Thrombus Permeability Is Associated With Improved Functional Outcome and Recanalization in Patients With Ischemic Stroke

Author:

Santos Emilie M.M.1,Marquering Henk A.1,den Blanken Mark D.1,Berkhemer Olvert A.1,Boers Anna M.M.1,Yoo Albert J.1,Beenen Ludo F.1,Treurniet Kilian M.1,Wismans Carrie1,van Noort Kim1,Lingsma Hester F.1,Dippel Diederik W.J.1,van der Lugt Aad1,van Zwam Wim H.1,Roos Yvo B.W.E.M.1,van Oostenbrugge Robert J.1,Niessen Wiro J.1,Majoie Charles B.1,Fransen Puck S.S.2,Beumer Debbie3,van den Berg Lucie A.4,Schonewille Wouter J.5,Vos Jan Albert6,Nederkoorn Paul J.4,Wermer Marieke J.H.7,van Walderveen Marianne A.A.8,Staals Julie9,Hofmeijer Jeannette10,van Oostayen Jacques A.11,Lycklama à Nijeholt Geert J.12,Boiten Jelis13,Brouwer Patrick A.14,Emmer Bart J.14,de Bruijn Sebastiaan F.15,van Dijk Lukas C.16,Kappelle L. Jaap17,Lo Rob H.18,van Dijk Ewoud J.19,de Vries Joost20,de Kort Paul L.M.21,van den Berg Jan S.P.22,van Hasselt Boudewijn A.A.M.23,Aerden Leo A.M.24,Dallinga René J.25,Visser Marieke C.26,Bot Joseph C.J.27,Vroomen Patrick C.28,Eshghi Omid29,Schreuder Tobien H.C.M.L.30,Heijboer Roel J.J.31,Keizer Koos32,Tielbeek Alexander V.33,den Hertog Heleen M.34,Gerrits Dick G.35,van den Berg-Vos Renske M.36,Karas Giorgos B.37,Sprengers Marieke E.S.38,Jenniskens Sjoerd F.M.39,van den Berg René38,Koudstaal Peter J.40,Boiten Jelis19,van Dijk Ewoud J.19,Wermer Marieke J.H.7,Flach H. Zwenneke23,Steyerberg Ewout W.41,Brown Martin M.42,Liebig Thomas43,Stijnen Theo44,Andersson Tommy45,Mattle Heinrich P.46,Wahlgren Nils47,Koudstaal Peter J.40,van der Heijden Esther40,Ghannouti Naziha40,Fleitour Nadine4,Hooijenga Imke4,Lindl-Velema Annemieke9,Puppels Corina5,Pellikaan Wilma5,Janssen Kirsten7,Aaldering Nicole10,Elfrink Marjan10,de Meris Joke13,Geerlings Annet19,van Vemde Gina22,de Ridder Ans17,Greebe Paut17,de Bont-Stikkelbroeck José21,Struijk Willy15,Simons Tiny30,Messchendorp Gert28,van der Minne Friedus28,Bongenaar Hester32,Bodde Karin26,Licher Silvan40,Boodt Nikki40,Ros Adriaan40,Venema Esmee40,Slokkers Ilse40,Ganpat Raymie-Jayce40,Mulder Maxim40,Saiedie Nawid40,Heshmatollah Alis40,Schipperen Stefanie40,Vinken Stefan40,van Boxtel Tiemen40,Koets Jeroen40,Boers Merel48,Borst Jordi38,Jansen Ivo38,Kappelhof Manon38,Lucas Marit48,Geuskens Ralph48,Barros Renan Sales48,Dobbe Roeland48,Csizmadia Marloes48,

Affiliation:

1. From the Departments of Radiology (E.M.M.S., H.A.M., O.A.B., A.M.M.B., L.F.B., K.M.T., C.W., K.N., C.B.M.), Biomedical Engineering and Physics (E.M.M.S., H.A.M., M.D.B., A.M.M.B.), and Neurology (Y.B.W.E.M.R.), Academic Medical Center, Amsterdam, The Netherlands; Departments of Radiology (E.M.M.S., A.L., W.J.N.), Medical Informatics (E.M.M.S., W.J.N.), Neurology (O.A.B., D.W.J.D.), and Public Health (H.F.L.), Erasmus MC University Medical Center, Rotterdam, The Netherlands; Department of Robotics...

