Clin Neuroradiol DOI 10.1007/s00062-014-0303-9

O r i g i n a l A rt i c l e

Acute Basilar Artery Occlusion with Underlying High-Grade Basilar Artery Stenosis: Multimodal Endovascular Therapy in a Series of Seven Patients D. Behme · W. Weber · A. Mpotsaris

Received: 18 October 2013 / Accepted: 18 March 2014 © Springer-Verlag Berlin Heidelberg 2014

Abstract Purpose  Acute basilar artery occlusion is associated with high rates of major morbidity and mortality. In rare cases, the underlying pathology is a high-grade stenosis of the basilar artery. We report on a series of seven cases with occluded high-grade basilar artery stenosis who received endovascular therapy at our center. Material and Methods  Our prospective database since October 2009 until September 2013 was screened for patients with acute basilar artery occlusion and underlying highgrade stenosis who underwent endovascular therapy. Case files were retrospectively reviewed for clinical, outcome, and technical data. Results  Seven patients were identified who suffered from an acute basilar artery occlusion based on a high-grade stenosis between October 2009 and September 2013. These patients were treated with an acute stenting of the basilar ar-

tery with or without a preceding mechanical thrombectomy. Median age was 75 (53–83) years; median prethrombectomy National Institute of Health Stroke scale score was 19 (7–28). A successful recanalization result defined as modified Thrombolysis In Cerebral Infarction grade 2b or higher was achieved in all cases. Two of the seven patients had a procedural complication consisting of a vessel dissection after angioplasty. A good clinical outcome according to the Solitaire flow restoration device versus the Merci Retriever in patients with acute ischaemic stroke (SWIFT) study criteria was achieved in three of the seven patients. One patient died during hospitalization in the acute phase. Conclusion  Mechanical thrombectomy combined with acute stenting of the basilar artery is technically feasible and may be an effective therapeutic option in the rare case of an acutely occluded high-grade stenosis of the basilar artery in patients with an otherwise poor prognosis. Keywords  Acute basilar artery occlusion · Basilar artery stenosis · Mechanical thrombectomy · Angioplasty with stenting

D. Behme, MD () · W. Weber · A. Mpotsaris Klinik für Radiologie, Neuroradiologie und interventionelle Therapie, Klinikum Vest, Knappschaftskrankenhaus Recklinghausen, Dorstener Str. 151, 45657 Recklinghausen, Germany e-mail: [email protected] W. Weber Abteilung für Radiologie und Neuroradiologie, Ruhr-Universität Bochum, Universitätsklinikum Bochum Langendreer, Bochum, Germany

Abbreviations ABAO Acute basilar artery occlusion BA Basilar artery IAT Intra-arterial thrombolysis IVT Intravenous thrombolysis MT Mechanical thrombectomy mRS Modified Rankin scale mTICI Modified Thrombolysis in Cerebral Infarction NIHSS National Institute of Health Stroke scale

A. Mpotsaris Institut und Poliklinik für Radiologie, Abteilung Neuroradiologie, Universität zu Köln, Universitätsklinikum, Köln, Germany

