Report of Flow Diverter Clinical Trials in Japan
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1 Journal of Neuroendovascular Therapy 2017; 11: Online May 21, 2016 DOI: /jnet.ra-diverter Report of Flow Diverter Clinical Trials in Japan Hidenori Oishi 1,2 and Nobuyuki Sakai 3 Objective: An outline and the results of clinical trials of flow diverters in Japan are reported. Subjects and Methods: There have been three flow diverters that have been evaluated by clinical trials in Japan: Pipeline, Surpass, and FRED. Since the clinical trials of Surpass and FRED are in progress as of January 2016, this report primarily focuses on Pipeline, which was approved for clinical use in April 2015 for the treatment of unruptured or chronic ruptured large/giant intracranial aneurysms. Results: The Japanese clinical trial of Pipeline was performed at four facilities by registering 22 patients, with 22 aneurysms. The procedure was completed in 21 (95.5%) of the 22 patients. The achievement rate of complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure, which was the primary endpoint, was 61.9%. Severe ipsilateral stroke or neurologic death within 180 days after the procedure, which was a major secondary endpoint, occurred in two patients (9.1%), and both events were subarachnoid hemorrhage due to rupture of the target aneurysm. Conclusion: The flow diverter is undoubtedly a revolutionary device in the treatment of large/giant intracranial aneurysms, but the results of the clinical trials in Japan were not satisfactory compared with previous reports. Therefore, the devices should be used carefully by comparing the safety and efficacy with those of existing endovascular treatment techniques including stent-assisted coil embolization and direct surgery in individual patients. Keywords flow diverter, pipeline, Japanese clinical trial Introduction The flow diverter (FD) is a new endovascular aneurysm repair device which simultaneously covers the neck and, being permanently deployed in the parent vessel unlike existing intracranial stents for coil embolization, changes the hemodynamics in the aneurysm, induces thrombosis, and leads to vascular repair and restructuring by neointima 1 Department of Neuroendovascular Therapy, Juntendo University School of Medicine, Bunkyo-ku, Tokyo, Japan 2 Department of Neurosurgery, Juntendo University School of Medicine, Bunkyo-ku, Tokyo, Japan 3 Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan Received: January 8, 2016; Accepted: April 11, 2016 Corresponding author: Hidenori Oishi. Department of Neuroendovascular Therapy, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyo-ku, Tokyo , Japan ohishi@juntendo.ac.jp 2017 The Editorial Committee of Journal of Neuroendovascular Therapy. All rights reserved. formation. To the present, clinical trials of FDs have been performed in Japan using Pipeline (Medtronic Neurovascular, Irving, CA, USA, Fig. 1), Surpass (Stryker Neurovascular, Fremont, CA, USA, Fig. 2), and FRED (Microvention, Tustin CA, USA, Fig. 3). Since the Japanese clinical trials of Surpass (Japanese clinical trial device number: SJN-1301) and FRED (Japanese clinical trial device number: TCD-14139) were still in progress as of January 2016, details including device characteristics will be discussed in a separate article to be carried in this journal. Table 1 shows the subject inclusion and exclusion criteria applied to the Japanese clinical trial of Pipeline. Pipeline was rated by the evaluation committee for the early introduction of medical devices with urgent clinical needs of the Ministry of Health, Labour and Welfare as a highly useful medical device for the treatment of cerebral aneurysms difficult to treat by conventional methods such as large or giant saccular aneurysms and fusiform aneurysms and, with completion of Japanese Japanese clinical trials, was approved for medical use in April The approved model was Pipeline Flex, which can be deployed more 124
