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Endovascular treatment of ischemic stroke due to isolated internal carotid artery occlusion: ETIS registry data analysis

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Abstract

Background

The best treatment for acute ischemic stroke (AIS) due to isolated cervical internal carotid artery occlusion (CICAO) (i.e., without associated occlusion of the circle of Willis) is still unknown. In this study, we aimed to describe EVT safety and clinical outcome in patients with CICAO.

Methods

We analyzed data of all consecutive patients, included in the Endovascular Treatment in Ischemic Stroke (ETIS) Registry between 2013 and 2020, who presented AIS and proven CICAO on angiogram and underwent EVT. We assessed carotid recanalization, procedural complications, National Institutes of Health Stroke Scale (NIHSS) at 24 h post-EVT, and 3-month favorable outcome (modified Rankin Scale, mRS ≤ 2 or equal to the pre-stroke value).

Results

Forty-five patients were included (median age: 70 years; range: 62–82 years). The median NIHSS before EVT was 14 (9–21). Carotid stenting was performed in 23 (51%) patients. Carotid recanalization at procedure end and on control imaging was observed in 37 (82%) and 29 (70%) patients, respectively. At day 1 post-EVT, the NIHSS remained stable or decreased in 25 (60%) patients; 12 (29%) patients had early neurologic deterioration (NIHSS ≥ 4 points). The rate of procedural complications was 36%, including stent thrombosis (n = 7), intracranial embolism (n = 7), and symptomatic intracranial hemorrhage (n = 1). At 3 months, 18 (40%) patients had a favorable outcome, and 10 (22%) were dead.

Conclusion

Our study suggests that EVT in AIS patients with moderate/severe initial deficit due to CICAO led to high rate of recanalization at day 1, and a 40% rate of favorable outcome at 3 months. There was a high rate of procedural complication which is of concern. Randomized controlled trials assessing the superiority of EVT in patients with CICAO and severe deficits are needed.

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Data availability statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

ASPECTS:

Alberta stroke program early CT score

CICAO:

Cervical isolated internal carotid artery occlusion

CT:

Computed tomography

DSA:

Digital subtraction angiography

END:

Early neurological deterioration

ETIS:

Endovascular treatment in ischemic stroke

EVT:

Endovascular treatment

ICA:

Internal carotid artery

IVT:

Intravenous thrombolysis

LVO:

Large vessel occlusion

MRI:

Magnetic resonance imaging

mRS:

Modified rankin scale

NIHSS:

National institutes of health stroke scale

References:

  1. Paciaroni M, Caso V, Venti M et al (2005) Outcome in patients with stroke associated with internal carotid artery occlusion. Cerebrovasc Dis 20:108–113. https://doi.org/10.1159/000086800

    Article  PubMed  Google Scholar 

  2. Damania D, Kung NT-M, Jain M et al (2016) Factors associated with recurrent stroke and recanalization in patients presenting with isolated symptomatic carotid occlusion. Eur J Neurol 23:127–132. https://doi.org/10.1111/ene.12819

    Article  CAS  PubMed  Google Scholar 

  3. Ter Schiphorst A, Gaillard N, Dargazanli C, Mourand I, Corti L, Charif M, Ayrignac X, Lippi A, Bouly S, Thibault L et al (2021) Symptomatic isolated internal carotid artery occlusion with initial medical management: a monocentric cohort. J Neurol 268:346–355

    Article  Google Scholar 

  4. Mazya MV, Cooray C, Lees KR et al (2018) Minor stroke due to large artery occlusion. When is intravenous thrombolysis not enough? Results from the SITS International Stroke Thrombolysis Register. Eur Stroke J 3:29–38. https://doi.org/10.1177/2396987317746003

