Material strengths of shear-induced platelet aggregation clots and coagulation clots.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 05 2024
20 05 2024
Historique:
received:
18
09
2023
accepted:
14
05
2024
medline:
21
5
2024
pubmed:
21
5
2024
entrez:
20
5
2024
Statut:
epublish
Résumé
Arterial occlusion by thrombosis is the immediate cause of some strokes, heart attacks, and peripheral artery disease. Most prior studies assume that coagulation creates the thrombus. However, a contradiction arises as whole blood (WB) clots from coagulation are too weak to stop arterial blood pressures (> 150 mmHg). We measure the material mechanical properties of elasticity and ultimate strength for Shear-Induced Platelet Aggregation (SIPA) type clots, that form under stenotic arterial hemodynamics in comparison with coagulation clots. The ultimate strength of SIPA clots averaged 4.6 ± 1.3 kPa, while WB coagulation clots had a strength of 0.63 ± 0.3 kPa (p < 0.05). The elastic modulus of SIPA clots was 3.8 ± 1.5 kPa at 1 Hz and 0.5 mm displacement, or 2.8 times higher than WB coagulation clots (1.3 ± 1.2 kPa, p < 0.0001). This study shows that the SIPA thrombi, formed quickly under high shear hemodynamics, is seven-fold stronger and three-fold stiffer compared to WB coagulation clots. A force balance calculation shows a SIPA clot has the strength to resist arterial pressure with a short length of less than 2 mm, consistent with coronary pathology.
Identifiants
pubmed: 38769378
doi: 10.1038/s41598-024-62165-1
pii: 10.1038/s41598-024-62165-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
11460Subventions
Organisme : L.P. Huang Chair Funds
ID : 150000059
Informations de copyright
© 2024. The Author(s).
Références
Bark, D. L. Jr. & Ku, D. N. Wall shear over high degree stenoses pertinent to atherothrombosis. J. Biomech. 43, 2970–2977. https://doi.org/10.1016/j.jbiomech.2010.07.011 (2010).
doi: 10.1016/j.jbiomech.2010.07.011
pubmed: 20728892
Stamler, J., Neaton, J. D. & Wentworth, D. N. Blood pressure (systolic and diastolic) and risk of fatal coronary heart disease. Hypertension 13(5 Suppl), I2-12. https://doi.org/10.1161/01.hyp.13.5_suppl.i2 (1989).
doi: 10.1161/01.hyp.13.5_suppl.i2
pubmed: 2490825
Möhlenbruch, M. et al. Mechanical thrombectomy compared to local-intraarterial thrombolysis in carotid T and middle cerebral artery occlusions. Clin. Neuroradiol. 22, 141–147. https://doi.org/10.1007/s00062-011-0099-9 (2012).
doi: 10.1007/s00062-011-0099-9
pubmed: 21971720
Liu, Y. et al. Analysis of human emboli and thrombectomy forces in large-vessel occlusion stroke. J. Neurosurg. JNS https://doi.org/10.3171/2019.12.JNS192187 (2020).
doi: 10.3171/2019.12.JNS192187
Yeo, L. L. L. et al. Why does mechanical thrombectomy in large vessel occlusion sometimes fail?. Clin. Neuroradiol. 29, 401–414. https://doi.org/10.1007/s00062-019-00777-1 (2019).
doi: 10.1007/s00062-019-00777-1
pubmed: 30895349
Gunning, G. M. et al. Clot friction variation with fibrin content; implications for resistance to thrombectomy. J. NeuroInterv. Surg. 10, 34. https://doi.org/10.1136/neurintsurg-2016-012721 (2018).
doi: 10.1136/neurintsurg-2016-012721
pubmed: 28044009
Duffy, S. et al. Novel methodology to replicate clot analogs with diverse composition in acute ischemic stroke. J. NeuroInterv. Surg. 9, 486. https://doi.org/10.1136/neurintsurg-2016-012308 (2017).
doi: 10.1136/neurintsurg-2016-012308
pubmed: 27127231
Pikija, S. et al. Intracranial thrombus morphology and composition undergoes time-dependent changes in acute ischemic stroke: A CT densitometry study. Int. J. Mol. Sci. 17, 1959. https://doi.org/10.3390/ijms17111959 (2016).
doi: 10.3390/ijms17111959
pubmed: 27886084
pmcid: 5133953
Yao, X. et al. Thrombelastography maximal clot strength could predict one-year functional outcome in patients with ischemic stroke. Cerebrovasc. Dis. 38, 182–190. https://doi.org/10.1159/000365652 (2014).
doi: 10.1159/000365652
pubmed: 25300785
Bitar, A. & Kreutz, R. P. Role of thrombelastography (TEG) in risk assessment and guidance of antithrombotic therapy in patients with coronary artery disease. Drug Dev. Res. 74, 533–540. https://doi.org/10.1002/ddr.21112 (2013).
