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Stenting of Mobile Calcified Emboli After Failed Thrombectomy in Acute Ischemic Stroke: Case Report and Literature Review
Journal Pre-proof Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review Matthew B. Potts, MD, Lucas da Matta, MD, Ramez N. Abdalla, MD, Ali Shaibani, MD, Sameer A. Ansari, MD, PhD, Babak S. Jahromi, MD, PhD, Michael C. Hurley PII:
S1878-8750(19)33128-6
DOI:
https://doi.org/10.1016/j.wneu.2019.12.096
Reference:
WNEU 13943
To appear in:
World Neurosurgery
Received Date: 25 August 2019 Revised Date:
14 December 2019
Accepted Date: 16 December 2019
Please cite this article as: Potts MB, da Matta L, Abdalla RN, Shaibani A, Ansari SA, Jahromi BS, Hurley MC, Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2019.12.096. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review
Matthew B. Potts, MD,1,2 Lucas da Matta, MD,1 Ramez N. Abdalla, MD,2 Ali Shaibani, MD,1,2 Sameer A. Ansari, MD, PhD,1,2 Babak S. Jahromi, MD, PhD,1,2 Michael C. Hurley1,2 Departments of 1Neurological Surgery and 2Radiology Northwestern Memorial Hospital Northwestern University Feinberg School of Medicine Chicago, IL 60611, USA.
Corresponding author: Matthew B. Potts, MD 676 N. St. Clair St., Suite 2210 Chicago, IL 60611 Email: [email protected] Phone: 312-695-6200 Fax: 312-695-0225
Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review
Matthew B. Potts, MD,1,2 Lucas da Matta, MD,1 Ramez N. Abdalla, MD,2 Ali Shaibani, MD,1,2 Sameer A. Ansari, MD, PhD,1,2 Babak S. Jahromi, MD, PhD,1,2 Michael C. Hurley1,2 Departments of 1Neurological Surgery and 2Radiology Northwestern Memorial Hospital Northwestern University Feinberg School of Medicine Chicago, IL 60611, USA.
Corresponding author: Matthew B. Potts, MD 676 N. St. Clair St., Suite 2210 Chicago, IL 60611 Email: [email protected] Phone: 312-695-6200 Fax: 312-695-0225
ABSTRACT BACKGROUND: Mobile calcified emboli are a rare cause of large vessel occlusion and acute ischemic stroke and pose unique challenges to standard mechanical thrombectomy techniques. Intracranial stenting has been reported as a rescue maneuver in cases of failed mechanical thrombectomy due to dissection or calcified atherosclerotic plaques, but its use for calcified emboli is not well-described. CASE DESCRIPTION: Here we present two cases of acute ischemic stroke caused by mobile calcified emboli. Standard mechanical thrombectomy techniques using aspiration catheters and stent-retrievers failed to remove these emboli so intracranial stenting was successfully performed in each case, albeit after overcoming unique challenges associated with the stenting of calcified emboli. CONCLUSION: Mobile calcified emboli are rare causes of acute ischemic stroke. Intracranial stenting can be used to successfully treat calcified emboli when mechanical thrombectomy has failed. We also review the literature on intracranial stenting as a salvage therapy for failed mechanical thrombectomy.
Introduction Endovascular thrombectomy for the treatment of acute ischemic stroke (AIS) caused by a large vessel occlusion has been shown to be both highly effective and safe compared to medical management alone.1 Thrombectomy is typically performed using either a stent-retriever, aspiration catheter, or a combination of both with the goal of achieving complete or nearcomplete reperfusion of the ischemic territory. Occasionally, however, thrombectomy fails to revascularize the occluded vessel and the subsequent use of stenting as a rescue treatment to
maintain patency of the target vessel has been reported.2-10 Risk factors for failure of thrombectomy include atherosclerotic plaques and calcified emboli. 2,11,12 Here, we report two cases of AIS caused by mobile calcified emboli for which mechanical thrombectomy failed and intracranial stenting was required.
Case Report Case 1: A middle-aged patient with a history of severe aortic stenosis underwent elective aortic valve replacement through a mini-thoracotomy. The patient’s aortic valve was noted to have calcifications extending into the left ventricle and excision of the aortic valve was reported to be difficult due to this calcification. The patient remained intubated post-operatively and was initially noted to have a symmetric neurologic exam however developed right hemiplegia after approximately four hours. Emergent head computed tomography (CT) showed hypoattenuation within the left insula and inferior frontal lobe as well as a hyperdense focus within the proximal left Sylvian fissure (Figure 1A-B). CT angiography (CTA) demonstrated this hyperdense focus to be located within the proximal M1 segment of the left middle cerebral artery (MCA) without complete occlusion (Figure 1C). CT perfusion imaging, evaluated using RAPID software (iSchemaView, CA, USA), demonstrated a small focus of infarct within the left insula (8cc, defined as cerebral blood flow <30%) and a larger surrounding region of ischemic penumbra within the left frontal, parietal, and temporal lobes (109cc, defined as Tmax >6s, Figure 1D). Given the significant perfusion mismatch and the patient’s persistent neurologic deficits, the decision was made to proceed with emergent cerebral angiography and possible mechanical thrombectomy.
