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Association of the Careggi Collateral Score with 3-month modified Rankin Scale score after thrombectomy for stroke with occlusion of the middle cerebral artery

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A Correction to this article was published on 24 December 2021

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Abstract

Background

The Careggi Collateral Score (CCS) (qualitative–quantitative evaluation) was developed from a single-centre cohort as an angiographic score to describe both the extension and effectiveness of the pial collateral circulation in stroke patients with occlusion of the anterior circulation. We aimed to examine the association between CCS (quantitative evaluation) and 3-month modified Rankin Scale (mRS) score in a large multi-center cohort of patients receiving thrombectomy for stroke with occlusion of middle cerebral artery (MCA).

Methods

We conducted a study on prospectively collected data from 1284 patients enrolled in the Italian Registry of Endovascular Treatment in Acute Stroke. According to the extension of the retrograde reperfusion in the cortical anterior cerebral artery (ACA)-MCA territories, CCS ranges from 0 (absence of retrograde filling) to 4 (visualization of collaterals until the alar segment of the MCA).

Results

Using CCS of 4 as reference, CCS grades were associated in the direction of unfavourable outcome on 3-month mRS shift (0 to 6); significant difference was found between CCS of 0 and CCS of 1 and between CCS of 3 and CCS of 4. CCS ≥ 3 was the optimal cut-off for predicting 3-month excellent outcome, while CCS ≥ 1 was the optimal cut-off for predicting 3-month survival. CCS of 0 and CCS < 3 were associated in the direction of unfavourable recanalization on TICI shift (0 to 3) compared with CCS ≥ 1 and CCS ≥ 3, respectively. Compared with CCS ≥ 3 as reference, CCS of 0 and CCS 1 to 2 were associated in the direction of unfavourable recanalization on TICI shift. There was no evidence of heterogeneity of effects of successful recanalization and procedure time ≤ 60 min on 3-month mRS shift across CCS categories.

Conclusion

The CCS could provide a future advantage for improving the prognosis in patients receiving thrombectomy for stroke with M1 or M1–M2 segment of the MCA occlusion.

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References

  1. Liebeskind DS (2003) Collateral circulation. Stroke 34:2279–2284

    Article  Google Scholar 

  2. Lima FO, Furie KL, Silva GS et al (2010) The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke 41:2316–2322

    Article  Google Scholar 

  3. Maas MB, Lev MH, Ay H et al (2009) Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke 40:3001–3005

    Article  Google Scholar 

  4. Menon BK, O’Brien B, Bivard A et al (2013) Assessment of leptomeningeal collaterals using dynamic CT angiography in patients with acute ischemic stroke. J Cereb Blood Flow Metab 33:365–371

    Article  Google Scholar 

  5. Menon BK, Smith EE, Modi J et al (2011) Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol 32:1640–1645

    Article  CAS  Google Scholar 

  6. Berkhemer OA, Jansen IG, Beumer D et al (2016) Collateral status on baseline computed tomographic angiography and intra-arterial treatment effect in patients with proximal anterior circulation stroke. Stroke 47:768–776

    Article  CAS  Google Scholar 

  7. Boers AM, Jansen IG, Berkhemer OA et al (2017) Collateral status and tissue outcome after intra-arterial therapy for patients with acute ischemic stroke. J Cereb Blood Flow Metab 37:3589–3598

    Article  Google Scholar 

  8. Menon BK, Qazi E, Nambiar V et al (2015) Differential effect of baseline computer tomographic angiography collaterals on clinical outcome in patients enrolled in the interventional management of stroke III trial. Stroke 46:1239–1244

    Article  Google Scholar 

  9. Jansen IG, Mulder MJ, Goldhoorn RJB et al (2019) Impact of single phase CT angiography collateral status on functional outcome over time: results from the MR CLEAN Registry. J Neurointerv Surg 11:866–873

    Article  Google Scholar 

  10. Gensicke H, Al-Ajlan F, Campbell B et al (2017) Comparing the impact of baseline collateral status assessed by different collateral scores and different imaging modalities on outcomes in acute ischemic patients: a meta-analysis from the HERMES collaboration. In: 3rd Eur Stroke Organ Conf 16–18th May 2017

  11. Higashida RT, Furlan AJ, Roberts H et al (2003) Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke 34:e109–e137

    Article  Google Scholar 

  12. Singer OC, Berkefeld J, Nolte CH et al (2015) Collateral vessels in proximal middle cerebral artery occlusion: the ENDOSTROKE study. Radiology 274:851–858

    Article  Google Scholar 

  13. Anadani M, Finitsis S, Clarençon F et al (2021) Collateral status reperfusion and outcomes after endovascular therapy: insight from the Endovascular Treatment in Ischemic Stroke (ETIS) Registry. J Neurointerv Surg. https://doi.org/10.1136/neurintsurg-2021-017553

    Article  PubMed  PubMed Central  Google Scholar 

  14. Mangiafico S, Consoli A, Renieri L et al (2013) Semi-quantitative and qualitative evaluation of pial leptomeningeal collateral circulation in acute ischemic stroke of the anterior circulation: the Careggi Collateral Score. Ital J Anat Embryol 118:277–287

