Journal Pre-proof Delayed rebleeding from pseudoaneurysm after mechanical thrombectomy using a stent retriever due to small artery avulsion confirmed by open surgery: A case report Taichiro Imahori, MD, PhD, Yusuke Okamura, MD, PhD, Junichi Sakata, MD, PhD, Hiroyasu Shose, MD, Shunsuke Yamanishi, MD, Eiji Kohmura, MD, PhD PII: S1878-8750(19)32585-9 DOI: https://doi.org/10.1016/j.wneu.2019.09.141 Reference: WNEU 13441 To appear in: World Neurosurgery Received Date: 6 September 2019 Revised Date: 25 September 2019 Accepted Date: 26 September 2019 Please cite this article as: Imahori T, Okamura Y, Sakata J, Shose H, Yamanishi S, Kohmura E, Delayed rebleeding from pseudoaneurysm after mechanical thrombectomy using a stent retriever due to small artery avulsion confirmed by open surgery: A case report, World Neurosurgery (2019), doi: https:// doi.org/10.1016/j.wneu.2019.09.141. 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All rights reserved. 1 2 3 4 Delayed rebleeding from pseudoaneurysm after mechanical thrombectomy using a stent retriever due to small artery avulsion confirmed by open surgery: A case report 5 6 Taichiro Imahori, MD, PhDa, Yusuke Okamura, MD, PhDa, Junichi Sakata, MD, PhDa, 7 Hiroyasu Shose, MDa, Shunsuke Yamanishi, MDa, Eiji Kohmura, MD, PhDb a 8 Department of Neurosurgery, Toyooka Hospital, Hyogo, Japan b 9 Department of Neurosurgery, Kobe University Graduate School of Medicine, Hyogo, 10 Japan 11 12 Name and address for correspondence 13 Taichiro Imahori, MD, PhD, 14 Department of Neurosurgery, Toyooka Hospital, 15 1094 Tobera, Toyooka-city, Hyogo 668-8501, Japan 16 E-mail: taichiro.imahori@gmail.com, Tel: +81-79-622-6111, Fax: +81-79-622-0088 17 *Present address: 18 Department of Neurosurgery, Hyogo Brain and Heart Center 19 520 Saisho, Himeji-city, Hyogo 670-0981, Japan 20 E-mail: taichiro.imahori@gmail.com, Tel: +81-79-293-3131, Fax: +81-79-295-8199 21 22 Running title 23 Pseudoaneurysm formation after mechanical thrombectomy 24 25 Key words 26 Acute ischemic stroke; mechanical thrombectomy; stent retriever; pseudoaneurysm; 27 subarachnoid hemorrhage; rebleeding 1 ABSTRACT 1 2 Background: Pseudoaneurysm after mechanical thrombectomy (MT) is rare but is one 3 of the potential complications associated with endovascular procedures. There is limited 4 information regarding its mechanism of formation and the potential risk of delayed 5 bleeding. 6 Case Description: An 84-year-old woman was admitted to our institution with right 7 hemiplegia and global aphasia. Magnetic resonance imaging and angiography revealed 8 occlusion of the M2 segment of the left middle cerebral artery with subtle acute 9 ischemic change in this territory. After initiating intravenous thrombolysis, MT was 10 performed for persistent occlusion of the M2. Successful revascularization was finally 11 achieved with a single pass of a Trevo XP 3 mm × 20 mm stent retriever; significant 12 deviation of the vessel occurred during withdrawal of the stent retriever. 13 Anticoagulation was initiated after confirming resolution of a small amount of 14 post-procedural subarachnoid hemorrhage one day after the procedure. However, 4 days 15 after the procedure, computed tomography and angiography revealed a massive Sylvian 16 hematoma with de novo formation of a small pseudoaneurysm at the site where the stent 17 retriever was deployed. Open surgery revealed a small artery avulsion at this site. The 18 lesion was closed by microsurgical suturing. 19 Conclusions: Angiographic and intraoperative findings showed that the mechanism of 20 formation of the pseudoaneurysm was small artery avulsion resulting from deviation of 21 the vessel during withdrawal of the stent retriever. When performing MT in a tortuous 22 distal vessel, the possibility of small artery avulsion should be kept in mind to both 23 prevent and manage critical hemorrhagic complications. 24 25 1 1 INTRODUCTION 2 Endovascular mechanical thrombectomy (MT) using a stent retriever has been 3 shown to be an effective and safe treatment for acute ischemic stroke caused by large 4 vessel occlusion.1 However, MT is associated with several procedure-related 5 complications, including vessel injury, embolization to a new or distal target vessel 6 territory, problems at the access site, contrast medium-related problems, and 7 post-procedural intracranial hemorrhage.2 It is important to be aware of the mechanisms 8 and potential risks when performing MT to be able to prevent and manage these 9 complications. Vessel perforation leading to disability or death is the most critical 10 hemorrhagic complication associated with vessel injury and is usually noticed on 11 angiography as extravasation of contrast or protrusion of the device outside the vessel. 