 71: 239–244. [DOI] [PubMed] [Google Scholar]
- 15.Phan K, Huo YR, Jia F, et al. Meta-analysis of stent-assisted coiling versus coiling-only for the treatment of intracranial aneurysms. J Clin Neurosci 2016; 31: 15–22. [DOI] [PubMed] [Google Scholar]
- 16.Chalouhi N, Jabbour P, Singhal S, et al. Stent-assisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke 2013; 44: 1348–1353. [DOI] [PubMed] [Google Scholar]
- 17.Feng MT, Wen WL, Feng ZZ, et al. Endovascular embolization of intracranial aneurysms: to use stent(s) or not? Systematic review and meta-analysis. World Neurosurg 2016; 93: 271–278. [DOI] [PubMed] [Google Scholar]
- 18.Sweid A, Herial N, Sajja K, et al. Early multicenter experience with the Neuroform Atlas stent: feasibility, safety, and efficacy. Neurosurgery 2020; 87: E321–E335. [DOI] [PubMed] [Google Scholar]
- 19.Daou B, Starke RM, Chalouhi N, et al. P2Y12 reaction units: effect on hemorrhagic and thromboembolic complications in patients with cerebral aneurysms treated with the pipeline embolization device. Neurosurgery 2016; 78: 27–33. [DOI] [PubMed] [Google Scholar]