La radiologia medica https://doi.org/10.1007/s11547-018-0857-8
NEURORADIOLOGY
Long‑term follow‑up in the endovascular treatment of intracranial aneurysms with flow‑diverter stents: update of a single‑centre experience Giuseppe Guzzardi1 · Carmelo Stanca1 · Paolo Cerini1 · Bruno Del Sette1 · Ignazio Divenuto2 · Emanuele Malatesta3 · Alessandro Carriero1 · Alessandro Stecco1 Received: 13 October 2017 / Accepted: 18 January 2018 © Italian Society of Medical Radiology 2018
Abstract Introduction Flow-diverter stents are becoming a useful tool in treating patients with intracranial aneurysms with suitable anatomical feature. Purpose of this study was to evaluate effectiveness and safety of endovascular treatment with flowdiverting stents (FD) in unruptured intracranial aneurysms. Methods From May 2009 and May 2014, we treated 49 patients with a total of 58 aneurysms, with FD technique. All patients were treated electively, under general anesthesia and were administered single antiplatelet drug 5 days before the procedure and double antiplatelet therapy for 3 months afterwards. Fifteen of the patients were asymptomatic, eight had headache, thirteen patients presented symptoms due to mass effect of the aneurysm on CNS structures, twelve were treated due to a post-surgical relapse and one patient presented relapsing TIAs due to distal embolization from the aneurysm dome. Choice of FD treatment was done according to aneurysm anatomy (fusiform over saccular, dome/neck ratio < 2) and whenever conventional treatment (coil embolization) appeared difficult (eg. Large aneurysm neck, fusiform aneurysms or difficult sac catheterization). We considered a dome/neck ratio > 2 as the only exclusion criteria. Results Successful stent deployment was achieved in 50 procedures out of 52 (94.34%) while overall mortality was 2% (1/49). Forty-eight patients were evaluated at long-term follow-up for a total of 56 treated aneurysms. At 3 months, follow-up 75% (42/56) of the aneurysms were excluded from intracranial circulation, at 6 months 80.35% (45/56) and at 12 months 84% (47/56). Stent patency was observed in 100% of patients at short and long-term follow-up, with only two cases of intimal hyperplasia at 3 months, without any further complications. Conclusions According to our study FD repair of unruptured intracranial aneurysms appeared to be a safe and effective technique, especially in selected patients with hostile anatomy for traditional embolization. Keywords Flow-diverter stent · Intracranial aneurysm · Endovascular treatment
Introduction
* Giuseppe Guzzardi
[email protected] 1
Unità di Radiologia Interventistica, SC Radiodiagnostica, Azienda Ospedaliero-Universitaria “Maggiore della Carità”, Corso Mazzini 18, 28100 Novara, Italy
2
Unità di Neuroradiologia, Istituto Humanitas, Rozzano, MI, Italy
3
UOC Neuroradiologia, Ospedale Maurizio Bufalini, Cesena, Italy
Cerebral aneurysms are a dilatation of an artery’s wall [1], usually due to focal weakness of the vessel, where high blood flow pressure cause the artery to expand [2]. Intracranial aneurysms affect 5% of the population, but only a small percentage shows symptoms due to mass effect, distal thrombosis or has a subarachnoid hemorrhage (SAH) due to aneurysm rupture [3]. In Willis circulation [4, 5], aneurysms are located in preferential sites: anterior communicating artery (20–50%), internal carotid artery, especially in the supraclinoid tract (15–20%), posterior communicating artery
13
Vol.:(0123456789)