12 Even when these angiographic features are not found during a procedure, 13 post-procedural subarachnoid hemorrhage (SAH) is commonly observed after MT and 14 is thought to be caused by vessel injury during the procedure. Pseudoaneurysm 15 associated with an endovascular procedure is rare but can occur after MT in such cases 16 with vessel injury.3–5 However, little is known about the mechanism of pseudoaneurysm 17 formation or the potential risk of delayed hemorrhage after MT. 18 Here we report a case of delayed rebleeding from pseudoaneurysm after MT using a 19 stent retriever due to small artery avulsion, which was confirmed by open surgery and 20 closed by direct microsurgical suturing. 21 22 23 2 CASE PRESENTATION 1 2 An 84-year-old woman was admitted to our institution with right hemiplegia and 3 global aphasia 60 minutes after onset of stroke. She had a history of atrial fibrillation 4 and had been taking aspirin 100 mg daily. The National Institutes of Health Stroke 5 Scale score was 31. Magnetic resonance angiography (MRA) revealed occlusion of the 6 distal M2 segment of the left middle cerebral artery (MCA; Figure 1A) and 7 diffusion-weighted imaging showed subtle acute ischemic change involving the left 8 MCA (Figure 1B). Cerebral angiography was performed after initiating intravenous 9 thrombolysis with alteplase. Written informed consent was obtained from a member of 10 the patient’s family before the procedure. 11 Endovascular Procedure 12 The endovascular procedure was performed under local anesthesia via femoral 13 access after systemic heparinization with a bolus dose of 3000 IU. An 8-French 14 balloon-guide catheter was placed in the cervical portion of the left internal carotid 15 artery. Initial angiography confirmed persistent occlusion of the distal M2 of the left 16 MCA (Figure 2A, 2B). An attempt was made to navigate to the MCA using an 17 intermediate support catheter (5 Max ACE; Penumbra, Alameda, CA, USA); however, 18 the catheter was finally placed at the C4 portion of the internal carotid artery because of 19 vessel tortuosity. The occlusion was crossed with a Trevo 14 microcatheter (Stryker, 20 Kalamazoo, MI, USA) and a microguidewire (Figure 2C). After injection of the 21 microcatheter showed the distal artery to be normal, a Trevo XP 3 mm × 20 mm stent 22 retriever (Stryker) was fully deployed across the occluded lesion (Figure 2D). The 23 deployed stent retriever was slowly pulled back under continuous aspiration through the 24 Penumbra catheter. Significant deviation of the vessel occurred during withdrawal of 25 the stent retriever, and was depicted by the location of the distal and proximal markers 26 of the stent retriever (Figure 2E). Post-procedure angiography confirmed successful 27 recanalization (Figure 2F–2H). No extravasation of contrast was detected during the 3 1 procedure. The total time from femoral access to arterial recanalization was 20 minutes 2 and the time from onset of stroke to arterial recanalization was 153 minutes. 3 Postprocedural Course 4 Computed tomography (CT) immediately after the endovascular procedure showed 5 a small amount of SAH (Figure 3A). Intravenous anticoagulation was not initiated after 6 the procedure. The patient’s neurologic symptoms were significantly improved on the 7 day following the procedure, with a National Institutes of Health Stroke Scale score of 4. 8 CT revealed marked resolution of the SAH. MRA performed one day after the 9 procedure confirmed successful revascularization, and diffusion-weighted imaging 10 showed only small ischemic change. Oral edoxaban (30 mg daily) was started 24 hours 11 after the procedure and continued. However, on day 4 after the procedure, the patient 12 complained of headache and her level of consciousness worsened suddenly. A CT scan 13 revealed a massive Sylvian hematoma and CT angiography (CTA) revealed a small 14 budge on the inferior division of the M2 portion of the middle cerebral artery, indicating 15 formation of a pseudoaneurysm. Open surgery was performed to minimize the risk of 16 further bleeding from the pseudoaneurysm 17 Open Surgery 18 A left frontotemporal craniotomy was performed, preserving the branches of the 19 superficial temporal artery. A thick SAH was seen in the Sylvian fissure (Figure 3A). 