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ORIGINAL ARTICLE
Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients Aihua Liu a,1, Tangming Peng b,1, Zenghui Qian a, Youxiang Li a, Chuhan Jiang a, Zhongxue Wu a, Xinjian Yang a,∗ a
Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing Neurosurgical Institute, Beijing, China b Department of Neurosurgery, The Affiliated Hospital of Luzhou Medical College, Luzhou, China
KEYWORDS Aneurysm; Enterprise; Outcome; Wide-necked; Rupture; Stent-assisted coiling; Subarachnoid hemorrhage
Summary Background and objective: Accumulated experience and improvement of stents dedicated to intracranial use have significantly widened the applicability of stent-assisted coiling (SAC) to ruptured wide-necked aneurysms. This retrospective study was designed to evaluate the safety and efficacy of SAC using the Enterprise stent for ruptured wide-necked intracranial aneurysms during ultra-early subarachnoid hemorrhage. Method: We reviewed data from 59 consecutive patients with ruptured wide-necked aneurysms who had SAC using the Enterprise stent performed within 48 hours of onset. Data collected and analyzed included: patient demographics; morphologic features of the aneurysm; treatment results and follow-up results. Clinical outcomes were evaluated by modified Rankin Scale (mRS). Results: In all 59 cases, SAC using the Enterprise stent was performed successfully, with no significant technical difficulties. Initial angiographic results were: complete occlusion in 38 cases; near occlusion in 17; and partial occlusion in four. Angiographic follow-up of 48 patients
∗
Corresponding author at: Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing Neurosurgical Institute, Tiantan Xili 6, Dongcheng District, Beijing, China (100050). Tel.: +86 10 67098852. E-mail address: [email protected] (X. Yang). 1 co-first author. http://dx.doi.org/10.1016/j.neurad.2014.11.005 0150-9861/© 2015 Published by Elsevier Masson SAS.
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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A. Liu et al. showed that 46 (95.8%) remained stable or improved, without regrowth, while regrowth was imaged in two patients. Medium-term clinical follow-up of 54 patients (mean, 26.9 months) showed that 88.9% had a good outcome (mRS: 0 in 34; 1 in eight; and 2 in six), and 11.1% poor outcomes (mRS: 3 in four; and 4 in two). Conclusion: Enterprise SAC is a safe and viable option for treatment of ruptured wide-necked aneurysms within 48 hours of ictus. © 2015 Published by Elsevier Masson SAS.
Introduction Endovascular embolization of ruptured intracranial aneurysms with detachable coils is associated with lower morbidity and mortality rates than clipping, as clearly demonstrated by the International Subarachnoid Aneurysm Trial [1,2]. Despite accumulated experience and technologically improved devices, endovascular embolization of ruptured wide-necked aneurysms within 48 hours of ictus has remained a technically challenging procedure. Various tools and techniques have been introduced to conquer this challenge; these include three-dimensional (3D) coils, balloon remodeling and dual microcatheters. The development of stents dedicated to intracranial use, which serve as a physical barrier to prevent coil extrusion into the parent vessel during the procedure, has considerably widened the applicability of coil embolization to wide-necked aneurysms. The Enterprise stent (Codman Neurovascular, Miami Lakes, FL, USA), which has been used in our center since 2009, is a self-expanding, closed-cell stent, that is specifically designed for wide-necked and fusiform intracranial aneurysms. Although an increasing number of reports have commended the safety and efficacy of intracranial stents in embolization of wide-necked aneurysms [3—7], previous studies mainly focused on unruptured aneurysms; there have been few systematic evaluations of the safety and efficacy of embolizing ruptured wide-necked aneurysms, especially in ultra-early (within 48 hours of ictus) subarachnoid hemorrhage. We performed this retrospective, single-center, study to evaluate the feasibility, safety and efficacy of using the Enterprise stent for stent-assisted coiling (SAC) of small and medium-size ruptured wide-necked aneurysms during ultraearly subarachnoid hemorrhage. Here we report the initial angiographic results, follow-up angiographic and clinical outcomes, incidence of procedure-related complications, and mortality.
Materials and methods Patient population With institutional Medical Ethics Committee approval, we retrospectively collected records from March 2009 to June 2013, of all intracranial aneurysm patients with subarachnoid hemorrhage who underwent endovascular embolization within 48 hours of onset. We analyzed data on 59 consecutive patients with ruptured wide-necked aneurysms during this
study period who were treated with Enterprise SAC either because their poor neurologic condition precluded clipping, or they refused clipping. Notably, one neurosurgeon and one neuro-intervention specialist determined the treatment strategy, and all 59 patients had common characteristics; ie, older age and clipping refusal.
Patient demographics and aneurysm characteristics Pre-operative patient demographic data included: age; gender; presentations; Hunt and Hess grade; neurological deficits at admission; and timing of endovascular embolization. All patients scheduled for Enterprise SAC had a detailed evaluation, with conventional angiography of bilateral internal carotid arteries and bilateral vertebral arteries, and rotational angiography with 3D reconstructions. Aneurysm features recorded, included: the maximum diameter of the aneurysm at the dome and neck; dome-to-neck ratio (DNR), and location. Table 1 summarizes the patient demographic data and aneurysm features. We defined wide-necked aneurysms as those with neck > 4 mm in diameter or those with a neck diameter < 4 mm but DNR < 2.
