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Original research
Quantification of clot spatial heterogeneity and its impact on thrombectomy
  1. Yang Liu1,
  2. Waleed Brinjikji1,2,
  3. Mehdi Abbasi1,
  4. Daying Dai1,
  5. Jorge L Arturo Larco2,
  6. Sarosh Irfan Madhani2,
  7. Adnan H Shahid2,
  8. Oana Madalina Mereuta1,
  9. Raul G Nogueira3,
  10. Peter Kvamme4,
  11. Kennith F Layton5,
  12. Josser E Delgado Almandoz6,
  13. Ricardo A Hanel7,
  14. Vitor Mendes Pereira8,
  15. Mohammed A Almekhlafi9,
  16. Albert J Yoo10,
  17. Babak S Jahromi11,
  18. Matthew J Gounis12,
  19. Biraj Patel13,
  20. Seán Fitzgerald14,
  21. Karen Doyle14,
  22. Diogo C Haussen3,
  23. Alhamza R Al-Bayati3,
  24. Mahmoud Mohammaden3,
  25. Leonardo Pisani3,
  26. Gabriel Martins Rodrigues3,
  27. Ike C Thacker5,
  28. Yasha Kayan6,
  29. Alexander Copelan6,
  30. Amin Aghaebrahim7,
  31. Eric Sauvageau7,
  32. Andrew M Demchuk9,
  33. Parita Bhuva10,
  34. Jazba Soomro10,
  35. Pouya Nazari11,
  36. Donald Robert Cantrell11,
  37. Ajit S Puri12,
  38. John Entwistle13,
  39. Ramanathan Kadirvel1,
  40. Harry J Cloft1,2,
  41. David F Kallmes1,2,
  42. Luis Savastano1,2
  1. 1 Radiology, Mayo Clinic, Rochester, Minnesota, USA
  2. 2 Neurosurgery, Mayo Clinic, Rochester, Minnesota, USA
  3. 3 Neurology, Emory University School of Medicine, Atlanta, Georgia, USA
  4. 4 Radiology, University of Tennessee Medical Center, Knoxville, Tennessee, USA
  5. 5 NeuroInterventional Radiology, Baylor University Medical Center, Dallas, Texas, USA
  6. 6 NeuroInterventional Radiology, Abbot Northwestern Hospital, Minneapolis, Minnesota, USA
  7. 7 Neurosurgery, Baptist Medical Center, Jacksonville, Florida, USA
  8. 8 Division of Neuroradiology, Department of Medical Imaging and Division of Neurosurgery, Department of Surgery, University Health Network - Toronto Western Hospital, Toronto, Ontario, Canada
  9. 9 Departments of Clinical Neurosciences, Radiology, and Community Health Sciences, Hotchkiss Brain Institute and Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
  10. 10 Neurointervention, Texas Stroke Institute, Plano, Texas, USA
  11. 11 Radiology and Neurosurgery, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
  12. 12 Radiology, New England Center for Stroke Research, University of Massachusetts Medical School, Worcester, Massachusetts, USA
  13. 13 Radiology and Neurosurgery, Carilion Clinic, Roanoke, Virginia, USA
  14. 14 Department of Physiology and CURAM-SFI Centre for Research in Medical Devices, National University of Ireland Galway, Galway, Ireland
  1. Correspondence to Dr Yang Liu, Radiology, Mayo Clinic, Rochester, Minnesota, USA; yliume{at}umich.edu

Abstract

Background Compositional and structural features of retrieved clots by thrombectomy can provide insight into improving the endovascular treatment of ischemic stroke. Currently, histological analysis is limited to quantification of compositions and qualitative description of the clot structure. We hypothesized that heterogeneous clots would be prone to poorer recanalization rates and performed a quantitative analysis to test this hypothesis.

Methods We collected and did histology on clots retrieved by mechanical thrombectomy from 157 stroke cases (107 achieved first-pass effect (FPE) and 50 did not). Using an in-house algorithm, the scanned images were divided into grids (with sizes of 0.2, 0.3, 0.4, 0.5, and 0.6 mm) and the extent of non-uniformity of RBC distribution was computed using the proposed spatial heterogeneity index (SHI). Finally, we validated the clinical significance of clot heterogeneity using the Mann–Whitney test and an artificial neural network (ANN) model.

Results For cases with FPE, SHI values were smaller (0.033 vs 0.039 for grid size of 0.4 mm, P=0.028) compared with those without. In comparison, the clot composition was not statistically different between those two groups. From the ANN model, clot heterogeneity was the most important factor, followed by fibrin content, thrombectomy techniques, red blood cell content, clot area, platelet content, etiology, and admission of intravenous tissue plasminogen activator (IV-tPA). No statistical difference of clot heterogeneity was found for different etiologies, thrombectomy techniques, and IV-tPA administration.

Conclusions Clot heterogeneity can affect the clot response to thrombectomy devices and is associated with lower FPE. SHI can be a useful metric to quantify clot heterogeneity.

  • thrombectomy
  • stroke
  • intervention
  • technology

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Not applicable.

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Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Not applicable.

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Footnotes

  • Twitter @MadhaniSarosh, @VitorMendesPer1, @AlmekhlafiMa, @FitzSeanT, @diogohaussen, @pisanileonardo, @drnimajax, @PouyaNazari5

  • Contributors YL, WB, and LS conceived the concept and YL designed the study. YL and MA performed data analysis and interpretation. MA, DD, JLAL, OMM, and SF performed histology. All the other authors provided leading effort in collecting patient clots and procedure data within their institutions in the Stroke Thromboembolism Registry of Imaging and Pathology (STRIP). YL drafted the article. The article was critically revised by YL, WB, DFK, and LS. WB, RK, DFK, and LS provided administrative, technical, supervisory, or other support. All authors reviewed the submitted version, and YL approved it on behalf of all the authors. YL and LS are guarantors of the integrity of the entire study.

  • Funding This work was supported by the National Institutes of Health (grant number NS105853).

  • Competing interests MJG is on the editorial board of the Journal of NeuroInterventional Surgery.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.