RESEARCH—HUMAN—CLINICAL STUDIES RESEARCH—HUMAN—CLINICAL STUDIES
The Use of the Pipeline Embolization Device in the Management of Recurrent Previously Coiled Cerebral Aneurysms Badih Daou, MD* Robert M. Starke, MD* Nohra Chalouhi, MD* Stavropoula Tjoumakaris, MD* Jean Khoury, MD* David Hasan, MD‡ Robert H. Rosenwasser, MD* Pascal M. Jabbour, MD* *Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, Pennsylvania; ‡Department of Neurosurgery, University of Iowa, Iowa City, Iowa Correspondence: Pascal M. Jabbour, MD, Associate Professor and Director, Division of Neurovascular Surgery and Endovascular Neurosurgery Department of Neurological Surgery, Thomas Jefferson University Hospital, 901 Walnut St, 3rd Floor, Philadelphia, PA 19107. E-mail: [email protected]
BACKGROUND: The biggest downside of cerebral aneurysm coiling is the high rates of recurrence and retreatments. With the increasing number of aneurysm recurrences after failed coiling procedures, the best retreatment strategy remains unknown. OBJECTIVE: To assess the efficacy and safety of the Pipeline Embolization Device (PED) in the treatment of recurrent previously coiled aneurysms. METHODS: Thirty-three patients who underwent treatment with the PED of a recurrent previously coiled aneurysm were retrospectively identified. Efficacy was assessed in terms of angiographic occlusion at the latest cerebral angiogram, recurrence and retreatment rates after PED placement, and clinical outcome at the latest follow-up. Safety was assessed by looking at the complications, morbidity, and mortality after PED treatment. RESULTS: The mean patient age was 53 years. The mean percent recurrence from coiling to PED placement was 34%. The mean time from coiling to PED placement was 40 months. PED treatment resulted in complete aneurysm occlusion in 76.7% of patients and nearcomplete aneurysm occlusion ($90%) in 10%, for a total rate of complete and near-complete aneurysm occlusion of 86.7%. All patients, including those with incomplete aneurysm occlusion, had a significant reduction in aneurysm size. Two aneurysms required another retreatment after PED placement (6.2%). Ninety-seven percent of patients had a good clinical outcome. Complications were observed in 1 patient (3%), who suffered an intracerebral hemorrhage. There were no mortalities. CONCLUSION: The use of the PED in the management of recurrent, previously coiled aneurysms is safe and effective in achieving aneurysm occlusion. KEY WORDS: Aneurysm, Flow diversion, Pipeline embolization device, Previously coiled, Recurrence Neurosurgery 77:692–697, 2015
Received, January 23, 2015. Accepted, May 21, 2015. Published Online, July 15, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
DOI: 10.1227/NEU.0000000000000901
E
ndovascular treatment is one of the key management strategies of cerebral aneurysms. With several types of endovascular interventions available, more types of aneurysms are becoming amenable to endovascular treatment, and more physicians are opting for this approach as a first-line treatment strategy. The main methods that are being used include coiling, stenting, stentassisted coiling, and the more recent flow diversion technique. The biggest downside of cerebral aneurysm coiling is the higher recurrence rates encountered with this technique, which leads to more retreatments to reduce the risk of future hemorrhage.1,2 About one-fifth of all coiled cerebral ABBREVIATIONS: mRS, modified Rankin Scale; PED, Pipeline Embolization Device
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aneurysms recur, and 10% of coiled aneurysms require another intervention.3 Recanalization and retreatment rates are lower with stent-assisted coiling, approximately 12% and 6%, respectively.4 With the increasing number of aneurysm recurrences after failed coiling procedures, several main questions remain: What is the best treatment for recurrent previously coiled aneurysms? Should the same endovascular technique be attempted again, should a different endovascular approach be used, or should we resort to surgical clipping? The Pipeline Embolization Device (PED) is the first and only flow diversion device approved by the US Food and Drug Administration. The use of the PED has gained popularity mainly because of its high success rate in achieving aneurysm occlusion and low aneurysm recurrence and retreatment rates, especially compared with other
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PED IN TREATING COILED CEREBRAL ANEURYSMS
endovascular treatment modalities.5,6 Although the overall efficacy of the PED has been well described in the management of cerebral aneurysms, the specific role of the PED in the management of recurrent, previously coiled aneurysms is still not well defined. The aim of this study is to assess the efficacy and safety of the PED in the treatment of recurrent previously coiled aneurysms and to compare the PED with other available endovascular approaches.
METHODS Patients Patients with cerebral aneurysms treated with the PED between May 2011 and July 2014 at a single institution were reviewed. Thirty-two patients who underwent treatment with the PED of a previously coiled recurrent aneurysm were retrospectively identified. Patients who had prior stent placement were excluded (Figure). PED treatment was offered for recurrent complex, wide-necked aneurysms, partially thrombosed aneurysms, and aneurysms with multiple recurrences treated unsuccessfully with other means. Baseline patient characteristics, aneurysm characteristics, and procedure characteristics were recorded. The study protocol was approved by the Institutional Review Board.
PED Procedure Patients were started on 75 mg/d clopidogrel and 81 mg/d aspirin for at least 10 days before the intervention. Preoperative platelet reactivity unit values were checked, and the PED procedure was performed if platelet inhibition was in the therapeutic range, with mainly 60 to 240 as the range used. During the procedure, patients received a bolus of intravenous heparin to maintain an activated clotting time of 2 to 3 times their baseline values. An angiographic evaluation was obtained to assess the dimensions of the aneurysms. The PED was sized according to the width of the inflow vessel to avoid any endoleak. Treatment with the PED was performed under general anesthesia and neurophysiological monitoring with an 8F gauge femoral sheath for access. A 6F shuttle sheath was usually placed in the carotid bulb, and a 070 Neuron catheter was placed at the level of the petrocavernous carotid junction. A Marksman (ev3, Irvine, California) microcatheter was then introduced distally to the M1-M2 junction. This triaxial system was used to maximize support during forward loading of the system, thus enhancing the opening of the PED and its conformation to the parent vessel while avoiding kickback. After embolization was accomplished, another angiogram was obtained. Heparin was stopped at the end of the procedure. Patients were evaluated in the hospital for any periprocedural complications. After discharge, patients were scheduled for clinical follow-up and a follow-up angiogram.7
Outcomes The efficacy and safety of the PED in the management of previously coiled recurrent cerebral aneurysms were the outcomes of interest. Efficacy was assessed in terms of angiographic occlusion at the latest cerebral angiogram, recurrence rate and retreatment rate after PED placement, and clinical outcome as measured by the modified Rankin Scale (mRS) at the latest available follow-up. Safety was assessed by looking at the complications, morbidity, and mortality after PED treatment of previously coiled recurrent aneurysms. mRS scores of 0 to 2 were considered favorable outcomes; mRS scores of 3 to 6 were considered poor outcomes. Angiographic evaluations were obtained to monitor for any recanalization or residual filling after PED treatment. Aneurysm occlusion at follow-up was categorized as complete (100%), near-complete ($90%), or incomplete (,90%).