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Introduction The prognosis of acute basilar artery occlusion (ABAO) is poor, and mortality rates ranging from 22 to 100 % have been reported when intra-arterial thrombolysis (IAT) or intravenous thrombolysis (IVT) was carried out [1–4]. Lindsberg and Mattle [4] reviewed several studies examining the therapy of ABAO reporting on recanalization rates from 53 to 65 % when IVT or IAT was carried out, respectively. The role of interventional endovascular therapy in ABAO is not yet clear, and data on mechanical thrombectomy (MT) in the posterior circulation remain scarce [5, 6]. Roth et al. [7] reported on eight patients who were treated with MT using the Solitaire FR (Covidien, Mansfield, MN) device resulting in a good revascularization outcome defined as Thrombolysis in Cerebral Infarction (TICI) grade > 2a in all cases and a good clinical outcome (modified Rankin scale (mRS) score ≤ 2) in 50 % of cases. In a series of 31 patients, Mourand et al. [8] reported on good recanalization results (TICI grade of 2b or higher) in 74 % of cases. In another recently published case series by Mordasini et al. [9], a successful revascularization was achieved in all cases, and a good clinical outcome (mRS score ≤ 2) was achieved in 28.6 % of cases. Several case reports and studies mentioned endovascular rescue therapies including percutaneous transluminal angioplasty (PTA) and stenting in cases of insufficient revascularization after MT alone [9, 10]. In the series published by Mordasini et al. [9], rescue therapy including PTA and stenting of the BA resulted in successful recanalization outcomes whenever carried out. As symptomatic BA stenosis without acute occlusion goes along with a high risk of stroke or death, stenting of the BA has become a common endovascular therapy in high-grade stenosis of the BA for several years. Excellent long-term clinical outcome defined as an mRS score of 1 or lower in 83.3 % of patients after approximately 27 months has been reported when symptomatic high-grade BAO was treated with BA stenting [11–13]. Overall, little is known about endovascular treatment options and clinical outcome in the rare case of an acutely occluded BA stenosis. We report on seven patients who suffered from ABAO that was etiologically based on a high-grade BA stenosis. These patients underwent endovascular therapy including MT followed by angioplasty and stenting or angioplasty and stenting alone. To our knowledge, this is the first study focusing on the endovascular therapy of an acutely occluded high-grade BA stenosis. Material and Methods Our prospective, ongoing neurointerventional database was screened for all patients who underwent endovascular ther-

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apy of an ABAO with underlying high-grade BA stenosis between October 2009 and September 2013. Five cases were identified during this period. All patients underwent plain computed tomography (CT) and CT angiography (CTA) scans on admission or before referral to our center for endovascular therapy. Angiographic image analysis was performed by a senior interventional neuroradiologist who was blinded to all clinical and outcome data. Revascularization results were graded according to the recommendations of the Cerebral Angiographic Revascularization Grading Collaborators using modified TICI (mTICI) grade: an mTICI grade of 2b or higher was defined as a good revascularization result [14]. Clinical status including National Institute of Health Stroke scale (NIHSS) and mRS was assessed at admission and discharge. Periprocedural and procedural complications were defined as symptomatic intracranial hemorrhage (sICH) according to European Cooperative Acute Stroke Study (ECASS) III criteria [15], vessel dissection, subarachnoid hemorrhage within 24 h (18–36 h), stent dislocation, and acute stent occlusion. Technical, clinical, and demographic data were entered into an Excel spreadsheet for retrospective analyses. According to the guidelines of the ethics committee, no approval was necessary for conducting this anonymized retrospective study. Endovascular Therapy All endovascular procedures were carried out under general anesthesia. The basic endovascular approach consisted of placing a 6F guiding catheter (Neuron, Penumbra Allameda, CA) into the cervical segment of the dominant vertebral artery (VA), followed by a microcatheter-based approach of the intradural portions of the VA and consequently the BA. Clot extraction maneuvers were carried out by passing the clot with a micro-guidewire and microcatheter, followed by a careful contrast agent injection through the microcatheter for verification of the correct positioning and consequent deployment of the stent retriever. PTA (whenever necessary) was carried out with a monorail balloon in accordance with the target vessel diameter aiming at a slight under-dilation. All stenting procedures were carried out utilizing the balloonexpandable Pharos Vitesse (Codman, Raynham, MA) stent. Periprocedural Antiplatelet Regimen If the patients had not been receiving prior dual antiplatelet therapy for other medical reasons at the time of treatment, eptifibatide was continuously infused for 24  h to prevent secondary stent occlusion. We decided for eptifibatide in contrast to acetylsalicylic acid (ASA) as early antiplatelet therapy because of its short half-life allowing for decompressive craniectomy in case of edematous brain swelling. The combination of recombinant tissue-type plasminogen