2 Repor t of Flow Diver ter Clinical Trials in Japan Fig. 3 TCD (FRED). Fig. 1 Pipeline (Medtronic/Covidien). Fig. 2 SJN-1301 (Surpass). easily and has the additional resheathing function compared with the previous Pipeline. It is indicated for large or giant and wide-necked intracranial aneurysms from the petrous to the superior hypophyseal segment of the internal carotid artery (except in the acute period after rupture), and post-marketing surveillance (PMS) until 3 years after the procedure is mandated. This article outlines clinical trials of FDs in Japan, focusing, particularly, on Pipeline, the clinical use of which has been started in some facilities, and compares the results with past reports. Representative Cases and Subjects of Clinical Trials of Various FDs Pipeline was approved by the Food and Drug Administration (FDA) of the United States in April 2011, on the basis of the results of a few clinical studies 1 4) represented by Pipeline for Uncoilable or Failed Aneurysms (PUFS). PUFS 1) was the most important since clinical trials in Japan have been designed following its protocol. Representative cases treated with Pipeline (Fig. 4), SJN-1301 (Fig. 5), and TCD (Fig. 6) are presented. All these FDs are intended to be used for the treatment of large/giant wide-necked saccular or fusiform intracranial aneurysms except those in the acute period after rupture, but they are applied to lesions at different sites. Pipeline is applied to lesions from the petrous to the superior hypophyseal segment of the internal carotid artery, SJN to those from the petrous segment to the terminal of the internal carotid artery, and TCD to those in a wider area of the anterior circulation, i.e., from the petrous segment of the internal carotid artery to the proximal parts of the anterior and middle cerebral arteries, plus the vertebrobasilar artery (except the terminal part of the basilar artery). The procedure differs slightly among facilities, but, at the facility of the principal author, it has been performed via the transfemoral approach under general anesthesia and general heparinization in all patients. A 7Fr ultra-long sheath (Shuttle, Cook Medical) was placed in the target internal carotid artery, a 6Fr distal support catheter (Navien, Medtronic/Covidien) was advanced through the sheath to a site near the aneurysm, the delivery catheter was guided from this site to distal parts of the vessel beyond the neck by a micro guidewire, and Pipeline was deployed and placed. Since the placement of a coil in the aneurysm was prohibited by the protocol of the clinical trial, it was not performed. The perioperative management was nearly the same as that in stent-assisted coil embolization, but implementation of strict 125
3 Oishi H and Sakai N Inclusion criteria Table 1 Inclusion/exclusion criteria for the Japanese sclinical trial of pipeline Aged 20 years or above and 75 years or less Having a single target cerebral aneurysm The target cerebral aneurysm being located in the petrous, cavernous, or ophthalmic (anterior clinoid, ophthalmic artery, superior hypophyseal artery) segment of the internal carotid artery The neck of the target cerebral aneurysm being 4 mm or unidentifiable, and the maximum dome diameter being 10 mm The diameters of the parent artery in the distal/proximal parts of the target cerebral aneurysm being mm Patients having consented in writing using the consent form approved by the clinical trial review committee Patients having intellectual abilities sufficient for the participation and being able to observe items required by the trial protocol Exclusion criteria (1) Patients having 2 or more cerebral aneurysms that require treatment within 180 days (2) Patients having suffered subarachnoid hemorrhage within the past 60 days (3) Patients having suffered intracranial hemorrhage within the past 42 days (4) Patients having undergone major surgery within the past 42 days (5) Patients having unstable neuropathy (exacerbation of clinical symptoms being observed within the past 30 days) (6) Patients with a history of irreversible hemorrhagic disease (7) Patients with a platelet count of less than /mm 3 or platelet dysfunction (8) Patients who are intolerant to, or have a history of adverse reaction or contraindications to, the drug used in the trial (9) Patients in whom a stent is already placed in the area of the target cerebral aneurysm (10) Patients with contraindications to CT scan or MRI (11) Patients with medically uncontrollable allergy to the angiographic contrast agent (12) Patients with severe allergy to platinum or cobalt-chromium alloy (13) Patients with relative contraindications to angiography (such as a serum creatinine level surpassing 