Clinical Neurology and Neurosurgery 208 (2021) 106862 Contents lists available at ScienceDirect Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro Case Report Endovascular treatment for ruptured cervical anterior spinal artery aneurysm caused by occlusive disease of bilateral vertebral arteries: A case report and literature review Shogo Shima a, b, *, Shinsuke Sato a, b, Tatsuki Motizuki a, Yasunari Niimi b a b Department of Neurosurgery, St. Luke’s International Hospital, 9–1 Akashi-cho, Chuo-ku, Tokyo 104–8560, Japan Department of Neuroendovascular therapy, St. Luke’s International Hospital, 9–1 Akashi-cho, Chuo-ku, Tokyo 104–8560, Japan A R T I C L E I N F O A B S T R A C T Keywords: Endovascular treatment Anterior spinal artery Spinal artery aneurysm Subarachnoid hemorrhage Vertebral artery Case report A cervical anterior spinal artery (ASA) aneurysm not concomitant with vascular malformations is extremely rare, and is treated by conservative management or direct surgery in most cases. The endovascular treatment approach for these lesions is not well-documented. We present a case of a ruptured flow-related cervical ASA aneurysm due to the occlusive disease of the bilateral vertebral arteries (VA) treated by endovascular therapy. A 77-year-old woman with acute onset of headache and right hemiparesis was transferred to our hospital. Computed tomog­ raphy revealed subarachnoid hemorrhage thick in the posterior fossa. A cerebral angiogram showed tandem stenosis of the left VA and the occlusion of the right VA at the V4 segment, with an enlarged C4 radi­ culomedullary artery and a subsequent aneurysm on the ASA. VA angiography revealed retrograde flow through the lesion and ASA axis to posterior circulation, suggesting a flow-related etiology of the aneurysm. We embolized the aneurysm using a flow-directed microcatheter and coils, preserving the ASA axis. Then, we dilated the VA stenosis using stents to prevent aneurysm recurrence by reducing hemodynamic stress on the ASA. 1. Introduction 2. Case presentation Anterior spinal artery (ASA) aneurysms are rare lesions that usually presents with spinal code compression or subarachnoid hemorrhage (SAH). The prevalence rate of SAH due to ASA aneurysm is less than 1%, and most are associated with a spinal vascular malformation [1]. Other etiologies including, connective tissue diseases, trauma, infection, vasculitis, and aortic coarctation, have been reported; however, a flow-related cervical ASA aneurysm without spinal arteriovenous mal­ formation (AVM) or arteriovenous fistula (AVF) is extremely rare [2–5]. Conservative management or direct surgery is commonly chosen as treatment because of its morphological and anatomical characteristics [6,7]. Therefore, the treatment strategy via endovascular approach for this rare lesion is not well known. We report the case of a ruptured ASA aneurysm associated with occlusive lesions of the bilateral vertebral arteries that was treated with endovascular therapy. We also reviewed the literature regarding the anatomical features and treatment of cer­ vical ASA aneurysms. A 77-year-old woman with acute onset of severe headache, nausea, and progressive disturbance of consciousness was transferred to our hospital. She had a past medical history of ischemic stroke, valvular disease, hypertension, and diabetes mellitus. On arrival, her con­ sciousness level was 12 on the Glasgow Coma Scale. Physical exami­ nation revealed right hemiparesis. Computed tomographic (CT) scan showed diffuse SAH in the basal cistern predominantly at the cranio­ cervical junction with hydrocephalus (Fig. 1). CT angiography revealed a dilated ASA and a subsequent 3-mm saccular aneurysm at the level of the third cervical vertebrae (C3) (Fig. 1). Cerebral angiography showed hypoplastic bilateral posterior communicating arteries, suggesting poor collateral supply from the anterior circulation to the posterior. Vertebral artery (VA) angiography revealed severe tandem stenosis of the left VA at V4 segment and occlusion of the right VA at the craniocervical junction. The hypertrophied radiculomedullary artery originated from the C4 level of the right VA, leading to the ASA. Retrograde collateral flow to the posterior circulation through the ASA axis was confirmed, which was thought to cause the saccular aneurysm and SAH (Fig. 2). * Corresponding author at: Department