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ORIGINAL ARTICLE
Year : 2010  |  Volume : 58  |  Issue : 6  |  Page : 825-832

Neuroform stent-assisted coiling of large and giant intracranial aneurysms: Angiographic and clinical outcomes in 71 consecutive patients


1 Beijing Neurosurgical Institute, Capital Medical University, Beijing - 100 050; Department of Neurosurgery, The General Hospital of Shenyang Military Command, Shenyang, 110016, P. R. China
2 Department of Neurosurgery, The General Hospital of Shenyang Military Command, Shenyang, 110016, P. R. China
3 Beijing Neurosurgical Institute, Capital Medical University, Beijing - 100 050

Date of Acceptance14-Jul-2010
Date of Web Publication10-Dec-2010

Correspondence Address:
Zhongxue Wu
Beijing Neurosurgical Institute, Capital Medical University, Beijing - 100 050, P. R. China

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.73737

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 » Abstract 

Background: Large and giant aneurysms still remain a therapeutic challenge both surgically and endovascularly. Objective: The authors report their clinical experience and follow-up results using Neuroform stent, as an adjunct in the treatment of large and giant aneurysms. Materials and Methods: A total of 71 consecutive patients with 72 large or giant intracranial aneurysms were treated with the Neuroform stent-assisted coiling. Both sequential technique and parallel technique were used. In all cases, embolization was completed by packing the aneurysm sac with a variety of commercially available coils. The technical feasibility of the procedure, procedure-related complications, angiographic results, clinical outcome, and follow-up angiography were evaluated. Results: In all the patients, the Neuroform stent system was delivered and deployed accurately, and occlusion was achieved. Immediate angiography demonstrated complete occlusion of the aneurysm in 59.7% of the patients, neck remnant in 26.4%, and incomplete occlusion in 13.9%. Procedure-related complication, morbidity, and mortality were 15.3, 4.2, and 1.4%, respectively. Favorable clinical outcome (modified Rankin Scale score 0-2) was observed in 83.3% of the patients (average follow-up time: 37.1 months). None of the treated aneurysm had rebleeding. Angiography follow-up was obtained in 81.7% (58/71 patients; 59/72 aneurysms; average follow-up time, 43.2 months). The overall recanalization rate was 28.8%. No delayed coil or stent migration was found. In-stent stenosis occurred as a delayed complication in one patient. Conclusions: The Neuroform stent-assisted coiling for large and giant intracranial aneurysms is safe and feasible with comparable incidences of morbidity and mortality.


Keywords: Endovascular embolization, giant, intracranial aneurysm, large, the Neuroform stent


How to cite this article:
Gao X, Liang G, Li Y, Wu Z. Neuroform stent-assisted coiling of large and giant intracranial aneurysms: Angiographic and clinical outcomes in 71 consecutive patients. Neurol India 2010;58:825-32

How to cite this URL:
Gao X, Liang G, Li Y, Wu Z. Neuroform stent-assisted coiling of large and giant intracranial aneurysms: Angiographic and clinical outcomes in 71 consecutive patients. Neurol India [serial online] 2010 [cited 2019 Jul 23];58:825-32. Available from: http://www.neurologyindia.com/text.asp?2010/58/6/825/73737



 » Introduction Top


Endovascular coiling of intracranial aneurysms has been increasingly accepted world­wide. The recent publication of a multiple-center randomized trial showing improved safety and clinical outcome in patients treated with endovascular methods as compared with open clipping has accelerated this trend. [1] The results of this trial have increased the number of patients being referred for endovascular treatment and thus further emphasizing the need to enhance the ability to treat intracranial aneurysms effectively. Large (15 - 25 mm in widest dimension) and giant (25 mm or greater in widest dimension) intracranial aneurysms still remain a therapeutic challenge both surgically and endovascularly because of the size, intraluminal thrombosis, calcification, neck dimensions, involvement of perforator arteries, and proximity to cranial nerves and the brainstem. The current endovascular therapeutic approaches include parent artery occlusion, trapping, endosaccular embolization with or without adjunctive techniques such as remodeling technique or stent assisted. However, none of the current strategies is hundred percent successful. The goal of the present study is to report our clinical experience and follow-up results of the use of Neuroform stent (Boston Scientific/Target Therapeutics, Fremont, CA) in patients with large and giant cerebral aneurysms.


