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Online February 8, 2017 Journal of Neuroendovascular Therapy 2017; 11: 192–196 DOI: 10.5797/jnet.cr.2016-0085

A Case of Embolic due to a Thrombosed Cerebral that Underwent Mechanical Thrombectomy

Ryuta Yasuda, Naoki Toma, Yoshinari Nakatsuka, Fumihiro Kawakita, Yasuyuki Umeda, Seiji Hatazaki, Mai Nampei, Masato Shiba, Hiroshi Sakaida, and Hidenori Suzuki

Objective: We report a case of embolic stroke due to a thrombosed cerebral aneurysm that underwent mechanical thrombectomy. Case Presentation: A 39-year-old female was brought to our hospital by an ambulance with sudden left hemiparesis and dysarthria. Detailed examination revealed a partially thrombosed aneurysm of the right internal carotid and of the right middle cerebral artery. Emergent mechanical thrombectomy was performed, and in cerebral (TICI) 2b recanalization was achieved. There was no other potential source of cerebral embolism, and the thrombosed aneurysm was considered an etiology for the embolism. After the endovascular treatment, antiplatelet and anticoagulant therapies were conducted, leading to the disappearance of the intra-aneurysmal . Conclusion: Mechanical thrombectomy is effective for embolic stroke due to an unruptured thrombosed cerebral aneurysm if devices are carefully manipulated in an area adjacent to the aneurysm.

Keywords▶ thrombosed cerebral aneurysm, thromboembolism, mechanical embolectomy

Introduction Social history: No history of smoking or alcohol consumption. Acute ischemic stroke (AIS) due to thromboembolism from Present illness: In February 2016, she was brought to our hos- unruptured thrombosed aneurysm is rare and its incidence pital by an ambulance because of sudden onset of left hemipa- is reported approximately 0.5% of unruptured .1,2) resis and dysarthria, with an onset-to-door time of 62 minutes. In this report, we describe a patient of embolic stroke Physical examination on admission: Right-handedness. due to a thrombosed cerebral aneurysm that underwent (height, 165 cm; body weight, 77.6 kg). Glasgow mechanical thrombectomy, and review the literature. Come Scale (GCS): E3, V5, and M6. Right conjugate devi- ation, dysarthria, left hypesthesia, and left hemiparesis Case Presentation were noted, resulting in the National Institutes of Health Stroke Scale score of 12 points. Patient: A 39-year-old female. Electrocardiography showed sinus rhythm and there was Medical history: Not contributory. However, she had taken no . CT did not reveal any- hemor an estrogen preparation for irregular menstruation until rhagic lesions, and a part of the right middle cerebral artery 1 week prior to the onset. (MCA) was visualized as a high signal intensity. No aortic dissection or thrombus was suggested on chest CT. Brain Department of Neurosurgery, Mie University Graduate School of MRI showed scattered high-signal-intensity areas in the Medicine, Tsu, Mie, Japan right MCA territory on diffusion-weighted images, resulting

Received: July 24, 2016; Accepted: November 3, 2016 in the Alberta Stroke Program Early CT Score of 7 points Corresponding author: Ryuta Yasuda. Department of Neurosurgery, (Fig. 1a). Brain MRA revealed that the right MCA was Mie University Graduate School of Medicine, 2-174 Edobashi, interrupted at the M1 segment. In the right internal carotid Tsu, Mie 514-8507, Japan artery (ICA), the presence of a thrombosed aneurysm mainly Email: [email protected] localized in the cavernous sinus was suggested (Fig. 1b). This work is licensed under a Creative Commons Attribution-NonCommercial- Endovascular treatment (EVT): Alteplase was not admin- NoDerivatives International License. istered although there was no contraindication, and the ©2017 The Japanese Society for Neuroendovascular Therapy patient was transferred to the cerebral room.