Acute Basilar Artery Occlusion with Underlying High-Grade Basilar Artery Stenosis

activator (rt-PA) and eptifibatide has been considered safe [16]. After intracranial hemorrhage and decompressive craniectomy were ruled out, the regimen was switched to a secondary prophylaxis of stent occlusion based on a dual antiplatelet therapy: under continuous intravenous infusion of eptifibatide, patients received a loading dose of 300 mg of clopidogrel and 500 mg of ASA. Patients receiving daily ASA medication prior to treatment did not receive an ASA loading dose. After 4 h of clopidogrel loading dose (and ASA), the administration of eptifibatide was stopped. Patients continued on lifelong ASA (100 mg/day) and additional clopidogrel (75 mg/day) for 8 weeks. If a Multiplate® testing 72 h after loading resulted in an insufficient efficacy of clopidogrel (nonresponder), we decided for prasugrel (10 mg/day) for the duration of 8 weeks. Results Between October 2009 and September 2013, seven patients (six male and one female; median age: 75 years, range: 53–83 years) with ABAO and underlying BA stenosis were treated by endovascular means. The median NIHSS score on admission was 19 (range: 7–28). Stroke etiology according to trial of ORG 10172 in acute stroke treatment (TOAST) criteria [17] was thrombembolic in all cases (Table 1). Six patients received MT with additional angioplasty and stenting of the underlying stenosis; in one case, no MT was performed. MT was carried out using the Solitaire AB or Solitaire FR device in three cases and the Penumbra Separator 3D combined with the Penumbra reperfusion catheter 054/5MAX for lesional aspiration [18] in three cases. Intra-

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arterial rt-PA was used in one case; intravenous rt-PA was administrated in three cases according to the guidelines of the German Neurological Society (Table 2). PTA followed by stenting was performed in five cases; in two cases, stenting was performed without previous PTA (Table 2). Median groin puncture-to-recanalization time was 130 min (range: 63–268 min). One patient died during the acute phase due to cardiac output failure. A PTA-related vessel dissection was observed in two patients: in Patient I (Tables 1 and 2; Fig.  1), control injection after successful stent placement showed a dissection extending the limits of the stent, leading to an inflow and outflow limitation (Fig.  1g, arrows). We decided to repeat the PTA including the dissected part at the V4-stent-junction (Fig. 1h, arrow). This maneuver improved only the outflow; we refrained from any further endovascular means. In Patient IV (Tables 1 and 2), we saw a circumscribed, 4-mm-long vessel wall dissection commencing slightly proximal to the exit point of the Pharos stent on the dorsal portion of the vessel. Repeated control injections after waiting for 15 min showed no hemodynamic relevance. No new thrombus formation was observed at the site of the dissection, most likely due to the immediate intravenous administration of eptifibatide after stent placement. No other intra- or postprocedural complications occurred. Revascularization result was an mTICI grade of 2b in four and an mTICI grade of 3 in three of the seven cases (Table 2). Good clinical outcome defined according to the Solitaire flow restoration device versus the Merci Retriever in patients with acute ischaemic stroke (SWIFT) study criteria [10] was achieved in three of the seven cases; an mRS score of 5 was reached in three cases; and one patient died in the acute phase (Table 1).

Table 1  Overview of patient data and clinical outcome Clinical status at Patient Age Sex Time from symptom onset/secondary worsen- admission ing to recanalization (min) NIHSS mRS Number I 64 Male 470 19 5 (1)a II 76 Male 850 17 4 III 53 Male 270 28 5 IV 75 Male 300 23 5 (3)b V 59 Male 380 20 5 VI 83 Male 370 16 5 (2)c VII 82 Female 450 7 4

Clinical status at discharge NIHSS mRS

Stroke etiology according TOAST criteria [17]

15 6 0 21 2 – 23

Thrombembolic Thrombembolic Thrombembolic Thrombembolic Thrombembolic Thrombembolic Thrombembolic

5 3 0 5 0 6 5

Median 75 – 380 19 5 11 5 – Mean 70.3 – – – – 441.4 (± 179.77) 18.6 (± 6.0) 11.7 (± 8.4) (± SD) (± 10.8) SD standard deviation, NIHSS National Institute of Health Stroke scale, mRS modified Rankin scale, ABAO acute basilar artery occlusion, TOAST trial of ORG 10172 in acute stroke treatment a

mRS score of 1 before BAO after poliomyelitis at the age of 5 years

b c

mRS score of 3 before ABAO after previous stroke

mRS score of 2 before ABAO after previous stroke

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4 Table 2  Overview of angiographic data Case i.v. Side of BA i.a. Number rt-PA rt-PA stenosis

