Special Issue Article
Stent-assisted coiling of cerebral aneurysms using the Enterprise and the Solitaire devices Yong-An Chen1,2, Mohammed Hussain3, Jing-Yuan Zhang2, Kun-Peng Zhang2, Qi Pang1 1
Department of Neurosurgery, Shandong Provincial Hospital, Shandong University, Jinan, China, 2Department of Neurosurgery, Yantai Yuhuangding Hospital, Qingdao University, School of Medicine, China, 3Department of Neurosurgery, Wayne State University, USA Objective: To evaluate the technical feasibility, peri- and post-procedural morbidity and mortality as well as clinical and angiographic follow-up using the Enterprise and the Solitaire stent currently available to be used for stent-assisted coiling of broad-based cerebral aneurysms. Material and methods: We conducted a retrospective study to investigate differences in aneurysms stented with the Enterprise (n 5 58) and Solitaire stents (n 5 19). Angiographic follow-up (mean: 8.25 onths) was available in 82.6% of patients treated with stent-assisted coiling. Results: All stents were successfully deployed. There is a higher acute in-stent thrombosis complication in Solitaire stent placement (P 5 0.012). However, we observed no significant differences in peri-procedural morbidity and mortality rate (P 5 0.253), angiographic results (P 5 0.411), recurrence rate (P 5 1.000), or long-term neurological deficit (P 5 0.435). Conclusion: Both stents exhibited similar immediate and mid-term results with major neurological morbidities and mortality rate being low. More thrombogenic complications overall were found in Solitaire group.
Keywords: Stent-assisted coiling, Cerebral aneurysm, Enterprise stent, Solitaire stent
Introduction The incidence, diagnosis, and various different treatment modalities for intracranial aneurysms have been documented extensively in the literature. The prevalence of intracranial saccular aneurysms have been reported to be 3.2% in the general population who have no comorbidity based on radiographic and autopsy series.1,2 The most feared complication of an aneurysmal rupture is the resultant subarachnoid hemorrhage (SAH), which occurs according to one report at an estimated rate of 6 to 16 per 100 000 and roughly 30 000 people per annum in North America.3 With complications accounting for 0.4–0.6% of all deaths, it becomes imperative to have efficient diagnostic and treatment modalities for this pathology.4 Treatment modalities have included neurosurgical clipping and endovascular techniques. The International Study of Unruptured Intracranial Aneurysms rates of poor neurological outcome at 1 year were 12.6 and 9.8% for those treated surgical and endovascular means, respectively.5 Another cohort study done by Alshekhlee et al. with patients Correspondence to: Q. Pang, Department of Neurosurgery, Shandong Provincial Hospital, Shandong University, 324#, Jingwu Weiqi Road, Jinan 250021, China. Email: [email protected]
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132814Y.0000000356
electively admitted to US hospitals over 6 years with the diagnosis of unruptured intracranial aneurysm showed that elective coiling of unruptured intracranial aneurysms was associated with fewer deaths and perioperative complications compared with elective clipping (0.6% versus 1.6% mortality and 4.3% versus 9.0% rates of stroke, respectively).6 Nevertheless, complications of endovascular coiling have also been documented that include thromboembolism that occurred in 12.5% of endovascular mediated aneurysmal treatment in one series.7 The Cerebral Aneurysmal Re-rupture after Treatment study documented intra-procedural aneurysmal rupture in 5% of 299 patients leading to an increased rate of morbidity and mortality with aneurysmal SAH treated with coil embolization.7 Owing to the rapidly evolving nature of neuro-interventional surgery newer techniques and devices have been introduced over the course of past few years. Novel procedures under investigation for the endovascular treatment of cerebral aneurysms have included stent-assisted coiling, balloon-assisted coiling, flow diverters/disruptors, and new embolic material.8 Despite a general increase in the interest of coil embolization in middle cerebral artery aneurysms, actual experience with stent-assisted coil
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embolization is limited to only a handful of small case series.9–11 Various advantages have been documented with stent-assisted coil embolization such as the facilitated treatment of wide necked and small aneurysms where the stent creates a barrier to prevent coil herniation into the parent artery. Preventing coil herniation in turn would decrease risk of parent artery occlusion and would also facilitate an overall increased coil packing density. An overall increased density of coiling would facilitate an increased rate of thrombosis and the presence of stents in the parent artery would provide a framework for endothelialization.9,12–14 In this study, we compare our experience with the Enterprise with the Solitaire stent devices, which were recently approved to be used in China for stent-assisted coiling of broad-based aneurysms. The Enterprise stent is a closed cell nitinol self-expanding and retractable stent that is designed to have flared ends to increase stent adherence against vessel wall.15 With enhanced navigability, flexibility, and presence of four radiopaque markers on each end, the stent serves to partially deploy during coiling of the aneurysm to allow for subsequent retraction and repositioning in addition to enhance apposition to the parent vessel wall.16 The Solitaire stent, on the other hand, is laser cut and comprised of nitinol in a honeycomb pattern with proximal coil and three distal markers.16 It has been used in stent remodeling approaches where the application is similar to a balloon yet without causing blood flow cessation.17,18 With an overall stronger radial strength, the strut gap length is also superior when compared to the Enterprise stent with studies reporting an overall greater ease of stent-assisted coiling.17,18 Studies have also reported an overall decreased thrombogenicity with Solitaire-assisted stent-mediated coiling of aneurysms.17 There are few results reported for each stent regarding outcomes, including stenting success rate, initial grade of occlusion, and complication rates.19,20 Mid-term results associated with either stent are restricted to a relatively small number of studies with angiographic follow-up durations of up to 6.9 months for the Enterprise stent and 6 months for the Solitaire stent, and long-term follow-up experience is scarce. The goal of this single-center study was to evaluate several parameters in the comparison of the Enterprise and Solitaire stents in stent-assisted coiling and related mid-term follow-up findings.
Materials and Methods Patients and aneurysm treatment We retrospectively analyzed imaging and medical charts of 71 consecutive patients who presented with 84 aneurysms that were treated with stent-assisted coil embolization between February to September
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2010 at our center. It should be noted that of the 71 patients, seven harboring seven aneurysms were treated with Neuroform and Silk flow diverter stent-assisted coil embolization and were therefore excluded from the analysis. As a result, 64 patients with 77 aneurysms were treated by Enterprise and Solitaire stent-assisted coiling (n 5 58 using the Enterprise and n 5 19 using the Solitaire stent). All of the 77 aneurysms underwent coiling after successful stent-placement. Stent-assisted coiling was performed in aneurysms with a dome-to-neck ratio ,2 or a neck diameter .4 mm and in broad-based aneurysms that were not approachable by conventional coil embolization. Aneurysms were coiled using the jailing technique. Coiling in all patients was performed under general anesthesia under sterile environment, using a common femoral artery approach. The procedure was performed under therapeutic heparinization with a goal of achieving an activated clotting time of approximately 300 seconds. Postprocedure, the patients were kept on heparin for 24 hours. Patients were preloaded with the dual antiplatelet agents: 75 mg clopidogrel daily and 100 mg aspirin daily for 3–5 days before treatment. If acute stenting was indicated, patients were preloaded with 300 mg clopidogrel 2 hours before treatment. Post-procedure, the patients were kept on a dual antiplatelet regimen for 1 month and then 100 mg aspirin for 6 months. In-stent thrombosis was confirmed by acute digital subtraction angiography.
Data collection and statistical analysis In addition to the clinical presentation and patient demographics, data were collected examining aneurysm size, location, morphology (fusiform versus saccular), angiographic result, rupture status, and peri-procedural morbidity and mortality. Pearson’s Chi-square and Fisher’s exact tests were determined to achieve demographic and contingency differentiation. Student’s t-test was used to determine statistical significance in continuous scaled parameters, including age and aneurysm size. A P , 0.05 was considered statistically significant.
Clinical and angiographic outcome measures Clinical data were obtained during admission from examinations conducted by stroke neurologists or neurosurgeons before and after the procedure. Patients were re-evaluated generally within 2 weeks after the intervention. During follow-up, clinical evaluations were acquired in conjunction with followup angiography. Technical success was defined in our study as correct placement of the stent and successful positioning of the coils into the body of the aneurysm without compromising the parent vessel. Aneurysmal occlusion during the immediate post-procedure angiography was objectified using a modification of
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Table 1 Baseline demographics of aneurysms treated using the Enterprise or Solitaire stent
Age (years¡SD) Sex (f/m) Mean max dimension (mm¡SD) Localization (ant/post) Morphology (saccular/fusiform) Unruptured/ruptured Angiographic results (complete/incomplete) Acute in-stent thrombosis complications (yes/no) Peri-procedural morbidity and mortality (yes/no) Clinical outcome (with/without new neurological deficits) Recurrence (present/absent)
Likelihood t-test (P ratio (P value) value)
Enterprise
Solitaire
53.34¡12.69 36/22 8.3¡8.0 48/10 54/4 46/12 40/18 1/57 1/57 1/57 5/53
48.74¡11.02 11/8 8.4¡7.7 16/3 17/2 13/6 11/8 4/15 2/17 1/18 1/17
OR
95% CI
0.161 0.791
0.840 0.293–2.411
0.977 1.000 0.633 0.359 0.411 0.012 0.253 0.435 1.000
0.900 1.588 0.585 1.616 15.200 3.294 3.167 1.247
0.220–3.682 0.267–9.444 0.178–1.798 0.556–4.698 1.580–146.234 0.431–25.175 0.188–53.233 0.221–7.023
Note: Numbers refer to aneurysms that were eventually treated by stents (n 5 58 with Enterprise and n 5 19 with Solitaire). F, female; M, male; mm, millimeters; ant, anterior circulation; post, posterior circulation; SD, standard deviation; OR, odds ratio; CI, confidence interval.
the Raymond classification scale, which was primarily developed for berry-shaped aneurysms.15 During the follow-up angiogram, in-stent stenosis, recanalization, and need for retreatment were evaluated.
clinical imaging studies followed by aneurysms that were previously discovered and had become clinically apparent, most frequently due to cranial nerve compression symptoms or headaches.
Results Characteristics of treated aneurysms
Success of stents
Eighty-one aneurysms in 64 patients qualified to undergo treatment by stent-assisted coiling (58 Enterprise and 19 Solitaire). Of the aneurysms intended to be treated, 75 (97.4%) aneurysms were treated with stents and coils, whereas 2 (2.6%) were treated with stents alone (Table 1). Sixty-four (83.1%) of the aneurysms were located in the anterior and 13 (16.9%) in the posterior circulation (Table 2). The mean aneurysm size was 8.31¡7.99 mm in the Enterprise and 8.38¡7.67 mm in the Solitaire stenttreated group. Of the aneurysms stented by Enterprise, 4 had fusiform morphology and 54 were saccular. Among the aneurysms stented by Solitaire 2 were fusiform and 17 were saccular morphology. In a total of 18 ruptured aneurysms (23.4%), 12 in the Enterprise group and 6 in the Solitaire group were treated. In terms of detection, 33 aneurysms were discovered incidentally (42.9%) during routine
Navigation and subsequent deployment of the Solitaire stent was comparable with the Enterprise stent. There were no cases of stent navigation and deployment failure among both groups. In nine patients, a single stent sufficiently covered the neck of two aneurysms. All the 58 aneurysms that were intended to be treated with Enterprise stent underwent successful navigation and deployment. Subsequent coiling was performed during the same session in 57 (98.3%) aneurysms. In addition, all 19 aneurysms intended to be treated with the Solitaire stent underwent successful navigation and deployment. In 18 (94.7%) aneurysms, subsequent coiling was performed in the same session.
Procedure related complications, morbidity and mortality We observed five cases (7.8%) of acute in-stent thrombosis in our patients (one in Enterprise group and four in Solitaire group) and therefore a
Table 2 Location and mean maximum diameter of aneurysms stented using either the Enterprise or Solitaire stent
ICA cavernouse segment ICA ophthalmic segment ICA supraclinoid segment MCA Acoma Pcoma Basilar apex Basilar trunk Vertebral artery Total (n)
Total (n)
Enterprise (n)
Mean dimension (mm)
Solitaire (n)
Mean dimension (mm)
13 28 3 3 2 15 3 6 4 77
9 25 3 1 0 10 2 6 2 58
11.7 5.7 10.7 25.0 0 6.6 2.7 14.7 10 8.3
4 3 0 2 2 5 1 0 2 19
19.0 6.8 0 4.3 3.3 5.7 12.0 0 3.5 8.4
Note: n, number of aneurysms; mm, millimeters; ICA, internal carotid artery; MCA, middle cerebral artery; Acoma, anterior communicating artery; Pcoma, posterior communicating artery.
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Note: F, female; M, male; mm, millimeters; ICA, internal carotid artery; ICH, intracerebral hemorrhage; Pcoma, posterior communicating artery; Acoma, anterior communicating artery; M2, the second segment of middle cerebral artery.
Medical Thromboembolism Solitaire Saccular
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6
Solitaire Ruptured 46, F
Pcoma
7
Saccular
Thromboembolism
Medical
Without neurological deficit Transient paralysis and without neurological deficit at follow-up Without neurological deficit at follow-up Solitaire Saccular Unruptured
20
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Cavernous ICA
Solitaire Unruptured 65, M
5
Saccular
Anti-platelet treatment-related ICH Thromboembolism
Medical
Medical Thromboembolism Enterprise Saccular Unruptured 59, F
4 and 6
Prentation
Ophthalmic ICA and Pcoma Acoma
Stent
Complication
Treatment Morphology Aneurysm size (mm) Aneurysm localization Patient age, gender
Table 3 Peri-procedural mortality and major complications in patients treated by stent-assisted coiling 464
Hemiparesis and aphasia Died
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Long-term neurological deficit
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significantly higher incidence of acute in-stent thrombosis caused by Solitaire stent placement (P 5 0.012). However, no difference were observed in periprocedural morbidity and mortality between both stent groups (P 5 0.253). Procedure related morbidity manifesting as long-term neurological sequela of right paralysis and partial expressive aphasia was observed in 1 (1.7%) of 58 cases that underwent Enterprise placement. In comparison, only one procedure related complication manifesting as transient paralysis was seen in the Solitaire stent group which resolved to baseline at follow-up visit. It should be noted that most of the minor and major peri-procedural complications observed in this study were related to thrombolysis and thromboembolism (Table 3). There was one death among the Solitairestented patients. This death occurred in a 65-year-old patient who was treated for an unruptured anterior communicating artery aneurysm and tolerated the stent placement without problems. However, during coil embolization, both anterior cerebral arteries disappeared on angiogram and it was decided immediately to halt the coil embolization process and administer urokinase to achieve thrombolysis. Eventually, both anterior cerebral arteries showed filling with contrast material; however, the patient died. The cause of death was secondary to intracerebral hemorrhage, while the patient was still on heparin infusion 6 hours post-urokinase treatment. We observed no death in the patient group treated with Enterprise.
Initial angiographic results On immediate post-treatment angiograms, the occlusion grade was as follows for the Enterprise group: Raymond class 1 in 40 (69.0%), Raymond class 2 in 9 (15.5%), and Raymond class 3 in 9 (15.5%) aneurysms; in the Solitaire group, we observed Raymond class 1 in 11 (57.9%), Raymond class 2 in 4 (21.05%), and Raymond class 3 in 4 aneurysms (21.05%).
Follow-up findings Of the 63 patients who survived intervention (98.4%), a follow-up angiogram was available in 57 patients (90.5%) at an average of 8.25 months (range: 3– 18 months). These 57 patients were found to have a total of 65 aneurysms. A total of six patients, each with two treated aneurysms, and one with three treated aneurysms remained stable during the entire observation period. None of the patients presenting initially with SAH experienced aneurysm rupture during the observation period. Five aneurysms in five patients (8.8%) showed recanalization (seen as worsening of the thrombosis within the aneurysm), all of which were treated initially with stent-assisted coiling. No significant in-construct stenosis (§50%) was identified at follow-up angiography.
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Discussion Over the course of a few years, endovascular neurosurgery has shown considerable evolution in terms of new devices and techniques to deal with intracranial pathology. Among the aneurysm subtype a wide aneurysm neck (i.e. 4 mm or more) turned out to be a major limitation for endovascular coil treatment.11 One solution to circumvent this limitation was the creation of an artificial border between the parent artery and the aneurysm orifice by deployment of a balloon-expandable coronary stent, with the technique now modified to use self-expanding stents. Self-expanding stents are therefore frequently used in the coiling of wide-necked and fusiform intracranial aneurysms. Data emanating from various sources have reinforced the efficacy of stents such as the Soiltaire and Enterprise in stentassisted endovascular aneurysmal coiling. For instance, Weber et al. reported a larger series of 30 patients with 31 aneurysms, with 100% successful deployment, and two ‘possible or probable devicerelated serious adverse events during the 6-month follow-up period’.21 There was no procedural-related morbidity or mortality seen.21 Moreover, across 11 series detailing 443 patients with 457 aneurysms, deployment failures were seen in only 1% of cases. Similarly, data spanning across five series on the Solitaire stent showed 102 aneurysms in 96 patients with initial complete occlusion seen in 55% of cases with occlusion at follow-up, increasing to 90%.17,18,22–24 With more than five different types of intracranial stents approved for stent-assisted coiling and an overall lack of long-term data on outcomes, it becomes important to establish comparison studies evaluating and comparing the different stents. Prior studies have outlined the characteristics of the Neuroform stent, including the stenting success rate, complication rates in ruptured and unruptured aneurysms, and in-stent stenosis rates.25,26 The Neuroform stent happens to be the first stent that was approved by the Food and Drug Administration in 2002 for the treatment of intra-cranial aneurysms. As such, there have been more data on its long-term outcomes, while comparatively there is relatively little published data regarding Enterprise and Solitaire stents.20,27 One study had shown that the success rate of stent deployment and aneurysmal obliteration was clearly higher in the Enterprise stent than Neuroform with both stents being associated with an overall low peri-procedural complication rate and mortality (4.2% versus 1.9%). There is relatively limited evidence about comparative benefit of using the Enterprise and Solitaire stents for stent-assisted coiling. The Solitaire stent was the first stent among its class that was fully retractable.20 Recently, data published from five series that followed 102 aneurysms in 96 patients
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showed deployment failure in only two cases (2%) with aneurysmal recanalization seen in 10% of cases overall. In addition, there were no reported cases of delayed instent stenosis with thromboembolic events reported in 3% of cases overall. Furthermore, hemorrhagic complications were seen only in 1% with permanent neurological morbidity and mortality also seen in 1%. On comparison, among the 443 patients with 457 aneurysms analyzed in 11 series, Enterprise stent deployment failures were seen in only 1% of cases overall with initial complete obliteration and follow-up obliteration rates being 68% and 54%, respectively.21,28–37 Delayed stent stenosis using the Enterprise stent was found to be relatively low (3%) and these were asymptomatic clinically. Aneurysmal recanalization was seen in 11% of cases overall with symptomatic thromboembolic and hemorrhagic complications being as low as 2% of all cases. Permanent neurological morbidity and mortality was seen in 2% and 1% of cases overall, respectively. In the current study, both stented groups were clinically and radiographically homogenous, which allowed for a good comparison of the stents. Both stents possessed good to excellent procedural feasibility in close agreement with previously reported success rates of 95.9–100% for the Solitaire and 90–100% for the Enterprise. In addition, both stents were associated with a comparably low peri-procedural complication rate and mortality. The complication rates observed in our study remain consistent with those that have been reported in the literature using exclusive stent-assisted aneurysmal coiling in ruptured as well as unruptured aneurysms (ranging from 0 to 16%).19,26,38 Mortality rates seen in our study were also comparable to those seen in studies that encompassed mainly unruptured aneurysms (0–4.6%) as well as studies with ruptured aneurysms (0–20%). In a multi-centered prospective study, Byrne et al. reported that long-term neurological complication occurred in 1.30% of patients treated with stent-assisted coiling and were mostly linked to thromboembolism.39 The one case of mortality seen in our study resulted from hemorrhage due to aneurysmal rupture during heparin therapy after thrombolysis. It should be noted that though bleeding episodes overall occurred at a relatively lower frequency in our experience with stent-assisted coiling, dual anti-platelet therapy facilitated bleeds after stent-assisted treatment remains a concern. For instance, combination therapy of aspirin/prasugrel has shown to predispose patients to a higher risk of hemorrhage during neurointerventional surgery compared with aspirin/ clopidogrel (19.4 versus 3.6%, P 5 0.02).19 In this study, initial angiographic results showed that overall 83.1% of aneurysms treated with stent-assistance had total flow cessation or had only minimal flow into the neck, which is consistent with previous reports.2,16
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However, 8.8% of followed aneurysms showed major recanalization. This is in contrast to reported data such as the one by Izar et al. who showed progressive occlusion of 36% of followed aneurysms.40 Hwang et al. in their 2-year follow-up study showed the rates of progressive aneurysmal occlusion in the stent group (17/40, 42.5%) versus non-stent group (34/86, 39.5%). In the same analysis, there was no statistically significant difference seen in aneurysmal recanalization between the stent and non-stent group (P 5 0.895) (7/40, 17.5% versus 18/86, 21.0%, respectively). Both available stents appear to have low rates of in-stent stenosis (one in Enterprise and four in Solitaire) indicating a good mid-term safety using either stent. When compared to a series of 213 patients with 110 patients available for follow-up, it was seen that significant (§50%) in-stent stenosis or occlusion was seen in 3% of patients. The causes of thromboembolic events may be attributed to antiplatelet resistance/noncompliance in patients post-stenting or secondary to a relatively poorer apposition of stiffer stents to the parent vessel wall around curves.16 Non-compliance of antiplatelet regimen has been documented to cause thromboembolic events and therefore, persistent use is required to avoid acute ischemic events. For instance, Ji et al. concluded from their analysis of antiplatelet medication persistence after ischemic stroke or transient ischemic attack in the Chinese population that at 3-month persistence, there was a significant association of less recurrent stroke and better functional outcomes.37
Conclusion Our study shows that the Enterprise and Solitaire stents are comparable devices with ease of navigation. Both stents exhibited similar immediate and mid-term followup results with low major neurological morbidities and mortality rate. Overall, more thrombogenic complications were found in Solitaire group. Further multi-centered prospective comparison studies between different types of stent-assisted aneurysmal coiling should be conducted with long-term follow-up to reinforce our data.
Disclaimer Statements Contributors YC participated in collection of data and manuscript preparation. YC and QP performed the statistical analysis. PZ and QP participated in study design and critically revised the manuscript. All authors read and approved the final manuscript. Funding None. Conflicts of interest The authors declare that they have no competing interests. Ethics approval The study was approved by the Ethics Review Board of Qingdao University.
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clinical and angiographic results in 31 aneurysms. Neuroradiology. 2007;49:555–61. Lubicz B, Collignon L, Raphaeli G, Bandeira A, Bruneau M, de Witte O. Solitaire stent for endovascular treatment of intracranial aneurysms: immediate and mid-term results in 15 patients with 17 aneurysms. J Neuroradiol. 2010;37:83–8. Liebig T, Henkes H, Reinartz J, Miloslavski E, Ku¨hne D. A novel self-expanding fully retrievable intracranial stent (SOLO): experience in nine procedures of stent-assisted aneurysm coil occlusion. Neuroradiology. 2006;48:471–8. Yavuz K, Geyik S, Pamuk AG, Koc O, Saatci I, Cekirge HS. Immediate and midterm follow-up results of using an electrodetachable, fully retrievable SOLO stent system in the endovascular coil occlusion of wide-necked cerebral aneurysms. J Neurosurg. 2007;107:49–55. Tahtinen OI, Vanninen RL, Manninen HI, Rautio R, Haapanen A, Niskakangas T, et al. Wide-necked intracranial aneurysms: treatment with stent-assisted coil embolization during acute (,72 hours) subarachnoid hemorrhage — experience in 61 consecutive patients. Radiology. 2009;253:199–208. Biondi A, Janardhan V, Katz JM, Salvaggio K, Riina HA, Gobin YP. Neuroform stent-assisted coil embolization of wide-neck intracranial aneurysms: strategies in stent deployment and midterm follow-up. Neurosurgery. 2007;61:460–8; discussion 468–9. Mocco J, Fargen KM, Albuquerque FC, Bendok BR, Boulos AS, Carpenter JS, et al. Delayed thrombosis or stenosis following Enterprise-assisted stent-coiling: is it safe? Midterm results of the interstate collaboration of Enterprise stent coiling. Neurosurgery. 2011;69:908–13; discussion 913–4. Higashida RT, Halbach VV, Dowd CF, Juravsky L, Meagher S. Initial clinical experience with a new self-expanding nitinol stent for the treatment of intracranial cerebral aneurysms: the Cordis Enterprise stent. AJNR Am J Neuroradiol. 2005;26:1751–6. Lubicz B, Francois O, Levivier M, Brotchi J, Baleriaux D. Preliminary experience with the enterprise stent for endovascular treatment of complex intracranial aneurysms: potential advantages and limiting characteristics. Neurosurgery. 2008;62:1063–9; discussion 1069–70. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. A new selfexpandable nitinol stent for the treatment of wide-neck aneurysms: initial clinical experience. AJNR Am J Neuroradiol. 2008;29:1405–8.
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31 Siddiqui MA, Bhattacharya J, Lindsay KW, Jenkins S. Horizontal stent-assisted coil embolisation of wide-necked intracranial aneurysms with the Enterprise stent — a case series with early angiographic follow-up. Neuroradiology. 2009;51:411–8. 32 Yang PF, Liu JM, Huang QH, Zhao WY, Hong B, Xu Y, et al. Preliminary experience and short-term follow-up results of treatment of wide-necked or fusiform cerebral aneurysms with a self-expanding, closed-cell, retractable stent. J Clin Neurosci. 2010;17:837–41. 33 Wang H, Xu D, Xiang Y, Li W, Chen Z, Chen S, et al. Endovascular treatment for wide-necked intracranial aneurysms with the Enterprise stent. Neurol India. 2011;59:548–52. 34 Xu X, Shang XM, Cui JZ, Wang DY. Endovascular treatment of intracranial aneurysms using coil embolization plus an Enterprise stent. Chin Med J (Engl). 2011;124:611–4. 35 Jeon P, Kim BM, Kim DI, Park SI, Kim KH, Kim DJ, et al. Reconstructive endovascular treatment of fusiform or ultrawide-neck circumferential aneurysms with multiple overlapping enterprise stents and coiling. AJNR Am J Neuroradiol. 2012;33:965–71. 36 Akbari SH, Reynolds MR, Kadkhodayan Y, Cross DT 3rd, Moran CJ. Hemorrhagic complications after prasugrel (Effient) therapy for vascular neurointerventional procedures. J Neurointerv Surg. 2013;5:337–43. 37 Ji R, Liu G, Shen H, Wang Y, Li H, Peterson E, et al. Persistence of secondary prevention medications after acute ischemic stroke or transient ischemic attack in Chinese population: data from China National Stroke Registry. Neurol Res. 2013;35:29–36. 38 Akpek S, Arat A, Morsi H, Klucznick RP, Strother CM, Mawad ME. Self-expandable stent-assisted coiling of widenecked intracranial aneurysms: a single-center experience. AJNR Am J Neuroradiol. 2005;26:1223–31. 39 Byrne JV, Beltechi R, Yarnold JA, Birks J, Kamran M. Early experience in the treatment of intra-cranial aneurysms by endovascular flow diversion: a multicentre prospective study. PLoS ONE. 2010;5:1–8. 40 Izar B, Rai A, Raghuram K, Rotruck J, Carpenter J. Comparison of devices used for stent-assisted coiling of intracranial aneurysms. PLoS ONE. 2011;6:e24875.
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Stent-assisted coiling of cerebral aneurysms using the Enterprise and the Solitaire devices Yong-An Chen1,2, Mohammed Hussain3, Jing-Yuan Zhang2, Kun-Peng Zhang2, Qi Pang1 1
Department of Neurosurgery, Shandong Provincial Hospital, Shandong University, Jinan, China, 2Department of Neurosurgery, Yantai Yuhuangding Hospital, Qingdao University, School of Medicine, China, 3Department of Neurosurgery, Wayne State University, USA Objective: To evaluate the technical feasibility, peri- and post-procedural morbidity and mortality as well as clinical and angiographic follow-up using the Enterprise and the Solitaire stent currently available to be used for stent-assisted coiling of broad-based cerebral aneurysms. Material and methods: We conducted a retrospective study to investigate differences in aneurysms stented with the Enterprise (n 5 58) and Solitaire stents (n 5 19). Angiographic follow-up (mean: 8.25 onths) was available in 82.6% of patients treated with stent-assisted coiling. Results: All stents were successfully deployed. There is a higher acute in-stent thrombosis complication in Solitaire stent placement (P 5 0.012). However, we observed no significant differences in peri-procedural morbidity and mortality rate (P 5 0.253), angiographic results (P 5 0.411), recurrence rate (P 5 1.000), or long-term neurological deficit (P 5 0.435). Conclusion: Both stents exhibited similar immediate and mid-term results with major neurological morbidities and mortality rate being low. More thrombogenic complications overall were found in Solitaire group.
Keywords: Stent-assisted coiling, Cerebral aneurysm, Enterprise stent, Solitaire stent
Introduction The incidence, diagnosis, and various different treatment modalities for intracranial aneurysms have been documented extensively in the literature. The prevalence of intracranial saccular aneurysms have been reported to be 3.2% in the general population who have no comorbidity based on radiographic and autopsy series.1,2 The most feared complication of an aneurysmal rupture is the resultant subarachnoid hemorrhage (SAH), which occurs according to one report at an estimated rate of 6 to 16 per 100 000 and roughly 30 000 people per annum in North America.3 With complications accounting for 0.4–0.6% of all deaths, it becomes imperative to have efficient diagnostic and treatment modalities for this pathology.4 Treatment modalities have included neurosurgical clipping and endovascular techniques. The International Study of Unruptured Intracranial Aneurysms rates of poor neurological outcome at 1 year were 12.6 and 9.8% for those treated surgical and endovascular means, respectively.5 Another cohort study done by Alshekhlee et al. with patients Correspondence to: Q. Pang, Department of Neurosurgery, Shandong Provincial Hospital, Shandong University, 324#, Jingwu Weiqi Road, Jinan 250021, China. Email: [email protected]
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132814Y.0000000356
electively admitted to US hospitals over 6 years with the diagnosis of unruptured intracranial aneurysm showed that elective coiling of unruptured intracranial aneurysms was associated with fewer deaths and perioperative complications compared with elective clipping (0.6% versus 1.6% mortality and 4.3% versus 9.0% rates of stroke, respectively).6 Nevertheless, complications of endovascular coiling have also been documented that include thromboembolism that occurred in 12.5% of endovascular mediated aneurysmal treatment in one series.7 The Cerebral Aneurysmal Re-rupture after Treatment study documented intra-procedural aneurysmal rupture in 5% of 299 patients leading to an increased rate of morbidity and mortality with aneurysmal SAH treated with coil embolization.7 Owing to the rapidly evolving nature of neuro-interventional surgery newer techniques and devices have been introduced over the course of past few years. Novel procedures under investigation for the endovascular treatment of cerebral aneurysms have included stent-assisted coiling, balloon-assisted coiling, flow diverters/disruptors, and new embolic material.8 Despite a general increase in the interest of coil embolization in middle cerebral artery aneurysms, actual experience with stent-assisted coil
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embolization is limited to only a handful of small case series.9–11 Various advantages have been documented with stent-assisted coil embolization such as the facilitated treatment of wide necked and small aneurysms where the stent creates a barrier to prevent coil herniation into the parent artery. Preventing coil herniation in turn would decrease risk of parent artery occlusion and would also facilitate an overall increased coil packing density. An overall increased density of coiling would facilitate an increased rate of thrombosis and the presence of stents in the parent artery would provide a framework for endothelialization.9,12–14 In this study, we compare our experience with the Enterprise with the Solitaire stent devices, which were recently approved to be used in China for stent-assisted coiling of broad-based aneurysms. The Enterprise stent is a closed cell nitinol self-expanding and retractable stent that is designed to have flared ends to increase stent adherence against vessel wall.15 With enhanced navigability, flexibility, and presence of four radiopaque markers on each end, the stent serves to partially deploy during coiling of the aneurysm to allow for subsequent retraction and repositioning in addition to enhance apposition to the parent vessel wall.16 The Solitaire stent, on the other hand, is laser cut and comprised of nitinol in a honeycomb pattern with proximal coil and three distal markers.16 It has been used in stent remodeling approaches where the application is similar to a balloon yet without causing blood flow cessation.17,18 With an overall stronger radial strength, the strut gap length is also superior when compared to the Enterprise stent with studies reporting an overall greater ease of stent-assisted coiling.17,18 Studies have also reported an overall decreased thrombogenicity with Solitaire-assisted stent-mediated coiling of aneurysms.17 There are few results reported for each stent regarding outcomes, including stenting success rate, initial grade of occlusion, and complication rates.19,20 Mid-term results associated with either stent are restricted to a relatively small number of studies with angiographic follow-up durations of up to 6.9 months for the Enterprise stent and 6 months for the Solitaire stent, and long-term follow-up experience is scarce. The goal of this single-center study was to evaluate several parameters in the comparison of the Enterprise and Solitaire stents in stent-assisted coiling and related mid-term follow-up findings.
Materials and Methods Patients and aneurysm treatment We retrospectively analyzed imaging and medical charts of 71 consecutive patients who presented with 84 aneurysms that were treated with stent-assisted coil embolization between February to September
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2010 at our center. It should be noted that of the 71 patients, seven harboring seven aneurysms were treated with Neuroform and Silk flow diverter stent-assisted coil embolization and were therefore excluded from the analysis. As a result, 64 patients with 77 aneurysms were treated by Enterprise and Solitaire stent-assisted coiling (n 5 58 using the Enterprise and n 5 19 using the Solitaire stent). All of the 77 aneurysms underwent coiling after successful stent-placement. Stent-assisted coiling was performed in aneurysms with a dome-to-neck ratio ,2 or a neck diameter .4 mm and in broad-based aneurysms that were not approachable by conventional coil embolization. Aneurysms were coiled using the jailing technique. Coiling in all patients was performed under general anesthesia under sterile environment, using a common femoral artery approach. The procedure was performed under therapeutic heparinization with a goal of achieving an activated clotting time of approximately 300 seconds. Postprocedure, the patients were kept on heparin for 24 hours. Patients were preloaded with the dual antiplatelet agents: 75 mg clopidogrel daily and 100 mg aspirin daily for 3–5 days before treatment. If acute stenting was indicated, patients were preloaded with 300 mg clopidogrel 2 hours before treatment. Post-procedure, the patients were kept on a dual antiplatelet regimen for 1 month and then 100 mg aspirin for 6 months. In-stent thrombosis was confirmed by acute digital subtraction angiography.
Data collection and statistical analysis In addition to the clinical presentation and patient demographics, data were collected examining aneurysm size, location, morphology (fusiform versus saccular), angiographic result, rupture status, and peri-procedural morbidity and mortality. Pearson’s Chi-square and Fisher’s exact tests were determined to achieve demographic and contingency differentiation. Student’s t-test was used to determine statistical significance in continuous scaled parameters, including age and aneurysm size. A P , 0.05 was considered statistically significant.
Clinical and angiographic outcome measures Clinical data were obtained during admission from examinations conducted by stroke neurologists or neurosurgeons before and after the procedure. Patients were re-evaluated generally within 2 weeks after the intervention. During follow-up, clinical evaluations were acquired in conjunction with followup angiography. Technical success was defined in our study as correct placement of the stent and successful positioning of the coils into the body of the aneurysm without compromising the parent vessel. Aneurysmal occlusion during the immediate post-procedure angiography was objectified using a modification of
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Table 1 Baseline demographics of aneurysms treated using the Enterprise or Solitaire stent
Age (years¡SD) Sex (f/m) Mean max dimension (mm¡SD) Localization (ant/post) Morphology (saccular/fusiform) Unruptured/ruptured Angiographic results (complete/incomplete) Acute in-stent thrombosis complications (yes/no) Peri-procedural morbidity and mortality (yes/no) Clinical outcome (with/without new neurological deficits) Recurrence (present/absent)
Likelihood t-test (P ratio (P value) value)
Enterprise
Solitaire
53.34¡12.69 36/22 8.3¡8.0 48/10 54/4 46/12 40/18 1/57 1/57 1/57 5/53
48.74¡11.02 11/8 8.4¡7.7 16/3 17/2 13/6 11/8 4/15 2/17 1/18 1/17
OR
95% CI
0.161 0.791
0.840 0.293–2.411
0.977 1.000 0.633 0.359 0.411 0.012 0.253 0.435 1.000
0.900 1.588 0.585 1.616 15.200 3.294 3.167 1.247
0.220–3.682 0.267–9.444 0.178–1.798 0.556–4.698 1.580–146.234 0.431–25.175 0.188–53.233 0.221–7.023
Note: Numbers refer to aneurysms that were eventually treated by stents (n 5 58 with Enterprise and n 5 19 with Solitaire). F, female; M, male; mm, millimeters; ant, anterior circulation; post, posterior circulation; SD, standard deviation; OR, odds ratio; CI, confidence interval.
the Raymond classification scale, which was primarily developed for berry-shaped aneurysms.15 During the follow-up angiogram, in-stent stenosis, recanalization, and need for retreatment were evaluated.
clinical imaging studies followed by aneurysms that were previously discovered and had become clinically apparent, most frequently due to cranial nerve compression symptoms or headaches.
Results Characteristics of treated aneurysms
Success of stents
Eighty-one aneurysms in 64 patients qualified to undergo treatment by stent-assisted coiling (58 Enterprise and 19 Solitaire). Of the aneurysms intended to be treated, 75 (97.4%) aneurysms were treated with stents and coils, whereas 2 (2.6%) were treated with stents alone (Table 1). Sixty-four (83.1%) of the aneurysms were located in the anterior and 13 (16.9%) in the posterior circulation (Table 2). The mean aneurysm size was 8.31¡7.99 mm in the Enterprise and 8.38¡7.67 mm in the Solitaire stenttreated group. Of the aneurysms stented by Enterprise, 4 had fusiform morphology and 54 were saccular. Among the aneurysms stented by Solitaire 2 were fusiform and 17 were saccular morphology. In a total of 18 ruptured aneurysms (23.4%), 12 in the Enterprise group and 6 in the Solitaire group were treated. In terms of detection, 33 aneurysms were discovered incidentally (42.9%) during routine
Navigation and subsequent deployment of the Solitaire stent was comparable with the Enterprise stent. There were no cases of stent navigation and deployment failure among both groups. In nine patients, a single stent sufficiently covered the neck of two aneurysms. All the 58 aneurysms that were intended to be treated with Enterprise stent underwent successful navigation and deployment. Subsequent coiling was performed during the same session in 57 (98.3%) aneurysms. In addition, all 19 aneurysms intended to be treated with the Solitaire stent underwent successful navigation and deployment. In 18 (94.7%) aneurysms, subsequent coiling was performed in the same session.
Procedure related complications, morbidity and mortality We observed five cases (7.8%) of acute in-stent thrombosis in our patients (one in Enterprise group and four in Solitaire group) and therefore a
Table 2 Location and mean maximum diameter of aneurysms stented using either the Enterprise or Solitaire stent
ICA cavernouse segment ICA ophthalmic segment ICA supraclinoid segment MCA Acoma Pcoma Basilar apex Basilar trunk Vertebral artery Total (n)
Total (n)
Enterprise (n)
Mean dimension (mm)
Solitaire (n)
Mean dimension (mm)
13 28 3 3 2 15 3 6 4 77
9 25 3 1 0 10 2 6 2 58
11.7 5.7 10.7 25.0 0 6.6 2.7 14.7 10 8.3
4 3 0 2 2 5 1 0 2 19
19.0 6.8 0 4.3 3.3 5.7 12.0 0 3.5 8.4
Note: n, number of aneurysms; mm, millimeters; ICA, internal carotid artery; MCA, middle cerebral artery; Acoma, anterior communicating artery; Pcoma, posterior communicating artery.
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Note: F, female; M, male; mm, millimeters; ICA, internal carotid artery; ICH, intracerebral hemorrhage; Pcoma, posterior communicating artery; Acoma, anterior communicating artery; M2, the second segment of middle cerebral artery.
Medical Thromboembolism Solitaire Saccular
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Solitaire Ruptured 46, F
Pcoma
7
Saccular
Thromboembolism
Medical
Without neurological deficit Transient paralysis and without neurological deficit at follow-up Without neurological deficit at follow-up Solitaire Saccular Unruptured
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Cavernous ICA
Solitaire Unruptured 65, M
5
Saccular
Anti-platelet treatment-related ICH Thromboembolism
Medical
Medical Thromboembolism Enterprise Saccular Unruptured 59, F
4 and 6
Prentation
Ophthalmic ICA and Pcoma Acoma
Stent
Complication
Treatment Morphology Aneurysm size (mm) Aneurysm localization Patient age, gender
Table 3 Peri-procedural mortality and major complications in patients treated by stent-assisted coiling 464
Hemiparesis and aphasia Died
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significantly higher incidence of acute in-stent thrombosis caused by Solitaire stent placement (P 5 0.012). However, no difference were observed in periprocedural morbidity and mortality between both stent groups (P 5 0.253). Procedure related morbidity manifesting as long-term neurological sequela of right paralysis and partial expressive aphasia was observed in 1 (1.7%) of 58 cases that underwent Enterprise placement. In comparison, only one procedure related complication manifesting as transient paralysis was seen in the Solitaire stent group which resolved to baseline at follow-up visit. It should be noted that most of the minor and major peri-procedural complications observed in this study were related to thrombolysis and thromboembolism (Table 3). There was one death among the Solitairestented patients. This death occurred in a 65-year-old patient who was treated for an unruptured anterior communicating artery aneurysm and tolerated the stent placement without problems. However, during coil embolization, both anterior cerebral arteries disappeared on angiogram and it was decided immediately to halt the coil embolization process and administer urokinase to achieve thrombolysis. Eventually, both anterior cerebral arteries showed filling with contrast material; however, the patient died. The cause of death was secondary to intracerebral hemorrhage, while the patient was still on heparin infusion 6 hours post-urokinase treatment. We observed no death in the patient group treated with Enterprise.
Initial angiographic results On immediate post-treatment angiograms, the occlusion grade was as follows for the Enterprise group: Raymond class 1 in 40 (69.0%), Raymond class 2 in 9 (15.5%), and Raymond class 3 in 9 (15.5%) aneurysms; in the Solitaire group, we observed Raymond class 1 in 11 (57.9%), Raymond class 2 in 4 (21.05%), and Raymond class 3 in 4 aneurysms (21.05%).
Follow-up findings Of the 63 patients who survived intervention (98.4%), a follow-up angiogram was available in 57 patients (90.5%) at an average of 8.25 months (range: 3– 18 months). These 57 patients were found to have a total of 65 aneurysms. A total of six patients, each with two treated aneurysms, and one with three treated aneurysms remained stable during the entire observation period. None of the patients presenting initially with SAH experienced aneurysm rupture during the observation period. Five aneurysms in five patients (8.8%) showed recanalization (seen as worsening of the thrombosis within the aneurysm), all of which were treated initially with stent-assisted coiling. No significant in-construct stenosis (§50%) was identified at follow-up angiography.
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Discussion Over the course of a few years, endovascular neurosurgery has shown considerable evolution in terms of new devices and techniques to deal with intracranial pathology. Among the aneurysm subtype a wide aneurysm neck (i.e. 4 mm or more) turned out to be a major limitation for endovascular coil treatment.11 One solution to circumvent this limitation was the creation of an artificial border between the parent artery and the aneurysm orifice by deployment of a balloon-expandable coronary stent, with the technique now modified to use self-expanding stents. Self-expanding stents are therefore frequently used in the coiling of wide-necked and fusiform intracranial aneurysms. Data emanating from various sources have reinforced the efficacy of stents such as the Soiltaire and Enterprise in stentassisted endovascular aneurysmal coiling. For instance, Weber et al. reported a larger series of 30 patients with 31 aneurysms, with 100% successful deployment, and two ‘possible or probable devicerelated serious adverse events during the 6-month follow-up period’.21 There was no procedural-related morbidity or mortality seen.21 Moreover, across 11 series detailing 443 patients with 457 aneurysms, deployment failures were seen in only 1% of cases. Similarly, data spanning across five series on the Solitaire stent showed 102 aneurysms in 96 patients with initial complete occlusion seen in 55% of cases with occlusion at follow-up, increasing to 90%.17,18,22–24 With more than five different types of intracranial stents approved for stent-assisted coiling and an overall lack of long-term data on outcomes, it becomes important to establish comparison studies evaluating and comparing the different stents. Prior studies have outlined the characteristics of the Neuroform stent, including the stenting success rate, complication rates in ruptured and unruptured aneurysms, and in-stent stenosis rates.25,26 The Neuroform stent happens to be the first stent that was approved by the Food and Drug Administration in 2002 for the treatment of intra-cranial aneurysms. As such, there have been more data on its long-term outcomes, while comparatively there is relatively little published data regarding Enterprise and Solitaire stents.20,27 One study had shown that the success rate of stent deployment and aneurysmal obliteration was clearly higher in the Enterprise stent than Neuroform with both stents being associated with an overall low peri-procedural complication rate and mortality (4.2% versus 1.9%). There is relatively limited evidence about comparative benefit of using the Enterprise and Solitaire stents for stent-assisted coiling. The Solitaire stent was the first stent among its class that was fully retractable.20 Recently, data published from five series that followed 102 aneurysms in 96 patients
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showed deployment failure in only two cases (2%) with aneurysmal recanalization seen in 10% of cases overall. In addition, there were no reported cases of delayed instent stenosis with thromboembolic events reported in 3% of cases overall. Furthermore, hemorrhagic complications were seen only in 1% with permanent neurological morbidity and mortality also seen in 1%. On comparison, among the 443 patients with 457 aneurysms analyzed in 11 series, Enterprise stent deployment failures were seen in only 1% of cases overall with initial complete obliteration and follow-up obliteration rates being 68% and 54%, respectively.21,28–37 Delayed stent stenosis using the Enterprise stent was found to be relatively low (3%) and these were asymptomatic clinically. Aneurysmal recanalization was seen in 11% of cases overall with symptomatic thromboembolic and hemorrhagic complications being as low as 2% of all cases. Permanent neurological morbidity and mortality was seen in 2% and 1% of cases overall, respectively. In the current study, both stented groups were clinically and radiographically homogenous, which allowed for a good comparison of the stents. Both stents possessed good to excellent procedural feasibility in close agreement with previously reported success rates of 95.9–100% for the Solitaire and 90–100% for the Enterprise. In addition, both stents were associated with a comparably low peri-procedural complication rate and mortality. The complication rates observed in our study remain consistent with those that have been reported in the literature using exclusive stent-assisted aneurysmal coiling in ruptured as well as unruptured aneurysms (ranging from 0 to 16%).19,26,38 Mortality rates seen in our study were also comparable to those seen in studies that encompassed mainly unruptured aneurysms (0–4.6%) as well as studies with ruptured aneurysms (0–20%). In a multi-centered prospective study, Byrne et al. reported that long-term neurological complication occurred in 1.30% of patients treated with stent-assisted coiling and were mostly linked to thromboembolism.39 The one case of mortality seen in our study resulted from hemorrhage due to aneurysmal rupture during heparin therapy after thrombolysis. It should be noted that though bleeding episodes overall occurred at a relatively lower frequency in our experience with stent-assisted coiling, dual anti-platelet therapy facilitated bleeds after stent-assisted treatment remains a concern. For instance, combination therapy of aspirin/prasugrel has shown to predispose patients to a higher risk of hemorrhage during neurointerventional surgery compared with aspirin/ clopidogrel (19.4 versus 3.6%, P 5 0.02).19 In this study, initial angiographic results showed that overall 83.1% of aneurysms treated with stent-assistance had total flow cessation or had only minimal flow into the neck, which is consistent with previous reports.2,16
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However, 8.8% of followed aneurysms showed major recanalization. This is in contrast to reported data such as the one by Izar et al. who showed progressive occlusion of 36% of followed aneurysms.40 Hwang et al. in their 2-year follow-up study showed the rates of progressive aneurysmal occlusion in the stent group (17/40, 42.5%) versus non-stent group (34/86, 39.5%). In the same analysis, there was no statistically significant difference seen in aneurysmal recanalization between the stent and non-stent group (P 5 0.895) (7/40, 17.5% versus 18/86, 21.0%, respectively). Both available stents appear to have low rates of in-stent stenosis (one in Enterprise and four in Solitaire) indicating a good mid-term safety using either stent. When compared to a series of 213 patients with 110 patients available for follow-up, it was seen that significant (§50%) in-stent stenosis or occlusion was seen in 3% of patients. The causes of thromboembolic events may be attributed to antiplatelet resistance/noncompliance in patients post-stenting or secondary to a relatively poorer apposition of stiffer stents to the parent vessel wall around curves.16 Non-compliance of antiplatelet regimen has been documented to cause thromboembolic events and therefore, persistent use is required to avoid acute ischemic events. For instance, Ji et al. concluded from their analysis of antiplatelet medication persistence after ischemic stroke or transient ischemic attack in the Chinese population that at 3-month persistence, there was a significant association of less recurrent stroke and better functional outcomes.37
Conclusion Our study shows that the Enterprise and Solitaire stents are comparable devices with ease of navigation. Both stents exhibited similar immediate and mid-term followup results with low major neurological morbidities and mortality rate. Overall, more thrombogenic complications were found in Solitaire group. Further multi-centered prospective comparison studies between different types of stent-assisted aneurysmal coiling should be conducted with long-term follow-up to reinforce our data.
Disclaimer Statements Contributors YC participated in collection of data and manuscript preparation. YC and QP performed the statistical analysis. PZ and QP participated in study design and critically revised the manuscript. All authors read and approved the final manuscript. Funding None. Conflicts of interest The authors declare that they have no competing interests. Ethics approval The study was approved by the Ethics Review Board of Qingdao University.
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