doi: 10.1002/ddr.21112
Johnson, S. et al. Review of mechanical testing and modelling of thrombus material for vascular implant and device design. Ann. Biomed. Eng. 45, 2494–2508. https://doi.org/10.1007/s10439-017-1906-5 (2017).
doi: 10.1007/s10439-017-1906-5
pubmed: 28849421
Di Martino, E. et al. Biomechanics of abdominal aortic aneurysm in the presence of endoluminal thrombus: Experimental characterisation and structural static computational analysis. Eur. J. Vasc. Endovasc. Surg. 15, 290–299. https://doi.org/10.1016/s1078-5884(98)80031-2 (1998).
doi: 10.1016/s1078-5884(98)80031-2
pubmed: 9610340
Gasser, T. C., Görgülü, G., Folkesson, M. & Swedenborg, J. Failure properties of intraluminal thrombus in abdominal aortic aneurysm under static and pulsating mechanical loads. J. Vasc. Surg. 48, 179–188. https://doi.org/10.1016/j.jvs.2008.01.036 (2008).
doi: 10.1016/j.jvs.2008.01.036
pubmed: 18486417
Teng, Z. et al. Layer- and direction-specific material properties, extreme extensibility and ultimate material strength of human abdominal aorta and aneurysm: A uniaxial extension study. Ann. Biomed. Eng. 43, 2745–2759. https://doi.org/10.1007/s10439-015-1323-6 (2015).
doi: 10.1007/s10439-015-1323-6
pubmed: 25905688
pmcid: 4611020
Ashton, J. H., Vande Geest, J. P., Simon, B. R. & Haskett, D. G. Compressive mechanical properties of the intraluminal thrombus in abdominal aortic aneurysms and fibrin-based thrombus mimics. J. Biomech. 42, 197–201. https://doi.org/10.1016/j.jbiomech.2008.10.024 (2009).
doi: 10.1016/j.jbiomech.2008.10.024
pubmed: 19058807
Xie, H. et al. Correspondence of ultrasound elasticity imaging to direct mechanical measurement in aging DVT in rats. Ultrasound Med. Biol. 31, 1351–1359. https://doi.org/10.1016/j.ultrasmedbio.2005.06.005 (2005).
doi: 10.1016/j.ultrasmedbio.2005.06.005
pubmed: 16223638
pmcid: 1343482
Chueh, J. Y. et al. Mechanical characterization of thromboemboli in acute ischemic stroke and laboratory embolus analogs. AJNR Am. J. Neuroradiol. 32, 1237–1244. https://doi.org/10.3174/ajnr.A2485 (2011).
doi: 10.3174/ajnr.A2485
pubmed: 21596804
pmcid: 7966072
van Dam, E. A. et al. Determination of linear viscoelastic behavior of abdominal aortic aneurysm thrombus. Biorheology 43, 695–707 (2006).
pubmed: 17148853
Schmitt, C., Hadj Henni, A. & Cloutier, G. Characterization of blood clot viscoelasticity by dynamic ultrasound elastography and modeling of the rheological behavior. J. Biomech. 44, 622–629. https://doi.org/10.1016/j.jbiomech.2010.11.015 (2011).
doi: 10.1016/j.jbiomech.2010.11.015
pubmed: 21122863
Slaboch, C. L., Alber, M. S., Rosen, E. D. & Ovaert, T. C. Mechano-rheological properties of the murine thrombus determined via nanoindentation and finite element modeling. J. Mech. Behav. Biomed. Mater. 10, 75–86. https://doi.org/10.1016/j.jmbbm.2012.02.012 (2012).
doi: 10.1016/j.jmbbm.2012.02.012
pubmed: 22520420
Henderson, N. M. & Thurston, G. B. A new method for the analysis of blood and plasma coagulation. Biomed. Sci. Instrum. 29, 95–102 (1993).
pubmed: 8329642
McCarty, W. J. et al. Biomechanical properties of mixtures of blood and synovial fluid. J. Orthop. Res. 29, 240–246. https://doi.org/10.1002/jor.21209 (2011).
doi: 10.1002/jor.21209
pubmed: 21226237
pmcid: 3057681
Riha, P., Wang, X., Liao, R. & Stoltz, J. F. Elasticity and fracture strain of whole blood clots. Clin. Hemorheol. Microcirc. 21, 45–49 (1999).
pubmed: 10517487
Ryan, E. A., Mockros, L. F., Weisel, J. W. & Lorand, L. Structural origins of fibrin clot rheology. Biophys. J. 77, 2813–2826. https://doi.org/10.1016/s0006-3495(99)77113-4 (1999).
doi: 10.1016/s0006-3495(99)77113-4
pubmed: 10545379
pmcid: 1300553
Hinnen, J. W., Rixen, D. J., Koning, O. H. J., van Bockel, J. H. & Hamming, J. F. Development of fibrinous thrombus analogue for in-vitro abdominal aortic aneurysm studies. J. Biomech. 40, 289–295. https://doi.org/10.1016/j.jbiomech.2006.01.010 (2007).
doi: 10.1016/j.jbiomech.2006.01.010
pubmed: 16516895
Lefkowitz, J. B. Coagulation pathway and physiology. In An Algorithmic Approach to Hemostasis Testing (ed. Kottke-Marchant, K.) 3–12 (College of American Pathologists, 2008).
