Embolus Analogues (EAs) can provide understanding of the mechanical characteristics of blood clots of cardiac origin. Bovine EAs (n = 29) were fabricated with varying concentrations of thrombin (0–20 NIHU/ml blood). Histological staining confirmed that EA composition compared sufficiently with human samples reported in literature. EAs were mechanically described under seven testing conditions: tensile, compression, shear wave ultrasound elastography (SWE), parallel plate rheometry, indentation, creep and relaxation. The Young modulus of bovine EAs in tension varied from 7 kPa (5% strain) to 84 kPa (50% strain). The compressive Young modulus increased with increasing thrombin concentration, which was in agreement with the SWE results. There was no significant difference in Young modulus throughout the clot (p < 0.05). The EAs displayed a non-linear response under parallel plate rheometry, creep and stress relaxation. The 3rd order Mooney–Rivlin constitutive equation and Standard Linear Solid model were used to fit the non-linear stress–strain response and time-dependent properties, respectively. This is the first study in which bovine EAs, with and without addition of thrombin, are histologically and mechanically described with corresponding proposed constitutive equations. The equations and experimental data determined can be applied for future numerical and experimental testing of mammalian EAs and cardiac source clots.
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Beldi, G., L. Beng, G. Siegel, S. Bisch-Knaden, and D. Candinas. Prevention of perioperative thromboembolism in patients with atrial fibrillation. Br. J. Surg. Nov. 94(11):1351–1355, 2007.
Bernal, M., F. Chammings, M. Couade, J. Bercoff, M. Tanter, and J. L. Gennisson. In vivo quantification of the nonlinear shear modulus in breast lesions: feasibility study. IEEE Trans. Ultrason. Ferroelectr. Frequ. Control 63(1):101–109, 2016.
Brophy, D. F., R. J. Martin, T. W. Gehr, and M. E. Carr. A hypothesis-generating study to evaluate platelet activity in diabetics with chronic kidney disease. Thromb. J. 3(1):3, 2005.
Campbell, W. B., B. M. Ridler, and T. H. Szymanska. Two-year follow-up after acute thromboembolic limb ischaemia: the importance of anticoagulation. Eur. J. Vasc. Endovasc. Surg. 19:169–173, 2000.
Carr, M. E., A. Krishnaswami, and E. J. Martin. Platelet contractile force (PCF) and clot elastic modulus (CEM) are elevated in diabetic patients with chest pain. Diabet. Med. 19(10):862–866, 2002.
Chueh, J. K., A. K. Wakhloo, G. H. Hendricks, C. F. Silva, J. P. Weaver, and M. J. Gounis. Mechanical characterisation of Thromboemboli in acute ischemic stroke and Laboratory Embolus Analogues. Am. J. Neuroradiol. 32:1237–1244, 2011.
Davie, E. W., and K. Fujikawa. Basic mechanisms in blood coagulation. Annu. Rev. Biochem. 44:799–829, 1975.
Dempfle, C. E., T. Kalsch, E. Elmas, N. Suvajac, T. Luecke, E. Muench, and M. Borggrefe. Impact of fibrinogen concentration in severely ill patients on mechanical properties of whole blood clots. Blood Coagul Fibrinolysis 19:765–770, 2008.
Eggebrecht, H., A. Schmermund, T. Voigtländer, P. Kahlert, R. Erbel, and R. H. Mehta. Risk of stroke after transcatheter aortic valve implantation (TAVI): a meta-analysis of 10,037 published patients. EuroIntervention 8:129–138, 2012.
Fuster, V., L. E. Ryden, D. S. Cannom, H. J. Crijns, A. B. Curtis, K. A. Ellenbogen, J. L. Halperin, J. Y. Le Heuzey, G. N. Kay, J. E. Lowe, S. B. Olsson, E. N. Prystowsky, J. L. Tamargo, S. Wann, S. C. Smith, Jr, A. K. Jacobs, C. D. Adams, J. L. Anderson, E. M. Antman, J. L. Halperin, S. A. Hunt, R. Nishimura, J. P. Ornato, R. L. Page, B. Riegel, S. G. Priori, J. J. Blanc, A. Budaj, A. J. Camm, V. Dean, J. W. Deckers, C. Despres, K. Dickstein, J. Lekakis, K. McGregor, M. Metra, J. Morais, A. Osterspey, J. L. Tamargo, and J. L. Zamorano. Guidelines for the management of patients with atrial fibrillation. Circulation 114:257–354, 2006.
Gennisson, J. L., M. Renier, S. Catheline, C. Barriere, J. Bercoff, M. Tanter, and M. Fink. Acoustoelasticity in soft solds: assessment of the non-linear shear modulus with acoustic radiation force. J. Acoust. Soc. Am. 122(6):3211–3219, 2007.
Gralla, J., G. Schroth, L. Remonda, A. Fleischmann, J. Fandino, J. Slotboom, and C. Brekenfeld. A dedicated animal model for mechanical thrombectomy in acute Stroke. AJNR 27:1357–1361, 2006.