192 Journal of Neuroendovascular Therapy Vol. 11, No. 4 (2017) A Case of Embolic Stroke due to a Thrombosed Cerebral Aneurysm

Fig. 1 (a) MRI diffusion-weighted images show high intensity signals in the territory of the right MCA. (b) Initial MRA (left) demonstrates disruption of the right MCA M1 segment. The MRA and FLAIR image (right) suggest the existence of a large thrombosed aneurysm at the right ICA, whose main part is in the cavern- ous sinus. (c) Follow-up MRA (left) and FLAIR image (right) obtained 1 month after admission demonstrate the disappearance of the intra-aneurysmal thrombus and complete recanalization of the aneurysm. Patency of the right MCA is preserved. ICA: internal carotid artery; MCA: middle cerebral artery

Initially, diagnostic angiography was performed through not achieved. At this point, the patient’s restless became right femoral puncture (door-to-puncture time: 65 minutes), marked and the 5MAX ACE had fallen to the and interruption at the right M1 segment and a large aneu- cervical region. As it appeared difficult to continue the rysm of the right ICA were detected. A contrast defect procedure safely, general anesthesia was promptly induced suggested partial thrombosis of the aneurysm (Fig. 2a). avoiding a decline in the blood pressure, and then the EVT Systemic heparinization was conducted to maintain the acti- was continued. A Trevo XP 4 × 20 mm (Stryker, MI, USA) vated clotting time at 200 seconds or more, and a 9 Fr was advanced (Fig. 2b) through the Penumbra 5MAX Optimo (Tokai Medical Products Inc., Aichi, Japan) was ACE carefully inserted again to the distal side of the aneu- inserted into the right cervical ICA. Using coaxial system of rysm. In spite of two passes of the Trevo XP, recanaliza- a Penumbra 5MAX ACE and a Penumbra 3MAX (Medico’s tion was not achieved. Finally, a Solitaire FR 4 × 15 mm Hirata Inc., Osaka, Japan), the Penumbra 5MAX ACE was (Covidien, CA, USA) was employed instead of the Trevo carefully advanced to the distal side of the aneurysm. The XP, leading to Thrombolysis in cerebral infarction (TICI) Penumbra 3MAX was then guided to the proximal end of 2b recanalization (Fig. 2c, onset-to-reperfusion time: the M1 thrombus, and a direct aspiration first pass technique 286 minutes). On final 3D angiography, the maximum (ADAPT)3) was performed. However, recanalization was diameter of the right ICA aneurysm was 17 mm, and a

Journal of Neuroendovascular Therapy Vol. 11, No. 4 (2017) 193 Yasuda R, et al.

Fig. 2 (a) Initial right ICAG demonstrates occlusion of the right MCA M1 segment as well as a partially thrombosed large aneurysm at the right carotid siphon. Develop- ment of collateral pathways is poor. (b) A Penumbra 5MAX ACE is placed at the right M1 (left, arrow) carefully passing the aneurysm. After confirming a microca- theter is in the true M2 lumen (left, arrowhead), a retriever is deployed (right, arrowhead). (c) Final right ICAG shows TICI 2b recanalization of the right MCA. ICAG: internal carotid angiogram; MCA: middle cerebral artery; TICI: thrombolysis in cerebral infarction contrast defect due to partial thrombosis was observed disorder or autoimmune disease, was ruled out. The results of (Fig. 3). her blood test were as follows: the count, prothrombin Postoperative course: Heparin was naturally reversed and time (PT), activated partial thromboplastin time (APTT), the intravenous administration argatroban was started fibrinogen level, D-dimer level, and a2-plasmin inhibitor (dose: 60 mg/day on the day of surgery and first postoper- complex (PIC) level were 316 × 103/µL, 15.7 seconds, 34.4%, ative day, 20 mg/day for 5 days starting from the second 251 mg/dL, 0.44 µg/mL, and 0.4 µg/m, respectively. The anti- postoperative day). Subsequently, clopidogrel at 75 mg/day SS-A and anti-SS-B antibodies were negative. The anti-DNA, and edoxaban at 30 mg/day were orally administered. On antinuclear, and anti-cardiolipin antibody levels were MRI the day after the EVT, the known infarcted focus in the 3.5 IU/mL, 40-fold, and 1.0 U/mL, respectively. The lupus right MCA territory became more visible, but no further anticoagulant was negative. Her protein C and S activities infarction or hemorrhagic complication was detected. The were 107% and 74%, respectively. Based on these results, possibility of cardiogenic embolism or any other disease thromboembolism related to the partially thrombosed aneu- that causes juvenile cerebral infarction, such as coagulation rysm of the right ICA was considered an etiology for the