 » Materials and Methods Top


This retrospective analysis includes 71 consecutive patients with 72 large or giant aneurysms treated with Neuroform stent-assisted coil embolization at two tertiary referral centers between July 2003 and December 2007. Therapeutic alternatives were discussed between neurosurgical and neurointerventional teams. Informed consent was taken from all the patients, and institutional review board approval was also obtained. The medical records, radiographic studies, and endovascular procedure reports were reviewed. Patient and aneurysm characteristics are shown in [Table 1]. All aneurysms had a wide neck (neck >4 mm). Eleven aneurysms were partially thrombosed, as confirmed on computed tomography (CT) or magnetic resonance (MR) imaging.
Table 1: Patient and aneurysm characteristics


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Endovascular treatment procedures

All procedures were performed under general anesthesia. Patients having unruptured aneurysms were premedicated with antiplatelet therapy, aspirin 300 mg, and clopidogrel 75 mg for three days before the procedure. Patients with ruptured aneurysms were loaded with aspirin 300 mg and clopidogrel 225 mg through nasogastric tube after general anesthesia. All patients received systemic heparinization with activated clotting time at about 300 seconds and continuous intravenous infusion of nimodipine, 2 mg/h to prevent vasospasm during the procedure. In patients having unruptured aneurysms, heparinization was started before puncture, and in patients who presented with acute subarachnoid hemorrhage (SAH), heparinization was started after aneurysm catheterization. A full three- or four-vessel cerebral angiogram was performed to permit a complete evaluation of the aneurysm, to measure the aneurysm neck, width, and height, and also to measure the parent artery proximal and distal to the aneurysm. A 6 F or 8 F sheath was introduced in the right femoral artery following a standard Seldinger puncture. A 6 F or 8 F Envoy guiding catheter (Johnson & Johnson, Miami Lakes, FL) was then guided into either the cervical internal carotid or vertebral artery, depending on the location of the aneurysm. The microcatheters were Prowler plus (Johnson & Johnson, Miami Lakes, FL) or Excelsior SL-10 (Boston Scientific/Target Therapeutics, Fremont, CA).

Twenty-nine aneurysms were treated with sequential technique. The stent delivery system was advanced over a 0.014-inch microwire and positioned until the aneurysm neck is centered between the ends of the stent. Then the stent was deployed to cover the aneurysm neck. After the stent delivery system with the wire was removed, a microcatheter with a preshaped microguidewire was used to enter the aneurysm through the interstices of the stent. Finally, detachable coils were introduced into the aneurysm and detached until occlusion of the aneurysm was achieved.

Forty-three aneurysms were treated with parallel technique. An exchange micro-guide-wire was navigated past the aneurysm into a peripheral branch of the parent artery with the help of a microcatheter; the Neuroform stent delivery system was brought up over the exchange microguidewire to cross the aneurysm neck. Then a microcatheter over a preshaped microguidewire was introduced into the aneurysm. At this time, half deployment technique was used. The stent was deployed to 50 to 60% of its opening, to narrow the aneurysm neck. After the first or second loop of the first coil was placed, the stent was fully deployed. The delivery system was removed and the aneurysm was coiled as usual.

After sufficient packing of the aneurysm, the microcatheter and the exchange micro-guide-wire were pulled back and the final check angiogram was performed. The catheter and sheath were removed, and homeostasis was achieved by use of an artery closure device. The patient was moved to the neurosurgery intensive care unit for monitoring and received low-molecular weight heparin calcium 4000 IU/12 h for the next 48 hours. Clopidogrel 75 mg/day was orally given for an additional 30 days, and aspirin 100 mg/day for six months.