Procedures Routine treatment for ruptured wide-necked aneurysms in our institution is to perform SAC rather than balloon remodeling for DNR from 0.67 to 2.00, while balloon remodeling is performed for aneurysms with DNR < 0.67. SAC was performed by interventional radiologists (A.L., Y.L., X.Y., C.J., or Z.W.) with at least 10 years of neurointervention experience. SAC with the Enterprise stent was performed or first attempted within 48 hours of onset for all patients. All procedures were performed on a biplane flat-panel digital-subtraction unit (GE, USA; or Siemens, Germany) under general anesthesia via unilateral femoral access. A 6-French Envoy (Cordis Neurovascular, Inc, USA.) guiding catheter was inserted into the parent artery, and Prowler Plus Select 0.021-inch microcatheter (Codman Neurovascular, Raynham, MA, USA) was advanced into the normal distal parent artery, to 2 cm beyond the target aneurysm; the Enterprise stent (4.5 mm × 22.0 mm, or 4.5 mm × 28.0 mm,) was then introduced through the catheter hub and placed via its delivery system so that it fully-spanned the aneurysm neck, extending 5.0 mm beyond both sides. The SAC procedures employed two different therapeutic techniques—either ‘‘sequential’’ or ‘‘jailing’’. In the sequential technique, the Enterprise stent was first
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Stent for wide-necked aneurysms during ultra-early subarachnoid hemorrhage Table 1
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Primary angiographic occlusion rate according to patient demographics and treated aneurysm characteristics.
Patient demographics
Degree of occlusion
Total
P value
Complete
Near
Partial
Gender Male Female
18 20
3 14
1 3
22 37
0.061
Age (years) > 60 < 60
11 27
3 14
3 1
17 32
0.406
Hypertension Yes No
21 17
9 8
2 2
32 27
0.814
Aneurysm size (mm) 4 ≥4
14 24
5 12
2 2
21 38
0.965
Aneurysm characteristics Diameter (mm) Neck width (mm) DNR for All aneurysms DNR for aneurysms with neck < 4 mm All aneurysms
4.2 ± 1.5 5.1 ± 2.2 0.88 ± 0.28 1.04 ± 0.33 38
5.0 ± 2.3 5.1 ± 2.3 1.01 ± 0.34 1.09 ± 0.30 17
4.9 ± 2.9 4.9 ± 2.6 0.99 ± 0.31 0.98 ± 0.44 4
4.5 ± 1.9 5.1 ± 2.2 0.93 ± 0.30 1.04 ± 0.31 59
0.755 0.957 0.468 0.891
DNR: dome-to-neck ratio.
deployed across the aneurysm neck and a coil microcatheter was gently introduced into the aneurysm sac through the stent mesh, through which the coils were then introduced one-by-one until the coil mesh was stable within the sac. In the jailing technique, a separate microcatheter was introduced into the aneurysm sac, and the first coil was then inserted into the sac (not detached), following which the stent was deployed parallel to the microcatheter, which was held stable between the stent and the vessel wall. Finally, subsequent coils were introduced into the sac until ideal packing was achieved. In all cases, aneurysm occlusion was evaluated on the basis of imaging immediately after introducing the last coil.
Pharmacology management Patients who were clearly conscious were given a loading dose of clopidogrel and aspirin (300 mg each) orally or rectally, 2 hours before scheduled stenting. Unconscious patients were administered tirofiban (20 g/kg) for 3 to 5 minutes, followed by intravenous injection of the remaining dose (2.5 g/kg/min) until it was finished. After the procedure, conscious patients were maintained on daily clopidogrel and aspirin (100 mg each) for 4 weeks, followed by aspirin alone (100 mg daily) for another 5 months; unconscious patients were maintained on daily clopidogrel and aspirin (200 mg each) for the first 2 days, and received the same medication as conscious patients thereafter. In addition, local heparinization was administered through the
hub of the guiding catheter during the procedure, and systemic heparinization after the introducing the first coil but before stent deployment. However, low-molecular-weight heparin (40 mg, every 12 hours, hypodermic injection) was only administered for 24 hours immediately after the procedure in those patients who had undergone intra-operative thrombolysis.
Follow-up Outcomes were defined based on clinical and angiographic criteria. Clinical outcomes, which were assessed by visits, telephone calls and an examination at the clinic, were evaluated using modified Rankin Scales (mRS) at the 6-month follow-up visit. For all patients, we recommended the first digital-subtraction angiography (DSA) follow-up 3 months after the procedure and a second 6 months later, with annual follow-up thereafter. Angiographic outcomes after Enterprise SAC of the ruptured aneurysms included the rate of initial occlusion and follow-up occlusion, and were categorized according to the Raymond Scales [8] as complete occlusion, near complete occlusion, and partial occlusion.
Results Patient demographics and aneurysm characteristics Our series of 59 patients had an average age of 64.5 ± 9.6 years (range 34—81 years); the majority (37;
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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62.7%) were female and 32 (55.9%) had a history of hypertension. In total, these patients harbored 62 aneurysms: 56 patients carried a single aneurysm, and three had two aneurysms each. Of the 62 aneurysms, by far the most common location was the posterior communicating artery (29 aneurysms), followed by the internal carotid artery (13), vertebral artery (9), anterior communicating artery (4), basilar artery (3), middle cerebral artery and posterior cerebral artery (2 each). Among the treated 59 aneurysms, thirty-eight aneurysms with wide necks (≥ 4 mm) and the other 21 had aneurysms with a small neck width (< 4 mm); The DNR of all treated aneurysms was < 2, and averaged 0.87 (range 0.67—1.77), and the DNR of aneurysms with neck size < 4 mm averaged 1.02 (range 0.67—1.77). Table 1 summarizes the patient demographics and aneurysm characteristics according to the primary angiographic results. None of the ruptured aneurysms had been previously treated.