    Article  PubMed  Google Scholar 

  5. Boulenoir N, Turc G, Henon H, Laksiri N, Mounier-Véhier F, Buttaz IG, Duong D-L, Papassin J, Yger M, Triquenot A et al (2021) Early neurological deterioration following thrombolysis for minor stroke with isolated internal carotid artery occlusion. Eur J Neurol 28:479–490

    Article  CAS  Google Scholar 

  6. Gliem M, Lee J-I, Barckhan A et al (2017) Outcome and treatment effects in stroke associated with acute cervical ICA occlusion. PLoS ONE 12:e0170247. https://doi.org/10.1371/journal.pone.0170247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Yeo LLL, Kong WY, Paliwal P et al (2016) Intravenous thrombolysis for acute ischemic stroke due to cervical internal carotid artery occlusion. J Stroke Cerebrovasc Dis 25:2423–2429. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.06.014

    Article  PubMed  Google Scholar 

  8. Pechlaner R, Knoflach M, Matosevic B et al (2013) Recanalization of extracranial internal carotid artery occlusion after i.v. thrombolysis for acute ischemic stroke. PLoS ONE 8:e55318. https://doi.org/10.1371/journal.pone.0055318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. EC/IC Bypass Study Group (1985) Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. N Engl J Med 313:1191–1200. https://doi.org/10.1056/NEJM198511073131904

    Article  Google Scholar 

  10. Powers WJ, Clarke WR, Grubb RL et al (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the carotid occlusion surgery study randomized trial. JAMA 306:1983–1992. https://doi.org/10.1001/jama.2011.1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Powers WJ, Rabinstein AA, Ackerson T et al (2019) Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke. https://doi.org/10.1161/STR.0000000000000211

    Article  PubMed  Google Scholar 

  12. Goyal M, Menon BK, van Zwam WH et al (2016) Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet 387:1723–1731. https://doi.org/10.1016/S0140-6736(16)00163-X

    Article  PubMed  Google Scholar 

  13. Bracard S, Ducrocq X, Mas JL et al (2016) Mechanical thrombectomy after intravenous alteplase versus alteplase alone after stroke (THRACE): a randomised controlled trial. Lancet Neurol 15:1138–1147. https://doi.org/10.1016/S1474-4422(16)30177-6

    Article  CAS  PubMed  Google Scholar 

  14. Nogueira RG, Jadhav AP, Haussen DC et al (2018) Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med 378:11–21. https://doi.org/10.1056/NEJMoa1706442

    Article  PubMed  Google Scholar 

  15. Albers GW, Marks MP, Kemp S et al (2018) Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med 378:708–718. https://doi.org/10.1056/NEJMoa1713973

    Article  PubMed  PubMed Central  Google Scholar 

  16. Mesnil D, de Rochemont R, Sitzer M, Neumann-Haefelin T et al (2004) Endovascular recanalization of acute atherothrombotic carotid artery occlusion holds up progressive stroke. Neuroradiology 46:583–586. https://doi.org/10.1007/s00234-004-1214-2

    Article  Google Scholar 

  17. Jovin TG, Gupta R, Uchino K et al (2005) Emergent stenting of extracranial internal carotid artery occlusion in acute stroke has a high revascularization rate. Stroke 36:2426–2430. https://doi.org/10.1161/01.STR.0000185924.22918.51

    Article  PubMed  Google Scholar 

  18. Dabitz R, Triebe S, Leppmeier U et al (2007) Percutaneous recanalization of acute internal carotid artery occlusions in patients with severe stroke. Cardiovasc Intervent Radiol 30:34–41. https://doi.org/10.1007/s00270-005-0286-7

    Article  PubMed  Google Scholar 

  19. Bae G-Y, Hong J-H, Sohn S-I, et al (2008) Emergent carotid stenting in acute stroke patients with steno-occlusion of proximal internal carotid artery

  20. Baik SK, Jeon U, Choo KS et al (2011) What is the real risk of dislodging thrombi during endovascular revascularization of a proximal internal carotid artery occlusion? Neurosurgery 68:1084–1091. https://doi.org/10.1227/NEU.0b013e31820a19fc