D. Behme et al.

TICI pre/ Stent/stent size Time from groin puncture to recana- post lization (min) 173 0/2b I 8 mg No Proximal Pharos Vitesse/4 × 18mm 63 1/3 II – Yes Proximal Solitaire AB SeQuent Pharos 4 × 20-mm/1 2.5 × 20-mm/1 Vitesse/3 × 15mm 137 0/2b III – Yes Proximal Solitaire FR – Pharos Vi4 × 20-mm/2 tesse/3.5 × 10mm 100 1/2b Pharos IV – Yes Distal – SeQuent 2(3) × 10-mm/2 Vitesse/3 × 10mm 130 0/2b V – No Middle Pharos Penumbra 3D/1 (+ 054 SeQuent 2 × 10-mm/1 Vitesse/3 × 10catheter) mm 107 0/3 – Pharos VI – No Proximal Penumbra 3D/2 Vitesse/3 × 10(5MAX reperfusion mm catheter) 268 0/3 SeQuent Pharos ViVII – No Proximal Penumbra 3D/4 1.5 × 20-mm/1 tesse/2.5 × 13(5MAX reperfusion mm catheter) i.a. intra-arterial, i.v. intravenous, BA basilar artery, PTA percutaneous transluminal angioplasty, TICI Thrombolysis In Cerebral Infarction grade, rt-PA recombinant tissue-type plasminogen activator Stent retriever/number PTA-balloon of passes size/number of PTA Solitaire AB SeQuent 4 × 20-mm/2 2.5 × 20-mm/3

Illustrative Case 1 A 64-year-old man with known BA stenosis woke up with hemiparesis, dysarthria, and dysphagia and was admitted to the general hospital of his place of residence. As the time of symptom onset was unclear, no IVT was carried out. After secondary worsening in the early evening with diplopia and somnolence, CTA revealed a BAO, and the patient was referred to our center for acute endovascular therapy (Fig. 1a–i). The initial angiogram showed a complete occlusion of the BA at the level of the vertebro-basilar junction (VBJ; Fig. 1a). There was a delayed filling of the BA apex after injecting the internal carotid artery (ICA) through the posterior communicating artery. A guiding catheter was placed into the left VA, and a micro-guidewire was navigated through the occluded BA followed by a microcatheter. The underlying proximal stenosis at the VBJ was then dilated with a 2.5 × 10-mm balloon (SeQuent, Braun, Melsungen, Germany) after the placement of the micro-guidewire at the right P1–P2-junction. A careful injection after PTA depicted a small channel of contrast agent in the BA with multiple thrombi (Fig. 1b, arrows). We decided for intra-arterial administration of 8 mg of rt-PA via a microcatheter from the level of the VBJ (Fig. 1c). After waiting for 15 min, the control showed no significant amelioration. A Solitaire AB (4 × 20 mm) stent retriever was placed from the apex of the BA down to the VBJ; after waiting for 5 min, with the Solitaire deployed multiple thrombi were extracted. This led to an

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improved filling of the BA and depicted clearly the underlying proximal high-grade stenosis (Fig. 1d–e, arrows). There was still thrombotic material in the BA. Consequently, we repeated the clot extraction maneuver, retrieving most of the thrombotic material in the mid and distal portion of the BA. The micro-guidewire was then navigated into the posterior cerebral artery (PCA), allowing for safe placement of the balloon-expandable Pharos Vitesse (4 × 18 mm; (Fig. 1f, arrow). At the time of stent placement, the intravenous administration of eptifibatide was started. The control injection after successful stent placement showed a dissection extending the limits of the stent, leading to an inflow and outflow limitation (Fig. 1g, arrows). Thus, we decided to repeat the PTA with a 2.5 × 20-mm balloon incorporating the dissected part at the V4-stent-junction (Fig. 1h, arrow). This maneuver improved the outflow, but not the inflow (Fig. 1i, arrow). At this time, we decided against repeating the PTA; after waiting for another 15 min, the control injection showed thrombembolic material in the left P1 segment (Fig. 1i, arrow on the left), but none in the BA. Inflow into the BA was still limited exactly at the point of the junction of the right and left VA (corresponding with the entry portion of the stent). In the late venous phase, there was still a pooling phenomenon of the contrast agent of the left VA (Fig. 1i, j, arrow on the right side). After careful evaluation of the final angiogram, we refrained from further endovascular therapeutic means including the placement of a second stent. A control CT scan after 24 h (Fig. 1k, l) depicted an infarction of the left paramedian brainstem and

