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ORIGINAL ARTICLE
Ahead of print publication  

Balloon Angioplasty Followed by Aspiration of Large-Vessel Occlusion (BAFALO): An efficient and protective treatment of tandem occlusion


1 Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital Hsin-Chu Branch, Hsin-Chu Hospital, Hsinchu City; Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
2 Department of Medical Imaging National Taiwan University Hospital, Taipei, Taiwan
3 Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei; Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital Hsin-Chu Branch, Biomedical Park Hospital, Hsinchu City, Taiwan
4 Department of Neurology, Stroke Center, National Taiwan University Hospital, Taipei, Taiwan

Date of Submission06-Feb-2022
Date of Decision08-Jul-2022
Date of Acceptance11-Jul-2022
Date of Web Publication28-Sep-2022

Correspondence Address:
Chung-Wei Lee,
Department of Medical Imaging, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei 100
Taiwan
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/fjs.fjs_34_22

  Abstract 


Background: Endovascular thrombectomy (EVT) for acute ischemic stroke associated with tandem lesion is challenging. Achieving rapid intracranial revascularization and managing the extracranial lesion without complications are the main challenges.
Materials and Methods: The balloon angioplasty followed by aspiration of large-vessel occlusion (BAFALO) technique was used to address this clinical issue. A review of a prospectively maintained stroke registry from January 2015 to April 2020 was performed. Patients had stroke with TO and treated with the BAFALO technique were included.
Results: Twelve patients were enrolled: 11 had anterior circulation stroke, and 1 had posterior circulation stroke. There were 10 ipsilateral internal carotid artery stenosis/occlusion, one left common carotid artery to subclavian artery bypass stenosis, and 1 vertebral artery orifice stenosis. The median National Institutes of Health Stroke Scale score was 16 (interquartile range [IQR]: 14–16). Revascularization with a Modified Thrombolysis in Cerebral Infarction score of 2b or more was achieved in 11 (92%) patients. The median puncture-to-revascularization time was 25 min (IQR: 19.5–31). Emergent stent implantation was performed in five (42%) patients. Three had distal protection devices (DPDs) with no distal embolization. Two patients did not use a DPD, and one had intracranial reocclusion. Eight (67%) proximal stenotic vessels remained patent. No symptomatic intracranial hemorrhage occurred. Eight (67%) patients had favorable clinical outcomes (modified Rankin Score 0–2 at 90 days).
Conclusion: While managing TO, the BAFALO technique could achieve rapid intracranial revascularization and treat extracranial lesions under embolic protection. These merits translate into favorable clinical outcomes.

Keywords: Acute stroke, endovascular thrombectomy, tandem lesion



How to cite this URL:
Chen KW, Lin YH, Hsu CH, Lu CJ, Tang SC, Lee CW, Chiang PY. Balloon Angioplasty Followed by Aspiration of Large-Vessel Occlusion (BAFALO): An efficient and protective treatment of tandem occlusion. Formos J Surg [Epub ahead of print] [cited 2022 Nov 26]. Available from: https://www.e-fjs.org/preprintarticle.asp?id=357310

Kuo-Wei Chen & Yen-Heng Lin, both authors contributed equally to this study.





  Introduction Top


The management of acute stroke with tandem lesion (TL) is complicated. It has limited response to intravenous thrombolytic therapy[1] and is technically challenge by endovascular thrombectomy (EVT). The concurrent extracranial lesion could hinder intracranial access and delay the time to revascularization.[2],[3],[4] Of the extracranial lesions, carotid stenosis is the most common and accounts for 15%–20% of cases of anterior circulation stroke.[1],[5]

The optimal technical strategy remains elusive.[6] The antegrade method is used to treat the extracranial lesion first, with angioplasty or stenting, followed by EVT.[7] The retrograde method has been used to treat intracranial occlusion and achieve revascularization before definite treatment of extracranial lesions.[8] The retrograde method is theoretically associated with a shorter time to revascularization than the antegrade method. However, in some cases, the extracranial lesion needs be managed to gain intracranial access.[6],[9] In the antegrade method, the reestablished carotid flow might propagate the intracranial thrombus to an unreachable vascular segment. Both of these methods have limitations, and new techniques have been proposed.[10],[11]