Evaluations and follow-up

The technical feasibility of the procedure, procedure-related complications, angiographic results, and clinical outcome were evaluated. Clinical follow-up data were collected by clinic visits, follow-up angiography, or telephone interview. For patients with ruptured aneurysms, MR-angiography was recommended. For all patients, six-months, one-year, three-year, and five-year follow-up angiogram were recommended. Complications included intraprocedural rupture, thromboembolism, vasospasm, coil protrusion, new mass effect. For each patient, the pre- and postembolization and follow-up (if possible) angiograms were reviewed and compared by two senior endovascular neurosurgeons not involved with the procedure for initial and follow-up occlusion grade. The occlusion grades include class 1: complete occlusion (no contrast filling the aneurysmal sac); class 2: neck remnant (residual contrast filling the aneurysmal neck); class 3: residual flow (residual contrast filling the aneurysmal body). [2] Recanalization was defined as more than 10% increase in contrast filling of the aneurysm; less than 10% increased filling was defined as unchanged. [3] Clinical outcome was graded according to modified Rankin Scale score (mRS): excellent (mRS 0 - 1), good (mRS 2), poor (mRS 3 - 4), and death (mRS 5).


 » Results Top


Technical feasibility and complications

In every patient, the Neuroform stent system was delivered and deployed to the intended location, even with severe vessel tortuousity was present. The wide neck of the aneurysm was accurately and completely covered in all patients. In the patients treated with sequential technique, microcatheter could be navigated through the interstices of the stent without difficulty. Immediate angiography outcome is summarized in [Table 2]. Large aneurysms did not show significantly higher complete occlusion rates compared with giant ones (P > 0.05, Chi-square test). On comparative analysis of ruptured vs unruptured aneurysms, the complete occlusion rate did not show significant difference (P > 0.05, Chi-square test).

Total 11 complications occurred, seven in the anterior circulation and four in the posterior circulation [Table 3]. Procedure-related morbidity was 4.2% and procedural-related mortality was 1.4%.

Thromboembolic events occurred in four patients. The patients were managed with local intra-artery administration of abciximab or urokinase, and mechanical disruption of clot with micro-wire was performed immediately. Complete or partial recanalization was achieved in three patients. Of these patients, one patient recovered completely, one patient developed residual mild neurological deficit but had independent daily activity, and one patient developed left hemiparesis and became dependent. A 58-year-old woman with ruptured posterior communicating artery (PcomA) aneurysm (Hunt-Hess grade I) developed a thrombus in the left internal carotid artery (ICA) terminus at the end of the primary endosaccular coiling procedure. Intra-arterial injection and mechanical disruption failed to open the vessel. Subsequently, mechanical dilation with balloon angioplasty was performed at thrombosed segment, and nearly complete recanalization was achieved successfully. The patient recovered well without any deficit.
Table 2: Immediate angiographic occlusion classification


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Table 3: Procedural-related complications in aneurysms


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Vasospasm occurred in two patients with ruptured aneurysms. One aneurysm was located at left paraclinoid ICA, and the other at basilar tip. They were managed with local administration of nimodipine and papaverine immediately. After the patients were returned to the intensive care unit, standard medical management for vasospasm was continued, including calcium channel blockers, hypertensive, hypervolemic, and hemodilution (3H) therapy. One patient resolved well and had no deficit. In the other patient with ruptured left paraclinoid ICA aneurysm (Hunt-Hess grade III), vasospasm was noted in the left supraclinoid ICA during postprocedure angiography. After immediate management, angiogram showed complete resolution of vasospasm. However, altered level of consciousness occurred 24 hours later after the treatment. CT scan showed left cerebral hemisphere infarction. Cerebral angiography revealed diffused severe bilateral anterior and posterior circulation vasospasm. An emergent decompressive craniotomy was performed. This patient took long time to recover from right hemiparesis and expressive aphasia. He was discharged to a skilled nursing facility. In two patients, while inserting small coils (diameter 2 mm), the last several loops in part protruded through the interstice after detachment. Fortunately, none of these patients developed neurological deficit. In none of the patient coil migration was observed.

Clinical outcome

All 71 patients with 72 treated aneurysms were clinically evaluated. Clinical follow-up was <1 month to 62 months, with a mean of 37.1 months. The mRS score was excellent in 49 patients, good in 11 patients, and poor in six patients at last follow-up. One patient died because of intraprocedural rupture, two patients with acute SAH (Hunt-Hess grade IV) died because of the initial severity of the hemorrhage during hospitalization, and one patient died from other disease. A 73-year-old patient died from contralateral putaminal hemorrhage seven months after discharge. Though he had a history of hypertension for nearly 20 years, posttreatment with antiplatelet might be a precipitating factor. None of the treated aneurysms had rebleeding.