An initial left internal carotid artery (ICA) injection revealed near complete occlusion of the proximal left MCA (Figure 2A-B) with extremely sluggish flow past the calcified obstruction and leptomeningeal collaterals from the left anterior and posterior cerebral arteries (ACA and PCA, respectively) providing retrograde filling of the left MCA branches. Although some sluggish flow was observed past the calcified lesion, this was not thought to be physiologically significant. In addition, the severity of the patient’s symptoms, large ischemic penumbra, and presumed embolic etiology (and not atherosclerotic plaque) led to the decision to attempt mechanical thrombectomy. This was performed using the following devices: 80cm Neuron Max sheath (Penumbra, CA, USA), ACE 68 aspiration catheter (Penumbra), Excelsior XT-27 microcatheter (Stryker, MI, USA), and a Solitaire 4 x 20 mm stent-retriever (Medtronic, MI, USA). The aspiration catheter was advanced up to the embolus and the microcatheter advanced past the embolus to allow deployment of the stent-retriever across the embolus. Once the stent-retriever was deployed, the microcatheter was removed. After five minutes, the stentretriever and aspiration catheter were removed together with the aspiration catheter and sheath both placed to suction. Subsequent control angiography showed persistence of the calcified obstruction. Two additional attempts at mechanical thrombectomy were made in the same fashion – one using the 4 x 20 mm Solitaire device and another using a 6 x 30 mm Solitaire. While flow across the embolus slightly improved, the embolus itself could not be retrieved. In fact, manipulation of the embolus pushed it distally within the M1 (Figure 2C), confirming that this was a mobile calcified embolus and not an atherosclerotic lesion. The decision was then made to place a permanent intracranial stent across the embolus in an attempt to improve flow through the MCA. An exchange-length microwire was advanced through the microcatheter into the inferior division of the left MCA and then the microcatheter and aspiration catheter were
removed. A 3.5 x 20 mm Wingspan intracranial stent (Stryker) delivery catheter was advanced over the exchange-length microwire and the stent was deployed across the embolus with its distal end in the inferior division of the left MCA and its proximal end in the proximal M1. Final control angiography demonstrated recanalization of the left M1 resulting in a Thrombolysis In Cerebral Infarction (TICI) 3 reperfusion (Figure 2D-E). Post-treatment CT demonstrated good expansion of the stent against the calcified embolus (Figure 2F). The patient was initially densely aphasic and plegic in the right arm. Post-treatment magnetic resonance imaging (MRI) demonstrated diffusion restriction within the left insula, putamen, caudate, and anteroinferior left frontal lobe as well as scattered foci of diffusion restriction throughout the remainder of the left MCA territory (Figure 2G). At the time of transfer to acute inpatient rehab on post-treatment day 12, the patient had dense expressive aphasia but could nod appropriately to questions and mimic commands. Strength was antigravity in the right arm and near full strength in the right leg. The patient was maintained on dual antiplatelet therapy with aspirin and clopidogrel for six months, at which time a repeat cerebral angiogram was performed showing persistent patency of the M1 segment of the left MCA (Figure 2H-I). At a one-year clinical follow-up, the patient’s language function had significantly improved and now was only notable for mild speech hesitancy. There was a persistent mild right facial droop and difficulty with fine motor movements of the right hand but otherwise full proximal right arm and right leg strength.
Case 2: An elderly patient with a history of hyperlipidemia, hypertension, coronary artery disease, pacemaker, and dialysis-dependent end-stage renal disease was undergoing an outpatient evaluation for left carotid stenosis by vascular surgery after presenting with brief intermittent episodes of expressive aphasia. The patient was treated with dual antiplatelet therapy using
aspirin and clopidogrel, as well as atorvastatin. CTA demonstrated a heavily-calcified atherosclerotic stenosis of the left ICA origin we well as a tandem calcified lesion at the left ICA terminus (Figure 3A-B). Due to the heavy calcification of both lesions, it was difficult to accurately grade the degree of stenosis at both sites on CT and the patient was referred to our service for a diagnostic cerebral angiogram under local anesthesia. The angiogram showed only moderate stenosis at the left ICA origin whereas the left ICA terminus was severely stenosed by a rounded intraluminal lesion concerning for a calfcific embolus (Figure 3C). The patient remained neurologically intact throughout the angiogram and was engaged in a fluent conversation about their medical history during manual compression of the femoral puncture site when they became abruptly mute and inattentive. Vital signs remained stable during this neurologic change. The left femoral artery was therefore accessed to re-evaluate the cerebral vasculature. These symptoms briefly resolved but then recurred and a repeat left ICA angiogram demonstrated worsened flow within the left MCA due to slight migration of the calcified embolus further into the left MCA origin, indicating this calcified lesion to be a mobile embolus and not an atherosclerotic lesion. After full heparinization and blood pressure augmentation, the patient’s neurologic exam again improved. An attempt was made to engage the embolus with an 064 Penumbra aspiration catheter using an adapt technique but this failed due to an inability to engage tight suction on the poorly pliable lesion. A Wingspan stent was then placed across the calcified embolus from the mid M1 segment into the supraclinoid ICA. The stent deployed well but there was difficulty retrieving the bumper on the delivery wire which slightly dislodged the stent proximally, compromising flow through the ICA, as demonstrated by reduced flow into the ipsilateral anterior cerebral artery (Figure 3D). The patient was awake during this procedure and had an improved exam with mild aphasia, so the decision was made to end the procedure and
transfer the patient to the neuro-intensive care unit. Over the following 24 hours, however, the patient’s neurologic function was found to be pressure dependent and therefore repeat angiography under general anesthesia was performed the following day during which angioplasty of the Wingspan stent was performed using a Gateway balloon (Stryker). This resulted in improved flow through the stent (Figure 3E). A subsequent head CT demonstrated a small left PCA infarct related to a non-occlusive left PCA embolus seen during the first attempt but no significant infarct within the left MCA territory (Figure 3F). Post-treatment, the patient was noted to have a right field cut but no weakness or language deficits. The patient could not get an MR due to a pacemaker. A P2Y12 response assay indicated resistance to clopidogrel so ticagrelor was started instead. The patient was subsequently transitioned from ticagrelor to coumadin due to developing a right upper extremity deep venous thrombosis. A clinic exam two months later, after completion of a course of rehabilitation, demonstrated right hemianopia, minimal word-finding difficulty, and mild loss of dexterity in the right hand. The patient expired approximately one year later due to progression of multiple non-neurologic medical issues.