(15–20%), middle cerebral artery (15–20%) and vertebrobasilar circulation (10%). We can distinguish two different types of aneurysms: “saccular” (accounting for 90% of aneurysms) which are a focal dilatation of the vessel with a distinguishable neck, or “fusiform”, which present a diffuse dilatation of the whole artery without any recognizable neck. According to the aneurysm size [4], we can distinguish four different types of aneurysms: small (5–7 mm), medium (7–10 mm), large (10–25 mm) or giant (> 25 mm). According to ISUIA study (International Study of Unruptured Intracranial Aneurysms) [5], the risk of rupture of unruptured intracranial aneurysms varies according to aneurysm dimensions and localization in Willis circulation, with higher chance of rupture in large/ giant aneurysms of posterior circulation. Intracranial aneurysms can be treated with either neurosurgical or endovascular approach. According to recent studies, neurosurgical treatment should be preferred in young patients, with aneurysms located in the anterior circulation and with low surgical risk [6]; surgical treatment, although more invasive, is usually definitive [6–8] with lower chance of relapse in aneurysm neck region (1.5–8%), affected by a morbidity of 20–22% and mortality of 8–10%. Endovascular treatment can be achieved with different kinds of approaches and techniques such as 1. Unassisted coiling [9, 10] using detachable metallic spirals to cause embolization of the aneurysms, 2. Remodeling technique [11, 12], which requires inflation of a high-compliant balloon in front of aneurysm’s neck during the deployment of metallic spirals inside aneurysm’s dome, to obtain a better filling of the aneurysm and reduce chances of relapse. 3. Intracranial stenting [13], which is preferred to treat large neck aneurysms to avoid spiral migration after detachment. 4. ONYX® embolization ( Medtronic®, Fridley MN, USA) [14], mainly used for large or giant aneurysms with wide neck; a liquid embolic agent made of Ethylene Vinyl Alcohol Copolymer is injected inside the aneurysm’s sac to obtain a complete occlusion. 5. Parent artery occlusion [15] which could be achieved with different materials such as spirals, balloons or liquid embolic agents to treat mainly giant aneurysms with wide neck and impossibility to spare the vessel; 6. Flow diversion stenting used to treat large, giant, fusiform or large-necked intracranial aneurysms, which, if treated with traditional endovascular technique, have a high rate of relapses and periprocedural complications. The aim of this treatment is reconstruction of the parent
13
La radiologia medica
artery wall, creating a biological seal to the aneurysm [16, 17]. After FD stent deployment, different degrees of contrast stasis are witnessed at angiographic controls; usually aneurysms progress to a complete thrombosis within 12 months with complete wall reconstruction, nevertheless the rate at which this process happens is hard to predict [17]. As reported in the literature and case series of patients treated with FD stenting, an antiplatelet therapy is necessary before and after the deployment of the device, increasing risk of hemorrhagic complications. Therefore, the use of these stents is greatly limited in patients that must be treated in emergency settings due to a subarachnoid hemorrhage; safety of these stents in this kind of patient is still to be assessed [18]. Our study is a retrospective analysis of patients with unruptured intracranial aneurysm, treated with flow diversion technique in our Interventional Radiology Department; we reviewed our data collected over 5 years of activity to assess the device effectiveness, safety and midterm followup results in treating unruptured intracranial aneurysms.
Materials and methods We retrospectively evaluated 49 patients, who underwent endovascular treatment with FD stenting for unruptured intracranial aneurysms from May 2009 and May 2014. A total of 59 aneurysms were treated. Indication of FD stenting was given according to aneurysm morphology (fusiform over saccular), the absence of a narrow neck (dome/neck ratio < 2) and whenever traditional endovascular approach (such as unassisted or assisted coiling) appeared difficult due to complex vascular anatomy resulting in difficult sac catheterization (Table 1). Exclusion criteria for the treatment were the presence of a narrow neck (dome/neck ratio > 2). The evaluation of anatomical characteristics of the aneurysms was performed with CT-Angio, using a 64 slice CT Lightspeed VCT 64 (GE®, Boston MA, USA) and/or Angio-MRI using an Achieva 1.5T ( Philips®, Amsterdam, NL), using TOF and/or CE-MRA techniques; since 2012 all preoperative evaluations were performed with MipPR reconstruction to better analyze vessel anatomy. Until 2012, procedures were executed with monoplane angiography Integris 5000 V (Philips®, Amsterdam, NL.), and since 2013 we performed 3D-RA with monoplane angiography Allura Xper Fd 20 (Philips®, Amsterdam, NL.). All patients were treated while under general anesthesia and with a unilateral femoral approach. We used four different types of FD stents, for a total of 68 stents, 55 PED (51 Pipeline-PED and 4 Pipeline-PED Flex; EV3®,
