Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke

Nikki Boodt; Philip R.W. Snouckaert Van Schauburg; Hajo M. Hund; Behrooz Fereidoonnezhad; J. Patrick McGarry; Ali C. Akyildiz; Adriaan C.G.M. Van Es; Simon F. De Meyer; Diederik W.J. Dippel; Hester F. Lingsma; Heleen M.M. Van Beusekom; Aad Van Der Lugt; Frank J.H. Gijsen

doi:10.1161/STROKEAHA.120.033527

Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke

Nikki Boodt^*, Philip R.W. Snouckaert Van Schauburg, Hajo M. Hund, Behrooz Fereidoonnezhad, J. Patrick McGarry, Ali C. Akyildiz, Adriaan C.G.M. Van Es, Simon F. De Meyer, Diederik W.J. Dippel, Hester F. Lingsma, Heleen M.M. Van Beusekom, Aad Van Der Lugt, Frank J.H. Gijsen

^*Corresponding author for this work

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Abstract

Background and Purpose: Mechanical properties of thromboemboli play an important role in the efficacy of endovascular thrombectomy (EVT) for acute ischemic stroke. However, very limited data on mechanical properties of human stroke thrombi are available. We aimed to mechanically characterize thrombi retrieved with EVT, and to assess the relationship between thrombus composition and thrombus stiffness. Methods: Forty-one thrombi from 19 patients with acute stroke who underwent EVT between July and October 2019 were mechanically analyzed, directly after EVT. We performed unconfined compression experiments and determined tangent modulus at 75% strain (E^t75) as a measure for thrombus stiffness. Thrombi were histologically analyzed for fibrin/platelets, erythrocytes, leukocytes, and platelets, and we assessed the relationship between histological components and E^t75with univariable and multivariable linear mixed regression. Results: Median E^t75was 560 (interquartile range, 393-1161) kPa. In the multivariable analysis, fibrin/platelets were associated with increased E^t75(aβ, 9 [95% CI, 5 to 13]) kPa, erythrocytes were associated with decreased E^t75%(aβ,-9 [95% CI,-5 to-13]) kPa. We found no association between leukocytes and E^t75. High platelet values were strongly associated with increased E^t75(aβ, 56 [95% CI, 38-73]). Conclusions: Fibrin/platelet content of thrombi retrieved with EVT for acute ischemic stroke is strongly associated with increased thrombus stiffness. For thrombi with high platelet values, there was a very strong relationship with thrombus stiffness. Our data provide a basis for future research on the development of next-generation EVT devices tailored to thrombus composition.

Original language	English
Pages (from-to)	2510-2517
Number of pages	8
Journal	Stroke
Volume	52
Issue number	8
DOIs	https://doi.org/10.1161/STROKEAHA.120.033527
Publication status	Published - Aug 2021

Bibliographical note

Sources of Funding: This study was funded and carried out by the Erasmus MC, University Medical Center Rotterdam. The study has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 777072 (INSIST [IN-Silico trials for treatment of acute Ischemic Stroke]), which played no role in study design and patient enrollment, nor in data collection, analy-sis, or writing of the article.

Publisher Copyright: © 2021 Lippincott Williams and Wilkins. All rights reserved.

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STROKEAHA.120.033527Licence: CC BY-NC-ND

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Boodt, N., Snouckaert Van Schauburg, P. R. W., Hund, H. M., Fereidoonnezhad, B., McGarry, J. P., Akyildiz, A. C., Van Es, A. C. G. M., De Meyer, S. F., Dippel, D. W. J., Lingsma, H. F., Van Beusekom, H. M. M., Van Der Lugt, A., & Gijsen, F. J. H. (2021). Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke. Stroke, 52(8), 2510-2517. https://doi.org/10.1161/STROKEAHA.120.033527