Discussion: Stroke remains one of the leading causes of death and morbidity worldwide, occurring at a rate of around 250 per 100,000 person-years, causing around 90 deaths per 100,000 person-years, and causing the loss of over 100 million disability-adjusted life years in 2010.13 Continuous effort in the development of preventive and therapeutic interventions in AIS has led to improved outcomes.13 Intravenous thrombolysis is the mainstay of therapy of early cases of AIS, but mechanical thrombectomy was recently shown to improve outcomes in selected patients with large-vessel occlusions (LVO) presenting up to 24 hours after symptom onset.14 Nevertheless,
mechanical thrombectomy in such patients is not always successful at restoring blood flow.1,15 One of the factors associated with a risk of failure is calcification of the culprit thromboembolus.12 Calcified embolic stroke can occur after instrumentation of the cardiovascular system (e.g., cardiac catheterization and carotid manipulation) or can occur spontaneously.16 Such calcified emboli are distinguished from calcified intracranial atherosclerotic plaques in that they are potentially mobile, as was seen in our cases. Calcified emboli can often be identified in the initial non-contrast head CT by their increased attenuation indices (generally greater than 90 Hounsfield units) and oval shape (as opposed to the elongated shape of other thrombi).12 Thromboemboli can be classified into recent (rich in red blood cells, usually arteriogenic), aged (rich in fibrin, usually cardiogenic), and calcified (rich in calcium phosphate).17 The histological composition of the emboli has been associated with the probability of therapeutic success.12 Fibrin-rich emboli are stiffer than red blood cell-rich emboli, leading to more difficult recanalization in mechanical thrombectomy models.18 Calcified emboli are even stiffer than fibrin-rich emboli,19 which can contribute to the higher therapeutic failure rates.12,16 Biomechanical properties of the emboli are probably not entirely responsible for this difference in outcomes, as patients with calcified emboli may have other risk factors for worse outcomes, including significant atherosclerotic and cardiac disease.12 It is important to note that in the two cases presented here, the mobile calcified emboli caused symptomatic near-occlusion. It is possible that a rigid calcified embolus may not completely occlude a vessel like a more flexible soft embolus can, thus allowing some flow past the lesion. In each case, this small amount of flow was not deemed physiologically significant, as was demonstrated by the patients’ significant neurologic symptoms.
When mechanical thrombectomy fails, American Stroke Association AIS guidelines suggest that using salvage technical adjuncts may be reasonable to achieve appropriate flow restoration.14 While the document presents intra-arterial thrombolysis as salvage therapy, intracranial stenting has also been used in such situations. We identified eight studies reporting on intracranial stenting as rescue therapy after failed mechanical thrombectomy in AIS, comprising 225 patients in total (Table 1).2-9 Successful recanalization rates ranged from 6592%, with an average of 76%, resulting in good functional outcomes (mRS ≤2) in 46.2%. These results are comparable to the overall success rates reported in a meta-analysis of 2015 stroke thrombectomy trials by Goyal et al., where mTICI 2b or 3 was achieved in 71% and 90-day functional outcomes of mRS ≤2 were achieved in 46%.1 Stenting, however, was associated with symptomatic ICH in 9.8%, compared to only 4.4% in prior randomized trials.1 One possible etiology of this increased risk of symptomatic ICH is the need for additional antiplatelet medications during or after stent placement. Studies of stenting as rescue therapy in AIS typically report the use of glycoprotein IIb/IIIa inhibitors, such as tirofiban and abciximab, at the time of stent deployment followed by dual antiplatelet therapy with aspirin and clopidogrel. In our case 1, the patient was already on aspirin after an aortic valve repair. We administered a loading dose of clopidogrel through a nasogastric tube immediately after stent placement. The second patient was already on dual antiplatelet therapy at the time of stenting although a subsequent clopidogrel response assay indicated clopidogrel resistance so the patient was transitioned to ticagrelor. The reported success rates of mechanical thrombectomy for calcified emboli are poor. Dobrocky et al. recently reported 8 cases, of which successful recanalization was only achieved in one.12 This was associated with a 50% mortality at 3 months. They even reported fracture of a
stent-retriever wire during an attempted thrombectomy in one patient and perforation of a distal MCA branch in another. Other groups have reported successful mechanical thrombectomy of calcified emboli using stent-retrievers.20,21 Although ultimately technically successful, our two cases demonstrate some of the difficulties in treating calcified emboli. In the first case, several attempts were made at recanalization using a combined strategy of aspiration plus stent-retriever. After three unsuccessful attempts, the decision was made to proceed with stenting. The obvious concern was the need for dual antiplatelet therapy in the setting of a recent surgical procedure (mini-thoracotomy). The risks and benefits of this were discussed with the patient’s cardiology team before proceeding. While the stent was successfully deployed and good flow restored, the overall groin to revascularization time was approximately 220 minutes. This was certainly prolonged by the several attempts at standard mechanical thrombectomy techniques and although a TICI 3 reperfusion was achieved, the patient’s post-operative MRI had a significant infarct burden. Based on this experience, we recommend a low threshold to attempt stenting in the setting of a calcified embolus if standard techniques do not work. The second case demonstrates that stenting may not be sufficient to restore normal flow and that additional angioplasty may be required. The Wingspan and Enterprise (Codman Neurovascular) stents are the most commonly reported stents used for rescue of failed thrombectomy, although many countries also have access to the detachable Solitaire AB (Medtronic).4 Of these intracranial stents, the Wingspan provides the greatest radial force.22 Given the rigidity of a calcified embolus, the radial force of an intracranial stent should be considered during stenting. If stenting does not result in satisfactory flow, balloon angioplasty can be considered, although care must be taken to avoid vessel injury or rupture.
In summary, mobile calcified emboli are rare causes of AIS that present unique challenges and the success rate of standard mechanical thrombectomy techniques is low. Such emboli are readily detected on non-contrast CT imaging. Intracranial stenting is a promising rescue therapy for failed mechanical thrombectomy that can be applied in the case of calcified emboli.
Figure Legends:
Figure 1. Case 1, pre-treatment imaging. Initial non-contrast head CT (A) showing a hyperdense focus within the region of the left internal carotid artery (ICA) terminus (arrow). This remained hyperdense on bone windows, suggesting a calcified mass (B, arrow). Subsequent CT angiography demonstrated this calcified mass to be located within the left ICA terminus at the origin of the left middle cerebral artery (MCA, C). CT perfusion, analyzed by RAPID software, demonstrated an area of apparent infarct within the left insula and basal ganglia with a larger area of surrounding ischemic penumbra within the left MCA territory (D).
