Transport physics and biorheology in the setting of hemostasis and thrombosis

Journal of Thrombosis and Haemostasis

Volumn 14, Issue 5, 2016, Pages 906-917

  Brass, L F ^a   Diamond, S L ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Institute for Medicine and Engineering   (United States)

Author keywords

Fibrin; Hemodynamics; Platelet; Shear stress; Thrombin; Von Willebrand factor

Indexed keywords

ADENOSINE DIPHOSPHATE; BLOOD CLOTTING FACTOR 11A; BLOOD CLOTTING FACTOR 12A; BLOOD CLOTTING FACTOR 8A; BLOOD CLOTTING FACTOR 9A; COLLAGEN; FIBRIN; FIBRINOGEN; PADGEM PROTEIN; POLYPHOSPHATE; THROMBIN; THROMBOPLASTIN; THROMBOXANE; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ARTERY BLOOD FLOW; ARTERY THROMBOSIS; BLOOD CLOTTING; BLOOD COMPONENT; BLOOD RHEOLOGY; BLOOD VESSEL PERMEABILITY; CYTOARCHITECTURE; ENZYME ACTIVATION; ENZYME RELEASE; ENZYME SUBSTRATE; ERYTHROCYTE KINETICS; FIBRIN FORMATION; FIBRIN POLYMERIZATION; FLOW RATE; HEMOSTASIS; HUMAN; MICROFLUIDICS; NONHUMAN; POROSITY; PRIORITY JOURNAL; REVIEW; SHEAR RATE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; TRANSPORT KINETICS; VON WILLEBRAND DISEASE; ANIMAL; BLOOD FLOW VELOCITY; CHEMISTRY; DIFFUSION; DRUG EFFECTS; FIBRINOLYSIS; FLOW KINETICS; MECHANICAL STRESS; METABOLISM; MOUSE; PATHOPHYSIOLOGY; STENOSIS, OCCLUSION AND OBSTRUCTION; THROMBOCYTE; THROMBOCYTE RICH PLASMA; THROMBOSIS;

ANIMALS; BLOOD COAGULATION; BLOOD FLOW VELOCITY; BLOOD PLATELETS; CONSTRICTION, PATHOLOGIC; DIFFUSION; FACTOR IXA; FACTOR VIIIA; FIBRIN; FIBRINOLYSIS; HEMOSTASIS; HUMANS; MICE; PLATELET ACTIVATION; PLATELET ADHESIVENESS; PLATELET-RICH PLASMA; POLYPHOSPHATES; POROSITY; RHEOLOGY; STRESS, MECHANICAL; THROMBIN; THROMBOPLASTIN; THROMBOSIS; VON WILLEBRAND FACTOR;

EID: 84963690617     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13280     Document Type: Review

References (124)

1. Goldsmith HL, Turitto VT. Rheological aspects of thrombosis and haemostasis: basic principles and applications. ICTH-Report-Subcommittee on Rheology of the International Committee on Thrombosis and Haemostasis. Thromb Haemost 1986; 55: 415-35.
2. Kefayati S, Holdsworth DW, Poepping TL. Turbulence intensity measurements using particle image velocimetry in diseased carotid artery models: effect of stenosis severity, plaque eccentricity, and ulceration. J Biomech 2014; 47: 253-63.
3. Arzani A, Dyverfeldt P, Ebbers T, Shadden SC. In vivo validation of numerical prediction for turbulence intensity in an aortic coarctation. Ann Biomed Eng 2012; 40: 860-70.
4. Sotiropoulos F, Borazjani I. A review of state-of-the-art numerical methods for simulating flow through mechanical heart valves. Med Biol Eng Comput 2009; 47: 245-56.
5. Sivanesan S, How TV, Black RA, Bakran A. Flow patterns in the radiocephalic arteriovenous fistula: an in vitro study. J Biomech 1999; 32: 915-25.
6. Davies PF, Civelek M, Fang Y, Fleming I. The atherosusceptible endothelium: endothelial phenotypes in complex haemodynamic shear stress regions in vivo. Cardiovasc Res 2013; 99: 315-27.
7. Ohayon J, Finet G, Le Floc'h S, Cloutier G, Gharib AM, Heroux J, Pettigrew RI. Biomechanics of atherosclerotic coronary plaque: site, stability and in vivo elasticity modeling. Ann Biomed Eng 2013; 42: 269-79.