@article{572eca5101504e4b8275e7beb5b6f87a,

title = "Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke",

abstract = "Background and Purpose: Mechanical properties of thromboemboli play an important role in the efficacy of endovascular thrombectomy (EVT) for acute ischemic stroke. However, very limited data on mechanical properties of human stroke thrombi are available. We aimed to mechanically characterize thrombi retrieved with EVT, and to assess the relationship between thrombus composition and thrombus stiffness. Methods: Forty-one thrombi from 19 patients with acute stroke who underwent EVT between July and October 2019 were mechanically analyzed, directly after EVT. We performed unconfined compression experiments and determined tangent modulus at 75% strain (Et75) as a measure for thrombus stiffness. Thrombi were histologically analyzed for fibrin/platelets, erythrocytes, leukocytes, and platelets, and we assessed the relationship between histological components and Et75with univariable and multivariable linear mixed regression. Results: Median Et75was 560 (interquartile range, 393-1161) kPa. In the multivariable analysis, fibrin/platelets were associated with increased Et75(aβ, 9 [95% CI, 5 to 13]) kPa, erythrocytes were associated with decreased Et75%(aβ,-9 [95% CI,-5 to-13]) kPa. We found no association between leukocytes and Et75. High platelet values were strongly associated with increased Et75(aβ, 56 [95% CI, 38-73]). Conclusions: Fibrin/platelet content of thrombi retrieved with EVT for acute ischemic stroke is strongly associated with increased thrombus stiffness. For thrombi with high platelet values, there was a very strong relationship with thrombus stiffness. Our data provide a basis for future research on the development of next-generation EVT devices tailored to thrombus composition.",

author = "Nikki Boodt and {Snouckaert Van Schauburg}, {Philip R.W.} and Hund, {Hajo M.} and Behrooz Fereidoonnezhad and McGarry, {J. Patrick} and Akyildiz, {Ali C.} and {Van Es}, {Adriaan C.G.M.} and {De Meyer}, {Simon F.} and Dippel, {Diederik W.J.} and Lingsma, {Hester F.} and {Van Beusekom}, {Heleen M.M.} and {Van Der Lugt}, Aad and Gijsen, {Frank J.H.}",

note = "Sources of Funding: This study was funded and carried out by the Erasmus MC, University Medical Center Rotterdam. The study has received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under grant agreement No. 777072 (INSIST [IN-Silico trials for treatment of acute Ischemic Stroke]), which played no role in study design and patient enrollment, nor in data collection, analy-sis, or writing of the article. Publisher Copyright: {\textcopyright} 2021 Lippincott Williams and Wilkins. All rights reserved.",

year = "2021",

month = aug,

doi = "10.1161/STROKEAHA.120.033527",

language = "English",

volume = "52",

pages = "2510--2517",

journal = "Stroke",

issn = "0039-2499",

publisher = "Wolters Kluwer Health",

number = "8",

}

Boodt, N, Snouckaert Van Schauburg, PRW, Hund, HM, Fereidoonnezhad, B, McGarry, JP, Akyildiz, AC, Van Es, ACGM, De Meyer, SF, Dippel, DWJ , Lingsma, HF , Van Beusekom, HMM , Van Der Lugt, A & Gijsen, FJH 2021, 'Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke', Stroke, vol. 52, no. 8, pp. 2510-2517. https://doi.org/10.1161/STROKEAHA.120.033527

TY - JOUR

T1 - Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke

AU - Boodt, Nikki

AU - Snouckaert Van Schauburg, Philip R.W.

AU - Hund, Hajo M.

AU - Fereidoonnezhad, Behrooz

AU - McGarry, J. Patrick

AU - Akyildiz, Ali C.

AU - Van Es, Adriaan C.G.M.

AU - De Meyer, Simon F.

AU - Dippel, Diederik W.J.

AU - Lingsma, Hester F.

AU - Van Beusekom, Heleen M.M.

AU - Van Der Lugt, Aad

AU - Gijsen, Frank J.H.