    Article  PubMed  Google Scholar 

  21. Kono K, Tanaka Y, Yoshimura R et al (2011) Emergent carotid artery stenting using a flow reversal system for acute atherosclerotic occlusion of the internal carotid artery. Acta Neurochir 153:2175–2180. https://doi.org/10.1007/s00701-011-1142-y

    Article  PubMed  Google Scholar 

  22. Matsubara N, Miyachi S, Tsukamoto N et al (2013) Endovascular intervention for acute cervical carotid artery occlusion. Acta Neurochir 155:1115–1123. https://doi.org/10.1007/s00701-013-1697-x

    Article  PubMed  Google Scholar 

  23. Dalyai RT, Chalouhi N, Singhal S et al (2013) Stent-assisted endovascular recanalization of extracranial internal carotid artery occlusion in acute ischemic stroke. World Neurosurg 79:143–148. https://doi.org/10.1016/j.wneu.2012.08.017

    Article  PubMed  Google Scholar 

  24. Choi JY, Lee JI, Lee TH et al (2014) Emergent recanalization with stenting for acute stroke due to athero-thrombotic occlusion of the cervical internal carotid artery: a single center experience. J Kor Neurosurg Soc 55:313. https://doi.org/10.3340/jkns.2014.55.6.313

    Article  CAS  Google Scholar 

  25. Kwak JH, Zhao L, Kim JK et al (2014) The outcome and efficacy of recanalization in patients with acute internal carotid artery occlusion. Am J Neuroradiol 35:747–753. https://doi.org/10.3174/ajnr.A3747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Son S, Choi DS, Oh MK et al (2015) Emergency carotid artery stenting in patients with acute ischemic stroke due to occlusion or stenosis of the proximal internal carotid artery: a single-center experience. J NeuroIntervent Surg 7:238–244. https://doi.org/10.1136/neurintsurg-2014-011141

    Article  Google Scholar 

  27. Cohen JE, Gomori JM, Leker RR et al (2016) Emergency revascularization of acute internal carotid artery occlusion: follow the spike, it guides you. J Clin Neurosci 29:95–99. https://doi.org/10.1016/j.jocn.2015.12.013

    Article  PubMed  Google Scholar 

  28. Jadhav A, Panczykowski D, Jumaa M et al (2018) Angioplasty and stenting for symptomatic extracranial non-tandem internal carotid artery occlusion. J NeuroIntervent Surg 10:1155–1160. https://doi.org/10.1136/neurintsurg-2018-013810

    Article  Google Scholar 

  29. Nakagawa N, Fukawa N, Tsuji K et al (2018) Urgent carotid artery stenting for carotid-related stroke-in-evolution. Oper Neurosurg 14:9–15. https://doi.org/10.1093/ons/opx073

    Article  Google Scholar 

  30. de Castro-Afonso LH, Nakiri GS, Moretti Monsignore L et al (2019) Endovascular reperfusion for acute isolated cervical carotid occlusions: the concept of “hemodynamic thrombectomy.” Intervent Neurol. https://doi.org/10.1159/000493021

    Article  Google Scholar 

  31. Mizowaki T, Fujita A, Inoue S et al (2020) Outcome and effect of endovascular treatment in stroke associated with acute extracranial internal carotid artery occlusion: single-center experience in Japan. J Stroke Cerebrovasc Dis 29:104824. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.104824

    Article  PubMed  Google Scholar 

  32. Desilles J-P, Consoli A, Redjem H et al (2017) Successful reperfusion with mechanical thrombectomy is associated with reduced disability and mortality in patients with pretreatment diffusion-weighted imaging-alberta stroke program early computed tomography score ≤6. Stroke 48:963–969. https://doi.org/10.1161/STROKEAHA.116.015202