La radiologia medica Table 1 Characteristic of treated patients Characteristic of treated patients Total # of patients Sex (M/F) Total # of aneurysm Age range (mean) Clinical manifestations Headache Mass effect with cranial nerve deficit No symptoms Transient ischemic attacks Relapses Aneurysm location Internal carotid artery-ophthalmic segment Internal carotid artery-cavernous segment Internal carotid artery-clinoid segment Internal carotid artery-communicating segment Vertebrobasilar circulation Anterior communicating artery Middle cerebral artery Aneurysm dimensions: Small (5–10 mm): 35 (60%) Large (11–24 mm): 18 (30%) Giant (> 25 mm): 5 (8.4%) Aneurysm morphology: Saccular Fusiform
49 15/34 59 24–83 (54.3) 8/49 (16.4%) 13/49 (26.5%) 15/49 (30.6%) 1/49 (2%) 12/49 (24.5%) 14/58 (24%) 9/58 (15.5%) 11/58 (19%) 11/58 (19%) 7/58 (12%) 4/58 (7%) 2/58 (3.5%) 35/58 (60.4%) 18/58 (31%) 5/58 (8.6%) 46/58 (79.3%) 12/58 (20.7%)
Irvine, CA-USA), 9 SILK (Balt®, Montmorency, France) 2 P64 (Phenox G mbH ®, Bochum, Germany), 2 FRED ® (Microvention , Tustin, CA-USA). All patients were treated electively; informed consent was obtained from all individual participants included in the study. After deployment of the stent, a series of angiographic controls was performed to assess technical success (evaluated as complete coverage of aneurysm neck and correct expansion of stent inside the vessel), after 2013 we always acquired 3D-RA images after stent deployment; all patients underwent a non-contrast CT scan at the end of the procedure to exclude cerebral hemorrhages. All patients were treated with ticlopidine 250 mg × 2 daily or clopidogrel 75 mg daily 5 days before the procedure; during the procedure, we administered heparin (50 UI/kg + 1000 UI/h) and acetylsalicylic acid 500 mg after stent deployment. After the procedure, all patients were treated with ticlopidine 250 mg × 2 daily or clopidogrel 75 mg daily and acetylsalicylic acid 300 mg daily for 3 months; from the third to the sixth months after the procedure, patients were
treated with only acetylsalicylic acid 300 mg daily. No antiplatelet resistance test was performed at our Institution. All patients underwent CT-Angio study at 3–7 days after the treatment to assess deployment and stability of the device. Follow-up was performed at our Institution provided Digital Subtraction Angiography (DSA) at 3, 6, 12 and 24 months after the procedure (Fig. 1), replaced by CTAngio, whereas the patient could not perform or refused to undergo the invasive examination. Aneurysm filling and contrast stasis at follow-up DSA were evaluated with the O’Kelly-Marotta (OKM) grading scale [19], which has been reported to have good intra- and interobserver agreement [20]. At each angiographic control, every treated aneurysm was graded with a letter according to the initial degree of filling (A: total filling, B: subtotal filling, C: entry remnant, D: no filling) and with a number which represents the degree of stasis observed through the angiographic phases (1: stasis in arterial phase, 2: stasis in capillary phase, 3: stasis in venous phase). We considered a complete occlusion as a grade D aneurysm. Clinical evaluation was performed at baseline before the procedure, at discharge and at each angiographic control with modified Rankin Scale (mRS). We analyzed different parameters as primary outcome, according to the literature: aneurysm occlusion, stent patency, patency of the covered vessel and of collateral branches as secondary outcome we evaluated short-term mortality, long-term morbidity with mild or severe deficit at follow-up.