2.5 mg/dl) (14) Possibly pregnant women in whom a negative gestation test cannot be confirmed (15) Patients in whom active infection has been confirmed during treatment (16) Patients with disorders of the heart, blood, brain, or intracranial blood vessels (severe heart failure, atrial fibrillation, known carotid artery stenosis, etc.) at a high risk of developing neurological events (17) Patients in whom the 180-day follow-up cannot be completed or those with life-threatening complications or disorders (18) Patients with more than 50% stenosis in the extracranial carotid artery (19) Patients with more than 50% stenosis in the intracranial portion of the treated vessel (20) Patients presently participating in a clinical trial of another drug or medical device in which major evaluations have not been completed or are expected to clinically interfere with the evaluation of this clinical trial 126
4 Repor t of Flow Diver ter Clinical Trials in Japan Fig year-old female with asymptomatic left ICA aneurysm. (A) Pretreatment working projection. (B) Pipeline 5 mm/10 mm was deployed. (C) Angiography showing flow stagnation ( eclipse sign ) just after pipeline deployment. (D) 6-month follow-up angiography showing complete aneurysm occlusion. ICA: internal carotid artery antiplatelet therapy is required in the Japanese clinical trial to avoid ischemic complications. In all procedures using these FDs, dual antiplatelet therapy with aspirin and clopidogrel is required to be initiated from at least about 1 week before the treatment, and to be continued until 6 months after the treatment. While the evaluation of platelet aggregation inhibition activity using the Verify Now system (Accumetrics Inc., San Diego, CA, USA) is not essential in the protocol, it is actually evaluated in many patients, and patients in whom the platelet aggregation inhibitory activity is considered insufficient are excluded from the subjects of clinical trials. Concerning the efficacy and safety, the primary endpoint was Complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure, and a secondary endpoint was severe ipsilateral stroke or neurologic deaths within 180 days after the procedure. Results In Japan, the clinical trial was performed at four facilities: Kobe City Medical Center General Hospital (seven patients), Juntendo University (six patients), Nagoya University (five patients), and Kyoto University (four patients), and a total of 127
5 Oishi H and Sakai N Fig year-old male with asymptomatic right ICA aneurysm. (A) Pretreatment working projection. (B) 6-month follow-up angiography, 2 devices (SJN mm/50 mm, 4 mm/30 mm) telescopically deployed, showing nearly complete aneurysm occlusion. ICA: internal carotid artery Fig year-old male with asymptomatic right vertebral artery fusiform aneurysm. (A) Pretreatment working projection. (B) TCD mm/23 mm was deployed. (C) 6-month follow-up angiography showing complete aneurysm occlusion. 22 patients (aged years with a mean of 63.5 years, 20 females), with 22 aneurysms were registered. The lesions were unruptured in 21 patients and in the chronic period after rupture in 1. Ten patients were symptomatic, with three having visual disturbance, five having oculomotor nerve palsy, and two having abducens nerve palsy. The sites of the aneurysms were the petrous segment in one (4.5%), cavernous segment in 11 (50%), genu of the internal carotid artery in two (9.1%), superior hypophyseal segment in two (9.1%), ophthalmic segment in four (18.2%), and anterior clinoid segment in two (9.1%). Regarding the size of the aneurysms, the mean dome diameter was 18.1 (10 35) mm, mean neck diameter was 8.9 ( ) mm, and mean dome/neck ratio was 2.1 ( ). The shape of the aneurysms was saccular in 21 and fusiform in one. The procedure was completed in 21 (95.5%) of the 22 lesions, and attempted in one. The number of Pipelines used was 31 (mean: 1.48/patient, 1 in 12 patients), complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure, which was the primary endpoint, was achieved in 61.9% of the patients (13/21, 95% confidence interval: %), and severe ipsilateral stroke or neurologic death within 180 days after the procedure, which was a major secondary endpoint, was observed in 9.1% of the patients (2/22, 95% confidence interval: %). Both patients who had events corresponding to the secondary endpoint had subarachnoid hemorrhage due to rupture of the target aneurysm. Discussion Occlusion effect According to the literature concerning the treatment for cerebral aneurysms using Pipeline, the mean complete occlusion rate 6 months after the treatment is 79.7 ( )%. 1 4) 128
6 Repor t of Flow Diver ter Clinical Trials in Japan Table 2 Achievement rates of primary and secondary endpoints in the PUFS study and the Japanese clinical trial of pipeline Primary endpoint Complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure Major secondary endpoint Occurrence of severe ipsilateral stroke or neurologic death related within 180 days after the procedure PUFS: pipeline for uncoilable or failed aneurysms; CI: confidence interval PUFS study (N = 103) 72.8% (75/103) 95%CI (63.5% 80.5%) 5.6% (6/107) 95%CI (2.6% 11.7%) Japanese clinical trial (N = 21) 61.9% (13/21) 95%CI (38.4% 81.9%) 9.1% (2/22) 95%CI (1.1% 29.2%) Table 3 Achievement rates of the primary endpoint in the PUFS study and the Japanese clinical trial of pipeline according to the morphological type of aneurysm PUFS study (N = 103) Japanese clinical trial (N = 21) Aneurysm size 18.3, , 17.0 Mean, median (mm) Achievement rate of primary endpoint in aneurysms 18 mm in diameter 72.7% (40/55) 58.3% (7/12) Achievement rate of primary endpoint in aneurysms >18 mm in diameter 72.9% (35/48) 66.7% (6/9) Neck length Mean, median (mm) 8.8, , 7.1 Achievement rate of primary endpoint in aneurysms 8 mm in diameter 75.5% (37/49) 75.0% (9/12) Achievement rate of primary endpoint in aneurysms >8 mm in diameter 70.4% (38/54) 44.4% (4/9) Dome/neck ratio Mean, median (mm) 1.78, , 1.70 Achievement rate of primary endpoint in aneurysms 1.8 in diameter 71.2% (42/59) 66.7% (8/12) Achievement rate of primary endpoint in aneurysms >1.8 in diameter 75.0% (33/44) 55.6% (5/9) Primary endpoint: Complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure. PUFS: pipeline for uncoilable or failed aneurysms Table 4 Achievement rates of the primary endpoint in the PUFS study and the Japanese sclinical trial of pipeline according to the site of aneurysm PUFS study (N = 103) Japanese clinical trial (N = 21) Petrous Cavernous segment 68.9% (31/45) 81.8% (9/11) Genu Superior hypophyseal segment 75.9% (44/58) 40.0% (4/10) Primary endpoint: Complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure. PUFS: pipeline for uncoilable or failed aneurysms When PUFS, 1) which is a pivotal study that showed the efficacy of Pipeline, and the Japanese clinical trial of Pipeline are compared, concerning the state of occlusion 180 days after treatment, complete occlusion was observed in 86.8%, the neck persisted in 5.5%, and the aneurysm persisted in 5.5% in PUFS, but in 61.9% (13/21), 9.5% (2/21), and 28.6% (6/21), respectively, in the Japanese trial, with a lower complete occlusion rate (Table 2). The causes of these differences are unclear, but sub-analysis suggested the involvement of some factors. Table 3 shows the achievement rates of the primary endpoint, i.e., differences in efficacy, according to the size, neck length, and dome/neck ratio. While the achievement rate of the primary endpoint showed no marked correlation with the aneurysm size or dome/neck ratio, it was 75% when the neck length was 8 mm or less but was clearly lower at 44.4% when the neck length exceeded 8 mm. However, no such effect was observed in PUFS. Table 4 shows the differences in the achievement rate of the primary endpoint according to the location of the aneurysm. The achievement rate was lower in lesions located from the genu to the 129
7 Oishi H and Sakai N Table 5 Achievement rates of the primary endpoint in the PUFS study and the Japanese clinical trial of Pipeline according to the presence or absence of obstruction of the blood flow PUFS study (N = 103) Japanese clinical trial (N = 21) Blood flow obstructed 73.3% (88/90) 68.8% (11/16) Blood flow not obstructed 69.2% (9/13) 40.0% (2/5) Device not overstretched Device overstretched Blood flow obstructed 73.3% (88/90) 80% (8/10) 50% (3/6) Blood flow not obstructed 69.2% (9/13) 100% (2/2) 0% (0/3) Primary endpoint: Complete occlusion of the target intracranial aneurysm and 50% or less stenosis of the parent artery 180 days after the procedure. PUFS: pipeline for uncoilable or failed aneurysms superior hypophyseal segment of the internal carotid artery than in those located from the petrous to the cavernous segment. Interestingly, when the device was placed over 1.5 times the nominal length, causing a decrease in the metal coverage rate of the neck due to overstretching of the device, the achievement rate of the primary endpoint was markedly reduced. It was 83.3% (10/12) when the device was not overstretched but was 33.3% (3/9) when it was overstretched. This suggests that complete occlusion is likely to be achieved if the device can be placed without overstretching but that the risk of incomplete occlusion increases if it is placed in an overstretched state. Theoretically, if the device is placed appropriately, the eclipse sign in the late phase of angiography due to laminar stagnation of the contrast agent in the aneurysm, indicating obstruction of the blood flow, is likely to appear with consequent complete occlusion of the aneurysm. As shown in Table 5, the achievement rate of the primary endpoint tended to be lower in patients who failed to show the eclipse sign in the Japanese clinical trial. However, whether or not obstruction of the blood flow occurred did not affect the achievement rate of the primary endpoint in the PUFS study, and favorable results were also obtained in the Japanese clinical trial if overstretching of the device was avoided regardless of whether the blood flow was obstructed or not. Therefore, it may be unnecessary to adhere to obstruction of the blood flow immediately after treatment. Number of devices used The mean number of devices used per aneurysm differed between PUFS (3.2) and the Japanese clinical trial (1.5). While no marked difference was observed in the neck length of the target aneurysms between the two trials, the use of devices more than 20 mm long was restricted in PUFS, and this possibly affected the results. However, it is occasionally difficult to deploy and place a device exceeding 20 mm in length, and, if there is nearly 2 mm difference between the maximum and minimum diameters of the parent vessel, telescoping of multiple devices matched to the vascular diameter is advantageous for avoiding insufficient apposition with the vascular wall or overstretching. The possibility that the outcome was affected by the therapeutic strategy of the operator cannot be excluded. Hemorrhagic complications According to the review of the literature by Murthy et al., hemorrhage in the cerebral parenchyma occurred in 2.3%, and subarachnoid hemorrhage occurred in 1.1% of the patients after treatment using Pipeline. 5) In PUFS, five cases (4.7%) of intracranial hemorrhage were reported, but they were all intraparenchymal hemorrhage unrelated to the target intracranial aneurysm, and no subarachnoid hemorrhage was observed. In the Japanese clinical trial, subarachnoid hemorrhage due to rupture of the target intracranial aneurysm occurred in two patients, i.e., one with unruptured aneurysm and one treated in the chronic period after rupture, 34 and 118 days, respectively, after treatment, and resulted in death. Since about 6 months to 1 year after placement of an FD is necessary until complete thrombosis of an aneurysm, the risk of rupture is considered to persist during this period. Furthermore, the severity of subarachnoid hemorrhage is considered to be increased by the necessity of performing multiple drug antiplatelet therapy for a period after treatment. As causes of rupture, changes in the shear stress of the aneurysmal wall, changes in the hemodynamics restricting the outflow more than the inflow, and autolysis of the arterial wall secondary to the red thrombus formation associated with inflammatory reaction have been reported. 15,16) Some reports suggest that the risk of postoperative rupture is high in giant aneurysms, symptomatic aneurysms that show rapid increase in size or instability of the aneurysmal wall, aneurysms with an aspect ratio greater than 1.6, and those that show jet-like blood flow inside before or after the placement of an FD and recommend coil embolization for such lesions. 15,17) The authors performed additional coil embolization in patients considered to 130
8 Repor t of Flow Diver ter Clinical Trials in Japan Fig year-old female with symptomatic left ICA aneurysm. The aneurysm showed risks of delayed rupture such as high aspect ratio >1.6 and inflow jet. (A) Pretreatment working projection. (B) Pipeline Flex 3.25 mm/20 mm was deployed. (C) Platinum coils were inserted from jailed microcatheter. (D) Posttreatment angiography showing sufficient aneurysm occlusion. ICA: internal carotid artery be at a high risk of postoperative rupture by treatment with Pipeline alone (Fig. 7). Ischemic complications According to the review of the literature by Murthy et al., ischemic stroke occurred in 1.9% of the patients. 5) Ischemic stroke occurred in four (3.7%) in PUFS but did not occur in the Japanese clinical trial of Pipeline. Careful evaluation of the inhibitory effect on platelet aggregation was performed before treatment using Verify Now, etc., and poor responders to antiplatelet drugs were excluded from the subjects. This may have been a reason for the absence of ischemic stroke. Conclusion The FD is undoubtedly a revolutionary device in the treatment of large/giant intracranial aneurysms except those in the acute period after rupture, but there remain a number of unsolved problems such as the necessity of technical proficiency for the placement of the FD to obtain the maximum therapeutic effect, persistence of the risk of intracranial hemorrhage after treatment because of a lack of the establishment of an appropriate dose and time of termination of antiplatelet medication, and a lack of confirmation of the long-term preventive effect against rupture or enlargement of the aneurysm 131
9 Oishi H and Sakai N and the necessity for measures to cope with them. Therefore, the FD should be used by carefully comparing its safety and efficacy with those of existing endovascular treatment techniques represented by stent-assisted coil embolization and direct surgery (bypass surgery, clipping), and it is necessary to develop the therapy while clarifying early experience in Japan by various investigations including the PMS. Acknowledgments The institutional principal investigators and co-investigators of the Japanese clinical trial of Pipeline were Nobuyuki Sakai and Hirotoshi Imamura at Kobe City Medical Center General Hospital, Hidenori Oishi and Munetaka Yamamoto at Juntendo University, Shigeru Miyaji and Takatsugu Izumi at Nagoya University, and Akira Ishii and Takayuki Kikuchi at Kyoto University. Disclosure Statement The author, Hidenori Oishi, has self-reported conflict of interest (COI) to the Japan Neurosurgical Society. The COI that the first author should disclose in connection with this paper are that he has received 1 million yen or more annually from Medtronic Japan for the time and effort required for the attendance (presentation) at conferences and 2 million yen or more annually from Medtronic Japan as a scholarship donation to the endowed chair. The author Nobuyuki Sakai has self-reported COI to the Japan Neurosurgical Society. The COI that the co-author should disclose in connection with this paper is that he has received 1 million yen or less from Medtronic Japan for the attendance (presentation) at conferences. References 1) Becske T, Kallmes DF, Saatci I, et al: Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology 2013; 267: ) Lylyk P, Miranda C, Ceratto R, et al: Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery 2009; 64: ; discussion ; quiz N6. 3) Nelson PK, Lylyk P, Szikora I, et al: The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol 2011; 32: ) Szikora I, Berentei Z, Kulcsar Z, et al: Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest experience with the pipeline embolization device. AJNR Am J Neuroradiol 2010; 31: ) Murthy SB, Shah S, Venkatasubba Rao CP, et al: Treatment of unruptured intracranial aneurysms with the pipeline embolization device. J Clin Neurosci 2014; 21: ) Kulcsar Z, Houdart E, Bonafe A, et al: Intra-aneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol 2011; 32: ) Tateshima S, Jones JG, Mayor Basto F, et al: Aneurysm pressure measurement before and after placement of a Pipeline stent: feasibility study using a inch pressure wire for coronary intervention. J Neurointerv Surg doi: /neurintsurg ) Siddiqui AH, Kan P, Abla AA, et al: Complications after treatment with pipeline embolization for giant distal intracranial aneurysms with or without coil embolization. Neurosurgery 2012; 71: E509 E513; discussion E
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