    PubMed  Google Scholar 

  15. Mangiafico M, Saia V, Nencini P et al (2014) Effect of the interaction between recanalization and collateral circulation on functional outcome in acute ischaemic stroke. Interv Neuroradiol 20:704–714

    Article  Google Scholar 

  16. Consoli A, Andersson T, Holmberg A et al (2016) CT perfusion and angiographic assessment of pial collateral reperfusion in acute ischemic stroke: the CAPRI study. J Neurointerv Surg 8:1211–1216

    Article  Google Scholar 

  17. Bang OY, Goyal M, Liebeskind DS (2015) Collateral circulation in ischemic stroke: assessment tools and therapeutic strategies. Stroke 46:3302–3309

    Article  Google Scholar 

  18. Vagal A, Aviv R, Sucharew H et al (2018) Collateral clock is more important than time clock for tissue fate. Stroke 49:2102–2107

    Article  Google Scholar 

Download references

Acknowledgements

We thank all patients and persons who participated in IRETAS.

Funding

“The project ‘‘Registro Nazionale Trattamento Ictus Acuto’’ (RFPS-2006-1-336562) was funded by Grants from the Italian Ministry of Health within the framework of 2006 Finalized Research Programmes (D.Lgs.n.502/1992).

Author information

Author notes

  1. Danilo Toni and Salvatore Mangiafico are equally contributing senior authors.

Authors and Affiliations

  1. Stroke Unit, DAI di Neuroscienze, Azienda Ospedaliera Universitaria Integrata, Piazzale A. Stefani 1, 37126, Verona, Italy

    Manuel Cappellari & Cecilia Zivelonghi

  2. Neurology and Stroke Unit, S. Corona Hospital, Pietra Ligure, Italy

    Valentina Saia

  3. Department of NEUROFARBA, Neuroscience Section, University of Florence, Florence, Italy

    Giovanni Pracucci & Domenico Inzitari

  4. Dipartimento di Scienze Biomediche, Sperimentali e Cliniche, Neuroradiologia, Università degli Studi di Firenze, Ospedale Universitario Careggi, Firenze, Italy

    Fainardi Enrico

  5. Service de Neuroradiologie Diagnostique et Thérapeutique Hôpital Foch, Suresnes, France

    Arturo Consoli

  6. Interventional Neurovascular Unit, Careggi University Hospital, Florence, Italy

    Arturo Consoli, Sergio Nappini & Salvatore Mangiafico

  7. Department of Neuroradiology, IRCCS Ospedale Policlinico San Martino, Genoa, Italy

    Lucio Castellan

  8. Unit of Neuroimaging and Neurointervention, University Hospital of Siena, Siena, Italy

    Sandra Bracco

  9. Interventional Neuroradiology Unit, Città della Salute e della Scienza-Molinette, Turin, Italy

    Mauro Bergui

  10. Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy

    Mirco Cosottini

  11. Diagnostic and Interventional Neuroradiology Unit-“SS. Annunziata” Hospital, Taranto, Italy

    Alessandra Briatico Vangosa

  12. UOC Neuroradiology, Department of Biomedical Sciences and of Morphologic and Functional Images, University of Messina, Messina, Italy

    Sergio Vinci

  13. Department of Neuroradiology, AUSL Romagna, M. Bufalini Hospital, Cesena, Italy

    Maria Ruggiero

  14. Vascular and Interventional Radiology Unit, Ospedale Civile Mazzini, Teramo, Italy

    Edoardo Puglielli

  15. UOS Neuroradiologia Interventistica, AOU Consorziale Policlinico, Bari, Italy

    Luigi Chiumarulo

  16. Department of Diagnostic Imaging and Interventional Radiology, Neuroradiology, Padua University Hospital, Padua, Italy

    Giacomo Cester

  17. Interventional Neuroradiology Unit, San Giovanni Bosco Hospital, Turin, Italy

    Chiara Comelli

  18. Interventional Neuroradiology Unit, Azienda Ospedaliera Annunziata, Cosenza, Italy

    Umberto Silvagni

  19. Department of Diagnostic Imaging and Interventional Radiology, University of Rome Tor Vergata, Rome, Italy

    Daniele Morosetti

  20. Department of Neuroradiology, S. Corona Hospital, Pietra Ligure, Italy

    Valentina Caldiera

  21. Neuroradiology Unit, Ospedale dell’Angelo, USSL3 Serenissima, Mestre, Italy

    Nicola Cavasin

  22. Vascular and Interventional Neuroradiology Department, Azienda Ospedaliera G. Brotzu, Cagliari, Italy

    Valeria Ledda

  23. Radiologia e Neuroradiologia Diagnostica e Interventistica, IRCCS Policlinico San Matteo, Pavia, Italy

    Giuseppina Sanfilippo

  24. Interventional Neuroradiology Unit, University Hospital Arcispedale S. Anna, Ferrara, Italy

    Andrea Saletti

  25. Neuroradiology Unit, Presidio Ospedaliero SS. Filippo e Nicola, Avezzano, Italy

    Pietro Filauri

  26. Neuroradiological Unit, Department of Radiology, Azienda Ospedaliera “SS Antonio e Biagio e C. Arrigo”, Alessandria, Italy

