Neurointervention.  2024 Jul;19(2):65-73. 10.5469/neuroint.2024.00087.

Traditional Thrombus Composition and Related Endovascular Outcomes: Catching up with the Recent Evidence

Affiliations
  • 1Department of Neurology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea

Abstract

Endovascular thrombectomy is the primary treatment for acute intracranial vessel occlusion and significantly improves recanalization success rate. However, achieving optimal recanalization remains a challenge. The histopathological components of thrombus composition play a crucial role in determining endovascular outcomes. This review aimed to consolidate the recent evidence on the impact of thrombus composition on mechanical properties and endovascular outcomes. The relationship between thrombus composition and mechanical properties was significant, with fibrin and/or platelet-rich thrombi being stiff, tough, elastic, and less deformable; fibrin-rich thrombi were sticky and had higher friction with the vessel wall. Erythrocyte composition was positively associated with successful recanalization, whereas lower platelet composition was associated with specific outcomes, such as the first-pass effect and complete recanalization. The number of thrombectomy device passes was possibly related to erythrocyte, platelet, and fibrin composition, with a smaller number of passes associated with erythrocyte-rich thrombi. Procedural time was consistently related to thrombus composition, with shorter times observed for erythrocyte-rich thrombi. The relationship between thrombus composition and secondary embolism remains inconclusive. Understanding the role of thrombus composition in endovascular outcomes is crucial to optimize stroke treatment. Although evidence suggests a link between thrombus composition and mechanical properties, further research is needed to establish stronger correlations and to reduce study variations. Exploring non-traditional thrombus components such as leukocytes and neutrophil extracellular traps is vital. Thrombus imaging could provide a practical solution for predicting thrombus composition before endovascular procedures. This review highlights the importance of thrombus composition for enhancing endovascular stroke treatment strategies.