RESULTS Patient Characteristics The mean patient age was 53 years (range, 34-75 years). Six patients were men (18.8%), and 26 patients were women (81.2%). Seventeen patients had a history of tobacco smoking (53%), and 21 patients had a history of hypertension (65.6%). Seventeen patients had presented initially (before the first endovascular intervention) in the setting of a subarachnoid hemorrhage (53%).
FIGURE. Flow diagram showing patient selection.
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Aneurysm Characteristics Aneurysm locations were as follows: 31% in the posterior communicating artery (n = 10), 22% in the carotid ophthalmic artery (n = 7), 19% in the superior hypophyseal artery (n = 6), 9% in the posterior inferior cerebellar artery (n = 3), 6% in the cavernous internal carotid artery (n = 2), 6% in the posterior wall of the internal carotid artery (n = 2), 3% in the anterior choroidal
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artery (n = 1), and 3% in the middle cerebral artery (n = 1). Thirty aneurysms were saccular; 1 aneurysm was fusiform; and 1 aneurysm was a pseudoaneurysm. The average initial aneurysm size before any treatment was attempted was 11 mm (range, 3.6-30 mm). The mean percent recurrence from the time of coiling to the time of PED placement was 34% (range, 10%-100% recurrence). Treatment Characteristics The mean number of coiling interventions prior to PED placement was 1.2, with 24 patients (75%) having had 1 coiling procedure before opting for PED placement and 8 patients (25%) having undergone 2 coiling procedures before PED placement. Coils that were used before cerebral aneurysm recurrence included the following: Guglielmi detachable coil (28%), Cerecyte (25%), Axium (18.7%), Orbit (15.6%), Target (12.5%), Cashmere (9%), Galaxy (6%), Deltapaq (6%), and Precidio (3%) coils. The mean time to aneurysm recurrence was 27 months (2.25 years). Of the 32 patients, 18 (56.2%) had aneurysm recurrence within the first year. The mean time from the initial endovascular treatment to PED placement was 40 months (3.3 years). The mean number of PEDs placed was 1.3, ranging from 1 to 5. The average procedure length for PED of recurrent previously coiled aneurysms was 51 minutes. Efficacy of PED Treatment of Recurrent Previously Coiled Aneurysms Angiographic Outcome Two patients did not have a follow-up angiographic evaluation. Of the 30 patients who had follow-up angiograms, PED treatment
resulted in complete aneurysm occlusion in 23 patients (76.7%) and near-complete aneurysm occlusion ($90%) in 3 patients (10%), for a total rate of complete and near-complete aneurysm occlusion of 86.7%. Four aneurysms (13.3%) were found to have incomplete occlusion (,90%) with residual filling after PED placement. All patients, including those with incomplete aneurysm occlusion, had a significant reduction in aneurysm size. Two of the incompletely occluded aneurysms had .50% reduction in size, and the 2 other aneurysms had minimal residual filling at the neck. The characteristics of patients with incomplete aneurysm occlusion are detailed in Table. The mean angiographic follow-up time from PED placement to the last available angiogram was 8 months (range, 6-16 months). Retreatment Two previously coiled aneurysms that were treated with the PED required another retreatment after PED placement (6.2%). One previously treated aneurysm required placement of a second PED and the other patient required clipping of his recurrent aneurysm. Clinical Outcome The mean follow-up period was 11.4 months (range, 1-31 months). Thirty-one patients (97%) had a good clinical outcome at the latest follow-up, with 27 patients (84.4%) having an mRS score of 0 and 4 patients (12.5%) having an mRS score of 1. One patient had an unfavorable outcome, with an mRS score of 4 (3%).
TABLE. Summary of Patients With Incomplete Aneurysm Occlusiona Age, y Sex Smoking Hypertension Presentation with subarachnoid hemorrhage Aneurysm location Aneurysm form Aneurysm initial size, mm Percent recurrence before PED Time to recurrence, mo Retreatment after PED PEDs used, n Interventions before PED, n Time of last angiogram after PED, months Result of last angiogram
46 Female No Yes No Posterior wall of internal carotid artery Pseudoaneurysm 18 50 6 None 1 1 12 .50% reduction in size
Complications mRS score at latest follow-up Latest clinical follow-up after treatment, mo Procedure time, min a
None 0 27 40
69 Female Yes Yes No Posterior inferior cerebellar artery Saccular 9 15 7 Clipping 1 2 11 Minimal filling at the neck
53 Female Yes No No Anterior choroidal
None 0 11 68
None 0 14 41
Saccular 4 30 39 None 1 1 6 .50% reduction in size
49 Female Yes No Yes Posterior communicating artery Saccular 9 15 92 PED 1 1 10 Minimal filling at the neck None 1 7 31
mRS, modified Rankin Scale; PED, Pipeline Embolization Device.
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Safety of PED Treatment of Recurrent Previously Coiled Aneurysms Complications were observed in only 1 patient (3%). This patient suffered a basal ganglia intracerebral hemorrhage with long-term morbidity (mRS score, 4). There were no mortalities.