20 First, a superficial temporal artery to MCA bypass was performed to prepare for 21 temporary or permanent occlusion of the affected artery (Figure 3B). Next, the Sylvian 22 fissure was opened until the distal M2 was visualized, and the affected artery was 23 identified at the bifurcation of the M2. A substantial amount of firm clot around the 24 affected artery was removed, revealing a small artery in the same location as that in 25 which the pseudoaneurysm was seen on preoperative CTA (Figure 3D). The origin of 26 the small artery was almost avulsed with clot (Figure 3E). The artery was totally 27 avulsed while dissecting with a little force using micro forceps (Figure 3F). The avulsed 4 1 lesion was then closed by direct microsurgical suturing with 10-0 nylon (Figure 3H). No 2 further rebleeding occurred after surgery. Three months later, the patient remained 3 dependent with severe aphasia and right hemiparesis. 4 5 1 DISCUSSION 2 We have encountered a case of delayed rebleeding from a pseudoaneurysm after MT 3 using a stent retriever that was confirmed by open surgery and closed by direct 4 microsurgical suturing. The angiographic and intraoperative findings revealed the 5 mechanism of pseudoaneurysm formation to be small artery avulsion resulting from 6 vessel deviation during withdrawal of a stent retriever through the tortuous distal vessel. 7 When treating such vessels, the possibility of small artery avulsion should be kept in 8 mind to both prevent and manage critical hemorrhagic complications. 9 In this case, the angiographic and intraoperative findings confirmed that the 10 mechanism of pseudoaneurysm formation after MT was small artery avulsion 11 associated with vessel deviation during MT. Misaki et al reported a similar case in 12 which rebleeding from a pseudoaneurysm occurred 8 hours after MT using a stent 13 retriever for acute M2 occlusion.3 In that case, although the findings during open 14 surgery indicated only minor injury on the surface of the vessel without any avulsion, 15 the authors speculated that the pseudoaneurysm was caused by avulsion of a fine vessel 16 when withdrawing the stent retriever. The findings in the present case confirm small 17 artery avulsion to be one of the mechanisms underlying formation of a pseudoaneurysm 18 after MT. Other possible mechanisms reported in the literature include direct damage to 19 the vessel wall and worsening dissection caused by the devices used for thrombectomy; 20 therefore, care also should be taken to avoid these problems during the procedure.4,5 21 This case highlights the importance of avoiding small artery avulsion during MT to 22 prevent formation of a pseudoaneurysm and subsequent bleeding. To minimize the risk 23 of small artery avulsion, careful endovascular approach is warranted. It has been 24 reported that MT in a small tortuous vessel using a stent retriever is associated with 25 hemorrhagic complications during the procedure, and stretching of the vessel is thought 26 to be the main cause.6,7 Several techniques, such as half partial deployment of the stent 27 retriever and use of a distal access catheter, have been reported to be useful for avoiding 6 1 stretching.7,8 When treating distal tortuous vessels, these techniques for avoiding the 2 vessel stretching should be considered to be used. 3 It is also important to be aware of the potential association of angiographic findings 4 indicating vessel deviation during the procedure with small artery avulsion. When 5 significant vessel deviation is demonstrated, it may be recommended to evaluate the 6 vessel closely with repeated angiography during endovascular procedure and 7 cerebrovascular imaging with MRA or CTA after procedure. Although the timing of 8 initiation of anticoagulation after MT is controversial, early anticoagulation may not be 9 preferable when both significant vessel deviation and post-procedural SAH are detected, 10 as in the present case. 11 There is limited information regarding the treatment of pseudoaneurysm following 12 MT. In our case, open surgery was performed in view of the risk of further bleeding at 13 the time of the occurrence of a massive Sylvian hematoma with deterioration of 14 consciousness. Care is needed when planning treatment in such cases and should take 15 into account the patient’s overall status. 