8. Bajd F, Vidmar J, Fabjan A, Blinc A, Kralj E, Bizjak N, Serša I. Impact of altered venous hemodynamic conditions on the formation of platelet layers in thromboemboli. Thromb Res 2012; 129: 158-63.
9. Fogelson AL, Neeves KB. Fluid mechanics of blood clot formation. Annu Rev Fluid Mech 2015; 47: 377-403.
10. Yeh C, Eckstein EC. Transient lateral transport of platelet-sized particles in flowing blood suspensions. Biophys J 1994; 66: 1706-16.
11. Vahidkhah K, Diamond SL, Bagchi P. Platelet dynamics in three-dimensional simulation of whole blood. Biophys J 2014; 106: 2529-40.
12. Nanne EE, Aucoin CP, Leonard EF. Shear rate and hematocrit effects on the apparent diffusivity of urea in suspensions of bovine erythrocytes. ASAIO J 2010; 56: 151-6.
13. Li R, Elmongy H, Sims C, Diamond S. Ex vivo recapitulation of trauma-induced coagulopathy and preliminary assessment of trauma patient platelet function under flow usign microfluidic technology. J Trauma Acute Care Surg 2016; 80: 440-9.
14. Lei H, Fedosov DA, Caswell B, Karniadakis GE. Blood flow in small tubes: quantifying the transition to the non-continuum regime. J Fluid Mech 2013; 722: 214-39.
15. Stalker TJ, Traxler EA, Wu J, Wannemacher KM, Cermignano SL, Voronov R, Diamond SL, Brass LF. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood 2013; 121: 1875-85.
16. Stalker TJ, Welsh JD, Tomaiuolo M, Wu J, Colace TV, Diamond SL, Brass LF. A systems approach to hemostasis: 3. Thrombus consolidation regulates intrathrombus solute transport and local thrombin activity. Blood 2014; 124: 1824-31.
17. Brass LF, Zhu L, Stalker TJ. Minding the gaps to promote thrombus growth and stability. J Clin Invest 2005; 115: 3385-92.
18. Voronov RS, Stalker TJ, Brass LF, Diamond SL. Simulation of intrathrombus fluid and solute transport using in vivo clot structures with single platelet resolution. Ann Biomed Eng 2013; 41: 1297-307.
19. Diamond SL. Engineering design of optimal strategies for blood clot dissolution. Annu Rev Biomed Eng 1999; 1: 427-62.
20. Welsh JD, Stalker TJ, Voronov R, Muthard RW, Tomaiuolo M, Diamond SL, Brass LF. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets. Blood 2014; 124: 1808-15.
21. Hathcock JJ, Nemerson Y. Platelet deposition inhibits tissue factor activity: in vitro clots are impermeable to factor Xa. Blood 2004; 104: 123-7.
22. Colace TV, Muthard RW, Diamond SL. Thrombus growth and embolism on tissue factor-bearing collagen surfaces under flow: role of thrombin with and without fibrin. Arterioscler Thromb Vasc Biol 2012; 32: 1466-76.
23. Welsh JD, Colace TV, Muthard RW, Stalker TJ, Brass LF, Diamond SL. Platelet-targeting sensor reveals thrombin gradients within blood clots forming in microfluidic assays and in mouse. J Thromb Haemost 2012; 10: 2344-53.
24. Tomaiuolo M, Stalker TJ, Welsh JD, Diamond SL, Sinno T, Brass LF. A systems approach to hemostasis: 2. Computational analysis of molecular transport in the thrombus microenvironment. Blood 2014; 124: 1816-23.
25. Flamm MH, Colace TV, Chatterjee MS, Jing H, Zhou S, Jaeger D, Brass LF, Sinno T, Diamond SL. Multiscale prediction of patient-specific platelet function under flow. Blood 2012; 120: 190-8.
26. Muthard RW, Diamond SL. Blood clots are rapidly assembled hemodynamic sensors: flow arrest triggers intraluminal thrombus contraction. Arterioscler Thromb Vasc Biol 2012; 32: 2938-45.
27. Okorie UM, Denney WS, Chatterjee MS, Neeves KB, Diamond SL. 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 2008; 111: 3507-13.
28. Leiderman K, Fogelson AL. Grow with the flow: a spatial-temporal model of platelet deposition and blood coagulation under flow. Math Med Biol 2011; 28: 47-84.