There is controversy regarding whether carotid stenting should be performed in conjunction with EVT. Without proper premedication, the rate of reocclusion is high,[12],[13] and the risk of hemorrhage should be balanced with the risk of rethrombosis.[14],[15] However, the procedures are often undertaken without an embolism protection device, either due to technical difficulty or sense of urgency.[6],[16],[17] The rate of recurrent thromboembolic events was 14% in a report by Labeyrie et al.[18]

The objective of this study is to demonstrate a technique of balloon angioplasty followed by aspiration of large-vessel occlusion (BAFALO). This is a robust technique with inherited proximal flow control and can achieve rapid intracranial revascularization. It can work in conjunction with distal protection devices (DPDs) during the treatment of extracranial lesions. The cases are described and the technical details are presented in this report.


  Methods Top


Patients

The study population was derived from the stroke registry of the National Taiwan University Hospital. This study was approved by the Research Ethics Committee of National Taiwan University Hospital (No. 202005131 RIND), and the informed consent was waived by the IRB. The database has been prospectively maintained since 1995 and includes baseline patient characteristics, risk factors, underlying diseases, neurological presentations, clinical outcomes, and time metrics. Patients who presented with acute ischemic stroke with the concurrent extracranial tandem steno-occlusive disease treated with EVT were identified. Those treated with the BAFALO technique were included.

Criteria for thrombectomy and clinical outcome assessment

All patients with suspected strokes were evaluated by a consulting neurologist. National Institutes of Health Stroke Scale (NIHSS) scores were recorded. The indications and contraindications for the administration of intravenous tissue plasminogen activator (t-PA) were based on the American Heart Association/American Stroke Association guidelines.[19] If large-vessel occlusion (LVO) was suspected, triphasic computed tomographic angiography and perfusion were performed. The following criteria for performing EVT were based on the National Health Insurance reimbursement regulations: (i) LVO in the internal carotid artery (ICA), middle cerebral artery M1 or M2 segment, anterior cerebral artery A1 segment, or vertebrobasilar artery; (ii) onset within 8 h for anterior circulation and 24 h for posterior circulation; and (iii) NIHSS score between 8 and 30.

EVT was performed mostly under local anesthesia with the application of lidocaine hydrochloride (2%, 5–10 mL) at the puncture site and a 1-mL intravenous bolus of fentanyl (0.05 mg/mL) as needed. General anesthesia was administered only to patients with poor consciousness, agitation, or other conditions that would compromise the airway. The procedure was performed by two board-certified interventional neuroradiologists (with 8 and 16 years of experience) and a board-certified interventional neurosurgeon (4 years of experience) using a biplane angiography machine. Contact aspiration thrombectomy (CAT) was used as frontline therapy. After the procedure, patients were transferred to the neurological intensive care unit. Follow-up brain magnetic resonance imaging or computed tomography scans were performed within 72 h of EVT, and the patency of intracranial and extracranial vessels was checked. Transcranial Doppler and carotid ultrasonography were performed within 24 h of EVT. All patients who survived had follow-up image studies at outpatient clinics.

The radiographic outcomes of EVT were evaluated according to the Modified Thrombolysis in Cerebral Infarction (mTICI) score. Successful revascularization was defined as an mTICI score of 2b or above. The clinical outcome was assessed after 3 months using the modified Rankin score (mRS). A favorable outcome was defined as mRS ≤2 at 90 days.