N1 - Sources of Funding: This study was funded and carried out by the Erasmus MC, University Medical Center Rotterdam. The study has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 777072 (INSIST [IN-Silico trials for treatment of acute Ischemic Stroke]), which played no role in study design and patient enrollment, nor in data collection, analy-sis, or writing of the article. Publisher Copyright: © 2021 Lippincott Williams and Wilkins. All rights reserved.

PY - 2021/8

Y1 - 2021/8

N2 - Background and Purpose: Mechanical properties of thromboemboli play an important role in the efficacy of endovascular thrombectomy (EVT) for acute ischemic stroke. However, very limited data on mechanical properties of human stroke thrombi are available. We aimed to mechanically characterize thrombi retrieved with EVT, and to assess the relationship between thrombus composition and thrombus stiffness. Methods: Forty-one thrombi from 19 patients with acute stroke who underwent EVT between July and October 2019 were mechanically analyzed, directly after EVT. We performed unconfined compression experiments and determined tangent modulus at 75% strain (Et75) as a measure for thrombus stiffness. Thrombi were histologically analyzed for fibrin/platelets, erythrocytes, leukocytes, and platelets, and we assessed the relationship between histological components and Et75with univariable and multivariable linear mixed regression. Results: Median Et75was 560 (interquartile range, 393-1161) kPa. In the multivariable analysis, fibrin/platelets were associated with increased Et75(aβ, 9 [95% CI, 5 to 13]) kPa, erythrocytes were associated with decreased Et75%(aβ,-9 [95% CI,-5 to-13]) kPa. We found no association between leukocytes and Et75. High platelet values were strongly associated with increased Et75(aβ, 56 [95% CI, 38-73]). Conclusions: Fibrin/platelet content of thrombi retrieved with EVT for acute ischemic stroke is strongly associated with increased thrombus stiffness. For thrombi with high platelet values, there was a very strong relationship with thrombus stiffness. Our data provide a basis for future research on the development of next-generation EVT devices tailored to thrombus composition.

AB - Background and Purpose: Mechanical properties of thromboemboli play an important role in the efficacy of endovascular thrombectomy (EVT) for acute ischemic stroke. However, very limited data on mechanical properties of human stroke thrombi are available. We aimed to mechanically characterize thrombi retrieved with EVT, and to assess the relationship between thrombus composition and thrombus stiffness. Methods: Forty-one thrombi from 19 patients with acute stroke who underwent EVT between July and October 2019 were mechanically analyzed, directly after EVT. We performed unconfined compression experiments and determined tangent modulus at 75% strain (Et75) as a measure for thrombus stiffness. Thrombi were histologically analyzed for fibrin/platelets, erythrocytes, leukocytes, and platelets, and we assessed the relationship between histological components and Et75with univariable and multivariable linear mixed regression. Results: Median Et75was 560 (interquartile range, 393-1161) kPa. In the multivariable analysis, fibrin/platelets were associated with increased Et75(aβ, 9 [95% CI, 5 to 13]) kPa, erythrocytes were associated with decreased Et75%(aβ,-9 [95% CI,-5 to-13]) kPa. We found no association between leukocytes and Et75. High platelet values were strongly associated with increased Et75(aβ, 56 [95% CI, 38-73]). Conclusions: Fibrin/platelet content of thrombi retrieved with EVT for acute ischemic stroke is strongly associated with increased thrombus stiffness. For thrombi with high platelet values, there was a very strong relationship with thrombus stiffness. Our data provide a basis for future research on the development of next-generation EVT devices tailored to thrombus composition.

UR - http://www.scopus.com/inward/record.url?scp=85110686008&partnerID=8YFLogxK

U2 - 10.1161/STROKEAHA.120.033527

DO - 10.1161/STROKEAHA.120.033527

M3 - Article

C2 - 34078112

AN - SCOPUS:85110686008

SN - 0039-2499

VL - 52

SP - 2510

EP - 2517

JO - Stroke

JF - Stroke

IS - 8

ER -

Mechanical Characterization of Thrombi Retrieved with Endovascular Thrombectomy in Patients with Acute Ischemic Stroke

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