Introduction The long term effect of Neuroform stent in progressive occlusion of intracranial aneurysms is not yet completely understood. Here the effect of the Neuroform stent in progressive occlusion of intracranial aneurysms and clinical outcome is reported.
Methods Consecutive patients treated with the Neuroform stent from January 2003 to July 2007 were prospectively enrolled. Patients' demographics, immediate and delayed rate of occlusion, and clinical outcomes using the National Institution of Health Stroke Scale (NIHSS) and the Glasgow Outcome Scale (GOS) were recorded.
Results Neuroform stent placement was attempted in 72 patients, including 10 ruptured cases. However, stent placement could not be accomplished in two patients who were not included for analysis. Mean age was 50±14 years and mean aneurysm diameter was 10.28±5.9 mm. Immediate complete occlusion was observed in 31 (44%), neck remnants in 29 (41%) and subtotal occlusion in 10 (14%). Angiographic follow-up was available in 59 cases; complete occlusion was observed in 48/59 (81%), neck remnant in 7/59 (13%) and recanalisation in 4/49 (7%). Of 39 patients with immediate incomplete obliteration, progressive complete occlusions were achieved in 25/31 (81%), no changes in two and recanalisation in four cases. The majority of patients had good outcomes (GOS 1 or NIHSS 0 in 66/70 (94%), GOS 2 or NIHSS 2 in one patient and GOS 3 or NIHSS 4 in three at the 90 day follow-up visit.
Conclusions The Neuroform stent assisted neck remodelling technique improves progressive obliteration of intracranial aneurysms with a low recanalisation rate and good clinical outcome.
- CEREBROVASCULAR DISEASE
- SUBARACHNOID HAEMORRHAGE
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Stent assisted coiling to overcome the challenges of current endovascular therapy has been discussed in small series1 2 and requires further evaluation to understand the long term effect of stent on durable occlusion of aneurysm. The mainstream use of balloon mounted coronary stents has been limited due to their high profile nature and lower flexibility, poor navigation capabilities in the tortuous cerebral blood vessels and the potential risk of vessel dissection, rupture and delayed stenosis.3–6 To minimise these barriers, the industries have subsequently shifted their focus to develop a self-deployable stent which is flexible enough to navigate through the tortuous cerebral architecture and strong enough to hold its configuration when a coil mass is encountered. The Neuroform stent (Boston Scientific Target, Fremont, California, USA) composed of a nickel–titanium alloy (nitinol) possessing a high degree of elasticity and deformability, was approved by the Food and Drug Administration for compassionate use in the treatment of wide necked aneurysms. Recently, a new intracranial stent ‘Enterprise’ (Cordis Neurovascular, Miami, Florida, USA) has also been approved by the Food and Drug Administration for compassionate use in the treatment of wide necked aneurysms. This study will only focus on the Neuroform stent in the treatment of intracranial aneurysm. It is our hypothesis that Neuroform stent treated patients will continue to demonstrate progressive occlusion of aneurysm after the initial treatment is completed. The primary objective of our study is to determine the rate of progressive occlusion of aneurysm in patients who underwent Neuroform stent assisted treatment of intracranial aneurysm. The secondary objective is to determine the clinical outcome (90 days or more) of patients treated with the Neuroform stent.
Patients undergoing placement of a Neuroform stent for the treatment of an intracranial wide necked and fusiform aneurysm were registered in a prospectively maintained database. From this database, consecutive patients who underwent Neuroform stent assisted coiling of an intracranial aneurysm were selected and the data were retrospectively analysed. Institutional Review Board approval was obtained prior to the treatment and retrieval of the data. During our study period, 355 patients with a diagnosis of intracranial aneurysm (unruptured 201, ruptured 154) were treated in our institution, of which 72 patients (wide necked 67, fusiform five) underwent attempted treatment with the Neuroform stent for their intracranial aneurysm. Of the 72 patients included, 62 were unruptured and 10 were ruptured. The decision of surgical clipping versus endovascular Neuroform stent assisted treatment of the aneurysm was made on agreement between a vascular neurosurgeon and a neuroendovascular specialist. To evaluate the rate of progressive occlusions, patients who underwent successful stent assisted coiling were included for analysis. Among patients with a ruptured aneurysm, the clinical severity of the subarachnoid haemorrhage was assessed using the Hunt and Hess grade and the radiographic grade was measured using the Fisher scale. The outcomes were predefined on the basis of radiographic and clinical criteria. The radiographic outcomes were defined as immediate occlusion (complete occlusion (100%), near complete occlusion or neck remnant (>95% but <100%) or subtotal occlusion <95%). The clinical outcomes were measured using National Institute of Health Stroke Scale (NIHSS) and the Glasgow Outcome Scale (GOS). Outcome was defined as good if the obtained GOS was 4 or higher and NIHSS 2 or less within 90 days or at a later follow-up visit for the ruptured aneurysm. For the unruptured aneurysm patients, a GOS of 5 was considered as a good outcome.