of Neurosurgery, St. Luke’s International Hospital, 9–1 Akashi-cho, Chuo-ku, Tokyo 104–8560, Japan. E-mail address: shisho@luke.ac.jp (S. Shima). https://doi.org/10.1016/j.clineuro.2021.106862 Received 17 July 2021; Received in revised form 27 July 2021; Accepted 29 July 2021 Available online 2 August 2021 0303-8467/© 2021 Elsevier B.V. All rights reserved. S. Shima et al. Clinical Neurology and Neurosurgery 208 (2021) 106862 Fig. 1. Computed tomography (CT) shows thick subarachnoid hemorrhage in the posterior fossa (a) and sagittal view of CT angiography shows a saccular aneurysm (arrow) of the anterior spinal artery at C3 level (b). Fig. 2. Anteroposterior (a) and lateral (b) view of the right vertebral artery (VA) angiography showing the right VA occlusion and an aneurysm (asterisks) on the anterior spinal artery (ASA). The aneurysm is fed by the C4 radicullomedullary artery (arrows). Retrograde collateral flow through the ASA axis to the basilar artery are observed (arrow heads). 2 S. Shima et al. Clinical Neurology and Neurosurgery 208 (2021) 106862 Fig. 3. Pre-coiling anteroposterior view of right VA angiography (a) showing a flow directed microcatheter placed in the aneurysm via C4 radiculomedullary artery (arrow). Post-coiling three-dimensional reconstructed image (b) show the complete obliteration of the aneurysm preserving the ASA axis. Fig. 4. Pre-treatment anteroposterior view of left VA angiography (a) showing the tandem stenosed VA lesions (arrows). Anteroposterior view of fluorography (b) shows the placed stents (white arrows; Neuroform Atlas 4.0 × 21 mm, black arrows; Wingspan 3.5 × 15 mm). The coil mass placed at the aneurysm is also obsereved (asterisk). Post-treatment anteroposterior view of left VA angiography (c) showing the dilated lesions. Endovascular treatment was performed in two stages. First, we embolized the ASA aneurysm to prevent recurrent hemorrhage. A 5-Fr guiding catheter (Fubuki; TOKAI MEDICAL PRODUCTS, Aichi, Japan) was placed in the right VA via 5-Fr femoral access. We then advanced a 1.5-Fr flow-directed catheter (Marathon; Medtronic, Minneapolis, MN, USA) over a microwire (CHIKAI 10; ASHI INTECC, Aichi, Japan) into the 3 S. Shima et al. Clinical Neurology and Neurosurgery 208 (2021) 106862 Table 1 Clinical characteristics of the patients with cervical anterior spinal artery aneurysm without AVF or AVM. Author &Published year Age (yrs) Sex Location Presentation Neurologic finding Size of anerysm (mm) Cause Treatment Clinical outcome Yonas 1980 42 F SAH Stiff neck, LOC 4×5×6 Not stated 66 F Compression Not stated Isolated Vincent 1981 Moore 1982 Kawamura 1999 Jiarakongmun 2002 Walz 2006 30 30 42 F F M C1–2 C1 C1 SAH SAH SAH Quadriplegia, bladder and bowel dysfunction Conservative management Direct surgery (Clip) Died Thomson 1980 Vertebrobasilar junction C1 4 Not stated 4×7 Direct surgery (Clip) Direct surgery (Clip) Direct surgery (Clip) Alive Alive Alive 39 M Cervical SAH Direct surgery (Clip) Alive 58 M C4 Coil embolization Alive Pollock 2009 55 F 36 Direct surgery (Trap & resection) Direct surgery (Clip) Alive Sharma 2010 Karakama 2010 Not stated Isolated Bilateral VA occlusion Coarctation of aorta Moyamoya disease Chiari 1 malformation Coarctation of aorta Dissection Conservative management Alive Trauma (odontoid screw placement) Isolated Conservative management Alive Conservative management C3–C6 laminectomy (decompression) Died Conservative management Embolization of parent A. Died Hemiaresis Headache 12×13 SAH Quadriparesis and quadriparesthesia Headache C2 SAH LOC 2 M C6 Hematomyelia Not stated 51 M C1 SAH Wilson 2011 86 M C1–2 SAH Takashima 2012 SantanaRamirez 2013 84 M C1 Hematomyelia Quadriplegia, urinary and fecal incontinence Neck pain, numbness of extremities, consciouness disturbance Neck pain, occipital neuralgia, occasional falls Quadriplegia 1 F C3–5 Compression Neckpain, quadriparesis 30×18×25 Yang 2013 47 M C2 Posterior fossa SAH Nagahata 2013 70 F NA(cervical) SAH Neck pain, semicomatose state Not stated NA(cervical) 11×11 2.5×1.3 Not stated Not stated 0.7×0.5 Not stated Not stated Congenital vessel abnormalities Not stated Carotid and vertebral rete mirabile Carotid and vertebral rete mirabile Dissection Not stated Not stated Headache, vomiting, consciousness disturbance Headache, neck pain 2 Headache, neck pain 3 Headache, nausea, and somnolence