Acute Basilar Artery Occlusion with Underlying High-Grade Basilar Artery Stenosis

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Fig. 1  Angiographic images of Case Example 1. a Left side: anteroposterior (AP) view; right side: lateral view. Occluded BA with an mTICI grade of 0. b Left side: AP view; right side: lateral view after PTA with SeQuent 2.4 × 20-mm (arrows). c Left side: AP view; right side: lateral view after 8 mg of rt-PA administration, partial recanalization of BA seen on the right side. d Deployment of Solitaire stent in AP and lateral projection (arrows). e After clot extraction (Solitaire), a proximal high-grade stenosis of the BA was uncovered (arrows).

f Roadmap image of Pharos 4 × 18-mm stent (arrow). g Dissection of BA leading to an in- and outflow limitation (arrows). h Roadmap image showing in-stent PTA (arrow). i Control after in-stent PTA. j Final control with occlusion of P2 segment on the left and inflow limitation of the stented BA (arrows). k Postinterventional CT image (24 h) showing contrast agent extravasation and infarction of the left paramedian brain stem. l CT image of the cerebrum did not show any infarction in the left posterior cerebral artery territory

local contrast agent extravasation but no infarction of the left PCA territory, presumably due to a perfusion of the left PCA territory by a PCA of fetal origin. Clinical status did

not improve significantly after endovascular therapy, and the patient was referred to a rehabilitation clinic with severe disability 6 days after treatment (mRS score of 5).

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Fig. 2  Angiographic images of Case Example 2. a Left side: anteroposterior (AP) view; right side: lateral view. Occluded BA with an mTICI grade of 0, terminal PICA variant of the right VA. b Deployment of Solitaire stent in AP and lateral view (arrows), distal BA occlusion, proximal thrombi. c Control after MT, thrombi in right P1 segment, occlusion of the left P1 segment and proximal BA stenosis

(arrows). d Deployment of Solitaire stent in left P2 segment (arrow). e Control after MT showing partial revascularization of the left PCA. f Roadmap image of Pharos 3.5 × 10-mm stent (arrow). g Unsubtracted image after stenting showing the stent (arrow). h Final control. i Posterior fossa CT image (24 h). j Control MRI (36 h) showing a cortical infarction of the right cerebellum

Illustrative Case 2

proximal BA (Fig. 2b, arrows). A careful injection through the guide depicted a channel through the deployed Solitaire and revealed thrombembolic material in the proximal third of the BA directly beyond an underlying high-grade proximal BA stenosis a few millimeters after the PICA origin of the right side (Fig. 2c, arrow on the right side). After the first clot extraction maneuver with the Solitaire, the BA and VBJ presented without any evidence of thrombotic material, although there was still an embolus visible in the P1 segment on the left leading to a full obstruction of the vessel and multiple smaller emboli in the P1–P2 junction on the right. We decided for a second clot extraction maneuver after deploying the Solitaire at the obstructed P2 segment on the left, leading to a partial recanalization of the PCA

A 53-year-old patient suffering from a sudden onset of vertigo and vomiting was primarily admitted to our hospital, arriving 90 min after onset in a comatose state. CTA revealed a BAO, and the patient was directly transferred to our angiography suite (Fig. 2a–j). The initial angiogram depicted a BAO at the level of the VBJ a few millimeters distal to the posterior inferior cerebellar artery (PICA) orifice (Fig. 2a). A microcatheter was navigated through the obstruction to the BA apex, where a careful contrast agent injection showed a retrograde filling of the BA down to its middle portion, revealing also embolic material in both PCAs. A Solitaire FR (4 × 20 mm) was deployed from the BA apex into the

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Acute Basilar Artery Occlusion with Underlying High-Grade Basilar Artery Stenosis