On comparative analysis of ruptured vs unruptured aneurysms, the long-term morbidity rates (mRS, 3 - 4) were 12.8% (5/39) and 3.1% (1/32), respectively. At hospital discharge, mortality rates were 7.7% (3/39) in patients with a ruptured aneurysm and 0% in patients with an unruptured aneurysm; on long-term clinical follow-up, these rates were 10.3% (4/39) and 3.1% (1/32), respectively.

Follow-up angiographic outcome

Follow-up angiography was performed in 58 patients with 59 coiled aneurysms. Angiographic follow-up was obtained from 6 to 62 months, with a mean of 43.2 months. Of the 56 patients, 49 (87.5%) patients had >1-year follow-up. Clinical and aneurysm characteristics of this group of patients are shown in [Table 4]. The main reasons that patients were lost to follow-up were the patients' refusal to return, economical problem, and travel distance.
Table 4: Recanalization rates


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In these 59 angiographically followed aneurysms, the follow-up angiograms of 17 aneurysms (28.8%) demonstrated recanalization [Table 4]. Fifteen of these aneurysms underwent successful re-embolization. The other two patients' angiogram showed an increasing remnant neck at the three-month follow-up examination, but the subsequent follow-up angiogram showed a stable appearance. Therefore, re-embolization was not a treatment option for them. No procedural complications were seen in the re-treatment.

Delayed complications

In the 58 follow-up patients, no delayed coil or stent migration was observed. However one delayed complication occurred. In-stent stenosis was confirmed in a 65-year-old male patient by follow-up angiography, 13 months after the procedure. The 4.5 Χ 15 mm Neuroform stent was deployed in the paraclinoid and communicating segments of right ICA to treat a PcomA aneurysm. High-grade stenosis within the stented segments of right ICA was observed. He suffered from a mild left hemiparesis. In view of the severity of the stenosis and symptoms while on aspirin, balloon angioplasty of the right ICA was performed. Postangioplasty control angiography demonstrated substantial improvement in the caliber and the patient recovered fully [Figure 1].
Figure 1: Three dimensional reconstruction (a) of the right ICA in anteroposterior view demonstrated a posterior communicating artery aneurysm. The Neuroform stent delivery system was brought up over the exchange microguidewire to cross the aneurysm neck. The stent was partly deployed to narrow the aneurysm neck after aneurysm catheterization (b). After the first coil was placed, the stent was fully deployed (c). Postprocedure angiogram (d) revealed complete occlusion. Thirteen-month follow-up angiogram of right common carotid artery (e) revealed high-grade stenosis within the stented segment of right ICA. Contralateral common carotid artery angiogram (f) revealed good compensation via the circle of Willis. Superselective angiogram (g) demonstrated that right ICA was not completely occlusive. Then, balloon angioplasty of the right ICA was performed (h). Postangioplasty control angiography demonstrated substantial improvement in the caliber, but flow to right cerebral anterior artery was still delayed (i).

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 » Discussion Top


The natural history of patients with a large or giant cerebral aneurysm is grim because they are associated with high morbidity and mortality, with two-year survival rates as low as 20%. [4] Treatment is generally considered because of this poor prognosis. Four therapeutic options which are currently available are as follows: surgical clipping, [5] parent-vessel occlusion, [6] the use of a covered stent, [7] and endosaccular embolization with detachable coils. [8] Direct clipping of the aneurysm neck is usually effective. However, risks associated with surgery may be unacceptable in large and giant aneurysms, especially when located in the posterior circulation. A mainstay of endovascular treatment for these lesions is parent vessel occlusion with or without bypass surgery. However, many patients may not tolerate test balloon occlusion (TBO) and thus may not be the candidates for parent vessel occlusion. In addition, there is a 5 to 10% risk of major stroke with associated morbidity and mortality even in patients who tolerate TBO. Exclusion of aneurysms from circulation with preservation of the parent vessel is therefore preferred. The use of covered stents placed across the aneurysm neck proved to be effective and safe, whereas it is not always possible. Selective endosaccular packing of cerebral aneurysms with detachable coils was introduced in the early 1990s. From then on, balloon- and stent-assisted coiling techniques, as well as better coil designs, have greatly improved the ability to coil large and giant aneurysms still preserving the parent vessel. In light of the small number of large and giant aneurysms and the recent evolution of coils and stents, there is limited knowledge about the treatment using all modalities available today. To the best of our knowledge, the Neuroform was the first self-expanding, Nitinol stent, delivered through a micro-catheter, with an open cell design approved for use to treat wide-necked cerebral aneurysms. It has a high degree of elasticity and thermal memory with a radial force adequate to constrain coils within an aneurysm. Till date, several studies have demonstrated the technical feasibility and efficacy of treating complicated intracranial aneurysms. [9],[10],[11] However, as a new device, there is limited knowledge on the long-term effects of the Neuroform stent on the cerebrovasculature.