Results We performed a total of 52 procedures in 49 different patients; two patients required a second treatment at 3 months due to incomplete coverage of the neck, one patient was retreated due to disease progression at 6 months. The mean age of the population was 54.3 years (range: 24–83 y.o.) (Table 1). Fifteen of the patients were asymptomatic and aneurysm diagnosis was incidental (30.6%), eight had headache (16.4%), thirteen patients presented symptoms due to mass effect of the aneurysm on CNS structures (26.5%), twelve were treated due to a post-surgical relapse (24.5%) and one patient presented relapsing TIAs with temporary neurologic dysfunctions due to distal embolization from the aneurysm dome (2%) (Table 1). Most aneurysms (51/58; 87.9%) were located in the anterior circulation (45 in the internal carotid artery, 4 in the anterior communicating artery and 2 in the middle cerebral artery) while only 12.1% of them (7/58) were located in posterior circulation (Table 1). Mean aneurysm size was
13
La radiologia medica
Fig. 1 DSA imaging of a large saccular aneurysm of the ophthalmic tract of right internal carotid artery with wide neck: a imaging before the procedure, b angiographic image after stent deployment, (c, d)
Angiography at 3 months in lateral and A-P views: the aneurysm is completely excluded (grade D of OKM scale)
12.7 mm (range, 6–40 mm) (Table 1). Regarding aneurysm morphology, 46 of 58 (79.3%) were saccular and 12 of 58 (20.7%) were fusiform (Table 1). Successful stent deployment was achieved in 50 of 52 procedures (96.15%); no additional endovascular treatment (such as deployment of coils inside aneurysm dome or balloon angioplasty inside the stent) was performed. Procedural complications occurred in only one case, in a patient that was being treated for middle cerebral artery aneurysms with
Pipeline-PED (1/49; 2%). Due to an incorrect opening of the distal end of the stent, a distal migration of the device occurred. We performed various attempts of retrieving the stent using Alligator Retrieval Device (EV3®, Irvine, CAUSA), although unsuccessful, with perforation of middle cerebral artery; CT scan performed after the procedure showed the presence of SAH associated with a large intraparenchymal hematoma and severe midline shift leading to the death of the patient 24 h later. In the other case of failure
13
La radiologia medica
of stent deployment, the length of the device was underestimated, therefore, it was not possible to achieve complete coverage of the aneurysm neck; stent was then retrieved before deployment and was replaced with a longer device with a good final angiographic result. Short-term morality was 2% (1/49). We enrolled a total of 48 patients in our follow-up, for a total of 56 treated aneurysms, follow-up ranged from 12 to 40 months with a mean follow-up time of 33 months. We registered a complete occlusion at 3 months in 75% of the aneurysms (42/56), at 6 months in 80.35% (45/56) and at 12 months in 84% (47/56). Out of the forty patients, which had an angiographic follow-up at 3 years, we registered a complete occlusion in 90% of the aneurysms (38/42) (Table 2). The other four patients (treated with two Pipeline-PEDs, one SILK and one FRED) had a delayed and partial opacification of the aneurysm’s dome confirming a partial thrombosis of the sac [19, 20] (Table 3). Patients who showed an unchanged perfusion of the aneurysm during follow-up were retreated (grade 1A of OKM scale); two patients, both treated with Pipeline-PED for Giant aneurysm of ICA, were retreated at 3 months due to an incomplete coverage of the neck. Only one, treated with SILK for a fusiform aneurysm of ICA, was retreated at 6 months due to disease progression at the proximal end of the FD. In our series, no cases of spontaneous aneurysm recanalization were found during follow-up DSAs; in only one patient we witnessed progression of the disease. No aneurysm rupture was registered in our patients during follow-up. In all the cases evaluated at follow-up, a complete stent patency was witnessed at 3, 6 and 12 months, without any signs of intra-stent thrombosis. Two patients presented a mild intimal hyperplasia, without signs of hemodynamic stenosis or clinical symptoms, one was treated with Pipeline-PED stent while the other with SILK. Both patients received double antiplatelet therapy (clopidogrel 75 mg daily and acetylsalicylic acid 300 mg daily) up to 6 months and single antiplatelet drug (acetylsalicylic acid 300 mg daily) up to 12 months, obtaining a complete stent patency at follow-up without registering any hemorrhagic
Table 3 OKM scale follow-up
IA IB IC IIA IIB IIC IIIA IIIB IIIC
3 months
6 months
12 months
2a 1 4
1a
4
1 4
1 5
2 42
2 45
2 47
2
a
Retreated patients
complications. Both patients presented a complete occlusion of the aneurysm at 12 months, suggesting that prolonged antiplatelet therapy does not affect significantly aneurysm occlusion rate. In only one patient, treated for an aneurysm of ICA at cavernous tract with Pipeline-PED, we registered a partial reduction of caliber of the ophthalmic artery at 6 months follow-up, with occlusion of collateral orbital vessel, causing a mild symptomatology (scotoma); these findings were present also at 12 months (Table 2). Four patients, treated due to the presence of giant or large aneurysm causing mass effect symptoms, presented mild and temporary worsening of the symptoms, with complete remission of the symptoms at 12 months. One patient, treated with Pipeline-PED Flex for a giant basilar aneurysm, had a severe worsening of the symptoms 4 months after the treatment, without registering any complications at angiographic and MRI controls. Longterm morbidity, with permanent deficits at follow-up, was 4% (2/48) (Table 4). Long-term mortality due to aneurysm related causes and intracranial bleeding was 0% at follow-up.