Figure 2. Case 1, intra- and post-treatment imaging. Digital subtraction angiography of the left internal carotid artery demonstrated the embolus at the origin of the left MCA with sluggish distal flow (A, AP; B, lateral). Attempts at mechanical thrombectomy using an aspiration catheter and stent-retriever failed to retrieve the calcified embolus but instead pushed it further distal into the left MCA (C, arrow), confirming this to be a mobile calcified embolus. An intracranial stent was therefore deployed across the calcified embolus (D, arrow shows stent), restoring flow through the left MCA territory (E, arrow shows calcified embolus). Posttreatment CT showed good expansion of the stent against the calcified embolus (F) and diffusion-weighted MRI showed infarction within the left basal ganglia and insula, as well as scattered infarcts within the left frontal and temporal lobes (G). A follow-up cerebral angiogram 6 months later showed persistent patency of the stent with good flow through the MCA (H-I).
Figure 3. Case 2. Initial non-contrast head CT showing a calcified mass within the region of the left ICA terminus (A). CTA (B) and diagnostic cerebral angiography (C) confirmed this calcified embolus to be within the left ICA terminus. After placement of a Wingspan stent (D), competitive flow was noted through the anterior communicating artery (arrow), indicating suboptimal flow across the stented calcified embolus within the ICA terminus. This corresponded to pressure-dependent symptoms post-treatment, prompting angioplasty the following day that resulted in improved flow through the ICA terminus (E). Post-treatment CT showed no infarct within the left MCA territory (F).
References: 1.
Goyal M, Menon BK, van Zwam WH, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723-1731. doi:10.1016/S01406736(16)00163-X.
2.
Chang Y, Kim B-M, Bang OY, et al. Rescue Stenting for Failed Mechanical Thrombectomy in Acute Ischemic Stroke: A Multicenter Experience. Stroke. 2018;49(4):958-964. doi:10.1161/STROKEAHA.117.020072.
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Zhou T. Intracranial stenting as a rescue therapy for acute ischemic stroke after stentriever thrombectomy failure. World Neurosurg. August 2018:1-25. doi:10.1016/j.wneu.2018.08.002.
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Nappini S, Limbucci N, Leone G, et al. Bail-out intracranial stenting with Solitaire AB device after unsuccessful thrombectomy in acute ischemic stroke of anterior circulation. Journal of Neuroradiology. June 2018:1-7. doi:10.1016/j.neurad.2018.05.004.
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Cornelissen SA, Andersson T, Holmberg A, et al. Intracranial Stenting after Failure of Thrombectomy with the emboTrap® Device. Clin Neuroradiol. 2018;372(5):1-7. doi:10.1007/s00062-018-0697-x.
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Acosta FD, Gómez EJ, Rey IB, Rodríguez FAB, Sepúlveda JJO, Fernández RO. Intracranial stents in the endovascular treatment of acute ischemic stroke.
Radiología (English Edition). 2017;59(3):218-225. doi:10.1016/j.rxeng.2017.01.001. 7.
Baracchini C, Farina F, Soso M, et al. Stentriever Thrombectomy Failure: A Challenge in Stroke Management. World Neurosurg. 2017;103:57-64. doi:10.1016/j.wneu.2017.03.070.
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Baek J-H, Kim B-M, Kim D-J, Heo J-H, Nam HS, Yoo J. Stenting as a Rescue Treatment After Failure of Mechanical Thrombectomy for Anterior Circulation Large Artery Occlusion. Stroke. 2016;47(9):2360-2363. doi:10.1161/STROKEAHA.116.014073.
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Linfante I, Samaniego EA, Geisbüsch P, Dabus G. Self-Expandable Stents in the Treatment of Acute Ischemic Stroke Refractory to Current Thrombectomy Devices. Stroke. 2011;42(9):2636-2638. doi:10.1161/STROKEAHA.111.618389.
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Argetsinger DS, Miller JW, Fletcher JJ. Intravenous thrombolysis, mechanical embolectomy, and intracranial stenting for hyperacute ischemic stroke in a patient with moyamoya disease. Journal of Clinical Neuroscience. 2016;29(C):173-175. doi:10.1016/j.jocn.2016.01.016.
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Tsang AC-O, Orru E, Klostranec JM, et al. Thrombectomy Outcomes of Intracranial Atherosclerosis-Related Occlusions. Stroke. 2019;50(6):1460-1466. doi:10.1161/STROKEAHA.119.024889.
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Dobrocky T, Piechowiak E, Cianfoni A, et al. Thrombectomy of calcified emboli in stroke. Does histology of thrombi influence the effectiveness of thrombectomy? J Neurointerv Surg. 2018;10(4):345-350. doi:10.1136/neurintsurg-2017-013226.
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Feigin VL, Forouzanfar MH, Lancet RKT, 2014. Global and regional burden of stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. Elsevier
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Powers WJ, Rabinstein AA, Ackerson T, et al. 2018 Guidelines for the Early Management of Patients With Acute Ischemic Stroke: A Guideline for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke. 2018;49(3):e46-e110. doi:10.1161/STR.0000000000000158.
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Cheang MY, Manning N, Churilov L, Mitchell P, Dowling R, Yan B. Recanalisation success is associated with good clinical outcome despite advanced age and stroke severity in patients treated with the Solitaire stentriever. Journal of Clinical Neuroscience. 2014;21(3):401-405. doi:10.1016/j.jocn.2013.05.005.
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Walker BS, Shah LM, Osborn AG. Calcified Cerebral Emboli, A “Do Not Miss” Imaging Diagnosis: 22 New Cases and Review of the Literature. AJNR Am J Neuroradiol. 2014;35(8):1515-1519. doi:10.3174/ajnr.A3892.
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Raghib MF, Mutzenbach JS, Rösler C, et al. Acute treatment of stroke due to spontaneous calcified cerebral emboli causing large vessel occlusion. 2018;47:5661. doi:10.1016/j.jocn.2017.10.042.
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Yuki I, Kan I, Vinters HV, et al. The Impact of Thromboemboli Histology on the Performance of a Mechanical Thrombectomy Device. AJNR Am J Neuroradiol. 2012;33(4):643-648. doi:10.3174/ajnr.A2842.
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Chueh JY, Wakhloo AK, Hendricks GH, Silva CF, Weaver JP, Gounis MJ. Mechanical Characterization of Thromboemboli in Acute Ischemic Stroke and Laboratory Embolus Analogs. AJNR Am J Neuroradiol. 2011;32(7):1237-1244. doi:10.3174/ajnr.A2485.
