Physical Parameters of Arterial Thrombus as a Porous Medium

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Abstract

The formation of a hemostatic thrombus is a key response of the hemostasis system to a wide range of possible vessel injuries. The basic mechanism of thrombus formation at high shear rate is platelet adhesion and aggregation. It is known that arterial thrombi are spatially heterogeneous. Such heterogeneity is thought to be due to the heterogeneous distribution of the platelet activators inside the thrombus. Spatiotemporal dynamics of molecules, which are involved in thrombus formation, depends on rates at which the substrates are transported. To explore the dynamics of arterial thrombus formation, continuum models that represent the thrombus as a porous media are currently widely used. Still, choosing parameters for these models is complicated due to a high level of uncertainty in the published experimental data. This review is focused on the analyses of the literature data on physical parameters of the arterial thrombus as a porous medium. Special attention is paid to the parameters of the thrombus shell, which is generally characterized by the higher values of porosity and permeability.

About the authors

E. S Bershadsky

Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences; N.M. Emanuel Institute of Biochemical Physics, Russian Academy of Sciences

Email: email@example.com
ul. Srednyaya Kalitnikovskaya 30, Moscow, 109029, Russia; ul. Kosygina 4, Moscow, 119334, Russia

D. Yu Nechipurenko

Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences; Faculty of Physics, M.V. Lomonosov Moscow State University; Dmitry Rogachev National Medical Research Centre of Pediatric Hematology, Oncology and Immunology

Email: ne4ipur@gmail.com
ul. Srednyaya Kalitnikovskaya 30, Moscow, 109029, Russia; Leninskie Gory 1/2, Moscow, 119991, Russia; ul. Samory Mashela 1, Moscow, 117997, Russia