    Ivan Gallesio

  27. Humanitas Clinical and Research Center-IRCCS, Rozzano, MI, Italy

    Nunzio Paolo Nuzzi

  28. Neuroradiology Unit, Ospedale S. Maria Misericordia, Rovigo, Italy

    Pitero Amistá

  29. Neuroradiology Unit, Azienda Ospedaliera Universitaria Integrata, Verona, Italy

    Mauro Plebani

  30. Neuroradiology Unit, Fondazione Poliambulanza, Brescia, Italy

    Marco Pavia

  31. UOC Neuroradiologia, AUO S. Giovanni di Dio e Ruggi D’Aragona, Salerno, Italy

    Daniele Romano

  32. Department of Human Neurosciences, Interventional Neuroradiology, Università degli Studi di Roma Sapienza, Rome, Italy

    Francesco Biraschi

  33. Neuroradiology Unit, Ospedale Universitario, Parma, Italy

    Roberto Menozzi

  34. Neuroradiology Unit, Spedali Civili, Brescia, Italy

    Roberto Gasparotti

  35. Neuroradiology Department, Ospedale di Circolo-ASST Sette Laghi, Varese, Italy

    Andrea Giorgianni

  36. Department of Neurology and Stroke Center, IRCCS Istituto delle Scienze Neurologiche di Bologna, Maggiore Hospital, Bologna, Italy

    Andrea Zini

  37. Emergency Department Stroke Unit, Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy

    Danilo Toni

Authors
  1. Manuel Cappellari
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  2. Valentina Saia
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  3. Giovanni Pracucci
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  4. Fainardi Enrico
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  5. Arturo Consoli
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  6. Sergio Nappini
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  7. Lucio Castellan
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  8. Sandra Bracco
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  9. Mauro Bergui
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  10. Mirco Cosottini
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  11. Alessandra Briatico Vangosa
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  13. Maria Ruggiero
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  14. Edoardo Puglielli
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  15. Luigi Chiumarulo
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  16. Giacomo Cester
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  18. Umberto Silvagni
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  19. Daniele Morosetti
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  20. Valentina Caldiera
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  21. Nicola Cavasin
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  22. Valeria Ledda
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  23. Giuseppina Sanfilippo
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  24. Andrea Saletti
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  26. Ivan Gallesio
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  27. Nunzio Paolo Nuzzi
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  29. Cecilia Zivelonghi
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  30. Mauro Plebani
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  31. Marco Pavia
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  32. Daniele Romano
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  33. Francesco Biraschi
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  34. Roberto Menozzi
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  35. Roberto Gasparotti
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  36. Andrea Giorgianni
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  37. Andrea Zini
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  38. Domenico Inzitari
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  39. Danilo Toni
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  40. Salvatore Mangiafico
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Consortia

The IRETAS Group

Contributions

MC: design and conceptualization of the study, acquisition of data, analysis and interpretation of the data, and drafting the manuscript for intellectual content. All authors: acquisition of data and revising the manuscript for intellectual content.

Corresponding author

Correspondence to Manuel Cappellari.

Ethics declarations

Conflicts of interest

Manuel Cappellari received consulting fees from Boehringer-Ingelheim and Pfizer-BMS, and advisory board from Daiichi Sankyo. Mauro Bergui received consulting fees from Penumbra Inc. Stryker Italia. Giacomo Cester declared to have speaker honoraria with Penumbra Inc. Andrea Saletti received consulting fees from Stryker. Nunzio Paolo Nuzzi received consulting fees from Penumbra Inc. Acandis GmbH. Daniele Romano received consulting fees from Penumbra Inc. Andrea Zini received speaker fees from Ceronovus and consulting fees from Boehringer-Ingelheim. Danilo Toni declared to have speaker honoraria and advisory board relationship with Abbott, Bayer, Boehringer Ingelheim, Daiichi Sankyo, Medtronic, and Pfizer. Salvatore Mangiafico received consulting fees from Cerenovus. The other authors report no disclosures.

Ethical approval

The present study was in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Need for ethical approval or patient consent for participation in the IRETAS varied among participating hospitals.

Informed consent

Informed consent to use of anonymized and aggregated data for participation in the IRETAS was obtained in all patients of each center.

Additional information

Group members are present in the supplementary material for “The IRETAS Group”.

Supplementary Information

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Supplementary file1 (DOCX 2489 KB)

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Cappellari, M., Saia, V., Pracucci, G. et al. Association of the Careggi Collateral Score with 3-month modified Rankin Scale score after thrombectomy for stroke with occlusion of the middle cerebral artery. J Neurol 269, 1013–1023 (2022). https://doi.org/10.1007/s00415-021-10898-8

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  • DOI: https://doi.org/10.1007/s00415-021-10898-8

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