Cadroy, Y., Horbett, T. A. & Hanson, S. R. Discrimination between platelet-mediated and coagulation-mediated mechanisms in a model of complex thrombus formation in vivo. J. Lab. Clin. Med. 113, 436–448 (1989).
pubmed: 2522978
Casa, L. D., Deaton, D. H. & Ku, D. N. Role of high shear rate in thrombosis. J. Vasc. Surg. 61, 1068–1080 (2015).
doi: 10.1016/j.jvs.2014.12.050
pubmed: 25704412
Ku, D. N. & Flannery, C. J. Development of a flow-through system to create occluding thrombus. Biorheology 44, 273–284 (2007).
pubmed: 18094451
Kim, D. A. & Ku, D. N. Structure of shear-induced platelet aggregated clot formed in an in vitro arterial thrombosis model. Blood Adv. 6, 2872–2883. https://doi.org/10.1182/bloodadvances.2021006248 (2022).
doi: 10.1182/bloodadvances.2021006248
pubmed: 35086138
pmcid: 9092419
Wellings, P. J. & Ku, D. N. Mechanisms of platelet capture under very high shear. Cardiovasc. Eng. Technol. 3, 161–170. https://doi.org/10.1007/s13239-012-0086-6 (2012).
doi: 10.1007/s13239-012-0086-6
Du, J., Kim, D., Alhawael, G., Ku, D. N. & Fogelson, A. L. Clot permeability, agonist transport, and platelet binding kinetics in arterial thrombosis. Biophys. J. https://doi.org/10.1016/j.bpj.2020.08.041 (2020).
doi: 10.1016/j.bpj.2020.08.041
pubmed: 33147477
pmcid: 7732729
Para, A. N. & Ku, D. N. A low-volume, single pass in-vitro system of high shear thrombosis in a stenosis. Thromb. Res. 131, 418–424. https://doi.org/10.1016/j.thromres.2013.02.018 (2013).
doi: 10.1016/j.thromres.2013.02.018
pubmed: 23535566
Clavería, V., Yang, P. J., Griffin, M. T. & Ku, D. N. Global thrombosis test: Occlusion by coagulation or SIPA?. TH Open 05, e400–e410. https://doi.org/10.1055/s-0041-1732341 (2021).
doi: 10.1055/s-0041-1732341
Griffin, M. T., Kim, D. & Ku, D. N. Shear-induced platelet aggregation: 3D-grayscale microfluidics for repeatable and localized occlusive thrombosis. Biomicrofluidics 13, 054106. https://doi.org/10.1063/1.5113508 (2019).
doi: 10.1063/1.5113508
pubmed: 31592301
pmcid: 6773594
Matsuo, O., Rijken, D. C. & Collen, D. Comparison of the relative fibrinogenolytic, fibrinolytic and thrombolytic properties of tissue plasminogen activator and urokinase in vitro. Thromb. Haemost. 45, 225–229 (1981).
doi: 10.1055/s-0038-1650175
pubmed: 7025339
do Amaral, R. J. F. C. et al. Functionalising collagen-based scaffolds with platelet-rich plasma for enhanced skin wound healing potential. Front. Bioeng. Biotechnol. https://doi.org/10.3389/fbioe.2019.00371 (2019).
doi: 10.3389/fbioe.2019.00371
pubmed: 31921799
pmcid: 6915093
Jones, D. S. Dynamic mechanical analysis of polymeric systems of pharmaceutical and biomedical significance. Int. J. Pharm. 179, 167–178. https://doi.org/10.1016/S0378-5173(98)00337-8 (1999).
doi: 10.1016/S0378-5173(98)00337-8
pubmed: 10053212
Menard, K. P. & Menard, N. Dynamic Mechanical Analysis (CRC Press, 2020).
doi: 10.1201/9780429190308
Silver, M. D., Baroldi, G. & Mariani, F. The relationship between acute occlusive coronary thrombi and myocardial infarction studied in 100 consecutive patients. Circulation 61, 219–227. https://doi.org/10.1161/01.CIR.61.2.219 (1980).
doi: 10.1161/01.CIR.61.2.219
pubmed: 7351048
Buehler, M. J. & Yung, Y. C. How protein materials balance strength, robustness, and adaptability. HFSP J. 4, 26–40. https://doi.org/10.2976/1.3267779 (2010).