DISCUSSION The high efficacy of the PED in achieving aneurysm occlusion with low recurrence and retreatment rates has made it a desirable tool in the management of cerebral aneurysms.6 With the growing number of recurrent aneurysms from failed coiling attempts, the PED is being used more often to manage this category of aneurysms. To the best of our knowledge, this is the first study to look specifically at the efficacy and safety of the PED in the management of recurrent previously coiled cerebral aneurysms. Our results show that the PED is efficient in the management of recurrent previously coiled cerebral aneurysms. The rate of complete and near-complete aneurysm occlusion in our study was 86.7%. Compared with other studies that assessed the role of the PED in the management of previously treated aneurysms, this rate was higher than what was previously reported.8,9 O’Kelly et al9 reported a complete or near-complete occlusion rate of all previously treated and untreated aneurysms of 83%. They reported that PED was less successful in previously treated aneurysms and added that previous treatment was a predictor of persistent aneurysm filling on follow-up angiogram. The type of initial treatment (endovascular or clipping) was not mentioned. McAuliffe et al8 reported that, in patients not previously treated, the aneurysm occlusion rate with the PED was 92.5%. However, in patients with prior treatment of the target aneurysm, the occlusion rate was 68.7%. It is noteworthy that, when they excluded 50 patients with a stent in situ, the occlusion rate was 90%, comparable to that seen in untreated aneurysms. A possible reason for the higher success rate observed in our study is that other reports that studied previously treated aneurysms did not differentiate between the prior treatment modalities used (coiling vs stenting vs microsurgical clipping). The rate of complete and near-complete occlusion of previously coiled aneurysms of 86.7% obtained in our study is comparable to the success rates reported in the literature for PED management of untreated cerebral aneurysms.5,10 This shows that PED deployment can be used with ease even in the presence of coils. This device has a high efficacy in treating previously coiled cerebral aneurysms, comparable to the efficacy seen with uncoiled aneurysms being treated with the PED as first-line strategy. These findings can be explained by the fact that the PED is a flow diverter that works on treating aneurysms by means of endoluminal reconstruction rather than aneurysm filling. It causes flow disruption across the aneurysm neck without the need for direct access into the aneurysm.11 For this reason, PED deployment should not be hampered by the presence of preexisting coils. All patients with incomplete aneurysm occlusion after treatment with the PED were women. No other patient,
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aneurysm, or treatment characteristics were common to all patients with unsuccessful treatment. There are multiple available endovascular treatment strategies for managing recurrent aneurysms. Recoiling can be attempted; a stent can be placed; or stent-assisted coiling can be performed. How does the PED compare with these other endovascular treatment modalities? Slob et al12 assessed the effect of recoiling of previously coiled aneurysms. They reported that, at the last angiographic follow-up, 76% of aneurysms achieved complete or near-complete aneurysm occlusion. Renowden et al13 reported that 11% of recoiled aneurysms developed a second recurrence. Sedat et al14 reported that recoiling resulted in complete occlusion in 56.8% of aneurysms, and 84% showed a stable occlusion at follow-up. Raymond et al reported that patients undergoing recoiling of a previously coiled aneurysm have a high incidence of recurrence, nearly 50% at long-term follow-up.15 Henkes et al16 reported that complete occlusion was achieved in only 46.9% of retreated aneurysms after the first retreatment attempt and in only 35.2% after the second retreatment. Overall, higher recurrence rates are reported with recoiling of previously coiled aneurysms than the rate seen with PED treatment, which demonstrates the high efficacy of this device in the management of this category of aneurysms. Another important benefit of PED treatment of recurrent previously coiled aneurysms is the number of interventions required to achieve aneurysm occlusion. Slob et al12 reported that 19.5% of previously coiled aneurysms required multiple coil treatments to achieve complete or near-complete aneurysm occlusion (4 of 41 patients required 3 coiling procedures, and 4 other patients required 4 coiling procedures). Ringer et al17 reported that 13.2% of patients required multiple retreatments to achieve aneurysm occlusion. In our study, 8 of 32 patients (25%) had 2 attempts at coiling before resorting to PED placement, which was the definitive and final treatment. Treatment with the PED may decrease the number of endovascular interventions needed in the management of recurrent coiled aneurysms. Therefore, it is important to note that PED therapy may improve treatment durability compared with recoiling, which may possibly reduce the number of repeat interventions required. The use of coils in conjunction with the PED to treat these recurrent aneurysms is also another promising technique; recent studies have shown high efficacy and safety of this technique.18,19 Complications were observed in only 1 patient (3%). This was a 54-year-old female patient who had a basal ganglia intracerebral hemorrhage. The patient had a recurrence of a giant (25 mm) cerebral aneurysm that was treated previously with 2 coiling procedures. She had a successful complete aneurysm occlusion on her latest follow-up angiogram after PED placement and had a mRS score of 4 on her 1-year follow-up. This was the only patient with poor clinical outcome on follow-up (mRS score of 0-2, 97%). Intracerebral hemorrhage is a well-known complication of PED treatment.6,10,20,21 This phenomenon can be explained by the hemorrhagic conversion of embolic infarcts aggravated in the
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setting of dual antiplatelet therapy. In addition, aneurysm size plays an important role in influencing outcome after PED placement.5 The giant aneurysm size in this patient was an additional factor to consider in her poor clinical outcome. The complication rate observed in this study is comparable to the complication rates observed with recoiling of previously coiled aneurysms. Renowden et al13 reported a 3% complication rate after recoiling of recurrent coiled aneurysms. Henkes et al16 found that the morbidity/mortality rate in 495 retreatment sessions was 2.2%. Sedat et al14 reported that the procedural permanent morbidity was 1.8%. Ringer et al17 reported that the total risk for retreatment mortality or permanent major disability was 1.28% per patient. Although these complication rates per procedure are similar, even lower with coiling than with the PED, the number of reinterventions required with each treatment tips the balance in favor of PED treatment. Although the risk of complications per procedure might be about 1% to 3% with coiling, when multiple coiling procedures are required, the risk accumulates and exceeds the observed risk with PED treatment. The use of stents in the treatment of recurrent aneurysms has shown to have promising results. Tahtinen et al22 studied the role of stent-assisted coil embolization in the management of recurrent cerebral aneurysms. Most of the aneurysms in their study were initially treated with coiling. They reported a complete occlusion rate of 59% after stent-assisted coiling of recurrent aneurysms, and 32% of aneurysms had a small neck remnant. The reported complication rate was 11%. Compared with our results, PED treatment showed a higher complete occlusion rate of nearly 77% and a lower major complication rate (3%). Chalouhi et al4 reported that incompletely occluded, previously coiled aneurysms were more likely to have recanalization after stent-assisted coiling (odds ratio, 3.4; 95% confidence interval, 1.4-8.1; P = .005). Other small studies that evaluated the role of stenting in the management of previously coiled aneurysms (n = 1123 and n = 824) reported excellent results on long-term angiographic follow-up, with high complete occlusion rates and minimal morbidity. Stenting and stent-assisted coiling of previously coiled aneurysms may be more effective than recoiling of these recurrent aneurysms and comparable to the results obtained with PED of previously coiled aneurysms. More studies are required to compare these 2 treatment strategies in the management of recurrent aneurysms. Although the average angiographic follow-up after treatment with the PED was only 8 months, noninvasive follow-up with magnetic resonance angiography or computed tomography angiography was continued for patients with complete or nearcomplete occlusion. It is has been well reported in the literature that the majority of aneurysms that are occluded at 6 months after PED treatment will remain occluded even if longer angiographic follow-ups are obtained.25,26 Deutschmann et al27 conducted a study on 12 patients with angiographic follow-up at 6 and 30 months after PED placement. They reported that once aneurysms were completely occluded at 6 months, no aneurysms showed any recurrence at the 30-month angiogram.
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Limitations The major limitations of this study include its retrospective, single-center nature, which may not always reflect the results of other institutions, and the modest sample size of patients with recurrent, previously coiled aneurysms who underwent treatment with the PED. Despite the encouraging results in the present study, long-term follow-up imaging and comparative studies are needed to better assess the efficacy of the PED in the treatment of recurrent aneurysms.