20.
Fassa A-A, Mazighi M, Himbert D, et al. Successful endovascular stroke rescue with retrieval of an embolized calcium fragment after transcatheter aortic valve replacement. Circ Cardiovasc Interv. 2014;7(1):125-126. doi:10.1161/CIRCINTERVENTIONS.113.000995.
21.
Uneda A, Kanda T, Suzuki K, Hirashita K, Yunoki M, Yoshino K. Acute Cerebral Artery Occlusion by a Calcified Embolus with False Patency Sign on Computed Tomographic Angiography. Journal of Stroke and Cerebrovascular Diseases. 2017;26(1):e5-e7. doi:10.1016/j.jstrokecerebrovasdis.2016.09.029.
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Krischek Ö, Miloslavski E, Fischer S, Shrivastava S, Henkes H. A Comparison of Functional and Physical Properties of Self-Expanding Intracranial Stents [Neuroform3, Wingspan, Solitaire, Leo(+), Enterprise]. Minim Invasive Neurosurg. 2011;54(01):21-28. doi:10.1055/s-0031-1271681.
Table 1. Published reports on intracranial stenting as salvage therapy after failure of mechanical thrombectomy in AIS.
Number of patients
NIHSS*
mTICI ≥ 2b
mRS ≤ 2 90-day
sICH
Zhou, 20183
47
20.3
80.9%
57.5%
8.5%
Nappini et al., 20184
17
20
70.6%
41.2%
12.3%
Cornelissen et al., 20185
12
16.5*
91.7%
66%
0
Chang et al., 20182
48
14*
64.6%
39.6%
16.7%
Delgado et al., 20176
42
19.2
71.4%
38.1%
4.8%
Baracchini et al., 20177
23
23*
73.9%
56.5%
4.3%
Baek et al., 20168
17
19*
83.3%
35.5%
11.8%
Linfante et al., 20119
19
19*
95%†
42%‡
16%
Total
225
NC
171 (76%)
104 (46.2%)
22 (9.8%)
Study
NIHSS: National Institutes of Health Stroke Scale (stroke symptom score) mTICI: modified Thrombolysis in Cerebral Infarction (reperfusion score) mRS: modified Rankin Scale (patient independence score) sICH: symptomatic intracerebral hemorrhage NC: not calculated *Studies with an asterisk reported median scores. Otherwise, the numbers indicate mean scores. †Linfante et al. used Thrombolysis in Myocardial Infarction (TIMI) score ≥ 2 as their reperfusion success marker. ‡Linfante et al. used 30-day mRS scores.
Abbreviations ACA, anterior cerebral artery AIS, acute ischemic stroke CT, computed tomography CTA, computed tomography angiography ICA, internal carotid artery ICH, intracerebral hemorrhage LVO, large vessel occlusion MCA, middle cerebral artery MRI, magnetic resonance imaging mRS, modified Rankin scale mTICI, modified thrombolysis in cerebral infarction NIHSS, National Institutes of Health Stroke Score PCA, posterior cerebral artery sICH, symptomatic intracerebral hemorrhage TICI, thrombolysis in cerebral infarction TIMI, thrombolysis in myocardial infarction
Disclosures The authors have no relevant disclosures related to this manuscript.
S1878-8750(19)33128-6
DOI:
https://doi.org/10.1016/j.wneu.2019.12.096
Reference:
WNEU 13943
To appear in:
World Neurosurgery
Received Date: 25 August 2019 Revised Date:
14 December 2019
Accepted Date: 16 December 2019
Please cite this article as: Potts MB, da Matta L, Abdalla RN, Shaibani A, Ansari SA, Jahromi BS, Hurley MC, Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2019.12.096. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review
Matthew B. Potts, MD,1,2 Lucas da Matta, MD,1 Ramez N. Abdalla, MD,2 Ali Shaibani, MD,1,2 Sameer A. Ansari, MD, PhD,1,2 Babak S. Jahromi, MD, PhD,1,2 Michael C. Hurley1,2 Departments of 1Neurological Surgery and 2Radiology Northwestern Memorial Hospital Northwestern University Feinberg School of Medicine Chicago, IL 60611, USA.
Corresponding author: Matthew B. Potts, MD 676 N. St. Clair St., Suite 2210 Chicago, IL 60611 Email: [email protected] Phone: 312-695-6200 Fax: 312-695-0225
Stenting of mobile calcified emboli after failed thrombectomy in acute ischemic stroke: case report and literature review
Matthew B. Potts, MD,1,2 Lucas da Matta, MD,1 Ramez N. Abdalla, MD,2 Ali Shaibani, MD,1,2 Sameer A. Ansari, MD, PhD,1,2 Babak S. Jahromi, MD, PhD,1,2 Michael C. Hurley1,2 Departments of 1Neurological Surgery and 2Radiology Northwestern Memorial Hospital Northwestern University Feinberg School of Medicine Chicago, IL 60611, USA.
Corresponding author: Matthew B. Potts, MD 676 N. St. Clair St., Suite 2210 Chicago, IL 60611 Email: [email protected] Phone: 312-695-6200 Fax: 312-695-0225
ABSTRACT BACKGROUND: Mobile calcified emboli are a rare cause of large vessel occlusion and acute ischemic stroke and pose unique challenges to standard mechanical thrombectomy techniques. Intracranial stenting has been reported as a rescue maneuver in cases of failed mechanical thrombectomy due to dissection or calcified atherosclerotic plaques, but its use for calcified emboli is not well-described. CASE DESCRIPTION: Here we present two cases of acute ischemic stroke caused by mobile calcified emboli. Standard mechanical thrombectomy techniques using aspiration catheters and stent-retrievers failed to remove these emboli so intracranial stenting was successfully performed in each case, albeit after overcoming unique challenges associated with the stenting of calcified emboli. CONCLUSION: Mobile calcified emboli are rare causes of acute ischemic stroke. Intracranial stenting can be used to successfully treat calcified emboli when mechanical thrombectomy has failed. We also review the literature on intracranial stenting as a salvage therapy for failed mechanical thrombectomy.