29. Muthard RW, Diamond SL. Side view thrombosis microfluidic device with controllable wall shear rate and transthrombus pressure gradient. Lab Chip 2013; 13: 1883-91.
30. Colace TV, Fogarty PF, Panckeri KA, Li R, Diamond SL. Microfluidic assay of hemophilic blood clotting: distinct deficits in platelet and fibrin deposition at low factor levels. J Thromb Haemost 2014; 12: 147-58.
31. Li R, Panckeri KA, Fogarty PF, Diamond SL. Recombinant factor VIIa enhances platelet deposition from flowing haemophilic blood but requires the contact pathway to promote fibrin deposition. Haemophilia 2014; 21: 266-74.
32. Onasoga-Jarvis AA, Leiderman K, Fogelson AL, Wang M, Manco-Johnson MJ, Di Paola JA, Neeves KB. 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 2013; 8: e78732.
33. Swieringa F, Kuijpers MJE, Lamers MME, van der Meijden PEJ, Heemskerk JWM. Rate-limiting roles of the tenase complex of factors VIII and IX in platelet procoagulant activity and formation of platelet-fibrin thrombi under flow. Haematologica 2015; 100: 748-56.
34. Alevriadou BR, Moake JL, Turner NA, Ruggeri ZM, Folie BJ, Phillips MD, Schreiber AB, Hrinda ME, McIntire LV. Real-time analysis of shear-dependent thrombus formation and its blockade by inhibitors of von Willebrand factor binding to platelets. Blood 1993; 81: 1263-76.
35. Goto S, Ikeda Y, Saldívar E, Ruggeri ZM. Distinct mechanisms of platelet aggregation as a consequence of different shearing flow conditions. J Clin Invest 1998; 101: 479-86.
36. Doggett TA, Girdhar G, Lawshe A, Schmidtke DW, Laurenzi IJ, Diamond SL, Diacovo TG. Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIb(alpha)-vWF tether bond. Biophys J 2002; 83: 194-205.
37. Doggett TA, Girdhar G, Lawshe A, Miller JL, Laurenzi IJ, Diamond SL, Diacovo TG. Alterations in the intrinsic properties of the GPIbα-VWF tether bond define the kinetics of the platelet-type von Willebrand disease mutation, Gly233Val. Blood 2003; 102: 152-60.
38. Chen J, Zhou H, Diacovo A, Zheng XL, Emsley J, Diacovo TG. Exploiting the kinetic interplay between GPIbα-VWF binding interfaces to regulate hemostasis and thrombosis. Blood 2014; 124: 3799-807.
39. Hollestelle MJ, Loots CM, Squizzato A, Renné T, Bouma BJ, de Groot PG, Lenting PJ, Meijers JCM, Gerdes VEA. Decreased active von Willebrand factor level owing to shear stress in aortic stenosis patients. J Thromb Haemost 2011; 9: 953-8.
40. Blackshear JL, Wysokinska EM, Safford RE, Thomas CS, Shapiro BP, Ung S, Stark ME, Parikh P, Johns GS, Chen D. Shear stress-associated acquired von Willebrand syndrome in patients with mitral regurgitation. J Thromb Haemost 2014; 12: 1966-74.
41. Crow S, Chen D, Milano C, Thomas W, Joyce L, Piacentino V, Sharma R, Wu J, Arepally G, Bowles D, Rogers J, Villamizar-Ortiz N. Acquired von Willebrand syndrome in continuous-flow ventricular assist device recipients. Ann Thorac Surg 2010; 90: 1263-9; discussion 1269.
42. Rauch A, Legendre P, Christophe OD, Goudemand J, van Belle E, Vincentelli A, Denis CV, Susen S, Lenting PJ. Antibody-based prevention of von Willebrand factor degradation mediated by circulatory assist devices. Thromb Haemost 2014; 112: 1014-23.
43. Bartoli CR, Kang J, Restle DJ, Zhang DM, Shabahang C, Acker MA, Atluri P. Inhibition of ADAMTS-13 by doxycycline reduces von Willebrand Factor Degradation during supraphysiological shear stress: therapeutic implications for left ventricular assist device-associated bleeding. JACC Heart Fail 2015; 3: 860-9.
44. Li R, Fries S, Li X, Grosser T, Diamond SL. Microfluidic assay of platelet deposition on collagen by perfusion of whole blood from healthy individuals taking aspirin. Clin Chem 2013; 59: 1195-204.
45. Li R, Diamond SL. Detection of platelet sensitivity to inhibitors of COX-1, P2Y, and P2Y using a whole blood microfluidic flow assay. Thromb Res 2013; 3848: 515-8.
46. Zhu S, Diamond SL. Contact activation of blood coagulation on a defined kaolin/collagen surface in a microfluidic assay. Thromb Res 2014; 134: 1335-43.
47. Zhu S, Travers RJ, Morrissey JH, Diamond SL. FXIa and platelet polyphosphate as therapeutic targets during human blood clotting on collagen/tissue factor surfaces under flow. Blood 2015; 126: 1494-502.
48. Chatterjee MS, Denney WS, Jing H, Diamond SL. Systems biology of coagulation initiation: kinetics of thrombin generation in resting and activated human blood. PLoS Comput Biol 2010; 6: 1000950.
49. Muthard RW, Welsh JD, Brass LF, Diamond SL. Fibrin, γ'-fibrinogen, and transclot pressure gradient control hemostatic clot growth during human blood flow over a collagen/tissue factor wound. Arterioscler Thromb Vasc Biol 2015; 35: 645-54.
50. Kuharsky AL, Fogelson AL. Surface-mediated control of blood coagulation: the role of binding site densities and platelet deposition. Biophys J 2001; 80: 1050-74.
51. Kastrup CJ, Runyon MK, Shen F, Ismagilov RF. Modular chemical mechanism predicts spatiotemporal dynamics of initiation in the complex network of hemostasis. Proc Natl Acad Sci U S A 2006; 103: 15747-52.
52. Onasoga-Jarvis AA, Puls TJ, O'Brien SK, Kuang L, Liang HJ, Neeves KB. Thrombin generation and fibrin formation under flow on biomimetic tissue factor-rich surfaces. J Thromb Haemost 2014; 12: 373-82.
53. Shen F, Kastrup CJ, Liu Y, Ismagilov RF. Threshold response of initiation of blood coagulation by tissue factor in patterned microfluidic capillaries is controlled by shear rate. Arterioscler Thromb Vasc Biol 2008; 28: 2035-41.
54. Fogelson AL, Hussain YH, Leiderman K. Blood clot formation under flow: the importance of factor XI depends strongly on platelet count. Biophys J 2012; 102: 10-8.
55. Neeves KB, Maloney SF, Fong KP, Schmaier AA, Kahn ML, Brass LF, Diamond SL. Microfluidic focal thrombosis model for measuring murine platelet deposition and stability: PAR4 signaling enhances shear-resistance of platelet aggregates. J Thromb Haemost 2008; 6: 2193-201.
56. Guy RD, Fogelson AL, Keener JP. Fibrin gel formation in a shear flow. Math Med Biol 2007; 24: 111-30.
57. Tijburg PN, Ijsseldijk MJ, Sixma JJ, de Groot PG. Quantification of fibrin deposition in flowing blood with peroxidase-labeled fibrinogen. High shear rates induce decreased fibrin deposition and appearance of fibrin monomers. Arterioscler Thromb 11: 211-20.
58. Neeves KB, Illing DAR, Diamond SL. Thrombin flux and wall shear rate regulate fibrin fiber deposition state during polymerization under flow. Biophys J 2010; 98: 1344-52.
59. Kim HJ, Vignon-Clementel IE, Coogan JS, Figueroa CA, Jansen KE, Taylor CA. Patient-specific modeling of blood flow and pressure in human coronary arteries. Ann Biomed Eng 2010; 38: 3195-209.
60. Schirmer CM, Malek AM. Patient based computational fluid dynamic characterization of carotid bifurcation stenosis before and after endovascular revascularization. J Neurointerv Surg 2012; 4: 448-54.
61. Long Q, Xu XY, Ramnarine KV, Hoskins P. Numerical investigation of physiologically realistic pulsatile flow through arterial stenosis. J Biomech 2001; 34: 1229-42.
62. Ojha M, Cobbold RS, Johnston KW, Hummel RL. Detailed visualization of pulsatile flow fields produced by modelled arterial stenoses. J Biomed Eng 1990; 12: 463-9.
63. Young DF, Tsai FY. Flow characteristics in models of arterial stenoses. II. Unsteady flow. J Biomech 1973; 6: 547-59.