Table 4 Complications, morbidity and mortality Table 2 Primary outcomes
Complications, morbidity and mortality
Primary outcomes Aneurysm occlusion (OKM scale grade D): At 3 months At 6 months At 12 months at 3 years Parent vessel patency at 12 months Collateral vessels patency at 12 months Stent patency at 12 months
75% (42/56) 80.35% (45/56) 84% (47/56) 90% (38/42) 100% (48/48) 98% (47/48) 100% (48/48)
Technical procedural complications Parent vessel thrombosis Ischemic complications Hemorrhagic complications Short-term mortality Long-term morbidity Collateral vessel occlusion with scotoma Mass effect symptoms Long-term mortality
1/49 (2%) 0/49 (0%) 0/49 (0%) 1/49 (2%) 1/49 (2%) 2/48 (4%) 1/48 (2%) 1/48 (2%) 0/48 (0%)
13
Discussion Flow-diverting stents are an important evolution of endovascular approach for the treatment of intracranial aneurysms, shifting the aim of the procedure from occluding the aneurysm’s dome to repairing the parent vessel wall [17, 21–24]. When comparing “traditional” endovascular techniques with FD stenting, we must take into account that the literature data regarding conventional endovascular embolization are results of over 30 years of studies and publications, while FD stents are quite new devices; therefore, the literature data available were collected on preliminary experiences [25–28]. Even though our study presents some limitations, such as the restricted number of patients treated and the retrospective evaluation of the collected data, our results are in agreement with the ones reported in the current FD literature [21–24], which show how FD stenting for intracranial aneurysms is a safe and effective treatment (especially in large necked and fusiform aneurysms) granting a high percentage of occlusion of the dome, with low risk of complications [25–27]. A recent meta-analysis of 18 studies from Briganti F et al [29] reported how FD stenting of intracranial aneurysms presents a good rate of aneurysms occlusion with low incidence of major complications (ranging from 0–23.1%, with mean incidence of 8.3%) such as occlusion or severe intra-stent stenosis, ischemic complications and hemorrhagic complications. Mortality rate was also reported ranging from 0.5 to 8% (mean rate 3.4%); permanent morbidity related to the procedure was reported, with a mean rate of 3.5%. (range 1–15%). Complication, morbidity and mortality rates reported in our study were comparable to the one reported in the meta-analysis. Thrombosis of the aneurysm is a gradual and predictable result of correct FD deployment; therefore, when treating large or giant aneurysms causing mass effect symptoms, this phenomenon could lead to a temporary worsening of the symptoms, due to an increased compression of surrounding CNS structure. Only after complete occlusion of the dome, we witnessed shrinking of the aneurysm, but this effect seemed still unpredictable and uncontrollable. Bhogal et al [30] recently reported a large case series of patients treated with FD stenting, and analyzed the rate of partial or complete occlusion occurring in side branches covered by the device. Side branch occlusion rate reported in their study was 20%, with a higher incidence for posterior communicating arteries (42.6%), anterior cerebral arteries (14.3%) and ophthalmic arteries (5.3%); reduction of vessel caliber was witnessed in the same arteries with an higher prevalence in anterior cerebral arteries (42.9%).
13
La radiologia medica
In our case series, we only reported one case of branch caliber reduction (1/56, 2%) involving the ophthalmic artery and causing occlusion of collateral orbital vessel. The OKM scale grading system [19] is a viable tool to assess the degree of aneurysm filling and contrast stasis, and it helps understanding the rate at which the aneurysm thrombosis occurs in different patients. In our case series, even though complete occlusion was not witnessed in all patients, we could see how each aneurysm progressed of grade at different DSA controls. This finding could hint that the process of aneurysm thrombosis, even if delayed, is always present after the deployment of FD stents; moreover, the high rate of inter- and intra-observer agreement helps in evaluating aneurysm thrombosis evolution since controls are not always performed by the same operator [20]. Since our study reported a few number of cases treated with different kind of stents, we could not obtain homogeneous groups to assess whether aneurysm exclusion was faster and more definitive with one brand than with another. Overall, all kinds of stent deployed achieved good results in a high percentage of treated patients without any significant differences between them. A recent research from Faught et al. [18] reported how current practice regarding antiplatelet therapy after intracranial stent deployment is heterogeneous, and in the literature, there is a lack of clinical trials that compare different medications for this kind of patients and procedure. Most common treatment regimen for patient undergoing elective treatments was acetylsalicylic acid 325 mg and clopidogrel 75 mg daily (for 7 days before the procedure), while for maintenance regimen treatment the most common association was acetylsalicylic acid 325 mg daily for life and clopidogrel 75 mg daily for 3 months. Even though our treatment regimen differs from the one suggested as the most common by Faught et al. we did not report any event of occlusion of the stent, while we witnessed only two cases of patients presenting asymptomatic mild neointimal hyperplasia that spontaneously resolved at follow-up, after 6 months of double antiplatelet therapy.
Conclusions In our study, FD stenting of unruptured intracranial aneurysm seems to be an effective and safe treatment, especially in selected patients with aneurysm presenting specific anatomical characteristic (large neck, fusiform). This treatment leads to high rate of complete occlusion of the aneurysm in most patient at 1 year after the procedure and is associated with low incidence of peri- and post-procedural complications. However, thrombosis and occlusion of the aneurysm could still be delayed in some patients; still no predictors of aneurysm occlusion rate are known and the exact timing
La radiologia medica
of this phenomenon could not be predicted. We will therefore need longer follow-ups, with wider group of patients, to evaluate the real potentials of these new generation devices for the treatment of intracranial aneurysms.
Compliance with ethical standards Conflict of interest All authors declare no conflict of interest. Ethical approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent Informed consent was obtained from all individual participants included in the study.
References 1. Ascenzi A, Mottura G (1997) Anatomia patologica: alterazioni Vascolari, 18:33–34 2. Austin GM, Schievink W, Williams W (1989) Controlled pressure-volume factors in the enlargement of intracranial aneurysm. Neurosurg 24:722–730 3. Linn FH, Gj Rinatekel (1996) Incidence of subarachnoid hemorrhage: role of region, years and rate of computed tomography: a meta-analysis. Stroke 27:625–629 4. Valavanis Anton (1994) Interventional Neuro-Radiology, 7th edn. Springer, Berlin, p 116 5. International Study of Unruptured Intracranial Aneurysm (1998) Unruptured intracranial aneurysm: risk of rupture and risk of surgical intervention. NEJM 339:1725–1733 6. International Subarachnoid Aneurys2 m Trial (ISAT) Collaborative Group (2002) International subarachnoid aneurysm trial of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysm: a