Heeringa, J., D. A. van der Kuip, A. Hofman, J. A. Kors, G. van Herpen, B. H. Stricker, T. Stijnen, G. Y. Lip, and J. C. Witteman. Prevalence, incidence and lifetime risk of atrial fibrillation: the Rotterdam study. Eur. Heart. J. 27:949–953, 2006.
Isogai, Y., A. Iida, I. Chikatsu, K. Mochizuki, and M. Abe. Dynamic viscoelasticity of blood during clotting in health and disease. Biorheology 10(3):411–424, 1973.
Jiang, Y., L. Guoyang, L. X. Qian, S. Liang, M. Destrade, and Y. Cao. Measuring the linear and non linear elastic properties of brain tissue with shear waves and inverse analysis. Biomech. Model Mechanobiol. 14:1119–1128, 2014.
Juliano, T. F., A. M. Forster, P. L. Drzal, T. Weerasooriya, P. Moy, and M. R. VanLandingham. Multiscale mechanical characterization of biomimetic physically associating gels. J. Mater. Res. 21(8):2084–2092, 2006.
Kan, I., I. Yuki, Y. Murayama, F. A. Vinuela, R. H. Kim, H. V. Vinters, and F. Vinuela. A novel method of thrombus preparation for use in a swine model for evaluation of thrombectomy devices. AJNR 31:1741–1743, 2010.
Kannel, W. B., and E. J. Benjamin. Status of the epidemiology of atrial fibrillation. Med. Clin. N. Am. 92:17–40, 2008.
Kay, R., J. Woo, L. Kreel, H. Y. Wong, R. Teoh, and M. G. Nicholls. Stroke subtypes among Chinese living in Hong Kong: the Shatin Stroke Registry. Neurology. 42:985–987, 1992.
Kline, J. A., and R. S. Runyon. Pulmonary embolism and deep vein thrombosis. In: Emergency Medicine Concepts and Clinical Practice7th, edited by J. A. Marx, R. S. Hockberger, and R. M. Walls. New York: Elsevier, 2010, pp. 1157–1169.
Krasokha, N., W. Theisen, S. Reese, P. Mordasini, C. Brekenfeld, J. Gralla, J. Slotboom, G. Schrott, and H. Monstadt. Mechanical properties of blood clots—a new test method. Mat wiss u Werkstofftech. 41:1019–1024, 2010.
Lalley, C., A. J. Reid, and P. J. Prendergast. Elastic behaviour of porcine coronary artery tissue under uniaxial and equibiaxial tension. Ann. Biomed. Eng. 32(10):1355–1364, 2004.
Maier, A., M. W. Gee, C. Reeps, H.-H. Eckstein, and W. A. Wall. Impact of calcifications on patient-specific wall stress analysis of abdominal aortic aneurysms. Biomech. Model. Mechanobiol. 9:511–521, 2010.
Menke, J., L. Lüthje, A. Kastrup, and J. Larsen. Thromboembolism in atrial fibrillation. Am. J. Cardiol. 105:502–510, 2010.
Prystowsky, E. N. The history of atrial fibrillation: the last 100 years. J. Cardiovasc. Electrophysiol. 19:575–582, 2008.
Robinson, R. A., L. H. Herbertson, S. Sarkar Das, R. A. Malinauskas, W. F. Pritchard, and L. W. Grossman. Limitations of using synthetic blood clots for measuring in vitro clot capture efficiency of inferior vena cava filters. Med. Dev. (Auckland, N.Z.) 6:49–57, 2013.
Schmitt, C., A. H. Henni, and G. Cloutier. Characterization of blood clot viscoelasticity by dynamic ultrasound elastography and modeling of the rheological behaviour. J. Biomech. 44:622–629, 2011.
Sigrist, R. M. S., J. Liau, A. El Kaffas, M. C. Chammas, and J. K. Willmann. Ultrasound elastography: reviwe of techniques and clinical applications. Theranostics 7(5):1303, 2017.
Whitbourne, P. G. S. Changes in the Clotting Viscoelasticity Caused by Cardiopulmonary Bypass (CPB) Surgery [dissertation]. MA: Cambridge Massachusetts Institute of Technology, 1998.
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Conflict of Interest
All authors declare that they have no conflicts of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Burkes Ltd., is an EU approved abattoir. This article does not contain any studies with human participants performed by any of the authors.
Associate Editors Ulrich Steinseifer and Ajit P. Yoganathan oversaw the review of this article.
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Malone, F., McCarthy, E., Delassus, P. et al. The Mechanical Characterisation of Bovine Embolus Analogues Under Various Loading Conditions. Cardiovasc Eng Tech 9, 489–502 (2018). https://doi.org/10.1007/s13239-018-0352-3
- Embolus analogues
- Mechanical testing
- Blood clots
- Cardiac source clots
- Constitutive equations