Unconsciousness, tetraparesis Headache, neck pain 3 Headache, neck pain, vomiting Neck pain, bilateral upper limb weakness 3 Not stated Not stated 5 Not stated Pahl 2014 43 F C1–2 SAH Aoun 2014 59 F C7 SAH Boeris 2015 22 M C4 Ashour 2015 72 M C2 Subdural hematoma SAH Erdi 2016 55 F C6 IVH Nakhla 2016 88 F C 5–6 SAH Singh 2016 38 M C4 SAH Singh 2017 18 M C7 SAH Simon-Gabriel 2018 Ren 2018 65 M SAH 57 F At the level of the medulla oblongata CC junction SAH Neck stiffness, drowsiness Headache Dabus 2018 60 s NA SAH Headache, neck pain Not stated Dissection Roka 2019 30 F Cervicomedullary junction Posterior fossa IVH 2 Isolated Turrini 2020 64 M C1 SAH Not stated Dissection Abdalkader 2020 70 s M C2 SAH Headache, vomiting, vertigo, gait abnormality Headache, vomiting, dizziness, numbness Headache, vomiting 3×2.5 50 s M C2–3 SAH Headache, neck pain, vomiting 5×2.5 Bilateral VA occlusion Not stated 7 10 Not stated 5.6×3.3 Coarctation of aorta Isolated, Dissection Bilateral VA occlusion Coarctation of aorta Herniated cervical disc Moya moya disease Coarctation of aorta Alive Alive Alive Embolization of parent A. Conservative management Alive Coil embolization Alive Conservative management Direct surgery (Clip & wrap) Coil embolization Alive Conservative management, no treatment Conservative management Conservative management, decompressive laminectomy Flow diverter stent at parent artery Direct surgery (Clip & resection) Conservative management Conservative management Alive Direct surgery (resection) Direct surgery (Clip) Alive Conservative management Alive Abbreviations: CC, craniocervical; SAH, subarachnoid hemorrhage; IVH, intraventricular hemorrhage; LOC, loss of consciousness; VA, vertebral artery 4 Alive Alive Alive Not stated Alive Alive Alive Alive Alive Alive S. Shima et al. Clinical Neurology and Neurosurgery 208 (2021) 106862 C4 radiculomedullary artery. The microcatheter was navigated and wedged into the aneurysm (Fig. 3), which was embolized with four platinum coils (ED coil; KANEKA MEDICS, Osaka, Japan). Control angiography showed complete obliteration of the aneurysm (Fig. 3). The second endovascular treatment was performed 14 days after the initial treatment to prevent the aneurysm recurrence due to the increased flow through the VA, in which we performed balloon angio­ plasty and stent placement for the tandem VA stenosis. A 6-Fr guiding catheter (Fubuki; TOKAI MEDICAL PRODUCTS, Aichi, Japan) was placed in the left VA, and a microcatheter (Excelsior SL-10; Stryker Neurovascular, Fremont, CA, USA) was navigated over a 0.014-inch microwire (Traxcess14; MicroVenton, Inc., Tustin, CA, USA) into the left VA passing through the stenosis segment. A Gateway 3.5 × 20 (Stryker Neurovascular, Fremont, CA, USA) balloon catheter was used to perform percutaneous transluminal angioplasty, and stenting was per­ formed using a Neuroform Atlas 4.0 × 21 mm stent (Stryker Neuro­ vascular, Fremont, CA, USA) along with a Wingspan 3.5 × 15 mm stent (Stryker Neurovascular, Fremont, CA, USA) (Fig. 4). Post-treatment angiography showed an expanded VA with improved flow. We also confirmed persistent occlusion of the ASA aneurysm. All procedures were performed without complications. After surgery for placement of a ventriculoperitoneal shunt, the patient was transferred to a rehabilita­ tion hospital at the neurologic baseline; her modified Rankin Scale score was 3. The patient’s family declined radiographic follow-up for the patient owing to her poor condition; however, she had no recurrent hemorrhage two years after treatment. using liquid material cannot be validated for all solitary ASA aneurysms because of the high risk of ASA occlusion. Simon-Gabriel et al. treated an ASA aneurysm by placing a flow diverter stent in the vertebral artery across the origin of the radiculomedullary artery; however, further validation is required on the effectiveness and safety of the flow diverter stent in treating a distant lesion without sacrificing the ASA [30]. In the present case, the aneurysm was located at the junction be­ tween the radicular component of the radiculomedullary artery and the ASA axis. Thus, while there was increased hemodynamic stress that formed the aneurysm, this location made endovascular treatment feasible. The saccular shape of the aneurysm and the dilated feeding artery facilitated the catheter navigation and coil