64. Banerjee RK, Back LH, Back MR, Cho YI. Physiological flow analysis in significant human coronary artery stenoses. Biorheology 2003; 40: 451-76.
65. Shankaran H, Alexandridis P, Neelamegham S. Aspects of hydrodynamic shear regulating shear-induced platelet activation and self-association of von Willebrand factor in suspension. Blood 2003; 101: 2637-45.
66. Singh I, Themistou E, Porcar L, Neelamegham S. Fluid shear induces conformation change in human blood protein von Willebrand factor in solution. Biophys J 2009; 96: 2313-20.
67. Colace TV, Diamond SL. Direct observation of von Willebrand Factor elongation and fiber formation on collagen during acute whole blood exposure to pathological flow. Arterioscler Thromb. Vasc. Biol. 2013; 33: 105-13.
68. Westein E, van der Meer AD, Kuijpers MJE, Frimat J-P, van den Berg A, Heemskerk JWM. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc Natl Acad Sci U S A 2013; 110: 1357-62.
69. Herbig BA, Diamond SL. Pathological von Willebrand factor fibers resist tissue plasminogen activator and ADAMTS13 while promoting the contact pathway and shear-induced platelet activation. J Thromb Haemost 2015; 13: 1699-708.
70. Bonazza K, Rottensteiner H, Schrenk G, Frank J, Allmaier G, Turecek PL, Scheiflinger F, Friedbacher G. Shear-dependent interactions of von Willebrand Factor with Factor VIII and Protease ADAMTS 13 demonstrated at a single molecule level by atomic force microscopy. Anal Chem 2015; 87: 150930065241003.
71. Le Behot A, Gauberti M, Martinez De Lizarrondo S, Montagne A, Lemarchand E, Repesse Y, Guillou S, Denis CV, Maubert E, Orset C, Vivien D. GpIba-VWF blockade restores vessel patency by dissolving platelet aggregates formed under very high shear rate in mice. Blood 2014; 123: 3354-63.
72. Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, Fu J, Carberry J, Fouras A, Jackson SP. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 2009; 15: 665-73.
73. Tovar-Lopez FJ, Rosengarten G, Westein E, Khoshmanesh K, Jackson SP, Mitchell A, Nesbitt WS. A microfluidics device to monitor platelet aggregation dynamics in response to strain rate micro-gradients in flowing blood. Lab Chip 2010; 10: 291-302.
74. Tovar-Lopez FJ, Rosengarten G, Nasabi M, Sivan V, Khoshmanesh K, Jackson SP, Mitchell A, Nesbitt WS. An investigation on platelet transport during thrombus formation at micro-scale stenosis. PLoS ONE 2013; 8: e74123.
75. Moake JL, Turner NA, Stathopoulos NA, Nolasco LH, Hellums JD. 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 Invest 1986; 78: 1456-61.
76. Chow TW, Hellums JD, Moake JL, Kroll MH. Shear stress-induced von Willebrand factor binding to platelet glycoprotein Ib initiates calcium influx associated with aggregation. Blood 1992; 80: 113-20.
77. Razdan K, Hellums JD, Kroll MH. Shear-stress-induced von Willebrand factor binding to platelets causes the activation of tyrosine kinase(s). Biochem J 1994; 302: 681-6.
78. Moake JL, Turner NA, Stathopoulos NA, Nolasco L, Hellums JD. 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 1988; 71: 1366-74.
79. Konstantopoulos K, Kamat SG, Schafer AI, Bañez EI, Jordan R, Kleiman NS, Hellums JD. Shear-induced platelet aggregation is inhibited by in vivo infusion of an anti-glycoprotein IIb/IIIa antibody fragment, c7E3 Fab, in patients undergoing coronary angioplasty. Circulation 1995; 91: 1427-31.
80. Moake JL, Rudy CK, Troll JH, Weinstein MJ, Colannino NM, Azocar J, Seder RH, Hong SL, Deykin D. Unusually large plasma factor VIII:von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura. N Engl J Med 1982; 307: 1432-5.
81. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw JD Jr, Ginsburg D, Tsai HM. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 2001; 413: 488-94.
82. Savage B, Saldivar E, Ruggeri ZM. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 1996; 84: 289-97.
83. De Visser MCH, Sandkuijl LA, Lensen RPM, Vos HL, Rosendaal FR, Bertina RM. Linkage analysis of factor VIII and von Willebrand factor loci as quantitative trait loci. J Thromb Haemost 2003; 1: 1771-6.