16 17 7 1 CONCLUSIONS 2 We have encountered a case of delayed rebleeding from a pseudoaneurysm after MT 3 using a stent retriever because of small artery avulsion that was confirmed by open 4 surgery and closed by direct microsurgical suturing. The findings in this patient show 5 that small artery avulsion is one of the mechanisms underlying formation of a 6 pseudoaneurysm after MT. When treating distal tortuous vessels, the possibility of small 7 artery avulsion should be kept in mind to prevent damage and manage critical 8 hemorrhagic complications. 9 10 11 12 13 14 Acknowledgements 15 None 16 17 Formatting of funding sources 18 None 19 20 Competing Interests Statement 21 The authors declare no personal, financial, or institutional interest in any of the drugs, 22 materials, or devices described in this article. 23 24 8 1 REFERENCES 2 1. 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(B) Magnetic resonance diffusion-weighted imaging on 5 admission shows subtle acute ischemic change involving the left middle cerebral artery 6 territory. 7 8 Figure 2. 9 (A, B) Initial angiographic images of the left internal carotid artery (anteroposterior and 10 lateral views) reveal occlusion of the distal M2 portion of the left middle cerebral artery. 11 (C) Injection of a microcatheter after passage of the clot shows the distal portion of this 12 artery to be normal. (D) A Trevo XP 3 mm × 20 mm stent retriever was fully deployed 13 across the occluded lesion. (E) The stent retriever was then withdrawn. Note the 14 significant deviation of the vessel during withdrawal of the stent retriever, depicted by 15 the location of the distal and proximal marker of the stent retriever (arrow). (F) The 16 occluded lesion was recanalized after one pass. (G, H) Final angiographic images of the 17 left internal carotid artery (anteroposterior and lateral views) show successful 18 recanalization. 19 20 Figure 3. 21 (A) A computed tomography (CT) scan obtained immediately after the endovascular 22 procedure shows a small amount of subarachnoid hemorrhage. (B) A CT scan acquired 23 one day following the procedure shows marked resolution of the subarachnoid 24 hemorrhage. (C) Magnetic resonance angiography performed one day after the 25 procedure confirms successful 26 diffusion-weighted image acquired one day following the procedure shows only small 27 ischemic change. (E) A CT scan taken 4 days after the procedure shows a massive revascularization. (D) A magnetic resonance 11 1 Sylvian hematoma. (F) A CT angiogram obtained 4 days after the procedure shows 2 formation of a small pseudoaneurysm (arrow) in the inferior division of the M2 portion 3 of the middle cerebral artery. 4 5 Figure 4. 6 Intraoperative photographs. (A) Thick subarachnoid hemorrhage was seen in the left 7 Sylvian fissure. (B) A superficial temporal artery to middle cerebral artery bypass was 8 initially performed to prepare for the possibility of occlusion of the affected artery. (C, 9 D) A substantial amount of firm clot was identified to be surrounding the affected artery 10 and was removed. (E, F) A small artery was observed at the same site as the 11 pseudoaneurysm detected on computed tomography angiography preoperatively. The 12 origin of the small artery was almost avulsed with clot. The artery was completely 13 avulsed with a little force using micro forceps. (G, H) The avulsed lesion was then 14 closed by direct microsurgical suturing. 15 16 12 1 ABBREVIATIONS 2 CT, computed tomography; CTA, computed tomographic angiography; MCA, middle 3 cerebral artery; MRA, Magnetic resonance angiography; MT, mechanical thrombectomy; 4 SAH, subarachnoid hemorrhage 5 6 1 1 Declarations of interest 2 We herein state, that this manuscript has not been published nor submitted elsewhere. 3 Furthermore, all authors have read and approved the manuscript. Finally, there are no 4 financial arrangements or other relationship that could be construed as a conflict of interest. 5 6 7 1