Clinical results We, successfully treated 59 ruptured wide-necked aneurysms using Enterprise stents in all cases, with no significant technical difficulties; of these, small size (< 4 mm) was achieved in 24, and medium size in 35. One patient (1.7%) in our series died; this patient had a history of hypertension and was admitted to our department unconscious and with poor neurologic grade (Hunt and Hess grade IV). The patient harbored a left-posterior communicating artery aneurysm, which primary conventional angiography showed was growing with irregular shape (three phyllodes), the left-middle cerebral artery was occluded and angiography showed characteristics of Moyamoya disease. The primary angiographic outcome was complete occlusion and the death occurred in the Intensive Care Unit (ICU) upon sudden herniation 1 week after successful Enterprise SAC. Medium-term clinical follow-up was achieved in 54 of the remaining 58 patients, with a mean of 26.9 months; 88.9% had good outcomes (mRS scores: 0 in 34, 1 in eight, and 2 in six) 11.1% poor outcomes (mRS scores: 3 in four, and 4 in two). Four of the six patients with poor outcomes, were Hunt and Hess grade IV, and the other two were grade II and III, respectively. One of these two patients had a severe heart attack 13 months after discharge, and the other was found to have lung cancer 21 months after discharge.
Angiographic results Primary angiographic results were achieved in all 59 patients after Enterprise SAC. Complete occlusion was achieved in 38 aneurysms, near occlusion in 17 aneurysms, and partial occlusion in 4. Conventional angiographic follow-up by DSA that extended longer than 3 months was available in 48 patients; of these, 46 (95.8%) remained stable without regrowth, including 34 with complete occlusion and 12 with near occlusion. However, recurrence was observed in two patients (4.2%), both of whom had a primary angiography outcome of near occlusion; DSA follow-up showed regrowth after 5 months and 8 months, respectively. Both patients were underwent a salvage procedure using an Enterprise stent, and the aneurysms had totally disappeared on DSA
follow-up after another 8 months and 11 months, respectively.
Procedure-related complications Five of our 59 patients (8.5%) experienced procedurerelated complications; however, one of these was a delayed in-stent thrombosis of the parent vessels which occurred after 47 days follow-up in a patient who had discontinued clopidogrel 1 month after the procedure. Cytochrome P450 2C19 (CYP2C19) genotyping revealed ‘‘2’’ and ‘‘3’’ alleles, which diminish the platelet response to clopidogrel. This relative loss of CYP2C19 function and discontinuation of pharmacotherapy may explain the delayed in-stent thrombosis, in which case the actual procedure-related complication rate may be four of 59 (6.8%). Among these four patients, two experienced coil extrusion into the parent artery, resulting in a thromboembolic complication during the procedure. Intravenous tirofiban given immediately as a rescue treatment resulted in complete resolution of the clot after about 50 minutes. The other two patients both had rebleeding during the procedure due to the coil microcatheter perforating the aneurysm wall during insertion into the aneurysm sac having successfully navigated the stentmicrocatheter; one rebleed was in a sequential technique. Rebleeding was managed with rapid-density packing of the aneurysm, followed by ICU treatment. One patient was discharged to another rehabilitation medical institution 14 days post-procedure with mRS 3, and had achieved mRS 2 by 18 months follow-up. The other patient was discharged to another rehabilitation medical institution 19 days postprocedure with mRS 4, and mRS was still 4 at 10 months follow-up.
Discussion Debate on the ideal management of ruptured intracranial aneurysms, especially within 48 hours of onset, is still open. The outcome of coil embolization is associated, in part, with aneurysm geometry. Aneurysms with wide necks are difficult to embolize by coiling alone. A wide-necked configuration also prevents density packing, resulting in higher rates of regrowth and often requiring subsequent retreatment. In addition, implanted coils may extrude from the aneurysm sac into the parent vessel, resulting in thromboembolic complications or parent or branch artery occlusion. Since the debut of self-expanding intracranial stents, SAC has broadened the indications for embolization of ruptured wide-necked aneurysms, with the Enterprise stent becoming a viable option for SAC of ruptured wide-necked aneurysms. This stent not only improves aneurysm-packing density and redirects flow, but also provides a physical matrix for endothelial regrowth and prevents coil extrusion into the parent artery. The balloon remodeling technique was also initially designed for the endovascular treatment wide-neck aneurysms. Recent published data also showed that balloon remodeling can obtain equivalent safety and better anatomic results compared with stanrdard coiling for ruptured and unruptured aneurysms [9]. Pierot, et al. [10] reported their prospective study of 782 patients with balloon remodeling or standard coiling, of which 160 patients
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Stent for wide-necked aneurysms during ultra-early subarachnoid hemorrhage were performed with balloon remodeling and 608 patients were underwent standard coiling. At the end of this prospective study, Pierot and his coworkers showed that the rate of adequate aneurysm occlusionwas significantly higher with balloon remodeling (94.9%) than that with standard coiling (88.7%). In our institution, balloon remodeling was always performed on aneurysms with DNR from 0.50 to 0.67, while stenting was the first therapeutic option for those with DNR > 0.67, even though the most commonly reported adverse events are thromboembolic events associated with stent application. A principal benefit of the Enterprise stent its delivery system, which provides excellent navigability and positioning that make it easy to deliver and deploy. In contrast, earlier studies with the Neuroform stent reported rates of inability to navigate or