Keyword

Thrombus; Histology; Thrombectomy; Stroke; Outcome

Reference

1. Choi DH, Yoo CJ, Park CW, Kim MJ. Gradual expansion of stent retriever in mechanical thrombectomy for curved middle cerebral artery: structural findings of the stent for predictable recanalization results. Acta Neurochir (Wien). 2019; 161:2003–2012.
Article
2. Haussen DC, Rebello LC, Nogueira RG. Optimizating clot retrieval in acute stroke: the push and fluff technique for closed-cell stentrievers. Stroke. 2015; 46:2838–2842.
3. Madjidyar J, Hermes J, Freitag-Wolf S, Jansen O. Stent-thrombus interaction and the influence of aspiration on mechanical thrombectomy: evaluation of different stent retrievers in a circulation model. Neuroradiology. 2015; 57:791–797.
4. van der Marel K, Chueh JY, Brooks OW, King RM, Marosfoi MG, Langan ET, et al. Quantitative assessment of device-clot interaction for stent retriever thrombectomy. J Neurointerv Surg. 2016; 8:1278–1282.
Article
5. Wiesmann M, Brockmann MA, Heringer S, Müller M, Reich A, Nikoubashman O. Active push deployment technique improves stent/vessel-wall interaction in endovascular treatment of acute stroke with stent retrievers. J Neurointerv Surg. 2017; 9:253–256.
6. Cahalane R, Boodt N, Akyildiz AC, Giezen JA, Mondeel M, van der Lugt A, et al. A review on the association of thrombus composition with mechanical and radiological imaging characteristics in acute ischemic stroke. J Biomech. 2021; 129:110816.
7. Cahalane RME, de Vries JJ, de Maat MPM, van Gaalen K, van Beusekom HM, van der Lugt A, et al. Tensile and compressive mechanical behaviour of human blood clot analogues. Ann Biomed Eng. 2023; 51:1759–1768.
Article
8. Heo JH, Nam HS, Kim YD, Choi JK, Kim BM, Kim DJ, et al. Pathophysiologic and therapeutic perspectives based on thrombus histology in stroke. J Stroke. 2020; 22:64–75.
9. Boeckh-Behrens T, Schubert M, Förschler A, Prothmann S, Kreiser K, Zimmer C, et al. The impact of histological clot composition in embolic stroke. Clin Neuroradiol. 2016; 26:189–197.
10. Kitano T, Hori Y, Okazaki S, Shimada Y, Iwamoto T, Kanki H, et al. An older thrombus delays reperfusion after mechanical thrombectomy for ischemic stroke. Thromb Haemost. 2022; 122:415–426.
11. Novotny J, Oberdieck P, Titova A, Pelisek J, Chandraratne S, Nicol P, et al. Thrombus NET content is associated with clinical outcome in stroke and myocardial infarction. Neurology. 2020; 94:e2346–e2360.
12. Staessens S, Denorme F, Francois O, Desender L, Dewaele T, Vanacker P, et al. Structural analysis of ischemic stroke thrombi: histological indications for therapy resistance. Haematologica. 2020; 105:498–507.
13. Staessens S, François O, Desender L, Vanacker P, Dewaele T, Sciot R, et al. Detailed histological analysis of a thrombectomy-resistant ischemic stroke thrombus: a case report. Thromb J. 2021; 19:11.
14. Douglas A, Fitzgerald S, Mereuta OM, Rossi R, O’Leary S, Pandit A, et al. Platelet-rich emboli are associated with von Willebrand factor levels and have poorer revascularization outcomes. J Neurointerv Surg. 2020; 12:557–562.
15. Abbasi M, Arturo Larco J, Mereuta MO, Liu Y, Fitzgerald S, Dai D, et al. Diverse thrombus composition in thrombectomy stroke patients with longer time to recanalization. Thromb Res. 2022; 209:99–104.
16. Boodt N, Snouckaert van Schauburg PRW, Hund HM, Fereidoonnezhad B, McGarry JP, Akyildiz AC, et al. Mechanical characterization of thrombi retrieved with endovascular thrombectomy in patients with acute ischemic stroke. Stroke. 2021; 52:2510–2517.
17. Johnson S, Chueh J, Gounis MJ, McCarthy R, McGarry JP, McHugh PE, et al. Mechanical behavior of in vitro blood clots and the implications for acute ischemic stroke treatment. J Neurointerv Surg. 2020; 12:853–857.
18. Cruts JMH, Giezen JA, van Gaalen K, Beurskens R, Ridwan Y, Dijkshoorn ML, et al. The association between human blood clot analogue computed tomography imaging, composition, contraction, and mechanical characteristics. PLoS One. 2023; 18:e0293456.
19. Weafer FM, Duffy S, Machado I, Gunning G, Mordasini P, Roche E, et al. Characterization of strut indentation during mechanical thrombectomy in acute ischemic stroke clot analogs. J Neurointerv Surg. 2019; 11:891–897.
20. Machi P, Jourdan F, Ambard D, Reynaud C, Lobotesis K, Sanchez M, et al. Experimental evaluation of stent retrievers’ mechanical properties and effectiveness. J Neurointerv Surg. 2017; 9:257–263.
21. Tutwiler V, Singh J, Litvinov RI, Bassani JL, Purohit PK, Weisel JW. Rupture of blood clots: mechanics and pathophysiology. Sci Adv. 2020; 6:eabc0496.
22. Liu S, Bao G, Ma Z, Kastrup CJ, Li J. Fracture mechanics of blood clots: measurements of toughness and critical length scales. Extrem Mech Lett. 2021; 48:101444.