CONCLUSION The use of the PED in the management of recurrent, previously coiled aneurysms is safe and effective in achieving aneurysm occlusion and is one of the most promising endovascular means in the management of this type of aneurysm. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Campi A, Ramzi N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2007;38(5):1538-1544. 2. Molyneux AJ, Kerr RS, Yu LM, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809-817. 3. Ferns SP, Sprengers ME, van Rooij WJ, et al. Coiling of intracranial aneurysms: a systematic review on initial occlusion and reopening and retreatment rates. Stroke. 2009;40(8):e523-e529. 4. Chalouhi N, Jabbour P, Singhal S, et al. Stent-assisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke. 2013;44(5):1348-1353. 5. Zanaty M, Chalouhi N, Starke RM, et al. Flow diversion versus conventional treatment for carotid cavernous aneurysms. Stroke. 2014;45(9):2656-2661. 6. Chalouhi N, Tjoumakaris S, Starke RM, et al. Comparison of flow diversion and coiling in large unruptured intracranial saccular aneurysms. Stroke. 2013;44(8): 2150-2154. 7. Chitale R, Gonzalez LF, Randazzo C, et al. Single center experience with Pipeline stent: feasibility, technique, and complications. Neurosurgery. 2012;71(3):679691; discussion 691. 8. McAuliffe W, Wycoco V, Rice H, Phatouros C, Singh TJ, Wenderoth J. Immediate and midterm results following treatment of unruptured intracranial aneurysms with the Pipeline Embolization Device. AJNR Am J Neuroradiol. 2012; 33(1):164-170. 9. O’Kelly CJ, Spears J, Chow M, et al. Canadian experience with the Pipeline Embolization Device for repair of unruptured intracranial aneurysms. AJNR Am J Neuroradiol. 2013;34(2):381-387. 10. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 2013;44(2):442-447. 11. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke. 2007;38(8):2346-2352. 12. Slob MJ, Sluzewski M, van Rooij WJ, Roks G, Rinkel GJ. Additional coiling of previously coiled cerebral aneurysms: clinical and angiographic results. AJNR Am J Neuroradiol. 2004;25(8):1373-1376. 13. Renowden SA, Koumellis P, Benes V, Mukonoweshuro W, Molyneux AJ, McConachie NS. Retreatment of previously embolized cerebral aneurysms: the
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risk of further coil embolization does not negate the advantage of the initial embolization. AJNR Am J Neuroradiol. 2008;29(7):1401-1404. Sedat J, Chau Y, Moubarak K, Vargas J, Lonjon M. Endovascular treatment of recurrent coiled aneurysms: assessment of complications and rebleeding during a decade in a single center. Interv Neuroradiol. 2012;18(1):14-19. Raymond J, Darsaut TE. An approach to recurrent aneurysms following endovascular coiling. J Neurointerv Surg. 2011;3(4):314-318. Henkes H, Fischer S, Liebig T, et al. Repeated endovascular coil occlusion in 350 of 2759 intracranial aneurysms: safety and effectiveness aspects. Neurosurgery. 2006;58(2):224-232; discussion 224-232. Ringer AJ, Rodriguez-Mercado R, Veznedaroglu E, et al. Defining the risk of retreatment for aneurysm recurrence or residual after initial treatment by endovascular coiling: a multicenter study. Neurosurgery. 2009;65(2):311-315; discussion 315. Nossek E, Chalif DJ, Chakraborty S, Lombardo K, Black KS, Setton A. Concurrent use of the Pipeline Embolization Device and coils for intracranial aneurysms: technique, safety, and efficacy. J Neurosurg. 2015;122(4):904-911. Lin N, Brouillard AM, Krishna C, et al. Use of coils in conjunction with the pipeline embolization device for treatment of intracranial aneurysms. Neurosurgery. 2015;76(2):142-149. Delgado Almandoz JE, Kadkhodayan Y, Crandall BM, Scholz JM, Fease JL, Tubman DE. Variability in initial response to standard clopidogrel therapy, delayed conversion to clopidogrel hyper-response, and associated thromboembolic and hemorrhagic complications in patients undergoing endovascular treatment of unruptured cerebral aneurysms. J Neurointerv Surg. 2014;6(10):767-773. Kallmes DF, Hanel R, Lopes D, et al. International retrospective study of the Pipeline Embolization Device: a multicenter aneurysm treatment study. AJNR Am J Neuroradiol. 2015;36(1):108-115. Tahtinen OI, Manninen HI, Vanninen RL, et al. Stent-assisted embolization of recurrent or residual intracranial aneurysms. Neuroradiology. 2013;55(10):12211231. Li YD, Li MH, Gao BL, et al. Endovascular treatment of recurrent intracranial aneurysms with re-coiling or covered stents. J Neurol Neurosurg Psychiatry. 2010;81 (1):74-79. Li MH, Zhu YQ, Fang C, et al. The feasibility and efficacy of treatment with a Willis covered stent in recurrent intracranial aneurysms after coiling. AJNR Am J Neuroradiol. 2008;29(7):1395-1400. Saatci I, Yavuz K, Ozer C, Geyik S, Cekirge HS. Treatment of intracranial aneurysms using the Pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol. 2012;33(8): 1436-1446. Yeung TW, Lai V, Lau HY, Poon WL, Tan CB, Wong YC. Long-term outcome of endovascular reconstruction with the Pipeline Embolization Device in the management of unruptured dissecting aneurysms of the intracranial vertebral artery. J Neurosurg. 2012;116(4):882-887. Deutschmann HA, Wehrschuetz M, Augustin M, Niederkorn K, Klein GE. Longterm follow-up after treatment of intracranial aneurysms with the Pipeline Embolization Device: results from a single center. AJNR Am J Neuroradiol. 2012; 33(3):481-486.
COMMENT
T
he authors have put together a well-written series of 32 retrospectively identified patients who have had recurrent, previously coiled
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aneurysms retreated with the Pipeline Embolization Device (PED). When a coiled aneurysm recurs to the point of requiring retreatment, there are several modalities available for that retreatment. Retreatment with additional coils begs the question of how we might expect a permanent result when this strategy has already failed once. For this reason, clipping, stentassisted coiling, and flow diversion are appealing options. Because both flow diversion and stent-coiling require antiplatelet medications, sometimes ruptured aneurysms are coiled for dome protection and then later retreated with one of these strategies. There are similar recent articles indicating that aneurysm retreatment with PED can be safe and effective.1 Retrospective studies, however, are vulnerable to selection bias. Although there were 3 posterior inferior cerebellar artery aneurysms and 1 middle cerebral artery aneurysm in the present work, the other 28 aneurysms treated in this study arose from the internal carotid artery. Therefore, care should be taken applying these results to aneurysms outside the internal carotid artery. The study by Chalouhi et al1 also notes that PED treatment of recurrent aneurysms may be less effective in previously stent-coiled aneurysms, so caution must be used in this situation also. In the past, aneurysm recurrences that were recoiled had a second recurrence at a rate of almost 50%.2 The complete and near-complete occlusion rate in the present study was 86%. Additionally, as the authors note, it has been shown that aneurysms occluded with PED 6 months out from treatment can be counted on to be still occluded at 30 months.3 Therefore, PED treatment of recurrence may constitute a significant improvement over simple recoiling. Other options for recurrence besides simple recoiling have been called for, as have trials to help guide decisions in retreatment.4 This trial is a good early step in this effort. Christopher Nickele Adam S. Arthur Memphis, Tennessee
1. Chalouhi N, Chitale R, Starke RM, et al. Treatment of recurrent intracranial aneurysms with the Pipeline Embolization Device. J Neurointerv Surg. 2014;6(1): 19-23. 2. Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34 (6):1398-1403. 3. Deutschmann HA, Wehrschuetz M, Augustin M, Niederkorn K, Klein GE. Longterm follow-up after treatment of intracranial aneurysms with the Pipeline Embolization Device: results from a single center. AJNR Am J Neuroradiol. 2012;33(3):481-486. 4. Raymond J, Darsaut TE. An approach to recurrent aneurysms following endovascular coiling. J Neurointerv Surg. 2011;3(4):314-318.
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The Use of the Pipeline Embolization Device in the Management of Recurrent Previously Coiled Cerebral Aneurysms Badih Daou, MD* Robert M. Starke, MD* Nohra Chalouhi, MD* Stavropoula Tjoumakaris, MD* Jean Khoury, MD* David Hasan, MD‡ Robert H. Rosenwasser, MD* Pascal M. Jabbour, MD* *Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, Pennsylvania; ‡Department of Neurosurgery, University of Iowa, Iowa City, Iowa Correspondence: Pascal M. Jabbour, MD, Associate Professor and Director, Division of Neurovascular Surgery and Endovascular Neurosurgery Department of Neurological Surgery, Thomas Jefferson University Hospital, 901 Walnut St, 3rd Floor, Philadelphia, PA 19107. E-mail: [email protected]
BACKGROUND: The biggest downside of cerebral aneurysm coiling is the high rates of recurrence and retreatments. With the increasing number of aneurysm recurrences after failed coiling procedures, the best retreatment strategy remains unknown. OBJECTIVE: To assess the efficacy and safety of the Pipeline Embolization Device (PED) in the treatment of recurrent previously coiled aneurysms. METHODS: Thirty-three patients who underwent treatment with the PED of a recurrent previously coiled aneurysm were retrospectively identified. Efficacy was assessed in terms of angiographic occlusion at the latest cerebral angiogram, recurrence and retreatment rates after PED placement, and clinical outcome at the latest follow-up. Safety was assessed by looking at the complications, morbidity, and mortality after PED treatment. RESULTS: The mean patient age was 53 years. The mean percent recurrence from coiling to PED placement was 34%. The mean time from coiling to PED placement was 40 months. PED treatment resulted in complete aneurysm occlusion in 76.7% of patients and nearcomplete aneurysm occlusion ($90%) in 10%, for a total rate of complete and near-complete aneurysm occlusion of 86.7%. All patients, including those with incomplete aneurysm occlusion, had a significant reduction in aneurysm size. Two aneurysms required another retreatment after PED placement (6.2%). Ninety-seven percent of patients had a good clinical outcome. Complications were observed in 1 patient (3%), who suffered an intracerebral hemorrhage. There were no mortalities. CONCLUSION: The use of the PED in the management of recurrent, previously coiled aneurysms is safe and effective in achieving aneurysm occlusion. KEY WORDS: Aneurysm, Flow diversion, Pipeline embolization device, Previously coiled, Recurrence Neurosurgery 77:692–697, 2015
Received, January 23, 2015. Accepted, May 21, 2015. Published Online, July 15, 2015. Copyright © 2015 by the Congress of Neurological Surgeons.
DOI: 10.1227/NEU.0000000000000901
E
ndovascular treatment is one of the key management strategies of cerebral aneurysms. With several types of endovascular interventions available, more types of aneurysms are becoming amenable to endovascular treatment, and more physicians are opting for this approach as a first-line treatment strategy. The main methods that are being used include coiling, stenting, stentassisted coiling, and the more recent flow diversion technique. The biggest downside of cerebral aneurysm coiling is the higher recurrence rates encountered with this technique, which leads to more retreatments to reduce the risk of future hemorrhage.1,2 About one-fifth of all coiled cerebral ABBREVIATIONS: mRS, modified Rankin Scale; PED, Pipeline Embolization Device
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aneurysms recur, and 10% of coiled aneurysms require another intervention.3 Recanalization and retreatment rates are lower with stent-assisted coiling, approximately 12% and 6%, respectively.4 With the increasing number of aneurysm recurrences after failed coiling procedures, several main questions remain: What is the best treatment for recurrent previously coiled aneurysms? Should the same endovascular technique be attempted again, should a different endovascular approach be used, or should we resort to surgical clipping? The Pipeline Embolization Device (PED) is the first and only flow diversion device approved by the US Food and Drug Administration. The use of the PED has gained popularity mainly because of its high success rate in achieving aneurysm occlusion and low aneurysm recurrence and retreatment rates, especially compared with other
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PED IN TREATING COILED CEREBRAL ANEURYSMS
endovascular treatment modalities.5,6 Although the overall efficacy of the PED has been well described in the management of cerebral aneurysms, the specific role of the PED in the management of recurrent, previously coiled aneurysms is still not well defined. The aim of this study is to assess the efficacy and safety of the PED in the treatment of recurrent previously coiled aneurysms and to compare the PED with other available endovascular approaches.
METHODS Patients Patients with cerebral aneurysms treated with the PED between May 2011 and July 2014 at a single institution were reviewed. Thirty-two patients who underwent treatment with the PED of a previously coiled recurrent aneurysm were retrospectively identified. Patients who had prior stent placement were excluded (Figure). PED treatment was offered for recurrent complex, wide-necked aneurysms, partially thrombosed aneurysms, and aneurysms with multiple recurrences treated unsuccessfully with other means. Baseline patient characteristics, aneurysm characteristics, and procedure characteristics were recorded. The study protocol was approved by the Institutional Review Board.
PED Procedure Patients were started on 75 mg/d clopidogrel and 81 mg/d aspirin for at least 10 days before the intervention. Preoperative platelet reactivity unit values were checked, and the PED procedure was performed if platelet inhibition was in the therapeutic range, with mainly 60 to 240 as the range used. During the procedure, patients received a bolus of intravenous heparin to maintain an activated clotting time of 2 to 3 times their baseline values. An angiographic evaluation was obtained to assess the dimensions of the aneurysms. The PED was sized according to the width of the inflow vessel to avoid any endoleak. Treatment with the PED was performed under general anesthesia and neurophysiological monitoring with an 8F gauge femoral sheath for access. A 6F shuttle sheath was usually placed in the carotid bulb, and a 070 Neuron catheter was placed at the level of the petrocavernous carotid junction. A Marksman (ev3, Irvine, California) microcatheter was then introduced distally to the M1-M2 junction. This triaxial system was used to maximize support during forward loading of the system, thus enhancing the opening of the PED and its conformation to the parent vessel while avoiding kickback. After embolization was accomplished, another angiogram was obtained. Heparin was stopped at the end of the procedure. Patients were evaluated in the hospital for any periprocedural complications. After discharge, patients were scheduled for clinical follow-up and a follow-up angiogram.7
Outcomes The efficacy and safety of the PED in the management of previously coiled recurrent cerebral aneurysms were the outcomes of interest. Efficacy was assessed in terms of angiographic occlusion at the latest cerebral angiogram, recurrence rate and retreatment rate after PED placement, and clinical outcome as measured by the modified Rankin Scale (mRS) at the latest available follow-up. Safety was assessed by looking at the complications, morbidity, and mortality after PED treatment of previously coiled recurrent aneurysms. mRS scores of 0 to 2 were considered favorable outcomes; mRS scores of 3 to 6 were considered poor outcomes. Angiographic evaluations were obtained to monitor for any recanalization or residual filling after PED treatment. Aneurysm occlusion at follow-up was categorized as complete (100%), near-complete ($90%), or incomplete (,90%).
RESULTS Patient Characteristics The mean patient age was 53 years (range, 34-75 years). Six patients were men (18.8%), and 26 patients were women (81.2%). Seventeen patients had a history of tobacco smoking (53%), and 21 patients had a history of hypertension (65.6%). Seventeen patients had presented initially (before the first endovascular intervention) in the setting of a subarachnoid hemorrhage (53%).
FIGURE. Flow diagram showing patient selection.
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Aneurysm Characteristics Aneurysm locations were as follows: 31% in the posterior communicating artery (n = 10), 22% in the carotid ophthalmic artery (n = 7), 19% in the superior hypophyseal artery (n = 6), 9% in the posterior inferior cerebellar artery (n = 3), 6% in the cavernous internal carotid artery (n = 2), 6% in the posterior wall of the internal carotid artery (n = 2), 3% in the anterior choroidal
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artery (n = 1), and 3% in the middle cerebral artery (n = 1). Thirty aneurysms were saccular; 1 aneurysm was fusiform; and 1 aneurysm was a pseudoaneurysm. The average initial aneurysm size before any treatment was attempted was 11 mm (range, 3.6-30 mm). The mean percent recurrence from the time of coiling to the time of PED placement was 34% (range, 10%-100% recurrence). Treatment Characteristics The mean number of coiling interventions prior to PED placement was 1.2, with 24 patients (75%) having had 1 coiling procedure before opting for PED placement and 8 patients (25%) having undergone 2 coiling procedures before PED placement. Coils that were used before cerebral aneurysm recurrence included the following: Guglielmi detachable coil (28%), Cerecyte (25%), Axium (18.7%), Orbit (15.6%), Target (12.5%), Cashmere (9%), Galaxy (6%), Deltapaq (6%), and Precidio (3%) coils. The mean time to aneurysm recurrence was 27 months (2.25 years). Of the 32 patients, 18 (56.2%) had aneurysm recurrence within the first year. The mean time from the initial endovascular treatment to PED placement was 40 months (3.3 years). The mean number of PEDs placed was 1.3, ranging from 1 to 5. The average procedure length for PED of recurrent previously coiled aneurysms was 51 minutes. Efficacy of PED Treatment of Recurrent Previously Coiled Aneurysms Angiographic Outcome Two patients did not have a follow-up angiographic evaluation. Of the 30 patients who had follow-up angiograms, PED treatment
resulted in complete aneurysm occlusion in 23 patients (76.7%) and near-complete aneurysm occlusion ($90%) in 3 patients (10%), for a total rate of complete and near-complete aneurysm occlusion of 86.7%. Four aneurysms (13.3%) were found to have incomplete occlusion (,90%) with residual filling after PED placement. All patients, including those with incomplete aneurysm occlusion, had a significant reduction in aneurysm size. Two of the incompletely occluded aneurysms had .50% reduction in size, and the 2 other aneurysms had minimal residual filling at the neck. The characteristics of patients with incomplete aneurysm occlusion are detailed in Table. The mean angiographic follow-up time from PED placement to the last available angiogram was 8 months (range, 6-16 months). Retreatment Two previously coiled aneurysms that were treated with the PED required another retreatment after PED placement (6.2%). One previously treated aneurysm required placement of a second PED and the other patient required clipping of his recurrent aneurysm. Clinical Outcome The mean follow-up period was 11.4 months (range, 1-31 months). Thirty-one patients (97%) had a good clinical outcome at the latest follow-up, with 27 patients (84.4%) having an mRS score of 0 and 4 patients (12.5%) having an mRS score of 1. One patient had an unfavorable outcome, with an mRS score of 4 (3%).
TABLE. Summary of Patients With Incomplete Aneurysm Occlusiona Age, y Sex Smoking Hypertension Presentation with subarachnoid hemorrhage Aneurysm location Aneurysm form Aneurysm initial size, mm Percent recurrence before PED Time to recurrence, mo Retreatment after PED PEDs used, n Interventions before PED, n Time of last angiogram after PED, months Result of last angiogram
46 Female No Yes No Posterior wall of internal carotid artery Pseudoaneurysm 18 50 6 None 1 1 12 .50% reduction in size
Complications mRS score at latest follow-up Latest clinical follow-up after treatment, mo Procedure time, min a
None 0 27 40
69 Female Yes Yes No Posterior inferior cerebellar artery Saccular 9 15 7 Clipping 1 2 11 Minimal filling at the neck
53 Female Yes No No Anterior choroidal
None 0 11 68
None 0 14 41
Saccular 4 30 39 None 1 1 6 .50% reduction in size
49 Female Yes No Yes Posterior communicating artery Saccular 9 15 92 PED 1 1 10 Minimal filling at the neck None 1 7 31
mRS, modified Rankin Scale; PED, Pipeline Embolization Device.
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Safety of PED Treatment of Recurrent Previously Coiled Aneurysms Complications were observed in only 1 patient (3%). This patient suffered a basal ganglia intracerebral hemorrhage with long-term morbidity (mRS score, 4). There were no mortalities.
DISCUSSION The high efficacy of the PED in achieving aneurysm occlusion with low recurrence and retreatment rates has made it a desirable tool in the management of cerebral aneurysms.6 With the growing number of recurrent aneurysms from failed coiling attempts, the PED is being used more often to manage this category of aneurysms. To the best of our knowledge, this is the first study to look specifically at the efficacy and safety of the PED in the management of recurrent previously coiled cerebral aneurysms. Our results show that the PED is efficient in the management of recurrent previously coiled cerebral aneurysms. The rate of complete and near-complete aneurysm occlusion in our study was 86.7%. Compared with other studies that assessed the role of the PED in the management of previously treated aneurysms, this rate was higher than what was previously reported.8,9 O’Kelly et al9 reported a complete or near-complete occlusion rate of all previously treated and untreated aneurysms of 83%. They reported that PED was less successful in previously treated aneurysms and added that previous treatment was a predictor of persistent aneurysm filling on follow-up angiogram. The type of initial treatment (endovascular or clipping) was not mentioned. McAuliffe et al8 reported that, in patients not previously treated, the aneurysm occlusion rate with the PED was 92.5%. However, in patients with prior treatment of the target aneurysm, the occlusion rate was 68.7%. It is noteworthy that, when they excluded 50 patients with a stent in situ, the occlusion rate was 90%, comparable to that seen in untreated aneurysms. A possible reason for the higher success rate observed in our study is that other reports that studied previously treated aneurysms did not differentiate between the prior treatment modalities used (coiling vs stenting vs microsurgical clipping). The rate of complete and near-complete occlusion of previously coiled aneurysms of 86.7% obtained in our study is comparable to the success rates reported in the literature for PED management of untreated cerebral aneurysms.5,10 This shows that PED deployment can be used with ease even in the presence of coils. This device has a high efficacy in treating previously coiled cerebral aneurysms, comparable to the efficacy seen with uncoiled aneurysms being treated with the PED as first-line strategy. These findings can be explained by the fact that the PED is a flow diverter that works on treating aneurysms by means of endoluminal reconstruction rather than aneurysm filling. It causes flow disruption across the aneurysm neck without the need for direct access into the aneurysm.11 For this reason, PED deployment should not be hampered by the presence of preexisting coils. All patients with incomplete aneurysm occlusion after treatment with the PED were women. No other patient,