194 Journal of Neuroendovascular Therapy Vol. 11, No. 4 (2017) A Case of Embolic Stroke due to a Thrombosed Cerebral Aneurysm

Fig. 3 3D rotational angiogram of the right ICA and its source image show aneurysmal filling defect due to intra-aneurysmal thrombus (arrow). ICA: internal carotid artery cerebral infarction. MRI 1 month after the EVT revealed no Therefore, administration of alteplase to AIS patients should recurrence of infarction and the patency of the right MCA was not be hesitated for the presence of cerebral aneurysm alone. maintained. The intra-aneurysmal thrombus had disappeared However, in the present case, because the aneurysm was and the aneurysm completely recanalized (Fig. 1c). At large and its relationship with the parent artery was unclear, the time the patient was referred to a rehabilitation hospital in performing EVT there were concerns that devices were 30 days after the onset, her modified Rankin Scale (mRS) was unable to pass the aneurysm or that devices migrate into the evaluated as grade 4 mainly due to left hemiparesis, which aneurysm which cause further distal embolism by releasing had improved to grade 2 at the time of 90 days after the onset. the residual thrombus. Considering the possibility of switch- ing EVT to embolectomy17) under craniotomy, administra- Discussion tion of alteplase was not performed intentionally. It is reported that the addition of EVT to administration of The incidence of unruptured cerebral aneurysms compli- alteplase did not increase the risk of aneurysmal hemorrhage cated by AIS is unexpectedly high. Oh et al.1) reported that in AIS patients harboring cerebral aneurysms.16) In the unruptured cerebral aneurysms accounted for 6.6% of AIS present case, besides device-related perforation of the aneu- patients, which is higher than the incidence of unruptured rysm, it was necessary to concern further distal embolism cerebral aneurysms in a general population (approximately because thrombus remained in the aneurysm. We considered 3%).4) However, the rate of unruptured cerebral aneurysms to minimalize the frequency for the 5MAX ACE to pass the causing AIS is much lower and it is reported approximately aneurysm during the EVT. In contrast to our case in which 0.5%.1,2) Although such condition is relatively rare, it is the presence of an aneurysm is known before EVT, there are commonly recognized and there have been several case some cases in which an aneurysm is hidden along an series or case reports in which an intra-aneurysmal throm- occluded vessel. In such cases, careful wire manipulation bus caused embolism of the distal cerebral artery, as demon- and fluoroscopic monitoring are necessary in advancing a strated in the present case, or growth of an intra-aneurysmal device to the distal side of the occluded vessel.10,11) Although thrombus led to occlusion of the parent artery.1,2,5–12) Penumbra systems10,11) and stent retrievers12) have been used Several studies reported that the administration of for mechanical thrombectomy in AIS patients harboring alteplase to AIS patients harboring unruptured cerebral cerebral aneurysms, in cases of a hidden aneurysms the for- aneurysms did not increase the risk of hemorrhage from the mer appears safer because there is no need to pass the site of aneurysms or symptomatic .13–16) occlusion.