    Article  PubMed  Google Scholar 

  33. Kernan WN, Ovbiagele B, Black HR et al (2014) Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals From the American Heart Association/American Stroke Association. Stroke 45:2160–2236. https://doi.org/10.1161/STR.0000000000000024

    Article  PubMed  Google Scholar 

  34. Legrand L, Tisserand M, Turc G et al (2015) Do FLAIR vascular hyperintensities beyond the DWI lesion represent the ischemic penumbra? Am J Neuroradiol 36:269–274. https://doi.org/10.3174/ajnr.A4088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. ter Schiphorst A, Charron S, Hassen WB, et al (2020) Tissue no-reflow despite full recanalization following thrombectomy for anterior circulation stroke with proximal occlusion: a clinical study. J Cereb Blood Flow Metab. https://doi.org/10.1177/0271678X20954929

  36. Prosser J, Butcher K, Allport L et al (2005) Clinical-diffusion mismatch predicts the putative penumbra with high specificity. Stroke 36:1700–1704. https://doi.org/10.1161/01.STR.0000173407.40773.17

    Article  PubMed  Google Scholar 

  37. Jovin TG, Chamorro A, Cobo E et al (2015) Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med 372:2296–2306. https://doi.org/10.1056/NEJMoa1503780

    Article  CAS  PubMed  Google Scholar 

  38. Seners P, Turc G, Tisserand M et al (2014) Unexplained early neurological deterioration after intravenous thrombolysis: incidence, predictors, and associated factors. Stroke 45:2004–2009. https://doi.org/10.1161/STROKEAHA.114.005426

    Article  CAS  PubMed  Google Scholar 

  39. Hacke W, Kaste M, Fieschi C et al (1998) Randomised double-blind placebo-controlled trial of thrombolytic therapy with intravenous alteplase in acute ischaemic stroke (ECASS II). The Lancet 352:1245–1251. https://doi.org/10.1016/S0140-6736(98)08020-9

    Article  CAS  Google Scholar 

  40. Weimar C, Goertler M, Harms L et al (2006) Distribution and outcome of symptomatic stenoses and occlusions in patients with acute cerebral ischemia. Arch Neurol 63:1287. https://doi.org/10.1001/archneur.63.9.1287

    Article  PubMed  Google Scholar 

  41. Yilmaz U, Körner H, Mühl-Benninghaus R et al (2017) Acute occlusions of dual-layer carotid stents after endovascular emergency treatment of tandem lesions. Stroke 48:2171–2175. https://doi.org/10.1161/STROKEAHA.116.015965

    Article  PubMed  Google Scholar 

  42. Eker OF, Bühlmann M, Dargazanli C et al (2018) Endovascular treatment of atherosclerotic tandem occlusions in anterior circulation stroke: technical aspects and complications compared to isolated intracranial occlusions. Front Neurol. https://doi.org/10.3389/fneur.2018.01046

    Article  PubMed  PubMed Central  Google Scholar 

  43. Pop R, Zinchenko I, Quenardelle V et al (2019) Predictors and clinical impact of delayed stent thrombosis after thrombectomy for acute stroke with tandem lesions. Am J Neuroradiol 40:533–539. https://doi.org/10.3174/ajnr.A5976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Pfaff JAR, Maurer C, Broussalis E et al (2020) Acute thromboses and occlusions of dual layer carotid stents in endovascular treatment of tandem occlusions. J NeuroIntervent Surg 12:33–37. https://doi.org/10.1136/neurintsurg-2019-015032

    Article  Google Scholar 

  45. Mokin M, Kass-Hout T, Kass-Hout O et al (2012) Intravenous thrombolysis and endovascular therapy for acute ischemic stroke with internal carotid artery occlusion: a systematic review of clinical outcomes. Stroke 43:2362–2368. https://doi.org/10.1161/STROKEAHA.112.655621

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Jessica Hattinguais and Amel Benali for their help in data collection. On behalf of the ETIS-Research Investigators: CHRU Montpellier: Cyril Dargazanli, Caroline Arquizan, Vincent Costalat, Grégory Gascou, Pierre-Henri Lefèvre, Imad Derraz, Carlos Riquelme, Nicolas Gaillard, Isabelle Mourand, Lucas Corti, Federico Cagnazzo, Adrien ter Schiphorst; Hôpital Foch: Adrien Wang, Serge Evrard, Maya.Tchikviladze, Nadia Ajili, Bertrand Lapergue, David Weisenburger-Lile, Lucas Gorza, Géraldine Buard, Oguzhan Coskun, Arturo Consoli, Federico Di Maria, Georges Rodesh, Sergio Zimatore, Morgan Leguen, Julie Gratieux, Fernando Pico, Haja Rakotoharinandrasana, Philippe Tassan, Roxanna Poll, Sylvie Marinier; CHRU-Nancy: Benjamin Gory, Serge Bracard, René Anxionnat, Marc Braun, Anne-Laure Derelle, Romain Tonnelet, Liang Liao, François Zhu, Emmanuelle Schmitt, Sophie Planel, Sébastien Richard, Lisa Humbertjean, Gioia Mione, Jean-Christophe Lacour, Nolwenn Riou-Comte, Gérard Audibert, Marcela Voicu, Lionel Alb, Marie Reitter, Madalina Brezeanu, Agnès Masson, Adriana Tabarna, Iona Podar; CHRU Bordeaux: Gaultier Marnat, Florent Gariel, Xavier Barreau, Jérôme Berge, Louis Veunac, Patrice Menegon, Igor Sibon, Ludovic Lucas, Stéphane Olindo, Pauline Renou, Sharmila Sagnier, Mathilde Poli, Sabrina Debruxelles, François Rouanet, Thomas Tourdias, Jean-Sebastien Liegey, Pierre Briau, Nicolas Pangon; CHRU Nantes: Romain Bourcier, Lili Detraz, Benjamin Daumas-Duport, Pierre-Louis Alexandre, Monica Roy, Cédric Lenoble, Hubert Desal, Benoît Guillon, Solène de Gaalon, Cécile Preterre; Fondation Rothschild: Michel Piotin, Raphaël Blanc, Hocine Redjem, Simon Escalard, Jean-Philippe Desilles, François Delvoye, Stanislas Smajda, Benjamin Maier, Solène Hebert, Mikaël Mazighi, Mikael Obadia, Candice Sabben, Pierre Seners, Igor Raynouard, Ovide Corabianu, Thomas de Broucker, Eric Manchon, Guillaume Taylor, Malek Ben Maacha, Thion Laurie-Anne, Lecler Augustin, Savatovsjy Julien; Hôpital Kremlin-Bicêtre: Laurent Spelle, Christian Denier, Olivier Chassin, Vanessa Chalumeau, Jildaz Caroff, Olivier Chassin, Laura Venditti

Funding

This research received no specific Grant from any funding agency in the public, commercial or not-for-profit sectors.

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Contributions

CA, AtS, RP, BL, MO, and CD: carried out the study design, planned the study data collection, participated to the interpretation of data, drafted and critically revised the manuscript, and approved the final version to be published. JL made the data analysis and interpretation, critically revised the manuscript, and approved the final version to be published. BR, GB, RS, MG, SI, GB, BR, DC, SL, CA, and CV: made substantial contributions to the acquisition of the data, critically revised the manuscript, and approved the final version to be published. All authors agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Caroline Arquizan.

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None declared.

Additional information

The ETIS Registry Investigators member names are listed in Acknowledgement section.

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ter Schiphorst, A., Peres, R., Dargazanli, C. et al. Endovascular treatment of ischemic stroke due to isolated internal carotid artery occlusion: ETIS registry data analysis. J Neurol 269, 4383–4395 (2022). https://doi.org/10.1007/s00415-022-11078-y

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