23. Fereidoonnezhad B, Dwivedi A, Johnson S, McCarthy R, McGarry P. Blood clot fracture properties are dependent on red blood cell and fibrin content. Acta Biomater. 2021; 127:213–228.
24. Gersh KC, Nagaswami C, Weisel JW. Fibrin network structure and clot mechanical properties are altered by incorporation of erythrocytes. Thromb Haemost. 2009; 102:1169–1175.
25. Freiherr von Seckendorff A, Delvoye F, Levant P, Solo Nomenjanahary M, Ollivier V, Bourrienne MC, et al. Modeling large vessel occlusion stroke for the evaluation of endovascular therapy according to thrombus composition. Front Neurol. 2022; 12:815814.
26. Gunning GM, McArdle K, Mirza M, Duffy S, Gilvarry M, Brouwer PA. Clot friction variation with fibrin content; implications for resistance to thrombectomy. J Neurointerv Surg. 2018; 10:34–38.
27. Yuki I, Kan I, Vinters HV, Kim RH, Golshan A, Vinuela FA, et al. The impact of thromboemboli histology on the performance of a mechanical thrombectomy device. AJNR Am J Neuroradiol. 2012; 33:643–648.
28. Hashimoto T, Hayakawa M, Funatsu N, Yamagami H, Satow T, Takahashi JC, et al. Histopathologic analysis of retrieved thrombi associated with successful reperfusion after acute stroke thrombectomy. Stroke. 2016; 47:3035–3037.
29. Shin JW, Jeong HS, Kwon HJ, Song KS, Kim J. High red blood cell composition in clots is associated with successful recanalization during intra-arterial thrombectomy. PLoS One. 2018; 13:e0197492.
30. Delvoye F, Di Meglio L, Consoli A, Nomenjanahary MS, Dupont S, Labreuche J, et al. High thrombus platelet content is associated with a lower rate of first pass effect in stroke treated by endovascular therapy. Eur Stroke J. 2022; 7:376–383.
31. Sporns PB, Hanning U, Schwindt W, Velasco A, Buerke B, Cnyrim C, et al. Ischemic stroke: histological thrombus composition and pre-interventional CT attenuation are associated with intervention time and rate of secondary embolism. Cerebrovasc Dis. 2017; 44:344–350.
32. Bhambri A, Adapa AR, Liu Y, Boeckh-Behrens T, Procházka V, Hernández-Fernández F, et al. Thrombus histology as it relates to mechanical thrombectomy: a meta-analysis and systematic review. Neurosurgery. 2021; 89:1122–1131.
33. Shimizu H, Hatakeyama K, Saito K, Shobatake R, Takahashi N, Deguchi J, et al. Age and composition of the thrombus retrieved by mechanical thrombectomy from patients with acute ischemic stroke are associated with revascularization and clinical outcomes. Thromb Res. 2022; 219:60–69.
34. Maekawa K, Shibata M, Nakajima H, Mizutani A, Kitano Y, Seguchi M, et al. Erythrocyte-rich thrombus is associated with reduced number of maneuvers and procedure time in patients with acute ischemic stroke undergoing mechanical thrombectomy. Cerebrovasc Dis Extra. 2018; 8:39–49.
35. Duffy S, McCarthy R, Farrell M, Thomas S, Brennan P, Power S, et al. Per-pass analysis of thrombus composition in patients with acute ischemic stroke undergoing mechanical thrombectomy. Stroke. 2019; 50:1156–1163.
36. Patil S, Darcourt J, Messina P, Bozsak F, Cognard C, Doyle K. Characterising acute ischaemic stroke thrombi: insights from histology, imaging and emerging impedance-based technologies. Stroke Vasc Neurol. 2022; 7:353–363.
37. Staessens S, François O, Brinjikji W, Doyle KM, Vanacker P, Andersson T, et al. Studying stroke thrombus composition after thrombectomy: what can we learn? Stroke. 2021; 52:3718–3727.
38. Simons N, Mitchell P, Dowling R, Gonzales M, Yan B. Thrombus composition in acute ischemic stroke: a histopathological study of thrombus extracted by endovascular retrieval. J Neuroradiol. 2015; 42:86–92.
39. Kaesmacher J, Boeckh-Behrens T, Simon S, Maegerlein C, Kleine JF, Zimmer C, et al. Risk of thrombus fragmentation during endovascular stroke treatment. AJNR Am J Neuroradiol. 2017; 38:991–998.
40. Ye G, Qi P, Chen K, Tan T, Cao R, Chen J, et al. Risk of secondary embolism events during mechanical thrombectomy for acute ischemic stroke: a single-center study based on histological analysis. Clin Neurol Neurosurg. 2020; 193:105749.
41. Maegerlein C, Friedrich B, Berndt M, Lucia KE, Schirmer L, Poppert H, et al. Impact of histological thrombus composition on preinterventional thrombus migration in patients with acute occlusions of the middle cerebral artery. Interv Neuroradiol. 2018; 24:70–75.
42. Sporns PB, Jeibmann A, Minnerup J, Broocks G, Nawabi J, Schön G, et al. Histological clot composition is associated with preinterventional clot migration in acute stroke patients. Stroke. 2019; 50:2065–2071.
43. Sporns PB, Krähling H, Psychogios MN, Jeibmann A, Minnerup J, Broocks G, et al. Small thrombus size, thrombus composition, and poor collaterals predict pre-interventional thrombus migration. J Neurointerv Surg. 2021; 13:409–414.
Full Text Links
  • NI
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr