Fluid mechanics of blood clot formation

Annual Review of Fluid Mechanics

Volumn 47, Issue , 2015, Pages 377-403

  Fogelson, Aaron L ^a   Neeves, Keith B ^b  

^a UNIVERSITY OF UTAH   (United States)

^b Department of Metallurgical and Materials Engineering   (United States)

Author keywords

biorheology; biotransport; coagulation; Platelets; thrombosis

Indexed keywords

BLOOD; COAGULATION; DYNAMICS; FLUID DYNAMICS; FLUID MECHANICS; HYDRODYNAMICS; MECHANICAL PROPERTIES; PLATELETS;

BIORHEOLOGY; BIOTRANSPORT; BLOOD CLOT FORMATION; HYDRODYNAMIC FORCES; HYDRODYNAMIC STRESS; MECHANICAL CHARACTERISTICS; MEDIATED INTERACTION; THROMBOSIS;

TRANSPORT PROPERTIES;

BLOOD; COAGULATION; CONCENTRATION (COMPOSITION); FLUID DYNAMICS; FLUID MECHANICS; HYDRODYNAMICS; LIGAND; NUMERICAL MODEL; RHEOLOGY;

EID: 84961291395     PISSN: 00664189     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-fluid-010814-014513     Document Type: Review

References (148)

1. Aarts PA, Steendijk P, Sixma JJ, Heethaar RM. 1986. Fluid shear as a possible mechanism for platelet diffusivity in flowing blood. J. Biomech. 19:799-805
2. Aarts PA, van den Broek SA, Prins GW, Kuiken GD, Sixma JJ, Heethaar RM. 1988. Blood platelets are concentrated near the wall and red blood cells, in the center in flowing blood. Arteriosclerosis 8:819-24
3. Alexander-Katz A, Netz RR. 2008. Dynamics and instabilities of collapsed polymers in shear flow. Macro-molecules 41:3363-74
4. Alexander-Katz A, Schneider MF, Schneider SW, Wixforth A, Netz RR. 2006. Shear-flow-induced unfolding of polymeric globules. Phys. Rev. Lett. 97:138101
5. Andrews RK, Berndt MC. 2004. Platelet physiology and thrombosis. Thromb. Res. 114:447-53
6. Arya M, Anvari B, Romo GM, Cruz MA, Dong JF, et al. 2002a. Ultralarge multimers of von Willebrand factor form spontaneous high-strength bonds with the platelet glycoprotein Ib-IX complex: studies using optical tweezers. Blood 99:3971-77
7. Arya M, Lopez JA, Romo GM, Dong JF, McIntire LV, et al. 2002b. Measurement of the binding forces between von Willebrand factor and variants of platelet glycoprotein Ibα using optical tweezers. Lasers Surg. Med. 30:306-12
8. Broos K, Feys HB, DeMeyer SF, Vanhoorelbeke K, Deckmyn H. 2011. Platelets at workin primary hemosta-sis. Blood Rev. 25:155-67
9. Charoenphol P, Huang RB, Eniola-Adefeso O. 2010. Potential role of size and hemodynamics in the efficacy of vascular-targeted spherical drug carriers. Biomaterials 31:1392-402
10. Chatterjee MS, Purvis JE, Brass LF, Diamond SL. 2010. Pairwise agonist scanning predicts cellular signaling responses to combinatorial stimuli. Nat. Biotechnol. 28:727-32
11. Chauhan AK, Motto DG, Lamb CB, Bergmeier W, Dockal M, et al. 2006. Systemic antithrombotic effects of ADAMTS13. J. Exp. Med. 208:767-76
12. Chen H, Angerer JI, Napoleone M, Reininger AJ, Schneider SW, et al. 2013. Hematocrit and flow rate regulate the adhesion of platelets to von Willebrand factor. Biomicrofluidics 7:064113
13. Chien S. 1987. Red cell deformability and its relevance to blood flow. Annu. Rev. Physiol. 49:177-92
14. Colace TV, Diamond SL. 2013. Direct observation of von Willebrand factor elongation and fiber formation on collagen during acute whole blood exposure to pathological flow. Arterioscler. Thromb. Vasc. Biol. 33:105-13
15. Colace TV, Muthard RW, Diamond SL. 2012. Thrombus growth and embolism on tissue factor-bearing collagen surfaces under flow: role of thrombin with and without fibrin. Arterioscler. Thromb. Vasc. Biol. 32:1466-76
16. Colman RW, Walsh PN. 1987. Mechanisms of platelet aggregation. In Hemostasis and Thrombosis: Basic Principles and Clinical Practice, ed. RW Colman, J Hirsh, VJ Marder, EW Salzman, pp. 594-605. Philadelphia: J.B. Lippincott
17. Crawley JTB, de Groot R, Xiang Y, Luken BM, Lane DA. 2011. von Willebrand factor unraveling the scissile bond: how ADAMTS-13 recognizes and cleaves. Blood 118:3212-21
18. Crowl L, Fogelson AL. 2011. Analysis of mechanisms for platelet near-wall excess under arterial blood flow conditions. J. Fluid Mech. 676:348-75
19. Dayananda KM, Singh I, Mondal N, Neelamegham S. 2010. von Willebrand factor self-association on platelet GPIbαunder hydrodynamic shear: effect on shear-induced platelet activation. Blood 116:3990-98
20. De Ceunynck K, Rocha S, Feys HB, De Meyer SF, Ujii H, et al. 2011. Local elongation of endothelial cell-anchored von Willebrand factor strings precedes ADAMTS13 protein-mediated proteolysis. J. Biol. Chem. 286:36361-67
21. Doggett TA, Girdhar G, Lawshe A, Schmidtke DW, Laurenzi IJ, et al. 2002. Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIbα-vWF tether bond. Biophys. J. 83:184-205
22. Dong JF. 2005. Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions. J. Thromb. Haemost. 3:1710-16
23. Doshi N, Orje JN, Molins B, Smith JW, Mitragotri S, Ruggeri ZM. 2012. Platelet mimetic particles for targeting thrombi in flowing blood. Adv. Mater. 24:3864-69
24. Eckstein EC, Bailey DG, Shapiro AH. 1977. Self-diffusion of particles in shear flow of a suspension. J. Fluid Mech. 79:191-208
25. Eckstein EC, Belgacem F. 1991. Model of platelet transport in flowing blood with drift and diffusion terms. Biophys. J. 60:53-69
26. Eckstein EC, Tilles AW, Millero FJ III. 1988. Conditions for the occurrence of large near-wall excesses of small particles during blood flow. Microvasc. Res. 36:31-39
27. Filipovic N, Kojic M, Tsuda A. 2008. Modelling thrombosis using dissipative particle dynamics method. Philos. Trans. R. Soc. A 366:3265-79
28. Flamm MH, Colace T, Chatterjee M, Jing H, Zhou S, et al. 2012. Multiscale prediction of patient-specific platelet function under flow. Blood 120:190-98
29. Flamm MH, Diamond SL. 2012. Multiscale systems biology and physics of thrombosis under flow. Ann. Biomed. Eng. 40:2355-64
30. Flamm MH, Sinno T, Diamond SL. 2011. Simulation of aggregating particles in complex flows by the lattice kinetic Monte Carlo method. J. Chem. Phys. 134:034905
31. Fogelson AL. 1984. A mathematical model and numerical method for studying platelet adhesion and aggregation during blood clotting. J. Comput. Phys. 56:111-34
32. Fogelson AL. 1992. Continuum models of platelet aggregation: formulation and mechanical properties. SIAM J. Appl. Math. 52:1089-110
33. Fogelson AL. 1993. Continuum models of platelet aggregation: mechanical properties and chemically-induced phase transitions. Contemp. Math. 141:279-94
34. Fogelson AL, Guy RD. 2004. Platelet-wall interactions in continuum models of platelet aggregation: formulation and numerical solution. Math. Med. Biol. 21:293-334
35. Fogelson AL, Guy RD. 2008. Immersed-boundary-type models of intravascular platelet aggregation. Comput. Methods Appl. Mech. Eng. 197:2087-104
36. Fogelson AL, Kuharsky AL, Yu H. 2003. Computational modeling of blood clotting: coagulation and three-dimensional platelet aggregation. In Polymer and Cell Dynamics: Multiscale Modeling and Numerical Simulations, ed. W Alt, M Chaplain, M Griebel, J Lenz, pp. 145-54. Basel: Birkhäuser-Verlag
37. Fogelson AL, Tania N. 2005. Coagulation under flow: the influence of flow-mediated transport on the initiation and inhibition of coagulation. Pathophysiol. Haemost. Thromb. 34:91-108
38. Freund JB. 2013. Numerical simulation of flowing blood cells. Annu. Rev. Fluid Mech. 46:67-95
39. Furie B, Furie B. 2005. Thrombus formation in vivo. J. Clin. Investig. 115:3355-62
40. Galbusera M, Zoja C, Donadelli R, Paris S, Morigi M, et al. 1997. Fluid shear stress modulates von Willebrand factor release from human vascular endothelium. Blood 90:1558-64
41. Gemmell CH, Nemerson Y, Turitto V. 1990. The effects of shear rate on the enzymatic activity of the tissue factor-factor VIIa complex. Microvasc. Res. 40:327-40
42. Goldsmith HL. 1971. Red cell motions and wall interactions in tube flow. Fed. Proc. 30:1578-90
43. Goto S, Salomon DR, Ikeda Y, Ruggeri ZM. 1995. Characterization of the unique mechanism mediating the shear-dependent binding of soluble von Willebrand factor to platelets. J. Biol. Chem. 270:23352-61
44. Grabowski EF, Friedman LI, Leonard EF. 1972. Effects of shear rate on the diffusion and adhesion of blood platelets to a foreign surface. Ind. Eng. Chem. Fundam. 11:224-32
45. Guy RD, Fogelson AL, Keener JP. 2007. Modeling fibrin gel formation in a shear flow. Math. Med. Biol. 24:111-30
46. Hathcock J, Nemerson Y. 2004. Platelet deposition inhibits tissue factor activity: in vitro clots are impermeable to factor Xa. Blood 104:123-27
47. Haynes LM, Dubief YC, Orfeo T, Mann KG. 2011. Dilutional control of prothrombin activation at physiologically relevant shear rates. Biophys. J. 100:765-73
48. Hoffman M, Monroe DM. 2001. A cell-based model of hemostasis. Thromb. Haemost. 85:958-65
49. Jackson SP. 2007. The growing complexity of platelet aggregation. Blood 109:5087-95
50. Jackson SP, Nesbitt WS, Kulkarni S. 2003. Signaling events underlying thrombus formation. J. Thromb. Haemost. 1:1602-12
51. Jackson SP, Nesbitt WS, Westein E. 2009. Dynamics of platelet thrombus formation. J. Thromb. Haemost. 7:17-20
52. Jesty J, Nemerson Y. 1995. The pathways of blood coagulation. In Williams Hematology, ed. E Beutler, M Lichtman, B Coller, pp. 1227-38. New York: McGraw-Hill. 5th ed.
53. Jin SY, Skipwith CG, Shang D, Zheng XL. 2009. von Willebrand factor cleaved from endothelial cells by ADAMTS-13 remains ultralarge in size. J. Thromb. Haemost. 7:1749-52
54. Kamada H, Imai Y, Nakamura M, Ishikawa T, Yamaguchi T. 2013. Computational study on thrombus formation regulated by platelet glycoprotein and blood flow shear. Microvasc. Res. 89:95-106
55. Kamada H, Tsubota K, Nakamura M, Wada S, Ishikawa T, Yamaguchi T. 2010. A three-dimensional particle simulation of the formation and collapse of a primary thrombus. Int. J. Numer. Methods Biomed. Eng. 26:488-500
56. Kasirer-Friede A, Kahn ML, Shattil SJ. 2014. Platelet integrins and immunoreceptors. Immunol. Rev. 218:247-64
57. Kastrup C, Shen F, Runyon M, Ismagilov R. 2007. Characterization of the threshold response of initiation of blood clotting to stimulus patch size. Biophys. J. 93:2969-77
58. Kim J, Zhang CZ, Zhang X, Springer TA. 2010. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466:992-95
59. Kim OV, Xu Z, Rosen ED, Alber MS. 2013. Fibrin networks regulate protein transport during thrombus development. PLoS Comput. Biol. 9:e1003095
60. Kuharsky AL, Fogelson AL. 2001. Surface-mediated control of blood coagulation: the role of binding site densities and platelet deposition. Biophys. J. 80:1050-74
61. Kumar A, Graham MD. 2012. Mechanism of margination in confined flows of blood and other multicompo-nent suspensions. Phys. Rev. Lett. 109:108102
62. Leiderman K, Fogelson AL. 2011. Grow with the flow: a spatial-temporal model of platelet deposition and blood coagulation under flow. Math. Med. Biol. 28:47-84
63. Leiderman K, Fogelson AL. 2013. The influence of hindered transport on the development of platelet thrombi under flow. Bull. Math. Biol. 75:1255-83
64. Leighton D, Acrivos A. 1987. The shear-induced migration of particles in concentrated suspensions. J. Fluid Mech. 181:415-39
65. Li Z, Delaney MK, O'Brien KA, Du X. 2010. Signaling during platelet adhesion and activation. Arterioscler. Thromb. Vasc. Biol. 30:2341-49
66. Litvinov RI, Barsegov V, Schissler AJ, Fisher AR, Bennett JS, et al. 2011. Dissociation of bimolecular αIIbβ3-fibrinogen complex under a constant tensile force. Biophys. J. 100:165-73
67. Litvinov RI, Mekler A, Shuman H, Bennett JS, Barsegov V, Weisel JW. 2012. Resolving two-dimensional kineticsofthe integrinαIIbβ3-fibrinogeninteractions using binding-unbinding correlation spectroscopy. J. Biol. Chem. 287:35275-85
68. Mackman N. 2012. New insights into the mechanisms of venous thrombosis. J. Clin. Investig. 122:2331-36
69. Mann KG, Nesheim ME, Church WR, Haley P, Krishnaswamy S. 1990. Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 76:1-16
70. Matsui H, Sugimoto M, Mizuno T, Tsuji S, Miyata S, et al. 2002. Distinct and concerted functions of von Willebrand factor and fibrinogen in mural thrombus growth under high shear flow. Blood 100:3604-10
71. Maxwell MJ, Westein E, Nesbitt WS, Giuliano S, Dopheide SM, Jackson SP. 2007. Identification of a 2-stage platelet aggregation process mediating shear-dependent thrombus formation. Blood 109:566-76
72. Miura S, Li CQ, Cao H, Wang H, Wardell MR, Sadler JE. 2000. Interaction of von Willebrand factor domain A1 with platelet glycoprotein Ibα-(1-289). J. Biol. Chem. 275:7539-46
73. Mizuno T, Sugimoto M, Matsui H, Hamada M, Shida Y, Yoshioka A. 2008. Visual evaluation of blood coagulation during mural thrombogenesis under high shear blood flow. Thromb. Res. 121:855-64
74. Moake JL, Turner NA, Stathopoulos NA, Nolasco LH, Hellums JD. 1986. Involvement of large plasma von Willebrand factor (vWF) multimers and unusually large vWF forms derived from endothelial cells in shear stress-induced platelet aggregation. J. Clin. Investig. 78:1456-61
75. Moake JL, Turner NA, Stathopoulos NA, Nolasco LH, Hellums JD. 1988. Shear-induced platelet aggregation can be mediated by vWF released from platelets, as well as by exogenous large or unusually large vWF multimers, requires adenosine diphosphate, and is resistant to aspirin. Blood 71:1366-74
76. Mody NA, King MR. 2008a. Platelet adhesive dynamics. Part I: characterization of platelet hydrodynamic collisions and wall effects. Biophys. J. 95:2539-55
77. Mody NA, King MR. 2008b. Platelet adhesive dynamics. Part II: high shear-induced transient aggregation via GP1bα-vWF-GP1bαbridging. Biophys. J. 95:2556-74
78. Mori D, Yano K, Tsubota K, Ishikawa T, Wada S, Yamaguchi T. 2008. Simulation of platelet adhesion and aggregation regulated by fibrinogen and von Willebrand factor. Thromb. Haemost. 99:108-15
79. Narsimhan V, Zhao H, Shaqfeh ESG. 2013. Coarse-grained theory to predict the concentration distribution of red blood cells in wall-bounded Couette flow at zero Reynolds number. Phys. Fluids 25:061901
80. Neeves KB, Illing DAR, Diamond SL. 2010. Thrombin flux and wall shear rate regulate fibrin fiber deposition state during polymerization under flow. Biophys. J. 98:1344-52
81. Neeves KB, Onasoga AA, Hansen RR, Lilly JJ, Venckunaite D, et al. 2013. Sources of variability in platelet accumulation on type 1 fibrillar collagen in microfluidic flow assays. PLoS ONE 8:e54680
82. Okorie UM, Denney WS, Chatterjee MS, Neeves KB, Diamond SL. 2008. Determination of surface tissue factor thresholds that trigger coagulation at venous and arterial shear rates: Amplification of 100 fM circulating tissue factor requires flow. Blood 111:3507-13
83. Onasoga-Jarvis AA, Leiderman K, Fogelson AL, Wang M, Manco-Johnson MJ, et al. 2013. The effect of factor VIII deficiencies and replacement and bypass therapies on thrombus formation under venous flow conditions in microfluidic and computational models. PLoS ONE 8:e78732
84. Onasoga-Jarvis AA, Puls TJ, O'Brien SK, Kuang L, Liang HJ, Neeves KB. 2014. Thrombin generation and fibrin formation under flow on biomimetic tissue factor-rich surfaces. J. Thromb. Haemost. 12:373-82
85. Peterson DM, Stathopoulos NA, Giorgio TD, Hellums JD, Moake JL. 1987. Shear-induced platelet aggregation requires von Willebrand factor and platelet membrane glycoproteins Ib and IIb-IIIa. Blood 69:625-28
86. Phillips RJ, Armstrong RC, Brown RA, Graham AL, Abbott JR. 1992. A constitutive equation for concentrated suspensions that accounts for shear-induced particle migration. Phys. Fluids 4:30-40
87. Pivkin IV, Richardson PD, Karniadakis G. 2006. Blood flow velocity effects and role of activation delay time on growth and form of platelet thrombi. Proc. Natl. Acad. Sci. USA 103:17164-69
88. Pivkin IV, Richardson PD, Karniadakis G. 2009. Effect of red blood cells on platelet aggregation. IEEE Eng. Med. Biol. Mag. 28:32-37
89. Popel AS, Johnson PC. 2005. Microcirculation and hemorheology. Annu. Rev. Fluid Mech. 37:43-69
90. Pries AR, Neuhaus D, Gaehtgens P. 1992. Blood viscosity in tube flow: dependence on diameter and hemat-ocrit. Am. J. Physiol. 263:H1770-78
91. Reasor DA, Mehrabadi M, Ku DN, Aidun CK. 2012. Determination of critical parameters in platelet margina-tion. Ann. Biomed. Eng. 41:238-49
92. Repke D, Gemmell CH, Guha A, Turitto VT, Broze GJ, Nemerson Y. 1990. Hemophilia as a defect of the tissue factor pathway of blood coagulation: effect of factors VIII and IX on factor X activation in a continuous-flow reactor. Proc. Natl. Acad. Sci. USA 87:7623-27
93. Ruggeri ZM. 2009. Platelet adhesion under flow. Microcirculation 16:58-83
94. Ruggeri ZM, Dent JA, Saldivar E. 1999. Contribution of distinct adhesive interactions to platelet aggregation in flowing blood. Blood 94:172-78
95. Ruggeri ZM, Orje JN, Habermann R, Federici AB, Reininger AJ. 2006. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108:1903-10
96. Savage B, Almus-Jacobs F, Ruggeri ZM. 1998. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 94:657-66
97. Savage B, Saldivar E, Ruggeri ZM. 1996. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84:289-97
98. Savage B, Sixma JJ, Ruggeri ZM. 2002. Functional self-association of von Willebrand factor during platelet adhesion under flow. Proc. Natl. Acad. Sci. USA 99:425-30
99. Schneider SW, Nuschele S, Wixforth A, Gorzelanny C, Alexander-Katz A, et al. 2007. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc. Natl. Acad. Sci. USA 104:7899-903
100. Shankaran H, Alexandridis P, Neelamegham S. 2003. Aspects of hydrodynamic shear regulating shear-induced platelet activation and self-association of von Willebrand factor in suspension. Blood 101:2637-45
101. Shankaran H, Neelamegham S. 2004. Hydrodynamic forces applied on intercellular bonds, soluble molecules, and cell-surface receptors. Biophys. J. 86:576-88
102. Shen F, Kastrup CJ, Liu Y, Ismagilov RF. 2008. Threshold response of initiation of blood coagulation by tissue factor in patterned microfluidic capillaries is controlled by shear rate. Arterioscler. Thromb. Vasc. Biol. 28:2035-41
103. Shim K, Anderson PJ, Tuley EA, Wiswall E, Sadler EJ. 2008. Platelet-VWF complexes are preferred substrates of ADAMTS13 under fluid shear stress. Blood 111:651-57
104. Sing CE, Alexander-Katz A. 2010. Elongational flow induces unfolding of von Willebrand factor at physiological flow rates. Biophys. J. 98:L35-37
105. Sing CE, Alexander-Katz A. 2011. Dynamics of collapsed polymers under the simultaneous influence of elongational and shear flows. J. Chem. Phys. 135:014902
106. Skorczewski T, Erickson LC, Fogelson AL. 2013. Platelet motion near a vessel wall or thrombus surface in two-dimensional whole blood simulations. Biophys. J. 104:1764-72
107. Skorczewski T, Griffith BE, Fogelson AL. 2014. Multi-bond models for platelet adhesion and cohesion. Contemp. Math. In press
108. Smart JR, Leighton DT. 1991. Measurement of the drift of a droplet due to the presence of a plane. Phys. Fluids A 3:21-28
109. Spiel AO, Gilbert JC, Jilma B. 2008. von Willebrand factor in cardiovascular disease: focus on acute coronary syndromes. Circulation 117:1449-59
110. Stalker TJ, Traxler EA, Wu J, Wannemacher KM, Cermignano SL, et al. 2013. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood 121:1875-85
111. Tangelder GJ, Slaaf DW, Teirlinck HC, Alewijnse R, Reneman RS. 1982. Localization within a thin optical section of fluorescent blood platelets flowing in a microvessel. Microvasc. Res. 23:214-30
112. Tangelder GJ, Teirlinck HC, Slaaf DW, Reneman RS. 1985. Distribution of blood platelets flowing in arterioles. Am. J. Physiol. 248:H318-23
113. Thomas WE, Vogel V, Sokurenko E. 2008. Biophysics of catch bonds. Annu. Rev. Biophys. 37:399-416
114. Thompson AJ, Mastria EM, Eniola-Adefeso O. 2013. The margination propensity of ellipsoidal micro/nanoparticles to the endothelium in human blood flow. Biomaterials 34:5863-71
115. Tilles AW, Eckstein EC. 1987. The near-wall excess of platelet-sized particles in blood flow: its dependence on hematocrit and wall shear rate. Microvasc. Res. 33:211-23
116. Tosenberger A, Ataullakhanov F, Bessonov N, Panteleev M, Tokarev A, Volpert V. 2013. Modelling of thrombus growth in flow with a DPD-PDE method. J. Theor. Biol. 337:30-41
117. Turitto VT, Baumgartner HR. 1975a. Platelet deposition on subendothelium exposed to flowing blood: mathematical analysis of physical parameters. ASAIO J. 21:593-601
118. Turitto VT, Baumgartner HR. 1975b. Platelet interaction with subendothelium in a perfusion system: physical role of red blood cells. Microvasc. Res. 9:335-44
119. Turitto VT, Benis AM, Leonard EF. 1972. Platelet diffusion in flowing blood. Ind. Eng. Chem. Fundam. 11:216-23
120. Turitto VT, Goldsmith HL. 1996. Rheology, transport and thrombosis in the circulation. In Textbook of Vascular Medicine, ed. J Loscalzo, M Creager, V Dzau, pp. 141-84. New York: Little, Brown. 2nd ed.
121. Turitto VT, Weiss HJ. 1980. Red blood cells: their dual role in thrombus formation. Science 207:541-43
122. Turner NA, Nolasco L, Moake JL. 2012. Generation and breakdown of soluble ultralarge von Willebrand factor multimers. Semin. Thromb. Hemost. 38:38-46