Balloon angioplasty followed by aspiration of large-vessel occlusion technique

The right femoral artery was accessed using the Seldinger technique. The guiding sheath (GS) (Neuron Max 088, Penumbra; Almeda, CA) or a combination of coaxial GSs (Neuron MAX 088 in 8-Fr Shuttle Sheath, Cook Medical; Bloomington, IN) was placed into the common carotid artery (CCA), or the subclavian artery in posterior circulation stroke. An angiographic run was performed to delineate the extracranial lesion. If a 0.035-inch guidewire could pass through the extracranial lesion, the angiographic catheter was advanced through the stenosis followed by the GS. If the catheter or GS could not pass through the stenosis, a 0.014-inch microwire was navigated through the lesion. A low-profile monorail balloon catheter (Emerge 3.5 mm or 4 mm, Boston Scientific; Marlborough, MA) was introduced across the lesion and slowly inflated to a size similar or slightly larger than the diameter of the GS. The GS was pushed through until in contact with the proximal end of the balloon. The balloon was then gradually deflated, and the GS was advanced simultaneously. This procedure was repeated until the GS passed through the stenosis. The GS was then advanced into the upper cervical or petrous portion of the ICA (or distal V2 segment). The balloon catheter was then retracted. Manual suction was applied to the GS to remove potential thrombi distal to the stenosis. After confirming backflow from the GS, a gentle second angiographic run was performed to study the intracranial occlusion. A reperfusion catheter (ACE 60 or 68, Penumbra) was advanced, and CAT was performed. [Figure 1] demonstrates the steps of the BAFALO technique.
Figure 1: Illustration of BAFALO technique Step-by-step demonstration of large-bore catheter tracking of the distal thrombus through stenosis. (a) Angioplasty was done at the stenosis (b) Tracking the large-bore catheter through the stenosis while slowly deflating the balloon. (c) Reach the intracranial clot and perform thrombectomy. BAFALO: Balloon angioplasty followed by aspiration of the large-vessel

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After successful EVT, the GS was pulled back proximal to the extracranial stenosis, usually to the distal CCA. Negative pressure was kept during retraction to aspirate the residual thrombus distal to the proximal lesion. Before GS retraction, a DPD (Spider FX, Medtronic, Dublin, Ireland; or FilterWire EZ, Boston Scientific) or a 0.014-inch microwire was kept in the ICA. The angiographic run was repeated every 10 min for 30 min to evaluate the evolution of extracranial lesions. If there was no obvious recoiling and the distal flow was adequate, the DPD was retrieved and the procedure was completed. Otherwise, a self-expandable stent was deployed along the microwire or protective device. Glycoprotein IIb/IIIa antagonist (tirofiban) infusion (0.25–0.50 mg) was started before stenting, followed by an intravenous maintenance dose of approximately 0.05 μg/kg/h for at least 24 h. After image follow-up the next day, tirofiban was shifted to oral antiplatelet therapy. [Figure 2] and [Supplementary Figure 1] illustrate the steps of carotid stenting following the BAFALO technique with emphasis on embolic protection.
Figure 2: Embolic protection in carotid stenting. A 76-year-old man presented with left-sided hemiplegia, aphasia, and a National Institutes of Health Stroke Scale score of 15. A. The control angiography through the guiding sheath (GS, large white arrow) (Neuron Max 088; Penumbra, Almeda, CA) revealed total occlusion of the right internal carotid artery (small white arrow). (a) 0.014-inch microwire (black arrows) was navigated through the occlusion. (b) Meticulous contrast injection through the microcatheter (Excelsior XT-27; Stryker Neurovascular, Fremont, CA) confirmed intraluminal passage (small white arrows). A balloon catheter (black arrows) (Sterling Monorail 4–30 mm; Boston Scientific, Marlborough, MA) was inflated suboptimally (notice the nonfilling of the distal end). The GS (large white arrow) was attached to the proximal end of the balloon. (c The balloon catheter (black arrows) was deflated gradually, and at the same time, the GS (large white arrow) was tracked through the stenotic segment using the BAFALO technique. (d) After EVT, a distal protection device (Spider FX; Medtronic, Dublin, Ireland) (black arrows) was deployed, and the GS was withdrawn to the common carotid artery. Angiography revealed severe carotid stenosis (small white arrow). (e) A carotid stent (small white arrows) (XACT 7–9 mm × 30 mm; Abbott, Chicago, IL) was deployed. The proximal flow control conferred by the balloon and GS caused contrast stagnation (small white arrows in b, d). GS: Guiding sheath, EVT: Endovascular thrombectomy

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Statistical analysis

Descriptive statistics of demographic data, angiographic data, and clinical outcomes are provided. Procedural details for individual patients are also provided. Because of the small sample size, inferential statistics were not used.