References

  1. Jackson S. P. The growing complexity of platelet aggre-gation. Blood, 109 (12), 5087–5095 (2007).
  2. Пантелеев М. А. и Свешникова А. Н. Тромбоциты и гемостаз. Онкогематология, 9 (2), 65–73 (2014).
  3. Westrick R. J., Winn M. E., and Eitzman D. T. Murine models of vascular thrombosis. Arteriosclerosis, thrombosis, and vascular biology, 27 (10), 2079–2093 (2007).
  4. Sachs U. J. and Nieswandt B. In vivo thrombus formation in murine models. Circ. Res., 100 (7), 979–991 (2007).
  5. Furie B. and Furie B. C. Thrombus formation in vivo. J. Clin. Invest., 115 (12), 3355–3362 (2005).
  6. Grande Gutierrez N., Mukherjee D., and Bark D., Jr. Decoding thrombosis through code: a review of computational models. J. Thromb Haemost., 22 (1), 35–47 (2024). doi: 10.1016/j.jtha.2023.08.021
  7. Nechipurenko D. Y., Shibeko A. M., Sveshnikova A. N.,and Panteleev M. A. In Silico Hemostasis Modeling and Prediction. Hamostaseologie, 40 (4), 524–535 (2020).
  8. Panteleev M. A., Andreeva A. A., and Lobanov A. I.Differential Drug Target Selection in Blood Coagulation: What can we get from Computational Systems Biology Models? Curr. Pharm. Des., 26 (18), 2109–2115 (2020).
  9. Shibeko A. M. and Panteleev M. A. Untangling thecomplexity of blood coagulation network: use of computational modelling in pharmacology and diagnostics. Brief Bioinform., 17 (3), 429–439 (2016).
  10. Anand M., Panteleev M., and Ataullakhanov F. Computational models of hemostasis: Degrees of complexity. Appl. Eng. Sci., 10, 100103 (2022).
  11. Stalker T. J., Traxler E. A., Wu J., Wannemacher K. M.,Cermignano S. L., Voronov R., Diamond S. L., and Brass L. F. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood, 121 (10), 1875–1885 (2013). doi: 10.1182/blood-2012-09-457739
  12. Welsh J. D., Poventud‐Fuentes I., Sampietro S., Diamond S. L., Stalker T. J., and Brass L. F. Hierarchical organization of the hemostatic response to penetrating injuries in the mouse macrovasculature. J. Thromb. Haemost., 15 (3), 526–537 (2017).
  13. Welsh J. D., Stalker T. J., Voronov R., Muthard R. W.,Tomaiuolo M., Diamond S. L., and Brass L. F. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets. Blood, 124 (11), 1808–1815 (2014).
  14. Tomaiuolo M., Stalker T. J., Welsh J. D., Diamond S. L.,Sinno T., and Brass L. F. A systems approach to hemostasis: 2. Computational analysis of molecular transport in the thrombus microenvironment. Blood, 124 (11), 1816–1823 (2014).
  15. Mirramezani M., Herbig B. A., Stalker T. J., Nettey L.,Cooper M., Weisel J. W., Diamond S. L., Sinno T., Brass L. F., Shadden S. C., and Tomaiuolo M. Platelet packing density is an independent regulator of the hemostatic response to injury. J. Thromb. Haemost., 16 (5), 973–983 (2018). doi: 10.1111/jth.13986
  16. Xu S., Xu Z., Kim O. V., Litvinov R. I., Weisel J. W.,and Alber M. Model predictions of deformation, embolization and permeability of partially obstructive blood clots under variable shear flow. J. Roy. Soc. Interface, 14 (136), 20170441 (2017).
  17. Kaneva V. N., Dunster J. L., Volpert V., AtaullahanovF., Panteleev M. A., and Nechipurenko D. Y. Modeling thrombus shell: linking adhesion receptor properties and macroscopic dynamics. Biophys. J., 120 (2), 334– 351 (2021).
  18. Masalceva A. A., Kaneva V. N., Panteleev M. A.,Ataullakhanov F., Volpert V., Afanasyev I., and Nechipurenko D. Y. Analysis of microvascular thrombus mechanobiology with a novel particle-based model. J. Biomechanics, 130, 110801 (2022).
  19. Tartakovsky D. M. and Dentz M. Diffusion in porousmedia: phenomena and mechanisms. Transport in Porous Media, 130, 105–127 (2019).
  20. Belyaev A. V., Panteleev M. A., and Ataullakhanov F. I.Threshold of microvascular occlusion: injury size defines the thrombosis scenario. Biophys. J., 109 (2), 450–456 (2015).
  21. Carman P. C. Fluid flow through a granular bed. Trans. Inst. Chem. Eng. Lond., 15, 150–156 (1937).
  22. Urumović K. and Urumović Sr. K. The referential grainsize and effective porosity in the Kozeny–Carman model. Hydrol. Earth System Sci., 20 (5), 1669–1680 (2016).
  23. Erdim E., Akgiray Ö., and Demir İ. A revisit of pressuredrop-flow rate correlations for packed beds of spheres. Powder Technol., 283, 488–504 (2015).
  24. Wadell H. Volume, shape, and roundness of quartz particles. J. Geol., 43 (3), 250–280 (1935).