Previous literature on endovascular coiling indicates that aneurysms with wide necks and larger aneurysms (>10 mm) tend to have lower rates of angiographic occlusion and higher rates of incomplete occlusion or aneurysm recanalization on mid- (6 - 12 months) and late-term (>1 year) follow-up angiography. [10],[11] In our series, the rate of complete and near complete occlusion (class 1 and class 2) was 86.1%, which was much higher than the earlier reports. [8],[12] The follow-up data in our series were also very encouraging. The overall recanalization rate was 28.8%, thus favoring Neuroform stent-assisted coiling. Compared with balloon remodeling, the stent can provide a permanent scaffold across the aneurysm neck to prevent coil protrusion into the parent artery and to alter the dynamics of blood flow and reduce flow into the aneurysm, which may conduce to thrombosis in the aneurysmal sac and prevent delayed coil compaction. In our experience, the use of "semi-deployment technique" during stent-assisted coiling, which means that the stent was deployed up to 50 to 60% of its opening to narrow the aneurysm neck, and then was fully deployed after the first or second loop of the first coil was placed, can help the first, which may provide an anatomically-compliant frame within the aneurysm and a stable scaffold that covers the neck.

In our experience, the stent size and the first coil play an important role. The stent was sized to a nominal diameter of 1.0 mm greater than the parent vessel at the targeted landing zone. The stent length was chosen to provide a 5 mm of extra coverage beyond the aneurysm neck on either side. In our series, the aneurysm was usually first framed by deploying one 3D coil, which may provide an anatomically-compliant frame within the aneurysm and a stable scaffold that covers the neck. The use of "semi-deployment technique," as described above, gives the advantage of optimizing the first coil basket. Sometimes the Neuroform stent may be insufficient to confine coils in an aneurysm because of open cell structure and the low radial force. The combination of stent placement with balloon remodeling was used in one case. This technique has been described elsewhere. [13] According to literature, Wingspan stent instead of the Neuroform may be a better choice. [14]

The goal of aneurysm treatment should be permanent exclusion of the aneurysm from the circulatory system to prevent rupture or rerupture. Aneurysm recanalization must be acknowledged as a failure to achieve this goal. However, not a single treated aneurysm had rebleeding during the follow-up, despite some aneurysms which were incompletely occluded and recanalized. The International Study of Unruptured Intracranial Aneurysms documented a rupture risk of 6.4% for giant aneurysms in the cavernous segment of the carotid artery, 40% in the anterior circulation, and 50% in the posterior circulation over a five-year period. [15] On the basis of these results, it can be concluded that the risk of rupture after occlusion of large and giant aneurysms may be substantially reduced. Aneurysm follow-up angiography and reembolization, if necessary, still should be done, though. We observed 17 (28.8%) aneurysms recanalized on follow-up angiograms, a figure much lower than the earlier studies. In our experience, the recanalization rate of nonstented wide-neck aneurysms is high. A stent placed across the aneurysm neck may prevent recanalization because of the hemodynamic changes and stent endothelialization. The stent is used not only to assist in coil delivery, but also to prevent recanalization; 76.5% (13/17) of the recanalized aneurysms were not completely occluded initially (class 2 or class 3). Therefore, sequential follow-up angiograms are mandatory, especially for those aneurysms showing incomplete occlusion. In our series, no adverse events were shown on follow-up angiograms or occurred during retreatment with detachable coils. The reported complication rates in patients treated for previously embolized aneurysms ranged between 2 and 3%. [16],[17] Follow-up procedures can be done safely, and the risk from retreatment with detachable coils does not negate the advantages of initial use of coil embolization. During initial treatment discussions, patients should be aware that large and giant aneurysms may require multiple treatments and will certainly require a significantly long-term follow-up.