Introduction Endovascular thrombectomy for the treatment of acute ischemic stroke (AIS) caused by a large vessel occlusion has been shown to be both highly effective and safe compared to medical management alone.1 Thrombectomy is typically performed using either a stent-retriever, aspiration catheter, or a combination of both with the goal of achieving complete or nearcomplete reperfusion of the ischemic territory. Occasionally, however, thrombectomy fails to revascularize the occluded vessel and the subsequent use of stenting as a rescue treatment to
maintain patency of the target vessel has been reported.2-10 Risk factors for failure of thrombectomy include atherosclerotic plaques and calcified emboli. 2,11,12 Here, we report two cases of AIS caused by mobile calcified emboli for which mechanical thrombectomy failed and intracranial stenting was required.
Case Report Case 1: A middle-aged patient with a history of severe aortic stenosis underwent elective aortic valve replacement through a mini-thoracotomy. The patient’s aortic valve was noted to have calcifications extending into the left ventricle and excision of the aortic valve was reported to be difficult due to this calcification. The patient remained intubated post-operatively and was initially noted to have a symmetric neurologic exam however developed right hemiplegia after approximately four hours. Emergent head computed tomography (CT) showed hypoattenuation within the left insula and inferior frontal lobe as well as a hyperdense focus within the proximal left Sylvian fissure (Figure 1A-B). CT angiography (CTA) demonstrated this hyperdense focus to be located within the proximal M1 segment of the left middle cerebral artery (MCA) without complete occlusion (Figure 1C). CT perfusion imaging, evaluated using RAPID software (iSchemaView, CA, USA), demonstrated a small focus of infarct within the left insula (8cc, defined as cerebral blood flow <30%) and a larger surrounding region of ischemic penumbra within the left frontal, parietal, and temporal lobes (109cc, defined as Tmax >6s, Figure 1D). Given the significant perfusion mismatch and the patient’s persistent neurologic deficits, the decision was made to proceed with emergent cerebral angiography and possible mechanical thrombectomy.
An initial left internal carotid artery (ICA) injection revealed near complete occlusion of the proximal left MCA (Figure 2A-B) with extremely sluggish flow past the calcified obstruction and leptomeningeal collaterals from the left anterior and posterior cerebral arteries (ACA and PCA, respectively) providing retrograde filling of the left MCA branches. Although some sluggish flow was observed past the calcified lesion, this was not thought to be physiologically significant. In addition, the severity of the patient’s symptoms, large ischemic penumbra, and presumed embolic etiology (and not atherosclerotic plaque) led to the decision to attempt mechanical thrombectomy. This was performed using the following devices: 80cm Neuron Max sheath (Penumbra, CA, USA), ACE 68 aspiration catheter (Penumbra), Excelsior XT-27 microcatheter (Stryker, MI, USA), and a Solitaire 4 x 20 mm stent-retriever (Medtronic, MI, USA). The aspiration catheter was advanced up to the embolus and the microcatheter advanced past the embolus to allow deployment of the stent-retriever across the embolus. Once the stent-retriever was deployed, the microcatheter was removed. After five minutes, the stentretriever and aspiration catheter were removed together with the aspiration catheter and sheath both placed to suction. Subsequent control angiography showed persistence of the calcified obstruction. Two additional attempts at mechanical thrombectomy were made in the same fashion – one using the 4 x 20 mm Solitaire device and another using a 6 x 30 mm Solitaire. While flow across the embolus slightly improved, the embolus itself could not be retrieved. In fact, manipulation of the embolus pushed it distally within the M1 (Figure 2C), confirming that this was a mobile calcified embolus and not an atherosclerotic lesion. The decision was then made to place a permanent intracranial stent across the embolus in an attempt to improve flow through the MCA. An exchange-length microwire was advanced through the microcatheter into the inferior division of the left MCA and then the microcatheter and aspiration catheter were
removed. A 3.5 x 20 mm Wingspan intracranial stent (Stryker) delivery catheter was advanced over the exchange-length microwire and the stent was deployed across the embolus with its distal end in the inferior division of the left MCA and its proximal end in the proximal M1. Final control angiography demonstrated recanalization of the left M1 resulting in a Thrombolysis In Cerebral Infarction (TICI) 3 reperfusion (Figure 2D-E). Post-treatment CT demonstrated good expansion of the stent against the calcified embolus (Figure 2F). The patient was initially densely aphasic and plegic in the right arm. Post-treatment magnetic resonance imaging (MRI) demonstrated diffusion restriction within the left insula, putamen, caudate, and anteroinferior left frontal lobe as well as scattered foci of diffusion restriction throughout the remainder of the left MCA territory (Figure 2G). At the time of transfer to acute inpatient rehab on post-treatment day 12, the patient had dense expressive aphasia but could nod appropriately to questions and mimic commands. Strength was antigravity in the right arm and near full strength in the right leg. The patient was maintained on dual antiplatelet therapy with aspirin and clopidogrel for six months, at which time a repeat cerebral angiogram was performed showing persistent patency of the M1 segment of the left MCA (Figure 2H-I). At a one-year clinical follow-up, the patient’s language function had significantly improved and now was only notable for mild speech hesitancy. There was a persistent mild right facial droop and difficulty with fine motor movements of the right hand but otherwise full proximal right arm and right leg strength.