  Results Top


In total, records of 363 patients undergoing EVT from January 2015 to April 2020 were reviewed. There were 15 cases of TOs, and 12 of these were treated with BAFALO technique. Eleven strokes occurred in the anterior circulation and one in the posterior circulation. Twelve patients (92%) were men. The mean age was 69.3 (standard deviation: 8.9) years [Table 1]. Two patients (17%) received intravenous t-PA. The median NIHSS score was 16 (interquartile range [IQR]: 14–16). The median onset-to-puncture time was 293 min (IQR: 201–369 min). The median puncture-to-revascularization time was 25 min (IQR: 19.5–31 min). The median procedure time was 50 min (IQR: 42–61 min). Successful revascularization (mTICI 2b or above) was achieved in 11 patients (92%). Emergent stent implantation was performed in five patients (42%). There was no symptomatic intracerebral hemorrhage (sICH). Eight (67%) patients had favorable outcomes at 90 days, and there was no mortality.
Table 1: Demographic data and clinical outcome of included subjects

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[Table 2] illustrates the details of the procedures. The sites of proximal occlusion were as follows: carotid bulb (N = 9), petrous ICA (N = 1), vertebral artery (VA) orifice (N = 1), and CCA–subclavian artery bypass graft (N = 1). Patient 7 had a left CCA orifice occlusion due to prior aortic arch surgery. Thus, bypass grafting was the only route of intracranial access. Transbrachial access was performed, and a guiding catheter was successfully tracked through the bypass graft [Figure 3]. In patients with acute stenting, protective devices were not used in the initial two cases. Thrombus migration and intracranial reocclusion occurred in one patient who was treated by repetitive thrombectomy (Patient 4). Patient 6 had initial revascularization, but repetitive local thrombosis occurred. EVT was repeated three times. Finally, we decided to give up because the occlusive site was M2 and the cervical lesion was also occluded.
Figure 3: Left M1 occlusion with the left CCA-SCA bypass stenosis. This 64-year-old man had a chronic Type B aortic intramural hematoma. He had a history of thoracic endovascular aortic repair with the left CCA chimney, left SCA proximal occlusion, and left CCA-SCA bypass 4 years previously. (a) Angiography of the left brachial artery revealed severe bypass graft stenosis and occlusion of the proximal CCA (black arrows). (b) A balloon catheter (Emerge 4 mm-20 cm; Boston Scientific, Marlborough, MA) was used to dilate the stenosis and track the guiding sheath (GS; large white arrow) (Neuron Max 088; Penumbra, Almeda, CA). (c and d) The balloon catheter was deflated gradually, and the GS was advanced across the stenosis. Endovascular thrombectomy was performed, and revascularization was achieved 11 min after groin puncture. CCA: Common carotid artery, SCA: Subclavian artery, GS: Guiding sheath

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Table 2: Procedure details of individual patient

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Four patients had in-hospital reocclusion of extracranial lesions without neurological deterioration. Only one patient was retreated for perfusion impairment seen on an imaging study and the extracranial ICA remained patent afterward (Patient 8). Patient 2 had sufficient VA flow from the cervical collaterals and had a favorable outcome. The other two cases (Patients 5 and 6) had large infarct volumes and fair collateral circulation from the contralateral hemisphere. They were not retreated due to a high risk of hemorrhagic transformation and uncertain benefit.


  Discussion Top


The challenges of treating TOs involved two aspects: achieving rapid revascularization and treating extracranial lesions without incurring complications.[20]

Rapid intracranial revascularization

In this study, eight patients (67%) had intracranial revascularization within 30 min of groin puncture. Nine (75%) patients had a total procedure time of 60 min. Fast revascularization translated into favorable outcomes for 67% of the patients. When comparing the data from 17 comprehensive Korean stroke centers, the mean puncture-to-revascularization time for TO was 344 min, with 41% achieving a favorable outcome.[21] In a study by Lockau et al. including 37 cases, the mean puncture-to-reperfusion time was 55 min, with 46% achieving a favorable outcome.[22] This finding suggested that the BAFALO technique could achieve rapid intracranial revascularization. Intracranial access could be established with simple moves. The key was to advance the GS across the extracranial lesions and eliminate the problems they create. The subsequent EVT could be performed in the same way as for a single occlusion. A GS was preferred over other guiding catheters in this technique because it is designed for direct insertion into vessels, and its tapering tip can pass through the stenotic lesion more easily. The rapid revascularization and relatively short procedure time enabled most procedures to be completed under local anesthesia, except in the case of one patient with basilar artery occlusion who was intubated at the emergency department due to coma.

Proximal flow control

Proximal flow control could reduce the occurrence of distal embolization and facilitate the efficacy of EVT.[23],[24],[25] This might make a significant difference in TOs since they were often accompanied by ICA thrombosis.[18],[26] The balloon angioplasty in the BAFALO technique was not aimed at treating the extracranial lesion but rather at anchoring and tracking the GS across the stenotic segment. The two work as a continuum and leave no space between the working system and the disease vessel [Figure 1]. Eker et al. discovered a trend of lower distal embolization in the retrograde method than in the antegrade method. This might be the result from decreased cervical flow when a large-bore catheter occupied the stenotic lumen during EVT.[9] In [Figure 2], there was contrast stasis in the cervical ICA, which indicated flow stagnation. The suboptimal inflation of the balloon could also avoid carotid bulb stimulation and cardiac suppression, which might aggravate ischemic injuries.

Balloon guide catheters (BGCs) are frequently used during EVT to create proximal flow control.[23],[24],[25] However, a BGC might not be able to cross a carotid stenosis.[10],[14] CCA deployment is was officially recommended, and its efficacy had not been justified. Some BGCs were not designed for passage through carotid stents with large profiles (up to 0.088 inches), and the optimal stent selection might be restricted.[10] In cases of total occlusion, a large clot burden was expected and might cause occlusion of the BGC.[10],[27] In our practice, coaxial 8-Fr and 6-Fr GSs were used while encountering TOs. If the 6-Fr GS became occluded, it could be retrieved outside of the body to clean the clot and repositioned through the 8-Fr GS sheath.

Application of distal protection devices

After EVT, focus was shifted to extracranial lesions. The GS was retrieved, and distal thrombus migration might occur after establishing extracranial flow.[6] In addition, emergent carotid stenting was often performed without protection due to technical difficulties or a sense of urgency.[6],[16],[17] Labeyrie et al. reported an early embolic recurrence rate of 14% in TOs. Therefore, the authors suggested coil occlusion of the cervical lesion to reduce recurrent embolization if the anatomy is favorable.[18] Yi et al. described the deployment of DPDs through a microcatheter during the first cross of extracranial lesions and performing aspirations.[11] However, the vascular anatomy might not be clear with an angiographic run through the microcatheter, and the DPD should be deployed with caution. Thrombus might be present along the cervical ICA, which cannot be reached by a DPD. Therefore, the use of a DPD at the first pass of carotid lesions might not be warranted. Proximal flow control might be more applicable.[9],[20] With the BAFALO technique, an ICA clot could be removed under proximal flow control. A thrombus near a carotid lesion could be aspirated through the GS after DPD deployment, and carotid stenting could be completed securely. In this study, only one patient had distal embolization during emergent carotid stenting without DPD.

It might be safer to treat carotid lesions after EVT than at the beginning of the procedure. There were concerns that stent struts might hinder the advancement of large-bore catheters and result in stent displacement or vascular perforation. Interaction between the tines of the stent retriever (SR) and carotid stent had been reported while retrieving the thrombus.[22],[28] Sometimes, carotid endarterectomy was required to remove the retained device.[28] Moreover, if acute in-stent thrombosis occurs, salvage therapies such as thrombolytic therapy might prolong the time to revascularization and sometimes cause procedure failure.[12],[13],[29] The BAFALO technique could bypass the need for a carotid stent to gain intracranial access at the beginning of EVT and leave the definite treatment of extracranial lesions after EVT.

Decision-making for carotid stenting

Whether carotid stenting should be performed simultaneously with EVT had been debated. Stenting without proper premedication was associated with a high rate of reocclusion.[12],[13] Hernández-Fernández et al. described 40 consecutive cases of carotid TOs. Emergent carotid stenting was performed in 32 cases, and nine (28.1%) had reocclusion during follow-up.[13] Meanwhile, the use of antiplatelets might increase the rate of sICH, and a meticulous assessment of the risks and benefits was warranted.[14],[15] Careful patient selection to avoid large infarct volume and checking the collateral circulation from other vascular territories might decrease complications.[9],[13]

After EVT, time could be spent on definitively addressing the carotid lesion.[9] The control angiogram was repeated every 10 min for 30 min. If there was recoil in the stenosis or insufficient distal flow, carotid stenting could be performed. In the current study, five (5/12) cases required emergent carotid stenting and one (1/12) case required delayed stenting. There was no incidence of sICH. All reocclusions of extracranial lesions remained asymptomatic. Only one patient was retreated due to perfusion impairment. These findings echoed those of previous studies that showed that patients with the long-standing steno-occlusive disease might have better collateral circulation or hemodynamic reserve and could tolerate proximal occlusion.[9],[13],[29] Angioplasty alone was associated with a higher rate of reocclusion than emergent stenting, but they had similar outcomes.[6],[20]

TO of posterior circulation

Basilar artery occlusion with VA stenosis has a dismal prognosis. Intracranial access through the sound side or the use of SR might be more effective in this situation.[30] At times, the contralateral side is inaccessible due to hypoplasia or excessive tortuosity, and reconstruction of the diseased vessels at the time of EVT is necessary.[31] A recent meta-analysis revealed faster and better revascularization in the direct aspiration first pass technique than SR as frontline therapy.[32] The BAFALO technique could be used to track the GS across the VA stenosis and perform CAT in a manner similar to anterior circulation stroke.

Comparison with other techniques

There are SR-based techniques aimed to amend the limitations of antegrade and retrograde methods by treating the two occlusions simultaneously.[10],[33],[34] A microwire and microcatheter are navigated across both occlusions, and an SR is deployed. An angioplasty balloon or carotid stent is delivered along the push wire of SR to treat the extracranial lesion. Care must be taken not to lose the position of the SR during device delivery.[34] The carotid stent must be deployed before retrieval of SR,[31] or must be deployed through a new microwire.[10] Embolic protection is insufficient. Sultan-Qurraie et al. described double protection with SR deployed over the orifice of the ACA, and BGC placed in the CCA.[33] However, its efficacy was unwarranted.[33]

Amuluru et al. described a series of 32 cases treated with the modified Dotter technique. The carotid lesion was crossed with a 0.035-inch guidewire and followed by the inner dilator of Neuron MAX 088.[27] In our experience, the majority of extracranial lesions could only be crossed with microwire. The two methods are complementary to each other.

The major limitation of this study was the relatively small number of cases and the retrospective design. This might cause selection bias and affect the outcome. The efficacy of the BAFALO technique should be confirmed with a larger sample size. Nonetheless, this study has described the technical details of every possible aspect of TO treatment, extended the application toward posterior circulation stroke, and discussed uncommon sites of stenosis.


  Conclusion Top


The BAFALO technique is a robust technique for dealing with acute stroke associated with TOs. This maneuver is simple and safe, and carotid stenting can be performed under standard protection. It is potentially applicable to both anterior and posterior circulation. Fast intracranial revascularization and favorable clinical outcomes can be achieved.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    -  Lin YH
    -  Hsu CH
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    -  Tang SC
    -  Lee CW
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