  25. Giles C. The platelet count and mean platelet volume.Br. J. Haematol., 48 (1), 31–37 (1981).
  26. Donev A., Cisse I., Sachs D., Variano E. A.,Stillinger F. H., Connelly R., Torquato S., and Chaikin P. M. Improving the density of jammed disordered packings using ellipsoids. Science, 303 (5660), 990–993 (2004). doi: 10.1126/science.1093010
  27. Darcy H. Les fontaines publiques de la ville de Dijon: exposition et application des principes à suivre et des formules à employer dans les questions de distribution d'eau, Ed. by V. Dalmont (Paris, 1856), vol. 1.
  28. Brinkman H. C. A calculation of the viscous force exerted by a flowing fluid on a dense swarm of particles. Flow, Turbulence and Combustion, 1 (1), 27–34 (1949).
  29. Thorn K. Spinning-disk confocal microscopy of yeast.Methods Enzymol., 470, 581–602 (2010).
  30. Takizawa H., Nishimura S., Takayama N., Oda A., Nishikii H., Morita Y., Kakinuma S., Yamazaki S., Okamura S., Tamura N., Goto Sh., Sawaguchi A., Manabe I., Takatsu K., Nakauchi H., Takaki S., and Eto K. Lnk regulates integrin alphaIIbbeta3 outside-in signaling in mouse platelets, leading to stabilization of thrombus development in vivo. J. Clin. Invest., 120 (1), 179-190 (2010). doi: 10.1172/JCI39503
  31. Baker-Groberg S. M., Phillips K. G., and McCarty O. J.Quantification of volume, mass, and density of thrombus formation using brightfield and differential interference contrast microscopy. J. Biomed. Optics, 18 (1), 016014 (2013).
  32. Phillips K. G., Velasco C. R., Li J., Kolatkar A., Luttgen M., Bethel K., B. Duggan, P. Kuhn, and McCarty O. J. T. Optical quantification of cellular mass, volume, and density of circulating tumor cells identified in an ovarian cancer patient. Front. Oncol., 2, 72 (2012). doi: 10.3389/fonc.2012.00072
  33. Barer R. Interference microscopy and mass determination. Nature, 169, 366–367 (1952).
  34. Paganin D. and Nugent K. A. Noninterferometricphase imaging with partially coherent light. Phys. Rev. Lett., 80, 2586–2589 (1998).
  35. Baker S. M., Phillips K. G., and McCarty O. J. Development of a label-free imaging technique for the quantification of thrombus formation. Cell. Mol. Bioeng., 5, 488–492 (2012).
  36. Hartmann S., Krafft A., Huch R., and Breymann C.Effect of altitude on thrombopoietin and the platelet count in healthy volunteers. Thromb. Haemost., 93 (1), 115–117 (2005).
  37. Du J., Kim D., Alhawael G., Ku D. N., andFogelson A. L. Clot permeability, agonist transport, and platelet binding kinetics in arterial thrombosis. Biophys. J., 119 (10), 2102–2115 (2020).
  38. Blair S. C., Berge P. A., and Berryman J. G. Usingtwo‐point correlation functions to characterize microgeometry and estimate permeabilities of sandstones and porous glass. J. Geophys. Res.: Solid Earth, 101 (B9), 20359–20375 (1996).
  39. Ahmed M. U., Kaneva V., Loyau S., Nechipurenko D.,Receveur N., Le Bris M., Janus-Bell E., Didelot M., Rauch A., Susen S., Chakfé N., Lanza F., Gardiner E. E., Andrews R. K., Panteleev M., Gachet Ch., JandrotPerrus M., and Mangin P. H. Pharmacological blockade of glycoprotein VI promotes thrombus disaggregation in the absence of thrombin. Arterioscler. Thromb. Vasc. Biol., 40 (9), 2127–2142 (2020). doi: 10.1161/ATVBAHA.120.314301
  40. Nader E., Skinner S., Romana M., Fort R., Lemonne N.,Guillot N., Gauthier A., Antoine-Jonville S., Renoux C., Hardy-Dessources M.-D., Stauffer E., Joly Ph., Bertrand Y., and Connes P. Blood rheology: key parameters, impact on blood flow, role in sickle cell disease and effects of exercise. Front. Physiol., 10, 1329 (2019). doi: 10.3389/fphys.2019.01329
  41. Silvain J., Collet J. P., Nagaswami C., Beygui F., Edmondson K. E., Bellemain-Appaix A., Cayla G., Pena A., Brugier D., Barthelemy O., Montalescot G., and Weisel J. W. Composition of coronary thrombus in acute myocardial infarction. J. Am. Coll. Cardiol., 57 (12), 1359–1367 (2011).
  42. Wufsus A. R., Macera N. E., and Neeves K. B. The hydraulic permeability of blood clots as a function of fibrin and platelet density. Biophys. J., 104 (8), 1812– 1823 (2013).
  43. Davies C. N. The separation of airborne dust and particles. Inst. Mech. Eng. (Lond.), B1, 185–213 (1952).
  44. Ethier C. R. Flow through mixed fibrous porous materials. J. AIChE, 37, 1227–1236 (1991).

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