(Fig. 2e). Then, a micro-guidewire was placed in the right P2 segment, and a Pharos Vitesse balloon-expandable stent (3.5 × 10 mm) was deployed in the high-grade proximal BA stenosis (Fig. 2f, arrows). The stent opened correctly, and the control angiogram showed no residual stenosis. Eptifibatide intravenous administration was started. The final control run 20 min later showed no residual thrombotic material either in the left or in the right PCA; the BA was fully recanalized (Fig. 2h). Control CT and magnetic resonance imaging (MRI) scan revealed a small cortical infarction of the right cerebellum. Clinically, the patient improved significantly after endovascular therapy and was discharged without any residual neurological symptoms (mRS score of 0). Discussion The aim of this retrospective study was to evaluate the effectiveness and safety of a multimodal endovascular interventional approach in case of an acutely occluded high-grade BA stenosis. Elective stenting of symptomatic high-grade BA stenosis may lead to favorable clinical outcome, whereas a conservative, noninterventional approach in symptomatic high-grade BA stenosis is reported to have a poorer prognosis [19, 20]. In view of still very limited data about the prognosis of ABAO in cases of an underlying high-grade stenosis, an acute MT alone might not be sufficient. Previously published studies featuring also a multimodal approach including MT and PTA included single cases as well where acute stenting was performed as a rescue therapy whenever MT did not lead to a successful revascularization result [8–10]. Mordasini et al. [9] reported on 3 of 14 patients who received additional stenting and 1 of 14 patients who received PTA additional to MT. Revascularization outcome was a TICI grade of 3 in one and 2b in two patients. Overall clinical outcome reported by Mordasini et al. [9] was good in 20 % of cases. Alas, there was no subgroup analysis for those patients who received a multimodal endovascular therapy. In the study by Mourand et al. [8], one patient received PTA and stenting following MT failure, which resulted in a good clinical outcome. A literature search in PubMed library based on the keywords “BAstenosis,” “ABAO,” “MT,” “PTA,”  and “acute stenting” revealed no reports dealing exclusively with acute stenting in ABAO with underlying high-grade stenosis. This study showed similar revascularization and early clinical outcome results compared with literature reports on IAT including MT or IVT for acute BA occlusion without evidence of an etiologically underlying high-grade BA stenosis [8, 9, 19, 21]. Technically, the individualized combination of the different endovascular means for achieving recanalization (MT, PTA, IAT, and acute stenting) led to a complete recanalization of the BA in all cases. Clinically, we observed a

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good outcome (SWIFT study criteria [10]) in three of our seven cases at discharge. The remaining four patients had an unfavorable outcome. One patient died during hospitalization in the acute phase. Median time from groin puncture to revascularization in our multimodal approach was 130 min (range: 63–268 min; Table 2). This is longer compared with 47 min (range: 10–252 min) reported by Mordasini et al. or 61 min (range: 15–243 min) reported by Mourand et al. whereby in both studies ABAO was treated by the means of MT alone in most cases [8, 9]. No sICH occurred, and besides vessel dissection in two cases, no other periprocedural complications were recorded. The limitations of this study are the single-center  retrospective design of the study, the very limited number of patients, the missing control group, and the missing clinical follow-up visit. Conclusion Endovascular therapy with an individualized combination of interventional means including MT and PTA with stenting, or stenting alone, is technically feasible and safe. Clinically, it can be an effective treatment option in patients with an otherwise poor prognosis in the rare case of an acutely occluded high-grade BA stenosis. Compared with the limited data on ABAO without underlying high-grade stenosis, the present study shows similar revascularization results and clinical outcome. No patient died during acute phase, and two patients were independent at discharge. From our point of view, patients with an acutely occluded high-grade BA stenosis may benefit significantly when endovascular therapy is carried out and by all means of endovascular stroke therapy. Grant support  None. Conflict of interest  The authors declare to have no conflict of interest.

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Acute Basilar Artery Occlusion with Underlying High-Grade Basilar Artery Stenosis: Multimodal Endovascular Therapy in a Series of Seven Patients.

Acute basilar artery occlusion is associated with high rates of major morbidity and mortality. In rare cases, the underlying pathology is a high-grade...
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