Wide necked aneurysms were defined as having a dome to neck ratios <2 or a neck >4 mm in diameter. An intracranial aneurysm was defined as fusiform if the aneurysm had an out pouching dilatation of the parent blood vessel affecting at least 270° of circumference of the lumen and had no discernible neck. All patients with unruptured aneurysms who received the Neuroform stent were treated with both aspirin 325 mg/day and clopidogrel 75 mg/day at least 5 days prior to their treatment. Patients were continued on both aspirin and clopidogrel daily for 4 weeks after the stenting procedure and thereafter on daily 325 mg aspirin alone.
For the unruptured aneurysms, some of the aneurysms were indented to treat in a single setting and some were indented to treat in a staged manner. Therefore, aneurysms that were not coiled completely were subsequently coiled in order to complete the procedure. The rate of progressive occlusion was evaluated when the procedure were considered completed.
For wide necked ruptured aneurysms, the stenting procedure was modified due to the risk of aggressive antiplatelet therapy and anticoagulation required for the procedure. In these instances, an attempt to secure the aneurysm by coiling alone was initiated first followed by Neuroform stent assisted coiling in 4–6 weeks from the initial procedure and these aneurysms were defined as residual aneurysms. Those wide neck aneurysms that could not be coiled safely underwent stent assisted coiling to occlude the aneurysm. In all patients who required ventricular drainage due to the presence of hydrocephalus, the ventricular catheter was placed at least 6 h prior to the procedure and administration of antithrombotic medications to prevent potential bleeding complications associated with ventriculostomy was performed. We also avoided postoperative routine anticoagulation in subarachnoid haemorrhage patient to prevent potential bleeding complications associated with ventriculostomy catheter.
All patients with the diagnosis of a wide necked aneurysm or fusiform aneurysm were enrolled. Based on the result of the International Study of Unruptured Intracranial Aneurysms Investigators, we have empirically chosen 7 mm as our cut-off for the unruptured intracranial aneurysm. Predefined exclusion criteria were active bleeding diatheses and/or a platelet count <100 000/dl.
Stent assisted coiling techniques have been previously described by the authors.7 8 Baseline serum activated coagulation time was obtained and intravenous heparin was administered to achieve activated coagulation time between 1.5 and 2 times the baseline value. A 6 F guiding catheter (Boston Scientific Target, Fremont, California, USA) which was flushed with continuous heparinised saline was placed in the proximal part of the vessels of interest (internal carotid, vertebral artery) under the direct guidance of fluoroscope and roadmaps. The aneurysm was crossed with a microcatheter (SL 10, Boston Scientific Target, Fremont, California, USA) and a microwire (Synchro 14, Boston Scientific Target, Fremont, California, USA, or Transcend 14, Cordis, Miami, Florida, USA). The microcatheter was swapped with an exchange length microwire (X-celerator 300 cm, eV3, Irvine, California, USA). The Neuroform stent delivery system was prepared and advanced over the exchange length microwire as a unit and subsequently deployed across the neck of the aneurysm. Recently, the authors have begun to use a direct approach in which a 200 cm 0.014 compatible microwire was back loaded through the stent delivery system and then the stent delivery system was advanced as a unit through the guiding catheter. To cover the neck of the aneurysm adequately, the stent was deployed at least 4 mm proximal and 4 mm distal to the neck on the parent artery. The aneurysm was catheterised by a direct approach in which the microcatheter was advanced through the cells of the Neuroform stent. The angiographic and clinical follow-up was planned for each patient at 3, 12, 18 and 36 months.
A database was created and maintained for all patients treated with a Neuroform stent for intracranial aneurysms in a tertiary care facility. Consecutive patients who underwent treatment of intracranial wide necked aneurysms using nitinol self-expandable stents from January 2003 to September 2007 were enrolled in this study for analysis. Patient demographics, including age, race, gender, cardiovascular risk factors, locations of aneurysms and types of aneurysms were collected. Long term (12–24 months) angiographic follow-up data, including the rate of immediate and delayed aneurysm occlusion, were retrieved. Additionally, 12–24 months of clinical outcomes using the NIHSS and GOS (including an angiographic outcome) were documented.
All data were analysed with SAS for Windows software V.9.1.3 (SAS Institute Inc). Categorical data were analysed using Fisher's exact test or χ2 tests as appropriate. Continuous data with normal distribution were reported as mean±SD and analysed with the Student's t test while those with non-normal distribution were reported as median (IQR) and analysed with the Wilcoxon two sample test.
Neuroform stent placement was attempted in 72 patients, including 10 ruptured and five fusiform aneurysm cases. However, stent placement could not be accomplished in two patients. These patients later went on to receive surgical clipping, leaving 70 patients for inclusion in the present analysis. A total of 72 Neuroform stents were utilised to repair 70 intracranial aneurysms, of which two patients (one basilar artery (BA) bifurcation aneurysm and other middle cerebral artery bifurcation aneurysm) required an additional stent. Mean age of the patients was 50±14 years; 60/70 (86%) were female; 57/70 (81%) were white; and 11 (16%) were African American. For detailed demographics, clinical characteristics, aneurysm size and location please see table 1.
Immediate complete occlusion was observed in 31 (44%) patients; neck remnants in 29 (41%); and subtotal occlusion in 10 (14%). On follow-up (12–36 months) angiography, complete occlusion (figures 1A,B and 2A–C) was observed in 48/59 (81%) patients, neck remnant in 7/59 (13%) and recanalisation in 4/59 (7%) (two posterior communicating artery (PcomA) with prior neck remnant, one BA bifurcation and one internal carotid artery (ICA)–cavernous with prior subtotal occlusion). Of 31/39 patients with immediate near complete or subtotal aneurysm occlusion, progressive complete obliteration of the aneurysm was observed in 25/31 (81%) patients, no changes in two and recanalisation in four cases. Regarding five fusiform aneurysms, four required stenting and coiling and one required stenting only. In the follow-up angiogram, three achieved complete occlusion, one near complete and one subtotal occlusion. Four patients with recanalised aneurysms (PComA two, BA bifurcation one, ICA–cavernous one) underwent further coiling of their aneurysms, two of which achieved complete aneurysm occlusion (PComA two), neck remnant in one (BA bifurcation) and subtotal occlusion in one (ICA–cavernous). Patient age, gender, cardiovascular risk factors, including the size and shape of the aneurysm, were not predictors of aneurysm occlusion.
The 90 day follow-up clinical data were available for all patients. GOS 1 or NIHSS 0 was observed in 66/70 (94%) cases. GOS 2 or NIHSS 2 was observed in one patient who had a prior disability from a ruptured aneurysm. GOS 3 or NIHSS 4–6 was observed in three other patients—two presented with Hunt and Hess III and Fisher 4 and the third patient had symptomatic unruptured BA trunk giant aneurysm with a pretreatment NIHSS of 6 and no worsening of symptoms after treatment.
Long term follow-up of 59 patients ranging between 12 to 36 months showed no incidence of rupture of the aneurysms and lasting good clinical outcome, as measured by GOS or NIHSS.
This study provides the longest long-term follow-up of Neuroform stent assisted treatment of intracranial aneurysms to date. Our study revealed that the Neuroform stent not only allowed us to safely treat wide necked and fusiform intracranial aneurysms with an endovascular approach but also improved delayed aneurysm occlusion (figures 1A,B and 2A–C). Long term clinical outcome, as measured by GOS and NIHSS, continued to be good in this series. In addition, there was no incidence of interval aneurysmal rupture.
Early experiences with regard to immediate occlusion of aneurysms with the Neuroform stent have been described in previous studies.1 9–11 However, only two studies12 13 provided long term (3–24 months) angiographic and clinical outcomes.
Initial 3–6 month follow-up data for Neuroform stent assisted coiling of aneurysms have been published in a recent article.12 In that study, 64 patients with 74 aneurysms were treated with 86 Neuroform stents. Immediate complete or near complete occlusion (>95%) was achieved in 28 (45.9%) and partial (<95%) occlusion was achieved in 33 (54%) cases. Follow-up data were compiled either by digital subtraction angiography (n=43) or by MR angiography (n=5) in 48 patients. Progressive thrombosis was observed in 25 (52%), recanalisation of the aneurysm occurred in 11 (23%) and no change in the previous rate of occlusion was observed in 12 (25%) patients.12
In another study,13 3–24 months of follow-up results showed that 42 patients with 46 wide necked intracranial aneurysms were treated with 47 Neuroform stents. Immediate complete occlusion was observed in 14/40 (35%) aneurysm, neck remnants in 18/40 (45%) and residual aneurysm in 8/40 (20%). On follow-up angiogram, completed occlusion was observed in 17/30 (57%) aneurysms, neck remnants in seven (23%) and residual in six (20%). The rate of progressive aneurysm occlusion was not clearly described but the progressive occlusion of aneurysm was observed in the range 45% –80%.13
The rate of immediate complete and near complete occlusions of aneurysms in our study was comparable with published studies,9–12 indicating the reproducibility of Neuroform stent assisted treatment of these complex aneurysms.
Definitive data on the long term effect of Neuroform stent use on progressive occlusion of aneurysms are not yet available to enable us to compare our study with others. Our study demonstrated a higher rate of progressive occlusion of aneurysms compared with a recent study12 where an initial 3–6 months of radiographic data were provided. The rate of recanalisation also appeared to be less in our study compared with that study.12 When our study is compared with a recent study13 where the follow-up was available for 3–24 months, the results are very similar. The duration of long term follow-up may well be a contributing factor to the differences in the rate of progressive obliteration of aneurysms among studies.12 13 It is our hypothesis that endothelialisation of the stent improves over time leading to better remodelling at the inflow zone of the aneurysm, resulting in reduction of blood flow into the aneurysm. The longer follow-up period may also have provided enough time for the formation of stable scar tissue inside the aneurysm and therefore better obliteration.
The mechanism of delayed improved occlusion (figures 1A,B and 2A–C) with Neuroform stent coiling may also be due to the technical and physiological properties of the Neuroform stent itself. Firstly, the stent provides durable protection of the parent vessel, especially in the case of broad necked or giant aneurysms. The stent also practically facilitates more complete packing of the aneurysm.9 Secondly, the stent redirects flow, disrupting the aneurysm inflow and outflow zones and resulting in ‘haemodynamic uncoupling’ of the parent vessel–aneurysm complex.9 Subsequently, the flow within the aneurysm becomes disordered, facilitating aneurysm thrombosis and coil compaction in the inflow zone. Thirdly, a stent provides a physical matrix for endothelial growth, promoting remodelling of the aneurysm neck as well as the parent vessel. It is our opinion that in this way stenting not only treats the aneurysm but also treats the diseased parent artery.9 These properties are valuable in the treatment of fusiform and dissecting aneurysms in which the goal is not only to achieve aneurysm thrombosis but also, and more importantly, to reconstruct the parent artery.
The limitation of our study is that this is not a randomised case controlled study and the number of cases may not be large enough to draw any definitive conclusion on predictors of progressive occlusion of an aneurysm.
In conclusion, stent assisted techniques may not only facilitate the treatment of complex difficult intracranial aneurysms but, more importantly, improve progressive durable occlusion of an aneurysm. A long term follow-up study with an intracranial stent might potentially further determine the effect of stent on durable occlusion of intracranial aneurysms.
Competing interests None.
Ethics approval This study was conducted with the approval of the Providence Hospital, Michigan and Upstate Medical University.
Provenance and peer review Not commissioned; externally peer reviewed.