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aneurysm, or treatment characteristics were common to all patients with unsuccessful treatment. There are multiple available endovascular treatment strategies for managing recurrent aneurysms. Recoiling can be attempted; a stent can be placed; or stent-assisted coiling can be performed. How does the PED compare with these other endovascular treatment modalities? Slob et al12 assessed the effect of recoiling of previously coiled aneurysms. They reported that, at the last angiographic follow-up, 76% of aneurysms achieved complete or near-complete aneurysm occlusion. Renowden et al13 reported that 11% of recoiled aneurysms developed a second recurrence. Sedat et al14 reported that recoiling resulted in complete occlusion in 56.8% of aneurysms, and 84% showed a stable occlusion at follow-up. Raymond et al reported that patients undergoing recoiling of a previously coiled aneurysm have a high incidence of recurrence, nearly 50% at long-term follow-up.15 Henkes et al16 reported that complete occlusion was achieved in only 46.9% of retreated aneurysms after the first retreatment attempt and in only 35.2% after the second retreatment. Overall, higher recurrence rates are reported with recoiling of previously coiled aneurysms than the rate seen with PED treatment, which demonstrates the high efficacy of this device in the management of this category of aneurysms. Another important benefit of PED treatment of recurrent previously coiled aneurysms is the number of interventions required to achieve aneurysm occlusion. Slob et al12 reported that 19.5% of previously coiled aneurysms required multiple coil treatments to achieve complete or near-complete aneurysm occlusion (4 of 41 patients required 3 coiling procedures, and 4 other patients required 4 coiling procedures). Ringer et al17 reported that 13.2% of patients required multiple retreatments to achieve aneurysm occlusion. In our study, 8 of 32 patients (25%) had 2 attempts at coiling before resorting to PED placement, which was the definitive and final treatment. Treatment with the PED may decrease the number of endovascular interventions needed in the management of recurrent coiled aneurysms. Therefore, it is important to note that PED therapy may improve treatment durability compared with recoiling, which may possibly reduce the number of repeat interventions required. The use of coils in conjunction with the PED to treat these recurrent aneurysms is also another promising technique; recent studies have shown high efficacy and safety of this technique.18,19 Complications were observed in only 1 patient (3%). This was a 54-year-old female patient who had a basal ganglia intracerebral hemorrhage. The patient had a recurrence of a giant (25 mm) cerebral aneurysm that was treated previously with 2 coiling procedures. She had a successful complete aneurysm occlusion on her latest follow-up angiogram after PED placement and had a mRS score of 4 on her 1-year follow-up. This was the only patient with poor clinical outcome on follow-up (mRS score of 0-2, 97%). Intracerebral hemorrhage is a well-known complication of PED treatment.6,10,20,21 This phenomenon can be explained by the hemorrhagic conversion of embolic infarcts aggravated in the
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setting of dual antiplatelet therapy. In addition, aneurysm size plays an important role in influencing outcome after PED placement.5 The giant aneurysm size in this patient was an additional factor to consider in her poor clinical outcome. The complication rate observed in this study is comparable to the complication rates observed with recoiling of previously coiled aneurysms. Renowden et al13 reported a 3% complication rate after recoiling of recurrent coiled aneurysms. Henkes et al16 found that the morbidity/mortality rate in 495 retreatment sessions was 2.2%. Sedat et al14 reported that the procedural permanent morbidity was 1.8%. Ringer et al17 reported that the total risk for retreatment mortality or permanent major disability was 1.28% per patient. Although these complication rates per procedure are similar, even lower with coiling than with the PED, the number of reinterventions required with each treatment tips the balance in favor of PED treatment. Although the risk of complications per procedure might be about 1% to 3% with coiling, when multiple coiling procedures are required, the risk accumulates and exceeds the observed risk with PED treatment. The use of stents in the treatment of recurrent aneurysms has shown to have promising results. Tahtinen et al22 studied the role of stent-assisted coil embolization in the management of recurrent cerebral aneurysms. Most of the aneurysms in their study were initially treated with coiling. They reported a complete occlusion rate of 59% after stent-assisted coiling of recurrent aneurysms, and 32% of aneurysms had a small neck remnant. The reported complication rate was 11%. Compared with our results, PED treatment showed a higher complete occlusion rate of nearly 77% and a lower major complication rate (3%). Chalouhi et al4 reported that incompletely occluded, previously coiled aneurysms were more likely to have recanalization after stent-assisted coiling (odds ratio, 3.4; 95% confidence interval, 1.4-8.1; P = .005). Other small studies that evaluated the role of stenting in the management of previously coiled aneurysms (n = 1123 and n = 824) reported excellent results on long-term angiographic follow-up, with high complete occlusion rates and minimal morbidity. Stenting and stent-assisted coiling of previously coiled aneurysms may be more effective than recoiling of these recurrent aneurysms and comparable to the results obtained with PED of previously coiled aneurysms. More studies are required to compare these 2 treatment strategies in the management of recurrent aneurysms. Although the average angiographic follow-up after treatment with the PED was only 8 months, noninvasive follow-up with magnetic resonance angiography or computed tomography angiography was continued for patients with complete or nearcomplete occlusion. It is has been well reported in the literature that the majority of aneurysms that are occluded at 6 months after PED treatment will remain occluded even if longer angiographic follow-ups are obtained.25,26 Deutschmann et al27 conducted a study on 12 patients with angiographic follow-up at 6 and 30 months after PED placement. They reported that once aneurysms were completely occluded at 6 months, no aneurysms showed any recurrence at the 30-month angiogram.
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Limitations The major limitations of this study include its retrospective, single-center nature, which may not always reflect the results of other institutions, and the modest sample size of patients with recurrent, previously coiled aneurysms who underwent treatment with the PED. Despite the encouraging results in the present study, long-term follow-up imaging and comparative studies are needed to better assess the efficacy of the PED in the treatment of recurrent aneurysms.
CONCLUSION The use of the PED in the management of recurrent, previously coiled aneurysms is safe and effective in achieving aneurysm occlusion and is one of the most promising endovascular means in the management of this type of aneurysm. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Campi A, Ramzi N, Molyneux AJ, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2007;38(5):1538-1544. 2. Molyneux AJ, Kerr RS, Yu LM, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809-817. 3. Ferns SP, Sprengers ME, van Rooij WJ, et al. Coiling of intracranial aneurysms: a systematic review on initial occlusion and reopening and retreatment rates. Stroke. 2009;40(8):e523-e529. 4. Chalouhi N, Jabbour P, Singhal S, et al. Stent-assisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke. 2013;44(5):1348-1353. 5. Zanaty M, Chalouhi N, Starke RM, et al. Flow diversion versus conventional treatment for carotid cavernous aneurysms. Stroke. 2014;45(9):2656-2661. 6. Chalouhi N, Tjoumakaris S, Starke RM, et al. Comparison of flow diversion and coiling in large unruptured intracranial saccular aneurysms. Stroke. 2013;44(8): 2150-2154. 7. Chitale R, Gonzalez LF, Randazzo C, et al. Single center experience with Pipeline stent: feasibility, technique, and complications. Neurosurgery. 2012;71(3):679691; discussion 691. 8. McAuliffe W, Wycoco V, Rice H, Phatouros C, Singh TJ, Wenderoth J. Immediate and midterm results following treatment of unruptured intracranial aneurysms with the Pipeline Embolization Device. AJNR Am J Neuroradiol. 2012; 33(1):164-170. 9. O’Kelly CJ, Spears J, Chow M, et al. Canadian experience with the Pipeline Embolization Device for repair of unruptured intracranial aneurysms. AJNR Am J Neuroradiol. 2013;34(2):381-387. 10. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke. 2013;44(2):442-447. 11. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke. 2007;38(8):2346-2352. 12. Slob MJ, Sluzewski M, van Rooij WJ, Roks G, Rinkel GJ. Additional coiling of previously coiled cerebral aneurysms: clinical and angiographic results. AJNR Am J Neuroradiol. 2004;25(8):1373-1376. 13. Renowden SA, Koumellis P, Benes V, Mukonoweshuro W, Molyneux AJ, McConachie NS. Retreatment of previously embolized cerebral aneurysms: the
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risk of further coil embolization does not negate the advantage of the initial embolization. AJNR Am J Neuroradiol. 2008;29(7):1401-1404. Sedat J, Chau Y, Moubarak K, Vargas J, Lonjon M. Endovascular treatment of recurrent coiled aneurysms: assessment of complications and rebleeding during a decade in a single center. Interv Neuroradiol. 2012;18(1):14-19. Raymond J, Darsaut TE. An approach to recurrent aneurysms following endovascular coiling. J Neurointerv Surg. 2011;3(4):314-318. Henkes H, Fischer S, Liebig T, et al. Repeated endovascular coil occlusion in 350 of 2759 intracranial aneurysms: safety and effectiveness aspects. Neurosurgery. 2006;58(2):224-232; discussion 224-232. Ringer AJ, Rodriguez-Mercado R, Veznedaroglu E, et al. Defining the risk of retreatment for aneurysm recurrence or residual after initial treatment by endovascular coiling: a multicenter study. Neurosurgery. 2009;65(2):311-315; discussion 315. Nossek E, Chalif DJ, Chakraborty S, Lombardo K, Black KS, Setton A. Concurrent use of the Pipeline Embolization Device and coils for intracranial aneurysms: technique, safety, and efficacy. J Neurosurg. 2015;122(4):904-911. Lin N, Brouillard AM, Krishna C, et al. Use of coils in conjunction with the pipeline embolization device for treatment of intracranial aneurysms. Neurosurgery. 2015;76(2):142-149. Delgado Almandoz JE, Kadkhodayan Y, Crandall BM, Scholz JM, Fease JL, Tubman DE. Variability in initial response to standard clopidogrel therapy, delayed conversion to clopidogrel hyper-response, and associated thromboembolic and hemorrhagic complications in patients undergoing endovascular treatment of unruptured cerebral aneurysms. J Neurointerv Surg. 2014;6(10):767-773. Kallmes DF, Hanel R, Lopes D, et al. International retrospective study of the Pipeline Embolization Device: a multicenter aneurysm treatment study. AJNR Am J Neuroradiol. 2015;36(1):108-115. Tahtinen OI, Manninen HI, Vanninen RL, et al. Stent-assisted embolization of recurrent or residual intracranial aneurysms. Neuroradiology. 2013;55(10):12211231. Li YD, Li MH, Gao BL, et al. Endovascular treatment of recurrent intracranial aneurysms with re-coiling or covered stents. J Neurol Neurosurg Psychiatry. 2010;81 (1):74-79. Li MH, Zhu YQ, Fang C, et al. The feasibility and efficacy of treatment with a Willis covered stent in recurrent intracranial aneurysms after coiling. AJNR Am J Neuroradiol. 2008;29(7):1395-1400. Saatci I, Yavuz K, Ozer C, Geyik S, Cekirge HS. Treatment of intracranial aneurysms using the Pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol. 2012;33(8): 1436-1446. Yeung TW, Lai V, Lau HY, Poon WL, Tan CB, Wong YC. Long-term outcome of endovascular reconstruction with the Pipeline Embolization Device in the management of unruptured dissecting aneurysms of the intracranial vertebral artery. J Neurosurg. 2012;116(4):882-887. Deutschmann HA, Wehrschuetz M, Augustin M, Niederkorn K, Klein GE. Longterm follow-up after treatment of intracranial aneurysms with the Pipeline Embolization Device: results from a single center. AJNR Am J Neuroradiol. 2012; 33(3):481-486.
COMMENT
T
he authors have put together a well-written series of 32 retrospectively identified patients who have had recurrent, previously coiled
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aneurysms retreated with the Pipeline Embolization Device (PED). When a coiled aneurysm recurs to the point of requiring retreatment, there are several modalities available for that retreatment. Retreatment with additional coils begs the question of how we might expect a permanent result when this strategy has already failed once. For this reason, clipping, stentassisted coiling, and flow diversion are appealing options. Because both flow diversion and stent-coiling require antiplatelet medications, sometimes ruptured aneurysms are coiled for dome protection and then later retreated with one of these strategies. There are similar recent articles indicating that aneurysm retreatment with PED can be safe and effective.1 Retrospective studies, however, are vulnerable to selection bias. Although there were 3 posterior inferior cerebellar artery aneurysms and 1 middle cerebral artery aneurysm in the present work, the other 28 aneurysms treated in this study arose from the internal carotid artery. Therefore, care should be taken applying these results to aneurysms outside the internal carotid artery. The study by Chalouhi et al1 also notes that PED treatment of recurrent aneurysms may be less effective in previously stent-coiled aneurysms, so caution must be used in this situation also. In the past, aneurysm recurrences that were recoiled had a second recurrence at a rate of almost 50%.2 The complete and near-complete occlusion rate in the present study was 86%. Additionally, as the authors note, it has been shown that aneurysms occluded with PED 6 months out from treatment can be counted on to be still occluded at 30 months.3 Therefore, PED treatment of recurrence may constitute a significant improvement over simple recoiling. Other options for recurrence besides simple recoiling have been called for, as have trials to help guide decisions in retreatment.4 This trial is a good early step in this effort. Christopher Nickele Adam S. Arthur Memphis, Tennessee
1. Chalouhi N, Chitale R, Starke RM, et al. Treatment of recurrent intracranial aneurysms with the Pipeline Embolization Device. J Neurointerv Surg. 2014;6(1): 19-23. 2. Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34 (6):1398-1403. 3. Deutschmann HA, Wehrschuetz M, Augustin M, Niederkorn K, Klein GE. Longterm follow-up after treatment of intracranial aneurysms with the Pipeline Embolization Device: results from a single center. AJNR Am J Neuroradiol. 2012;33(3):481-486. 4. Raymond J, Darsaut TE. An approach to recurrent aneurysms following endovascular coiling. J Neurointerv Surg. 2011;3(4):314-318.
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