It is also important to note that symptoms of mass effect were resolved or alleviated in 71.4% (10/14) of our patients. Satoh et al., who examined embolization rates by using aneurysm models constructed of glass tubes, showed that the maximum percentage of volumic occlusion was 32.0 to 33.3%, even though the aneurysms were packed as tightly as possible with coils. [18] These results suggest that endosaccular packing is an unlikely cause of symptoms related to mass effect. Most of these symptoms were due to haemodynamic stress and can be alleviated with the shrinkage of aneurysms after embolization. Recently, bioactive coils are a promising technical advancement that may lead to better long-term results. In our series, bioactive and fiber-coated coils were packed in the center part of the aneurysms, which may probably result in thrombogenesis to reduce dead spaces between the coil intertwinings.

In our series, the overall procedure-related complication, morbidity, and mortality were 15.3, 4.2, and 1.4%, respectively, and that of cumulative excellent or good clinical outcome rate was 84.5%, reflecting better outcome than open surgical series. Most of these complications occurred during the initial periods of introduction of this treatment in our center. Thromboembolism is the most common procedure-related adverse event. [19] In the series reported by Qureshi et al., [20] thromboembolism accounted for about half the complications and in the series by Park et al., [21] of the 27 complications, nine were related to thromboembolism. In our series thromboembolic events occurred in four patients, two of whom developed neurologic deficits. Our findings suggest that Neuroform-assisted coiling does not increase the risk of thromboembolism, similar to the earlier observations. [19] This low rate of thromboembolic events could be achieved with adequate heparinization, dual pre- and postoperative antiplatelet therapy, short duration of endovascular manipulation, and sufficient precaution not to introduce embolus into the circulation. Additionally, the use of bioactive coils (e.g. Matrix coil) in conjunction with the stent should be avoided. Partially thrombosed aneurysms can be coiled using the balloon remodeling technique, and then the stent is delivered across the aneurysm neck at the end of the procedure. Once thromboembolic event is observed, local intra-arterial administration of abciximab or urokinase and mechanical disruption of clot with microwire are necessary. Sometimes mechanical dilation with balloon angioplasty can be done. In-stent stenosis is a rare event and may be caused by inflammatory reaction with subsequent intimal hyperplasia. Additional follow-up will be critical to delineate the incidence of this phenomenon.

There are controversial reports about the benefits of the dual antiplatelet therapy. [22],[23] The optimal regimen has not yet been defined. In our practice, dual antiplatelet therapy (aspirin 300 mg and clopidogrel 75 mg) is given for three days before the treatment of unruptured aneurysms. For acutely ruptured aneurysms, antiplatelet treatment (aspirin 300 mg and clopidogrel 225 mg through nasogastric tube) is initiated after general anesthesia. Our posttreatment regimens generally consist of four-week continuation of the dual therapy and then six-month aspirin, unless there are contraindications. We had no preoperative rebleeding by using this protocol in the 39 ruptured aneurysm cases. If there is any evidence that the patient will need ventricular drainage surgery, this should be done before interventional therapy. On the basis of our experience, this might not only prevent fatal increase of intracranial pressure, but might also reduce subsequent bleeding complications if the patient is on anticoagulation and antiplatelet regimen. We believe that the risk of dual antiplatelet therapy should be weighed against the potential benefit, and that antiplatelet and anticoagulation therapy should be tailored according to the results of ongoing researches.

In conclusion, the Neuroform stent-assisted coiling for large and giant intracranial aneurysms is safe and feasible with comparable incidences of morbidity and mortality. Follow-up results are encouraging. The need for retreatment is common, but complications associated with retreatment are few. Nevertheless, additional, large series with long-term follow-up are necessary to determine the durability of these promising results.

 
 » References Top

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23.Katsaridis V, Papagiannaki C, Violaris C. Embolization of acutely ruptured and unruptured wide-necked cerebral aneurysms using the neuroform2 stent without pretreatment with antiplatelets: A single center experience. AJNR Am J Neuroradiol 2006;27:1123-8.  Back to cited text no. 23
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]

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