randomized trial. Lancet 360:1267–1274 7. Cantore et al (2008) Surgical treatment of giant intracranial aneurysms: current viewpoint. Neurosurg 63:279–290 8. David et al (1999) Late angiographic follow-up review of surgically treated aneurysms. J Neurosurg 91:396–401 9. Valavanis Anton (1994) Interventional Neuro-Radiology. Springer, Berlin, pp 111–121 10. Lasjaunias P (2001) Quality factors in interventional neuroradiology. Acta Neurochir Suppl 78:101–105 11. Moret J, Cognard C, Weill A, Castaings L, Rey A (1997) The remodelling technique in the treatment of wide neck intracranial aneurysm. Interv Neur 3:21–35 12. Lasjaunias P, Brugge Ter et al (2001) Surgical Neuroangiography, vol 2. Springer, Berlin, p 1030 13. Lasjaunias P (2001) Towards European standards in neuroradiology. Acta Neurochir Suppl 78:97–100 14. Cekirge et al (2006) Intrasaccular combination of metallic coils and onyx liquid embolic agent for endovascular treatment of cerebral aneurysms. J Neurosurg 105:706–712 15. Benson CM, Pelz DM, Lownie SP (2015) Parent artery occlusion: a well-established technique. Am J Neuroradiol 36(6):E53
16. Kallmes DF, Ding YH, Dai D et al (2009) A second generation, endoluminal, flow-disrupting device for treatment of saccular aneurysms. AJNR 20:1153–1158 17. Fiorella D, Lylyk P, Kelly ME, Albuquerque FC, McDougall CG, Nelson PK (2009) Curative cerebrovascular reconstruction with the pipeline embolization device: the emergence of definitive endovascular therapy for intracranial aneurysms. J Neurointerv Surg 1(1):56–65 18. Faught RW, Satti SR, Hurst RW, Pukenas BA, Smith MJ (2014) Heterogeneous practice patterns regarding antiplatelet medications for neuroendovascular stenting in the USA: a multicenter survey. J Neurointerv Surg 6(10):774–779 19. O’Kelly CJ, Krings T, Fiorella D, Marotta TR (2010) A novel grading scale for the angiographic assessment of intracranial aneurysms treated using flow diverting stents. Interv Neuroradiol 16:133–137 20. Joshi MD, O’Kelly CJ, Krings T, Fiorella D, Marotta TR (2013) Observer variability of an angiographic grading scale used for the assessment of intracranial aneurysms treated with flow-diverting stents. Am J Neuroradiol 34:1589–1592 21. Kulcsar Z, Ernemann U, Wetzel SG, Bock A, Goerike S, Panagiotopulos V et al (2010) High-profile flow diverter (SILK) implantation in the basilar artery. Efficacy in the treatment of aneurysms and the role of the perforators. Stroke 41(8):1690–1696 22. Szikora I, Berentei Z, Kulcsar Z, Marosfoi M, Vajda ZS, Lee W et al (2010) Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest experience with the Pipeline embolization device. AJNR 1:1139–1147 23. Lubciz B, Collignon L, Raphaeli G et al (2010) Flow-diverter stent for the endovascular treatment of intracranial aneurysms: a prospective study in 29 patients with 34 aneurysms. Stroke 41:2247–2253 24. Lylyk P, Miranda C, Cerrato R, Ferrario A, Scrivano E, Luna HR et al (2009) Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization devide: the buenos aires experience. Neurosurg 64:632–643 25. Nelson PK (2008) Pipeline for the intracranial treatment of aneurysm (PITA) trial. International Stroke Conference, New Orleans. Feb 20–22 26. Berge J, Biondi A, Machi P, Brunel H, Pierot L, Gabrillargues J et al (2012) Flow-diverter silk stent for the treatment of intracranial aneurysms: 1 year follow-up in a multicenter study. AJNR 33(6):1150–1155 27. Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bäzner H et al (2012) Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology 54(4):369–382 28. Malatesta E, Nuzzi NP, Divenuto I, Fossaceca R, Lombardi M, Cerini P et al (2013) Endovascular treatment of intracranial aneurysms with flow-diverter stents: preliminary single-centre experience. Radiol Med 118(6):971–983 29. Briganti F, Leone G, Marseglia M, Mariniello G, Caranci F, Brunetti A et al (2015) Endovascular treatment of cerebral aneurysms using flow-diverter devices: a systematic review. Neuroradiol J 28(4):365–375 30. Bhogal P, Ganslandt O, Bäzner H, Henkes H, Pérez MA (2017) The Fate of side branches covered by flow diverters-results from 140 patients. World Neurosurg 103:789–798
13