Case 2: An elderly patient with a history of hyperlipidemia, hypertension, coronary artery disease, pacemaker, and dialysis-dependent end-stage renal disease was undergoing an outpatient evaluation for left carotid stenosis by vascular surgery after presenting with brief intermittent episodes of expressive aphasia. The patient was treated with dual antiplatelet therapy using
aspirin and clopidogrel, as well as atorvastatin. CTA demonstrated a heavily-calcified atherosclerotic stenosis of the left ICA origin we well as a tandem calcified lesion at the left ICA terminus (Figure 3A-B). Due to the heavy calcification of both lesions, it was difficult to accurately grade the degree of stenosis at both sites on CT and the patient was referred to our service for a diagnostic cerebral angiogram under local anesthesia. The angiogram showed only moderate stenosis at the left ICA origin whereas the left ICA terminus was severely stenosed by a rounded intraluminal lesion concerning for a calfcific embolus (Figure 3C). The patient remained neurologically intact throughout the angiogram and was engaged in a fluent conversation about their medical history during manual compression of the femoral puncture site when they became abruptly mute and inattentive. Vital signs remained stable during this neurologic change. The left femoral artery was therefore accessed to re-evaluate the cerebral vasculature. These symptoms briefly resolved but then recurred and a repeat left ICA angiogram demonstrated worsened flow within the left MCA due to slight migration of the calcified embolus further into the left MCA origin, indicating this calcified lesion to be a mobile embolus and not an atherosclerotic lesion. After full heparinization and blood pressure augmentation, the patient’s neurologic exam again improved. An attempt was made to engage the embolus with an 064 Penumbra aspiration catheter using an adapt technique but this failed due to an inability to engage tight suction on the poorly pliable lesion. A Wingspan stent was then placed across the calcified embolus from the mid M1 segment into the supraclinoid ICA. The stent deployed well but there was difficulty retrieving the bumper on the delivery wire which slightly dislodged the stent proximally, compromising flow through the ICA, as demonstrated by reduced flow into the ipsilateral anterior cerebral artery (Figure 3D). The patient was awake during this procedure and had an improved exam with mild aphasia, so the decision was made to end the procedure and
transfer the patient to the neuro-intensive care unit. Over the following 24 hours, however, the patient’s neurologic function was found to be pressure dependent and therefore repeat angiography under general anesthesia was performed the following day during which angioplasty of the Wingspan stent was performed using a Gateway balloon (Stryker). This resulted in improved flow through the stent (Figure 3E). A subsequent head CT demonstrated a small left PCA infarct related to a non-occlusive left PCA embolus seen during the first attempt but no significant infarct within the left MCA territory (Figure 3F). Post-treatment, the patient was noted to have a right field cut but no weakness or language deficits. The patient could not get an MR due to a pacemaker. A P2Y12 response assay indicated resistance to clopidogrel so ticagrelor was started instead. The patient was subsequently transitioned from ticagrelor to coumadin due to developing a right upper extremity deep venous thrombosis. A clinic exam two months later, after completion of a course of rehabilitation, demonstrated right hemianopia, minimal word-finding difficulty, and mild loss of dexterity in the right hand. The patient expired approximately one year later due to progression of multiple non-neurologic medical issues.
Discussion: Stroke remains one of the leading causes of death and morbidity worldwide, occurring at a rate of around 250 per 100,000 person-years, causing around 90 deaths per 100,000 person-years, and causing the loss of over 100 million disability-adjusted life years in 2010.13 Continuous effort in the development of preventive and therapeutic interventions in AIS has led to improved outcomes.13 Intravenous thrombolysis is the mainstay of therapy of early cases of AIS, but mechanical thrombectomy was recently shown to improve outcomes in selected patients with large-vessel occlusions (LVO) presenting up to 24 hours after symptom onset.14 Nevertheless,
mechanical thrombectomy in such patients is not always successful at restoring blood flow.1,15 One of the factors associated with a risk of failure is calcification of the culprit thromboembolus.12 Calcified embolic stroke can occur after instrumentation of the cardiovascular system (e.g., cardiac catheterization and carotid manipulation) or can occur spontaneously.16 Such calcified emboli are distinguished from calcified intracranial atherosclerotic plaques in that they are potentially mobile, as was seen in our cases. Calcified emboli can often be identified in the initial non-contrast head CT by their increased attenuation indices (generally greater than 90 Hounsfield units) and oval shape (as opposed to the elongated shape of other thrombi).12 Thromboemboli can be classified into recent (rich in red blood cells, usually arteriogenic), aged (rich in fibrin, usually cardiogenic), and calcified (rich in calcium phosphate).17 The histological composition of the emboli has been associated with the probability of therapeutic success.12 Fibrin-rich emboli are stiffer than red blood cell-rich emboli, leading to more difficult recanalization in mechanical thrombectomy models.18 Calcified emboli are even stiffer than fibrin-rich emboli,19 which can contribute to the higher therapeutic failure rates.12,16 Biomechanical properties of the emboli are probably not entirely responsible for this difference in outcomes, as patients with calcified emboli may have other risk factors for worse outcomes, including significant atherosclerotic and cardiac disease.12 It is important to note that in the two cases presented here, the mobile calcified emboli caused symptomatic near-occlusion. It is possible that a rigid calcified embolus may not completely occlude a vessel like a more flexible soft embolus can, thus allowing some flow past the lesion. In each case, this small amount of flow was not deemed physiologically significant, as was demonstrated by the patients’ significant neurologic symptoms.
When mechanical thrombectomy fails, American Stroke Association AIS guidelines suggest that using salvage technical adjuncts may be reasonable to achieve appropriate flow restoration.14 While the document presents intra-arterial thrombolysis as salvage therapy, intracranial stenting has also been used in such situations. We identified eight studies reporting on intracranial stenting as rescue therapy after failed mechanical thrombectomy in AIS, comprising 225 patients in total (Table 1).2-9 Successful recanalization rates ranged from 6592%, with an average of 76%, resulting in good functional outcomes (mRS ≤2) in 46.2%. These results are comparable to the overall success rates reported in a meta-analysis of 2015 stroke thrombectomy trials by Goyal et al., where mTICI 2b or 3 was achieved in 71% and 90-day functional outcomes of mRS ≤2 were achieved in 46%.1 Stenting, however, was associated with symptomatic ICH in 9.8%, compared to only 4.4% in prior randomized trials.1 One possible etiology of this increased risk of symptomatic ICH is the need for additional antiplatelet medications during or after stent placement. Studies of stenting as rescue therapy in AIS typically report the use of glycoprotein IIb/IIIa inhibitors, such as tirofiban and abciximab, at the time of stent deployment followed by dual antiplatelet therapy with aspirin and clopidogrel. In our case 1, the patient was already on aspirin after an aortic valve repair. We administered a loading dose of clopidogrel through a nasogastric tube immediately after stent placement. The second patient was already on dual antiplatelet therapy at the time of stenting although a subsequent clopidogrel response assay indicated clopidogrel resistance so the patient was transitioned to ticagrelor. The reported success rates of mechanical thrombectomy for calcified emboli are poor. Dobrocky et al. recently reported 8 cases, of which successful recanalization was only achieved in one.12 This was associated with a 50% mortality at 3 months. They even reported fracture of a
stent-retriever wire during an attempted thrombectomy in one patient and perforation of a distal MCA branch in another. Other groups have reported successful mechanical thrombectomy of calcified emboli using stent-retrievers.20,21 Although ultimately technically successful, our two cases demonstrate some of the difficulties in treating calcified emboli. In the first case, several attempts were made at recanalization using a combined strategy of aspiration plus stent-retriever. After three unsuccessful attempts, the decision was made to proceed with stenting. The obvious concern was the need for dual antiplatelet therapy in the setting of a recent surgical procedure (mini-thoracotomy). The risks and benefits of this were discussed with the patient’s cardiology team before proceeding. While the stent was successfully deployed and good flow restored, the overall groin to revascularization time was approximately 220 minutes. This was certainly prolonged by the several attempts at standard mechanical thrombectomy techniques and although a TICI 3 reperfusion was achieved, the patient’s post-operative MRI had a significant infarct burden. Based on this experience, we recommend a low threshold to attempt stenting in the setting of a calcified embolus if standard techniques do not work. The second case demonstrates that stenting may not be sufficient to restore normal flow and that additional angioplasty may be required. The Wingspan and Enterprise (Codman Neurovascular) stents are the most commonly reported stents used for rescue of failed thrombectomy, although many countries also have access to the detachable Solitaire AB (Medtronic).4 Of these intracranial stents, the Wingspan provides the greatest radial force.22 Given the rigidity of a calcified embolus, the radial force of an intracranial stent should be considered during stenting. If stenting does not result in satisfactory flow, balloon angioplasty can be considered, although care must be taken to avoid vessel injury or rupture.