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Antithrombotic therapy for thrombosed cerebral aneu- 4) Vlak MH, Algra A, Brandenburg R, et al: Prevalence of rysms complicated by AIS has not been established. unruptured intracranial aneurysms, with emphasis on sex, Although many studies adopted antiplatelet therapy for age, comorbidity, country, and time period: a systematic follow-up,5) some authors conducted anticoagulant therapy review and meta-analysis. Lancet Neurol 2011; 10: 626–636. in the acute phase, and then, switched it to antiplatelet ther- 5) Qureshi AI, Mohammad Y, Yahia AM, et al: Ischemic events associated with unruptured intracranial aneurysms: apy,9) and others combined two antiplatelet drugs.10) In the multicenter clinical study and review of the literature. present case, considering the possibility of a hypercoagula- Neurosurgery 2000; 46: 282–289; discussion 289–290. bility state related to an estrogen preparation before the 6) Friedman JA, Piepgras DG, Pichelmann MA, et al: Small admission, an anticoagulant was administered in addition to cerebral aneurysms presenting with symptoms other than an antiplatelet, leading to the disappearance of the intra- rupture. 2001; 57: 1212–1216. aneurysmal thrombus. Anticoagulant therapy might be 7) Schaller B, Lyrer P: Focal neurological deficits following combined for individual patients depending on the presence spontaneous thrombosis of unruptured giant aneurysms. or absence of an underlying disease or thrombus volume. Eur Neurol 2002; 47: 175–182. Concerning future treatment for cerebral aneurysms, it is 8) Smrcka M, Ogilvy ChS, Koroshetz W: Small aneurysms as reported that stroke onset of thrombosed aneurysms suggests a cause of thromboembolic stroke. Bratisl Lek Listy 2002; impending aneurysmal rupture, and thus early treatment of the 103: 250–253. aneurysms is desirable.18) However, in the present case, we 9) Shimada T, Toyoda K, Hagiwara N, et al: Recurrent embolic stroke originating from an internal carotid aneurysm in a selected a strategy to treat the aneurysm in the chronic stage, young adult. J Neurol Sci 2005; 232: 115–117. taking priority over recovery-phase rehabilitation for the fol- 10) Torikoshi S, Akiyama Y: A Concealed lowing reasons: since the locus of the aneurysm was the cav- detected after recanalization of an occluded vessel: a case ernous sinus, the risk of is lower report and literature review. Interv Neurol 2016; 4: 90–95. than that of aneurysms in other sites, and her mRS grade was 11) Kühn AL, Hou SY, Spilberg G, et al: Visualization of a 4, which requires aggressive rehabilitation in the acute stage. small hidden intracranial aneurysm during endovascular thrombectomy for acute MCA occlusion. J Vasc Interv Conclusion Neurol 2014; 7: 47–49. 12) Singh J, Wolfe SQ: Stent retriever thrombectomy with We encountered a patient with cerebral embolism due to an aneurysm in target vessel: Technical note. Interv Neu- unruptured thrombosed cerebral aneurysm. Mechanical roradiol 2016; 22: 544–547. thrombectomy for such a type of cerebral embolism is 13) The Japan Stroke Society. Guidelines for Proper Execution effective if devices are carefully manipulated at an area of Intravenous rt-PA (alteplase) Therapy. 2nd Edition. Jpn J Stroke (in Japanese) http://www.jsts.gr.jp/img/rt-PA02.pdf adjacent to the cerebral aneurysm. After the EVT, anti- (accessed July, 01, 2016). platelet and anticoagulant therapies were performed, lead- 14) Edwards NJ, Kamel H, Josephson SA: The safety of intra- ing to the disappearance of the intra-aneurysmal thrombus. venous thrombolysis for ischemic stroke in patients with pre-existing cerebral aneurysms: a case series and review Disclosure Statement of the literature. Stroke 2012; 43: 412–416. 15) Mittal MK, Seet RC, Zhang Y, et al: Safety of intravenous There is no conflict of interest for the author and coauthors. thrombolysis in acute ischemic stroke patients with saccu- lar intracranial aneurysms. J Stroke Cerebrovasc Dis 2013; References 22: 639–643. 16) Mowla A, Singh K, Mehla S, et al: Is acute reperfusion ther- 1) Oh YS, Lee SJ, Shon YM, et al: Incidental unruptured intra- apy safe in acute ischemic stroke patients who harbor unrup- cranial aneurysms in patients with acute ischemic stroke. tured intracranial aneurysm? Int J Stroke 2015; 10: 113–118. Cerebrovasc Dis 2008; 26: 650–653. 17) Inoue T, Tamura A, Tsutsumi K, et al: Surgical embolec- 2) Calviere L, Viguier A, Da Silva NA, et al: Unruptured tomy for large vessel occlusion of anterior circulation. Br J intracranial aneurysm as a cause of cerebral . Clin Neurosurg 2013; 27: 783–790. Neurol Neurosurg 2011; 113: 28–33. 18) Guillon B, Daumas-Duport B, Delaroche O, et al: Cerebral 3) Turk AS, Frei D, Fiorella D, et al: ADAPT FAST study: a ischemia complicating intracranial aneurysm: a warning direct aspiration first pass technique for acute stroke throm- sign of imminent rupture? AJNR Am J Neuroradiol 2011; bectomy. J Neurointerv Surg 2014; 6: 260–264. 32: 1862–1865.

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