placement. We could treat the aneurysm with coils preserving the ASA axis, even though the aneurysm had a wide neck. Then, we added stents placement for the VA stenosis in the chronic phase of SAH. Considering the flow-related eti­ ology and rupture of the aneurysm, we thought that decreasing the hemodynamic stress was necessary to prevent the recurrence or de novo formation of the aneurysm. This is a reasonable strategy based on pre­ vious literature reporting that the treatment of vascular malformations results in the resolution of the spinal artery aneurysms [34]. Given that spinal artery aneurysms are typically located on the parent artery rather than its branching sites, it is possible to accomplish selective endovas­ cular embolization of ASA aneurysms. 4. Conclusions We report a case of a ruptured solitary ASA aneurysm caused by a hemodynamic mechanism treated with endovascular approach. Endo­ vascular treatment could be a treatment option for this rare disease when the morphological and anatomical features are favorable. 3. Discussion Spinal aneurysms are thought to be secondary to traumatic, hemo­ dynamic, and inflammatory stress on the arterial wall and are classified as type 1, i.e., spinal aneurysms associated with AVMs, and type 2, i.e., isolated aneurysms [8]. Type 2 ASA aneurysms are exceedingly rare[9]. We reviewed 29 case reports and 30 patients with cervical ASA aneu­ rysms that were not associated with AVM or AVF (Table 1) [2,4,6,7, 9–33]. Fifteen cases had dissecting etiology or no underlying diseases. The aneurysm in most cases was at the upper cervical spine, and the two cases of unruptured aneurysm presented with spinal cord compression that caused quadriplegia. All cases of ruptured aneurysm presented with SAH, except for two cases with hematomyelia, two cases with intra­ ventricular hemorrhage, and one case with subdural hematoma. The mean age was 49.9, with a slight male predominance (n = 16, 55%). The aneurysms were mainly fusiform shape or pseudoaneurysms. In our case, flow-related etiology was assumed based on the angioarchitecture; chronic occlusive disease of the bilateral VAs seemed to demand the collateral flow through the ASA axis to the posterior circulation. The right C4 radiculomedullary artery and the ascending limb of the ASA were larger than descending limb of the ASA, suggesting compensatory enlargement. This etiology led to our treatment strategy. The wait-and-see management or hematoma evacuation is usually chosen as treatment for a ruptured aneurysm, without treating the lesion. An ASA aneurysm is located on the ventral side of the spinal cord, which makes it technically challenging to access by surgery. In most cases, conservative management was performed because of compro­ mised patient condition, surgical morbidity, and approach-related problems. The possibility of the spontaneous resolution of the ASA aneurysm without any intervention has been suggested; however, in some cases, acute enlargement of the aneurysm was observed within a few weeks after onset [6,19,34]. Moreover, the exact historical out­ comes of untreated spinal artery aneurysms and the risk of rebleeding are unclear. Therefore, the feasibility of the endovascular treatment should be considered in any case of an ASA aneurysm. There are few reports in the literature regarding endovascular treatment of ruptured ASA aneurysms. Cobb et al. treated a thoracic ASA aneurysm using the Onyx liquid embolic system, but it was after con­ firming the spinal cord infarction [35]. Embolization of the aneurysm Ethics approval and consent to participate The St. Luke’s International Hospital Research Ethics Committee (Tokyo, Japan) approved the study protocol. (Research number: 21R021). Funding The authors did not receive support from any organization for the submitted work. CRediT authorship contribution statement Shogo Shima contributed to report design, acquisition and inter­ pretation of the data, and drafting the article. Shinsuke Sato contrib­ uted to acquisition and interpretation of the data. Tatsuki Motizuki contributed to acquisition of the data. Yasunari Niimi contributed to interpretation of the data and supervision. Data availability The data and material that support the findings of this report are available from the corresponding author. Acknowledgments None. 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