In summary, mobile calcified emboli are rare causes of AIS that present unique challenges and the success rate of standard mechanical thrombectomy techniques is low. Such emboli are readily detected on non-contrast CT imaging. Intracranial stenting is a promising rescue therapy for failed mechanical thrombectomy that can be applied in the case of calcified emboli.
Figure Legends:
Figure 1. Case 1, pre-treatment imaging. Initial non-contrast head CT (A) showing a hyperdense focus within the region of the left internal carotid artery (ICA) terminus (arrow). This remained hyperdense on bone windows, suggesting a calcified mass (B, arrow). Subsequent CT angiography demonstrated this calcified mass to be located within the left ICA terminus at the origin of the left middle cerebral artery (MCA, C). CT perfusion, analyzed by RAPID software, demonstrated an area of apparent infarct within the left insula and basal ganglia with a larger area of surrounding ischemic penumbra within the left MCA territory (D).
Figure 2. Case 1, intra- and post-treatment imaging. Digital subtraction angiography of the left internal carotid artery demonstrated the embolus at the origin of the left MCA with sluggish distal flow (A, AP; B, lateral). Attempts at mechanical thrombectomy using an aspiration catheter and stent-retriever failed to retrieve the calcified embolus but instead pushed it further distal into the left MCA (C, arrow), confirming this to be a mobile calcified embolus. An intracranial stent was therefore deployed across the calcified embolus (D, arrow shows stent), restoring flow through the left MCA territory (E, arrow shows calcified embolus). Posttreatment CT showed good expansion of the stent against the calcified embolus (F) and diffusion-weighted MRI showed infarction within the left basal ganglia and insula, as well as scattered infarcts within the left frontal and temporal lobes (G). A follow-up cerebral angiogram 6 months later showed persistent patency of the stent with good flow through the MCA (H-I).
Figure 3. Case 2. Initial non-contrast head CT showing a calcified mass within the region of the left ICA terminus (A). CTA (B) and diagnostic cerebral angiography (C) confirmed this calcified embolus to be within the left ICA terminus. After placement of a Wingspan stent (D), competitive flow was noted through the anterior communicating artery (arrow), indicating suboptimal flow across the stented calcified embolus within the ICA terminus. This corresponded to pressure-dependent symptoms post-treatment, prompting angioplasty the following day that resulted in improved flow through the ICA terminus (E). Post-treatment CT showed no infarct within the left MCA territory (F).
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Table 1. Published reports on intracranial stenting as salvage therapy after failure of mechanical thrombectomy in AIS.
Number of patients
NIHSS*
mTICI ≥ 2b
mRS ≤ 2 90-day
sICH
Zhou, 20183
47
20.3
80.9%
57.5%
8.5%
Nappini et al., 20184
17
20
70.6%
41.2%
12.3%
Cornelissen et al., 20185
12
16.5*
91.7%
66%
0
Chang et al., 20182
48
14*
64.6%
39.6%
16.7%
Delgado et al., 20176
42
19.2
71.4%
38.1%
4.8%
Baracchini et al., 20177
23
23*
73.9%
56.5%
4.3%
Baek et al., 20168
17
19*
83.3%
35.5%
11.8%
Linfante et al., 20119
19
19*
95%†
42%‡
16%
Total
225
NC
171 (76%)
104 (46.2%)
22 (9.8%)
Study
NIHSS: National Institutes of Health Stroke Scale (stroke symptom score) mTICI: modified Thrombolysis in Cerebral Infarction (reperfusion score) mRS: modified Rankin Scale (patient independence score) sICH: symptomatic intracerebral hemorrhage NC: not calculated *Studies with an asterisk reported median scores. Otherwise, the numbers indicate mean scores. †Linfante et al. used Thrombolysis in Myocardial Infarction (TIMI) score ≥ 2 as their reperfusion success marker. ‡Linfante et al. used 30-day mRS scores.
Abbreviations ACA, anterior cerebral artery AIS, acute ischemic stroke CT, computed tomography CTA, computed tomography angiography ICA, internal carotid artery ICH, intracerebral hemorrhage LVO, large vessel occlusion MCA, middle cerebral artery MRI, magnetic resonance imaging mRS, modified Rankin scale mTICI, modified thrombolysis in cerebral infarction NIHSS, National Institutes of Health Stroke Score PCA, posterior cerebral artery sICH, symptomatic intracerebral hemorrhage TICI, thrombolysis in cerebral infarction TIMI, thrombolysis in myocardial infarction
Disclosures The authors have no relevant disclosures related to this manuscript.