123. Turner NA, Nolasco L, Ruggeri ZM, Moake JL. 2009. Endothelial cell ADAMTS-13 and VWF: production, release, and VWF string cleavage. Blood 114:5102-11
124. Wang NT, Fogelson AL. 1999. Computational methods for continuum models of platelet aggregation. J. Comput. Phys. 151:649-75
125. Wang W, Diacovo TG, Chen J, Freund JB, King MR. 2013a. Simulation of platelet, thrombus and erythrocyte hydrodynamic interactions in a 3D arteriole with in vivo comparison. PLoS ONE 8:e76949
126. Wang W, King MR. 2012. Multiscale modeling of platelet adhesion and thrombus growth. Ann. Biomed. Eng. 40:2345-54
127. Wang W, Mody NA, King MR. 2013b. Multiscale model of platelet translocation and collision. J. Comput. Phys. 244:223-35
128. Watts T, Barigou M, Nash GB. 2013. Comparative rheology of the adhesion of platelets and leukocytes from flowing blood: Why are platelets so small? Am. J. Physiol. 304:H1483-94
129. Weisel JW. 2005. Fibrinogen and fibrin. Adv. Protein Chem. 70:247-99
130. Weiss HJ, Turitto VT, Baumgartner HR. 1986. Role of shear rate and platelets in promoting fibrin formation on rabbit subendothelium: studies utilizing patients with quantitative and qualitative platelet defects. J. Clin. Investig. 78:1072-82
131. Welsh JD, Colace TV, Muthard RW, Stalker TJ, Brass LF, Diamond SL. 2012. Platelet-targeting sensor reveals thrombin gradients within blood clots forming in microfluidic assays and in mouse. J. Thromb. Haemost. 10:2344-53
132. Westein E, van der Meerc A, Kuijpers MJE, Frimat JP, van den Berg A, Heemskerk JWM. 2013. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc. Natl. Acad. Sci. USA 110:1357-62
133. Woldhuis B, Tangelder GJ, Slaaf DW, Reneman RS. 1992. Concentration profile of blood platelets differs in arterioles and venules. Am. J. Physiol. 262:H1217-23
134. Wu T, Lin J, Cruz MA, Dong JF, Zhu C. 2010. Force-induced cleavage of single VWFA1A2A3 tridomains by ADAMTS-13. Blood 115:370-78
135. Wufsus AR, Macera NE, Neeves KB. 2013. The hydraulic permeability of blood clots as a function of fibrin and platelet density. Biophys. J. 104:1812-23
136. Xu C, Wootton D. 2004. Platelet near-wall excess in porcine whole blood in artery-sized tubes under steady and pulsatile flow conditions. Biorheology 41:113-25
137. Xu Z, Chen N, Kamocka MM, Rosen ED, Alber M. 2008. A multiscale model of thrombus development. J. R. Soc. Interface 5:705-22
138. Xu Z, Chen N, Shadden SC, Marsden JE, Kamocka MM, et al. 2009. Study of blood flow impact on growth of thrombi using a multiscale model. Soft Matter 5:769-79
139. Xu Z, Kamocka MM, Alber M, Rosen ED. 2011. Computational approaches to studying thrombus development. Aterioscler. Thromb. Vasc. Biol. 31:500-5
140. Xu Z, Lioi J, Mu J, Kamocka MM, Liu X, et al. 2010. A multiscale model of venous thrombus formation with surface-mediated control of blood coagulation cascade. Biophys. J. 98:1723-32
141. Yago T, Lou J, Wu T, Yang J, Miner J, et al. 2008. Platelet glycoprotein Ibαforms catch bonds with human WT vWF but not with type 2B von Willebrand disease v WF. J. Clin. Investig. 118:3195-207
142. Yeh C, Calvez AC, Eckstein EC. 1994. An estimated shape function for drift in a platelet-transport model. Biophys. J. 67:1252-59
143. Ying J, Ling Y, Westfield L, Sadler J, Shao JY. 2010. Unfolding the A2 domain of von Willebrand factor with the optical trap. Biophys. J. 98:1685-93
144. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA. 2009. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 324:1330-34
145. Zhao H, Shaqfeh ESG, Narsimhan V. 2012. Shear-induced particle migration and margination in a cellular suspension. Phys. Fluids 24:011902
146. Zhao R, Kameneva M, Antaki J. 2007. Investigation of platelet margination phenomena at elevated shear stress. Biorheology 44:161-77
147. Zhou Z, Nguyen TC, Guchhait P, Dong JF. 2010. Von Willebrand factor, ADAMTS-13, and thrombotic thrombocytopenic purpura. Semin. Thromb. Hemost. 36:71-81
148. Zydney AL, Colton CK. 1988. Augmented solute transport in the shear flow of a concentrated suspension. Physicochem. Hydrodyn. 10:77-96