2. Departments of Neurology and Radiology, Erasmus MC University Medical Center

3. Department of Neurology, Erasmus MC University Medical Center; Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht [CARIM]

4. Department of Neurology, Academic Medical Center, Amsterdam

5. Department of Neurology, Sint Antonius Hospital, Nieuwegein

6. Department of Radiology, Sint Antonius Hospital, Nieuwegein

7. Department of Neurology, Leiden University Medical Center

8. Department of Radiology, Leiden University Medical Center

9. Department of Neurology, Maastricht University Medical Center and Cardiovascular Research Institute Maastricht [CARIM]

10. Department of Neurology, Rijnstate Hospital, Arnhem

11. Department of Radiology, Rijnstate Hospital, Arnhem

12. Department of Radiology, MC Haaglanden, The Hague

13. Department of Neurology, MC Haaglanden, The Hague

14. Department of Radiology, Erasmus MC University Medical Center

15. Department of Neurology, HAGA Hospital, The Hague

16. Department of Radiology, HAGA Hospital, The Hague

17. Department of Neurology, University Medical Center Utrecht

18. Department of Radiology, University Medical Center Utrecht

19. Department of Neurology, Radboud University Medical Center, Nijmegen

20. Department of Neurosurgery, Radboud University Medical Center, Nijmegen

21. Department of Neurology, Sint Elisabeth Hospital, Tilburg

22. Department of Neurology, Isala Klinieken, Zwolle

23. Department of Radiology, Isala Klinieken, Zwolle

24. Department of Neurology, Reinier de Graaf Gasthuis, Delft

25. Department of Radiology, Reinier de Graaf Gasthuis, Delft

26. Department of Neurology, VU Medical Center, Amsterdam

27. Department of Radiology, VU Medical Center, Amsterdam

28. Department of Neurology, University Medical Center Groningen, The Netherlands

29. Department of Radiology, University Medical Center Groningen, The Netherlands

30. Department of Neurology, Atrium Medical Center, Heerlen

31. Department of Radiology, Atrium Medical Center, Heerlen

32. Department of Neurology, Catharina Hospital, Eindhoven

33. Department of Radiology, Catharina Hospital, Eindhoven

34. Department of Neurology, Medical Spectrum Twente, Enschede

35. Department of Radiology, Medical Spectrum Twente, Enschede

36. Department of Neurology, Sint Lucas Andreas Hospital, Amsterdam, The Netherlands

37. Department of Radiology, Sint Lucas Andreas Hospital, Amsterdam, The Netherlands

38. Department of Radiology, Academic Medical Center, Amsterdam

39. Department of Radiology, Radboud University Medical Center, Nijmegen

40. Department of Neurology, Erasmus MC University Medical Center

41. Department of Public Health, Erasmus MC University Medical Center

42. UCL Institute of Neurology, National Hospital for Neurology and Neurosurgery, London, United Kingdom

43. Med. Fakultät, Uniklinik Köln, Germany

44. Department of Medical Statistics and Bioinformatics, Leiden University Medical Center

45. Department of Radiology, Karolinska Univeristy Hospital, Stockholm, Sweden

46. Department of Neurology, University Hospital of Bern, Switzerland

47. Department of Neurology, Karolinska Univeristy Hospital, Stockholm, Sweden

48. Department of Biomedical Engineering and Physics, Academic Medical Center, Amsterdam

Abstract

Background and Purpose— Preclinical studies showed that thrombi can be permeable and may, therefore, allow for residual blood flow in occluded arteries of patients having acute ischemic stroke. This perviousness may increase tissue oxygenation, improve thrombus dissolution, and augment intra-arterial treatment success. We hypothesize that the combination of computed tomographic angiography and noncontrast computed tomography imaging allows measurement of contrast agent penetrating a permeable thrombus, and it is associated with improved outcome. Methods— Thrombus and contralateral artery attenuations in noncontrast computed tomography and computed tomographic angiography images were measured in 184 Multicenter Randomized Clinical trial of Endovascular treatment of acute ischemic stroke in the Netherlands (MR CLEAN) patients with thin-slice images. Two quantitative estimators of the thrombus permeability were introduced: computed tomographic angiography attenuation increase (Δ) and thrombus void fraction (ε). Patients were dichotomized as having a pervious or impervious thrombus and associated with outcome, recanalization, and final infarct volume. Results— Patients with Δ≥10.9 HU (n=81 [44%]) and ε≥6.5% (n=77 [42%]) were classified as having a pervious thrombus. These patients were 3.2 (95% confidence interval, 1.7–6.4) times more likely to have a favorable outcome, and 2.5 (95% confidence interval, 1.3–4.8) times more likely to recanalyze, for Δ based classification, and similarly for ε. These odds ratios were independent from intravenous or intra-arterial treatment. Final infarct volume was negatively correlated with both perviousness estimates (correlation coefficient, −0.39 for Δ and −0.40 for ε). Conclusions— This study shows that simultaneous measurement of thrombus attenuation in noncontrast computed tomography and computed tomographic angiography allows for quantification of thrombus perviousness. Thrombus perviousness is strongly associated with improved functional outcome, smaller final infarct volume, and higher recanalization rate.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Advanced and Specialised Nursing,Cardiology and Cardiovascular Medicine,Clinical Neurology

Reference28 articles.

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