doi: 10.2976/1.3267779
pubmed: 20676305
pmcid: 2880027
Liu, Z. L., Bresette, C., Aidun, C. K. & Ku, D. N. SIPA in 10 milliseconds: VWF tentacles agglomerate and capture platelets under high shear. Blood Adv. 6, 2453–2465. https://doi.org/10.1182/bloodadvances.2021005692 (2022).
doi: 10.1182/bloodadvances.2021005692
pubmed: 34933342
pmcid: 9043924
Ruggeri, Z. M., Orje, J. N., Habermann, R., Federici, A. B. & Reininger, A. J. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108, 1903–1910 (2006).
doi: 10.1182/blood-2006-04-011551
pubmed: 16772609
pmcid: 1895550
Shen, L. & Lorand, L. Contribution of fibrin stabilization to clot strength. Supplementation of factor XIII-deficient plasma with the purified zymogen. J. Clin. Invest. 71, 1336–1341. https://doi.org/10.1172/jci110885 (1983).
doi: 10.1172/jci110885
pubmed: 6853717
pmcid: 436996
Tutwiler, V. et al. Shape changes of erythrocytes during blood clot contraction and the structure of polyhedrocytes. Sci. Rep. 8, 17907. https://doi.org/10.1038/s41598-018-35849-8 (2018).
doi: 10.1038/s41598-018-35849-8
pubmed: 30559364
pmcid: 6297136
Lam, W. A. et al. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat. Mater. 10, 61–66. https://doi.org/10.1038/nmat2903 (2011).
doi: 10.1038/nmat2903
pubmed: 21131961
Seners, P. et al. Thrombus length predicts lack of post-thrombolysis early recanalization in minor stroke with large vessel occlusion. Stroke 50, 761–764. https://doi.org/10.1161/STROKEAHA.118.023455 (2019).
doi: 10.1161/STROKEAHA.118.023455
pubmed: 30802186
Kamalian, S. et al. Clot length distribution and predictors in anterior circulation stroke. Stroke 44, 3553–3556. https://doi.org/10.1161/STROKEAHA.113.003079 (2013).
doi: 10.1161/STROKEAHA.113.003079
pubmed: 24105699
pmcid: 3927722
Uchida, Y. et al. Characterization of coronary fibrin thrombus in patients with acute coronary syndrome using dye-staining angioscopy. Arterioscler. Thromb. Vasc. Biol. 31, 1452–1460. https://doi.org/10.1161/atvbaha.110.221671 (2011).
doi: 10.1161/atvbaha.110.221671
pubmed: 21415387
Marder, V. J. et al. Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke 37, 2086–2093. https://doi.org/10.1161/01.Str.0000230307.03438.94 (2006).
doi: 10.1161/01.Str.0000230307.03438.94
pubmed: 16794209
Little, W. C. et al. Can coronary angiography predict the site of a subsequent myocardial infarction in patients with mild-to-moderate coronary artery disease?. Circulation 78, 1157–1166. https://doi.org/10.1161/01.CIR.78.5.1157 (1988).
doi: 10.1161/01.CIR.78.5.1157
pubmed: 3180375
Kilic, S., Kocabas, U., Can, L. H., Yavuzgil, O. & Zoghi, M. The severity of coronary arterial stenosis in patients with acute ST-elevated myocardial infarction: A thrombolytic therapy study. Cardiol. Res. 9(1), 11 (2018).
doi: 10.14740/cr639w
pubmed: 29479380
pmcid: 5819623
Chitsaz, A., Nejat, A. & Nouri, R. Three-dimensional numerical simulations of aspiration process: Evaluation of two penumbra aspiration catheters performance. Artif. Organs 42, E406-e419. https://doi.org/10.1111/aor.13300 (2018).
doi: 10.1111/aor.13300
pubmed: 30444047
Tobin, N., Li, M., Hiller, G., Azimi, A. & Manning, K. B. Clot embolization studies and computational framework for embolization in a canonical tube model. Sci. Rep. 13, 14682. https://doi.org/10.1038/s41598-023-41825-8 (2023).
doi: 10.1038/s41598-023-41825-8
pubmed: 37673915
pmcid: 10482921
Khalil, I. S. M. et al. Rubbing against blood clots using helical robots: Modeling and in vitro experimental validation. IEEE Robot. Autom. Lett. 2, 927–934. https://doi.org/10.1109/LRA.2017.2654546 (2017).
doi: 10.1109/LRA.2017.2654546
Welsh, J. D. et al. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets. Blood 124, 1808–1815. https://doi.org/10.1182/blood-2014-01-550335 (2014).
doi: 10.1182/blood-2014-01-550335
pubmed: 24951424
pmcid: 4162110