deploy of 4—14%, and rates of inaccurate deployment of 7.8—8%, compared to an inaccurate deployment rate of 1.3% for the Enterprise stent [11—14]. In our patient series, successful stent navigation and deployment was achieved in 100% of cases, with no instances of stent migration. Similarly, several other recent small case series reported experiencing no instances of inaccurate deployment or inability to deploy with the Enterprise stent [15—17]. Another benefit of the Enterprise stent is its denser packing of the aneurysm sac and neck. In this SAC technique, the stent is deployed across the parent artery 5 mm beyond each side of the aneurysm neck and serves as a physical framework to reconstruct the parent artery for subsequent introduction of coils into the aneurysm sac. In this way, the stent can prevent coils from extruding into the parent vessel, achieve denser aneurysmal packing and reduce the chance of coil compaction, resulting in lower rates of regrowth in wide-necked aneurysms. Raymond and coworkers [18], reported retrospective data on 501 aneurysms with a regrowth rate of 33.6% and regrowth in 76 of 191 aneurysms (39.8%) that were treated acutely after rupture. However, their high regrowth rate was mainly due to using traditional detachable coils without the assistance of an aneurysm neck bridge device. Regarding wide-necked ruptured aneurysms, reported regrowth rates are 0.0—13.8% with intracranial SAC versus 0.0—8.8% with the Enterprise stent [15,19—21]. Most aneurysms in our series were located in the tortuous internal carotid artery system, which has greater parent vessel size and is regarded as having a higher risk of regrowth due to incomplete stent apposition in Enterprise SAC. However, among 48 patients with angiographic follow-up, regrowth was evident in only two (4.2%), which is a lower rate than in previously reports of SAC. Previous studies of SAC for ruptured wide-necked aneurysms within 48 hours of onset have reported high rates of procedure-related adverse events (21.4%, including 9.0% for rebleeding) and adverse outcomes [22]; the most severe procedure-related adverse event was hemorrhage. Chung et al. [23] aslo reported a series of 72 patients with wide-necked anrueysms underwent SAC within 72 hours of onset, and in his data, the thromboembolic complications was 12.5% and stent-related hemorrhage event was 2.8%. However, Enterprise SAC did not increase the rate of procedure-related complications in ruptured wide-necked aneurysms. In our study, five patients (8.5%) had procedurerelated adverse events, two (3.4%) of which were due to
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microguidewire perforation. The hemorrhage event rate (3.4%) using the Enterprise stent in our series was considerably lower than has been previously reported; this may be because using smaller coils, operating carefully, using local heparinization and not using LMWH except in case of a thrombolic event, helped to prevent hemorrhages from occurring during the procedure. Acute subarachnoid hemorrhage is a hypercoagulable state that incurs a high likelihood of thrombosis, and there are an increasing number of published reports of thromboembolic complications associated with stenting. For example, Golshani and coworkers [20] reported that six of 36 patients (19%) experienced thrombotic complications during SAC of ruptured aneurysms. However, only one patient with thromboembolic complications in their series, had preoperative clopidogrel, which suggests that pre-operative clopidogrel may reduce the incidence of intra-operative thromboembolic events. There was also a high rate of thrombotic complications (11.5%) in another report, in which a loading dose of acetylsalicylic acid (250—500 mg) was administered in 43 of 61 (70%) cases of ruptured aneurysm cases that were treated with SAC in the acute phase [22]. These reports suggest that high thromboembolic event rates may be due to irregular administration of clopidogrel and aspirin. In our series, conventional pharmacologic management may have contributed to a lower thromboembolic event rate (3/59, 5.1%). Besides administering pharmacotherapy, the other routine used during the SAC procedure in our institution helped to prevent thromboembolic events: few patients (3/59, 5.1%) underwent the sequential technique compared with the stent-jail technique (56/59, 94.9%), because the later reduces navigation time, resulting in quicker packing and lower incidence of thromboembolic events. In our patient series, 48 of 54 cases (88.9%) had a good medium-term outcome on clinical follow-up, and the short-term outcome on angiographic follow-up was stable or improved in 46 of 48 aneurysms (95.8%) for which data were available; meanwhile, with a single fatality, mortality was only 1.7%. These findings further affirm that the Enterprise stent is a feasible, efficacious and safe option for treating ruptured wide-necked aneurysms in ultra-early subarachnoid hemorrhage. This study does have limitations; it was retrospective, included only a relatively small number of patients, had nonstandardized procedural protocols and criteria for stenting, and variable, sometimes inadequate, patient follow-up. Nevertheless, to our knowledge, there are no published reports of any larger single-center case series of Enterprise SAC for ruptured wide-necked aneurysms performed within 48 hours of subarachnoid hemorrhage.
Conclusion Notwithstanding the limitations of this study, SAC appears a safe and viable option for treating ruptured wide-necked aneurysms within 48 hours of subarachnoid hemorrhage.
Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Funding: This article is supported by the National Natural Science Foundation of China (No. 30901557,81220108007, 81441038), High Level Health Technique Talent Training Plan of Beijing Health System (No. 2011-3-036), Nova Plan of Beijing Municipal Science and technology (No. 2007A043), Beijing Natural Science Foundation (No. 7142032), the Specific Research Projects for Capital Health Development (2014-3-2044) and the Interdisciplinary Cooperation Projectsthe of the Nova Plan of Beijing Municipal Science and Technology (No. Z141107001814120).
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Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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ORIGINAL ARTICLE
Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients Aihua Liu a,1, Tangming Peng b,1, Zenghui Qian a, Youxiang Li a, Chuhan Jiang a, Zhongxue Wu a, Xinjian Yang a,∗ a
Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing Neurosurgical Institute, Beijing, China b Department of Neurosurgery, The Affiliated Hospital of Luzhou Medical College, Luzhou, China
KEYWORDS Aneurysm; Enterprise; Outcome; Wide-necked; Rupture; Stent-assisted coiling; Subarachnoid hemorrhage
Summary Background and objective: Accumulated experience and improvement of stents dedicated to intracranial use have significantly widened the applicability of stent-assisted coiling (SAC) to ruptured wide-necked aneurysms. This retrospective study was designed to evaluate the safety and efficacy of SAC using the Enterprise stent for ruptured wide-necked intracranial aneurysms during ultra-early subarachnoid hemorrhage. Method: We reviewed data from 59 consecutive patients with ruptured wide-necked aneurysms who had SAC using the Enterprise stent performed within 48 hours of onset. Data collected and analyzed included: patient demographics; morphologic features of the aneurysm; treatment results and follow-up results. Clinical outcomes were evaluated by modified Rankin Scale (mRS). Results: In all 59 cases, SAC using the Enterprise stent was performed successfully, with no significant technical difficulties. Initial angiographic results were: complete occlusion in 38 cases; near occlusion in 17; and partial occlusion in four. Angiographic follow-up of 48 patients
∗
Corresponding author at: Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing Neurosurgical Institute, Tiantan Xili 6, Dongcheng District, Beijing, China (100050). Tel.: +86 10 67098852. E-mail address: [email protected] (X. Yang). 1 co-first author. http://dx.doi.org/10.1016/j.neurad.2014.11.005 0150-9861/© 2015 Published by Elsevier Masson SAS.
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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A. Liu et al. showed that 46 (95.8%) remained stable or improved, without regrowth, while regrowth was imaged in two patients. Medium-term clinical follow-up of 54 patients (mean, 26.9 months) showed that 88.9% had a good outcome (mRS: 0 in 34; 1 in eight; and 2 in six), and 11.1% poor outcomes (mRS: 3 in four; and 4 in two). Conclusion: Enterprise SAC is a safe and viable option for treatment of ruptured wide-necked aneurysms within 48 hours of ictus. © 2015 Published by Elsevier Masson SAS.
Introduction Endovascular embolization of ruptured intracranial aneurysms with detachable coils is associated with lower morbidity and mortality rates than clipping, as clearly demonstrated by the International Subarachnoid Aneurysm Trial [1,2]. Despite accumulated experience and technologically improved devices, endovascular embolization of ruptured wide-necked aneurysms within 48 hours of ictus has remained a technically challenging procedure. Various tools and techniques have been introduced to conquer this challenge; these include three-dimensional (3D) coils, balloon remodeling and dual microcatheters. The development of stents dedicated to intracranial use, which serve as a physical barrier to prevent coil extrusion into the parent vessel during the procedure, has considerably widened the applicability of coil embolization to wide-necked aneurysms. The Enterprise stent (Codman Neurovascular, Miami Lakes, FL, USA), which has been used in our center since 2009, is a self-expanding, closed-cell stent, that is specifically designed for wide-necked and fusiform intracranial aneurysms. Although an increasing number of reports have commended the safety and efficacy of intracranial stents in embolization of wide-necked aneurysms [3—7], previous studies mainly focused on unruptured aneurysms; there have been few systematic evaluations of the safety and efficacy of embolizing ruptured wide-necked aneurysms, especially in ultra-early (within 48 hours of ictus) subarachnoid hemorrhage. We performed this retrospective, single-center, study to evaluate the feasibility, safety and efficacy of using the Enterprise stent for stent-assisted coiling (SAC) of small and medium-size ruptured wide-necked aneurysms during ultraearly subarachnoid hemorrhage. Here we report the initial angiographic results, follow-up angiographic and clinical outcomes, incidence of procedure-related complications, and mortality.
Materials and methods Patient population With institutional Medical Ethics Committee approval, we retrospectively collected records from March 2009 to June 2013, of all intracranial aneurysm patients with subarachnoid hemorrhage who underwent endovascular embolization within 48 hours of onset. We analyzed data on 59 consecutive patients with ruptured wide-necked aneurysms during this
study period who were treated with Enterprise SAC either because their poor neurologic condition precluded clipping, or they refused clipping. Notably, one neurosurgeon and one neuro-intervention specialist determined the treatment strategy, and all 59 patients had common characteristics; ie, older age and clipping refusal.
Patient demographics and aneurysm characteristics Pre-operative patient demographic data included: age; gender; presentations; Hunt and Hess grade; neurological deficits at admission; and timing of endovascular embolization. All patients scheduled for Enterprise SAC had a detailed evaluation, with conventional angiography of bilateral internal carotid arteries and bilateral vertebral arteries, and rotational angiography with 3D reconstructions. Aneurysm features recorded, included: the maximum diameter of the aneurysm at the dome and neck; dome-to-neck ratio (DNR), and location. Table 1 summarizes the patient demographic data and aneurysm features. We defined wide-necked aneurysms as those with neck > 4 mm in diameter or those with a neck diameter < 4 mm but DNR < 2.
Procedures Routine treatment for ruptured wide-necked aneurysms in our institution is to perform SAC rather than balloon remodeling for DNR from 0.67 to 2.00, while balloon remodeling is performed for aneurysms with DNR < 0.67. SAC was performed by interventional radiologists (A.L., Y.L., X.Y., C.J., or Z.W.) with at least 10 years of neurointervention experience. SAC with the Enterprise stent was performed or first attempted within 48 hours of onset for all patients. All procedures were performed on a biplane flat-panel digital-subtraction unit (GE, USA; or Siemens, Germany) under general anesthesia via unilateral femoral access. A 6-French Envoy (Cordis Neurovascular, Inc, USA.) guiding catheter was inserted into the parent artery, and Prowler Plus Select 0.021-inch microcatheter (Codman Neurovascular, Raynham, MA, USA) was advanced into the normal distal parent artery, to 2 cm beyond the target aneurysm; the Enterprise stent (4.5 mm × 22.0 mm, or 4.5 mm × 28.0 mm,) was then introduced through the catheter hub and placed via its delivery system so that it fully-spanned the aneurysm neck, extending 5.0 mm beyond both sides. The SAC procedures employed two different therapeutic techniques—either ‘‘sequential’’ or ‘‘jailing’’. In the sequential technique, the Enterprise stent was first
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Stent for wide-necked aneurysms during ultra-early subarachnoid hemorrhage Table 1
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Primary angiographic occlusion rate according to patient demographics and treated aneurysm characteristics.
Patient demographics
Degree of occlusion
Total
P value
Complete
Near
Partial
Gender Male Female
18 20
3 14
1 3
22 37
0.061
Age (years) > 60 < 60
11 27
3 14
3 1
17 32
0.406
Hypertension Yes No
21 17
9 8
2 2
32 27
0.814
Aneurysm size (mm) 4 ≥4
14 24
5 12
2 2
21 38
0.965
Aneurysm characteristics Diameter (mm) Neck width (mm) DNR for All aneurysms DNR for aneurysms with neck < 4 mm All aneurysms
4.2 ± 1.5 5.1 ± 2.2 0.88 ± 0.28 1.04 ± 0.33 38
5.0 ± 2.3 5.1 ± 2.3 1.01 ± 0.34 1.09 ± 0.30 17
4.9 ± 2.9 4.9 ± 2.6 0.99 ± 0.31 0.98 ± 0.44 4
4.5 ± 1.9 5.1 ± 2.2 0.93 ± 0.30 1.04 ± 0.31 59
0.755 0.957 0.468 0.891
DNR: dome-to-neck ratio.
deployed across the aneurysm neck and a coil microcatheter was gently introduced into the aneurysm sac through the stent mesh, through which the coils were then introduced one-by-one until the coil mesh was stable within the sac. In the jailing technique, a separate microcatheter was introduced into the aneurysm sac, and the first coil was then inserted into the sac (not detached), following which the stent was deployed parallel to the microcatheter, which was held stable between the stent and the vessel wall. Finally, subsequent coils were introduced into the sac until ideal packing was achieved. In all cases, aneurysm occlusion was evaluated on the basis of imaging immediately after introducing the last coil.
Pharmacology management Patients who were clearly conscious were given a loading dose of clopidogrel and aspirin (300 mg each) orally or rectally, 2 hours before scheduled stenting. Unconscious patients were administered tirofiban (20 g/kg) for 3 to 5 minutes, followed by intravenous injection of the remaining dose (2.5 g/kg/min) until it was finished. After the procedure, conscious patients were maintained on daily clopidogrel and aspirin (100 mg each) for 4 weeks, followed by aspirin alone (100 mg daily) for another 5 months; unconscious patients were maintained on daily clopidogrel and aspirin (200 mg each) for the first 2 days, and received the same medication as conscious patients thereafter. In addition, local heparinization was administered through the
hub of the guiding catheter during the procedure, and systemic heparinization after the introducing the first coil but before stent deployment. However, low-molecular-weight heparin (40 mg, every 12 hours, hypodermic injection) was only administered for 24 hours immediately after the procedure in those patients who had undergone intra-operative thrombolysis.
Follow-up Outcomes were defined based on clinical and angiographic criteria. Clinical outcomes, which were assessed by visits, telephone calls and an examination at the clinic, were evaluated using modified Rankin Scales (mRS) at the 6-month follow-up visit. For all patients, we recommended the first digital-subtraction angiography (DSA) follow-up 3 months after the procedure and a second 6 months later, with annual follow-up thereafter. Angiographic outcomes after Enterprise SAC of the ruptured aneurysms included the rate of initial occlusion and follow-up occlusion, and were categorized according to the Raymond Scales [8] as complete occlusion, near complete occlusion, and partial occlusion.
Results Patient demographics and aneurysm characteristics Our series of 59 patients had an average age of 64.5 ± 9.6 years (range 34—81 years); the majority (37;
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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62.7%) were female and 32 (55.9%) had a history of hypertension. In total, these patients harbored 62 aneurysms: 56 patients carried a single aneurysm, and three had two aneurysms each. Of the 62 aneurysms, by far the most common location was the posterior communicating artery (29 aneurysms), followed by the internal carotid artery (13), vertebral artery (9), anterior communicating artery (4), basilar artery (3), middle cerebral artery and posterior cerebral artery (2 each). Among the treated 59 aneurysms, thirty-eight aneurysms with wide necks (≥ 4 mm) and the other 21 had aneurysms with a small neck width (< 4 mm); The DNR of all treated aneurysms was < 2, and averaged 0.87 (range 0.67—1.77), and the DNR of aneurysms with neck size < 4 mm averaged 1.02 (range 0.67—1.77). Table 1 summarizes the patient demographics and aneurysm characteristics according to the primary angiographic results. None of the ruptured aneurysms had been previously treated.
Clinical results We, successfully treated 59 ruptured wide-necked aneurysms using Enterprise stents in all cases, with no significant technical difficulties; of these, small size (< 4 mm) was achieved in 24, and medium size in 35. One patient (1.7%) in our series died; this patient had a history of hypertension and was admitted to our department unconscious and with poor neurologic grade (Hunt and Hess grade IV). The patient harbored a left-posterior communicating artery aneurysm, which primary conventional angiography showed was growing with irregular shape (three phyllodes), the left-middle cerebral artery was occluded and angiography showed characteristics of Moyamoya disease. The primary angiographic outcome was complete occlusion and the death occurred in the Intensive Care Unit (ICU) upon sudden herniation 1 week after successful Enterprise SAC. Medium-term clinical follow-up was achieved in 54 of the remaining 58 patients, with a mean of 26.9 months; 88.9% had good outcomes (mRS scores: 0 in 34, 1 in eight, and 2 in six) 11.1% poor outcomes (mRS scores: 3 in four, and 4 in two). Four of the six patients with poor outcomes, were Hunt and Hess grade IV, and the other two were grade II and III, respectively. One of these two patients had a severe heart attack 13 months after discharge, and the other was found to have lung cancer 21 months after discharge.
Angiographic results Primary angiographic results were achieved in all 59 patients after Enterprise SAC. Complete occlusion was achieved in 38 aneurysms, near occlusion in 17 aneurysms, and partial occlusion in 4. Conventional angiographic follow-up by DSA that extended longer than 3 months was available in 48 patients; of these, 46 (95.8%) remained stable without regrowth, including 34 with complete occlusion and 12 with near occlusion. However, recurrence was observed in two patients (4.2%), both of whom had a primary angiography outcome of near occlusion; DSA follow-up showed regrowth after 5 months and 8 months, respectively. Both patients were underwent a salvage procedure using an Enterprise stent, and the aneurysms had totally disappeared on DSA
follow-up after another 8 months and 11 months, respectively.
Procedure-related complications Five of our 59 patients (8.5%) experienced procedurerelated complications; however, one of these was a delayed in-stent thrombosis of the parent vessels which occurred after 47 days follow-up in a patient who had discontinued clopidogrel 1 month after the procedure. Cytochrome P450 2C19 (CYP2C19) genotyping revealed ‘‘2’’ and ‘‘3’’ alleles, which diminish the platelet response to clopidogrel. This relative loss of CYP2C19 function and discontinuation of pharmacotherapy may explain the delayed in-stent thrombosis, in which case the actual procedure-related complication rate may be four of 59 (6.8%). Among these four patients, two experienced coil extrusion into the parent artery, resulting in a thromboembolic complication during the procedure. Intravenous tirofiban given immediately as a rescue treatment resulted in complete resolution of the clot after about 50 minutes. The other two patients both had rebleeding during the procedure due to the coil microcatheter perforating the aneurysm wall during insertion into the aneurysm sac having successfully navigated the stentmicrocatheter; one rebleed was in a sequential technique. Rebleeding was managed with rapid-density packing of the aneurysm, followed by ICU treatment. One patient was discharged to another rehabilitation medical institution 14 days post-procedure with mRS 3, and had achieved mRS 2 by 18 months follow-up. The other patient was discharged to another rehabilitation medical institution 19 days postprocedure with mRS 4, and mRS was still 4 at 10 months follow-up.
Discussion Debate on the ideal management of ruptured intracranial aneurysms, especially within 48 hours of onset, is still open. The outcome of coil embolization is associated, in part, with aneurysm geometry. Aneurysms with wide necks are difficult to embolize by coiling alone. A wide-necked configuration also prevents density packing, resulting in higher rates of regrowth and often requiring subsequent retreatment. In addition, implanted coils may extrude from the aneurysm sac into the parent vessel, resulting in thromboembolic complications or parent or branch artery occlusion. Since the debut of self-expanding intracranial stents, SAC has broadened the indications for embolization of ruptured wide-necked aneurysms, with the Enterprise stent becoming a viable option for SAC of ruptured wide-necked aneurysms. This stent not only improves aneurysm-packing density and redirects flow, but also provides a physical matrix for endothelial regrowth and prevents coil extrusion into the parent artery. The balloon remodeling technique was also initially designed for the endovascular treatment wide-neck aneurysms. Recent published data also showed that balloon remodeling can obtain equivalent safety and better anatomic results compared with stanrdard coiling for ruptured and unruptured aneurysms [9]. Pierot, et al. [10] reported their prospective study of 782 patients with balloon remodeling or standard coiling, of which 160 patients
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Stent for wide-necked aneurysms during ultra-early subarachnoid hemorrhage were performed with balloon remodeling and 608 patients were underwent standard coiling. At the end of this prospective study, Pierot and his coworkers showed that the rate of adequate aneurysm occlusionwas significantly higher with balloon remodeling (94.9%) than that with standard coiling (88.7%). In our institution, balloon remodeling was always performed on aneurysms with DNR from 0.50 to 0.67, while stenting was the first therapeutic option for those with DNR > 0.67, even though the most commonly reported adverse events are thromboembolic events associated with stent application. A principal benefit of the Enterprise stent its delivery system, which provides excellent navigability and positioning that make it easy to deliver and deploy. In contrast, earlier studies with the Neuroform stent reported rates of inability to navigate or deploy of 4—14%, and rates of inaccurate deployment of 7.8—8%, compared to an inaccurate deployment rate of 1.3% for the Enterprise stent [11—14]. In our patient series, successful stent navigation and deployment was achieved in 100% of cases, with no instances of stent migration. Similarly, several other recent small case series reported experiencing no instances of inaccurate deployment or inability to deploy with the Enterprise stent [15—17]. Another benefit of the Enterprise stent is its denser packing of the aneurysm sac and neck. In this SAC technique, the stent is deployed across the parent artery 5 mm beyond each side of the aneurysm neck and serves as a physical framework to reconstruct the parent artery for subsequent introduction of coils into the aneurysm sac. In this way, the stent can prevent coils from extruding into the parent vessel, achieve denser aneurysmal packing and reduce the chance of coil compaction, resulting in lower rates of regrowth in wide-necked aneurysms. Raymond and coworkers [18], reported retrospective data on 501 aneurysms with a regrowth rate of 33.6% and regrowth in 76 of 191 aneurysms (39.8%) that were treated acutely after rupture. However, their high regrowth rate was mainly due to using traditional detachable coils without the assistance of an aneurysm neck bridge device. Regarding wide-necked ruptured aneurysms, reported regrowth rates are 0.0—13.8% with intracranial SAC versus 0.0—8.8% with the Enterprise stent [15,19—21]. Most aneurysms in our series were located in the tortuous internal carotid artery system, which has greater parent vessel size and is regarded as having a higher risk of regrowth due to incomplete stent apposition in Enterprise SAC. However, among 48 patients with angiographic follow-up, regrowth was evident in only two (4.2%), which is a lower rate than in previously reports of SAC. Previous studies of SAC for ruptured wide-necked aneurysms within 48 hours of onset have reported high rates of procedure-related adverse events (21.4%, including 9.0% for rebleeding) and adverse outcomes [22]; the most severe procedure-related adverse event was hemorrhage. Chung et al. [23] aslo reported a series of 72 patients with wide-necked anrueysms underwent SAC within 72 hours of onset, and in his data, the thromboembolic complications was 12.5% and stent-related hemorrhage event was 2.8%. However, Enterprise SAC did not increase the rate of procedure-related complications in ruptured wide-necked aneurysms. In our study, five patients (8.5%) had procedurerelated adverse events, two (3.4%) of which were due to
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microguidewire perforation. The hemorrhage event rate (3.4%) using the Enterprise stent in our series was considerably lower than has been previously reported; this may be because using smaller coils, operating carefully, using local heparinization and not using LMWH except in case of a thrombolic event, helped to prevent hemorrhages from occurring during the procedure. Acute subarachnoid hemorrhage is a hypercoagulable state that incurs a high likelihood of thrombosis, and there are an increasing number of published reports of thromboembolic complications associated with stenting. For example, Golshani and coworkers [20] reported that six of 36 patients (19%) experienced thrombotic complications during SAC of ruptured aneurysms. However, only one patient with thromboembolic complications in their series, had preoperative clopidogrel, which suggests that pre-operative clopidogrel may reduce the incidence of intra-operative thromboembolic events. There was also a high rate of thrombotic complications (11.5%) in another report, in which a loading dose of acetylsalicylic acid (250—500 mg) was administered in 43 of 61 (70%) cases of ruptured aneurysm cases that were treated with SAC in the acute phase [22]. These reports suggest that high thromboembolic event rates may be due to irregular administration of clopidogrel and aspirin. In our series, conventional pharmacologic management may have contributed to a lower thromboembolic event rate (3/59, 5.1%). Besides administering pharmacotherapy, the other routine used during the SAC procedure in our institution helped to prevent thromboembolic events: few patients (3/59, 5.1%) underwent the sequential technique compared with the stent-jail technique (56/59, 94.9%), because the later reduces navigation time, resulting in quicker packing and lower incidence of thromboembolic events. In our patient series, 48 of 54 cases (88.9%) had a good medium-term outcome on clinical follow-up, and the short-term outcome on angiographic follow-up was stable or improved in 46 of 48 aneurysms (95.8%) for which data were available; meanwhile, with a single fatality, mortality was only 1.7%. These findings further affirm that the Enterprise stent is a feasible, efficacious and safe option for treating ruptured wide-necked aneurysms in ultra-early subarachnoid hemorrhage. This study does have limitations; it was retrospective, included only a relatively small number of patients, had nonstandardized procedural protocols and criteria for stenting, and variable, sometimes inadequate, patient follow-up. Nevertheless, to our knowledge, there are no published reports of any larger single-center case series of Enterprise SAC for ruptured wide-necked aneurysms performed within 48 hours of subarachnoid hemorrhage.
Conclusion Notwithstanding the limitations of this study, SAC appears a safe and viable option for treating ruptured wide-necked aneurysms within 48 hours of subarachnoid hemorrhage.
Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.
Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
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Funding: This article is supported by the National Natural Science Foundation of China (No. 30901557,81220108007, 81441038), High Level Health Technique Talent Training Plan of Beijing Health System (No. 2011-3-036), Nova Plan of Beijing Municipal Science and technology (No. 2007A043), Beijing Natural Science Foundation (No. 7142032), the Specific Research Projects for Capital Health Development (2014-3-2044) and the Interdisciplinary Cooperation Projectsthe of the Nova Plan of Beijing Municipal Science and Technology (No. Z141107001814120).
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Please cite this article in press as: Liu A, et al. Enterprise stent-assisted coiling for wide-necked intracranial aneurysms during ultra-early (48 hours) subarachnoid hemorrhage: A single-center experience in 59 consecutive patients. J Neuroradiol (2015), http://dx.doi.org/10.1016/j.neurad.2014.11.005