84. Konstantopoulos K, Chow TW, Turner NA, Hellums JD, Moake JL. Shear stress-induced binding of von Willebrand factor to platelets. Biorheology 1997; 34: 57-71.
85. Shankaran H, Neelamegham S. Hydrodynamic forces applied on intercellular bonds, soluble molecules, and cell-surface receptors. Biophys J 2004; 86: 576-88.
86. Pareti FI, Lattuada A, Bressi C, Zanobini M, Sala A, Steffan A, Ruggeri ZM. Proteolysis of von Willebrand factor and shear stress-induced platelet aggregation in patients with aortic valve stenosis. Circulation 2000; 102: 1290-5.
87. Loeffelbein F, Funk D, Nakamura L, Zieger B, Grohmann J, Siepe M, Kroll J, Stiller B. Shear-stress induced acquired von Willebrand syndrome in children with congenital heart disease. Interact Cardiovasc Thorac Surg 2014; 19: 926-32.
88. Goda M, Jacobs S, Rega F, Peerlinck K, Jacquemin M, Droogne W, Vanhaecke J, Van Cleemput J, Van den Bossche K, Meyns B. Time course of acquired von Willebrand disease associated with two types of continuous-flow left ventricular assist devices: HeartMate II and CircuLite Synergy Pocket Micro-pump. J Heart Lung Transplant 2013; 32: 539-45.
89. Turner N, Nolasco L, Moake J. Generation and breakdown of soluble ultralarge von Willebrand factor multimers. Semin Thromb Hemost 2012; 38: 38-46.
90. Thomas GM, Brill A, Mezouar S, Crescence L, Gallant M, Dubois C, Wagner DD. Tissue factor expressed by circulating cancer cell-derived microparticles drastically increases the incidence of deep vein thrombosis in mice. J Thromb Haemost 2015; 13: 1310-9.
91. Von Brühl M-L, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Köllnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209: 819-35.
92. Aleman MM, Walton BL, Byrnes JR, Wolberg AS. Fibrinogen and red blood cells in venous thrombosis. Thromb Res 2014; 133(Suppl): S38-40.
93. Goel MS, Diamond SL. Adhesion of normal erythrocytes at depressed venous shear rates to activated neutrophils, activated platelets, and fibrin polymerized from plasma. Blood 2002; 100: 3797-803.
94. Aleman MM, Byrnes JR, Wang J-G, Tran R, Lam WA, Di Paola J, Mackman N, Degen JL, Flick MJ, Wolberg AS. Factor XIII activity mediates red blood cell retention in venous thrombi. J Clin Invest 2014; 124: 3590-600.
95. Byrnes JR, Duval C, Wang Y, Hansen CE, Ahn B, Mooberry MJ, Clark MA, Johnsen JM, Lord ST, Lam W, Meijers JCM, Ni H, Ariëns RAS, Wolberg AS. Factor XIIIa-dependent retention of red blood cells in clots is mediated by fibrin α-chain crosslinking. Blood 2015; 126: 1940-8.
96. Fuchs TA, Brill A, Wagner DD. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol 2012; 32: 1777-83.
97. Lee Y-U, Lee AY, Humphrey JD, Rausch MK. Histological and biomechanical changes in a mouse model of venous thrombus remodeling. Biorheology 2015; 52: 235-45.
98. Wang Y, Pierce I, Gatehouse P, Wood N, Firmin D, Xu XY. Analysis of flow and wall shear stress in the peroneal veins under external compression based on real-time MR images. Med Eng Phys 2012; 34: 17-27.
99. Maloney SF, Brass LF, Diamond SL. P2Y12 or P2Y1 inhibitors reduce platelet deposition in a microfluidic model of thrombosis while apyrase lacks efficacy under flow conditions. Integr Biol (Camb) 2010; 2: 183-92.
100. Jung J, Hassanein A, Lyczkowski RW. Hemodynamic computation using multiphase flow dynamics in a right coronary artery. Ann Biomed Eng 2006; 34: 393-407.
101. Zhang J-M, Luo T, Tan SY, Lomarda AM, Wong ASL, Keng FYJ, Allen JC, Huo Y, Su B, Zhao X, Wan M, Kassab GS, Tan RS, Zhong L. Hemodynamic analysis of patient-specific coronary artery tree. Int J Numer Method Biomed Eng 2015; 31: e02708.
102. Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood 1996; 88: 1525-41.
103. Lawrence MB, McIntire LV, Eskin SG. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood 1987; 70: 1284-90.
104. Fedosov DA, Pan W, Caswell B, Gompper G, Karniadakis GE. Predicting human blood viscosity in silico. Proc Natl Acad Sci U S A 2011; 108: 11772-7.
105. Lawrence MB, Kansas GS, Kunkel EJ, Ley K. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L, P, E). J Cell Biol 1997; 136: 717-27.
106. Kadash KE, Lawrence MB, Diamond SL. Neutrophil string formation: hydrodynamic thresholding and cellular deformation during cell collisions. Biophys J 2004; 86: 4030-9.
107. Karino T, Motomiya M. Flow through a venous valve and its implication for thrombus formation. Thromb Res 1984; 36: 245-57.
108. Dong J-F. Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions. J Thromb Haemost 2005; 3: 1710-6.
109. Keshavarz-Motamed Z, Garcia J, Kadem L. Fluid dynamics of coarctation of the aorta and effect of bicuspid aortic valve. PLoS ONE 2013; 8: e72394.
110. LaDisa JF, Alberto Figueroa C, Vignon-Clementel IE, Kim HJ, Xiao N, Ellwein LM, Chan FP, Feinstein JA, Taylor CA. Computational simulations for aortic coarctation: representative results from a sampling of patients. J Biomech Eng 2011; 133: 091008.
111. Javadzadegan A, Yong ASC, Chang M, Ng ACC, Yiannikas J, Ng MKC, Behnia M, Kritharides L. Flow recirculation zone length and shear rate are differentially affected by stenosis severity in human coronary arteries. Am J Physiol Heart Circ Physiol 2013; 304: H559-66.
112. Kefayati S, Milner JS, Holdsworth DW, Poepping TL. In vitro shear stress measurements using particle image velocimetry in a family of carotid artery models: effect of stenosis severity, plaque eccentricity, and ulceration. PLoS ONE 2014; 9: e98209.
113. Schneider SW, Nuschele S, Wixforth A, Gorzelanny C, Alexander-Katz A, Netz RR, Schneider MF. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U S A 2007; 104: 7899-903.
114. Chan CHH, Pieper IL, Fleming S, Friedmann Y, Foster G, Hawkins K, Thornton CA, Kanamarlapudi V. The effect of shear stress on the size, structure, and function of human von Willebrand factor. Artif Organs 2014; 38: 741-50.
115. Girdhar G, Xenos M, Alemu Y, Chiu W-C, Lynch BE, Jesty J, Einav S, Slepian MJ, Bluestein D. Device thrombogenicity emulation: a novel method for optimizing mechanical circulatory support device thromboresistance. PLoS ONE 2012; 7: e32463.
116. Leverett LB, Hellums JD, Alfrey CP, Lynch EC. Red blood cell damage by shear stress. Biophys J 1972; 12: 257-73.
117. Wufsus AR, Macera NE, Neeves KB. The hydraulic permeability of blood clots as a function of fibrin and platelet density. Biophys J 2013; 104: 1812-23.
118. Collet J-P, Shuman H, Ledger RE, Lee S, Weisel JW. The elasticity of an individual fibrin fiber in a clot. Proc Natl Acad Sci 2005; 102: 9133-7.
119. Wufsus AR, Rana K, Brown A, Dorgan JR, Liberatore MW, Neeves KB. Elastic behavior and platelet retraction in low- and high-density fibrin gels. Biophys J 2015; 108: 173-83.
120. Slaboch CL, Alber MS, Rosen ED, Ovaert TC. Mechano-rheological properties of the murine thrombus determined via nanoindentation and finite element modeling. J Mech Behav Biomed Mater 2012; 10: 75-86.
121. Ying J, Ling Y, Westfield LA, Sadler JE, Shao J-Y. Unfolding the A2 domain of von Willebrand factor with the optical trap. Biophys J 2010; 98: 1685-93.
122. Litvinov RI, Barsegov V, Schissler AJ, Fisher AR, Bennett JS, Weisel JW, Shuman H. Dissociation of bimolecular αIIbβ3-fibrinogen complex under a constant tensile force. Biophys J 2011; 100: 165-73.
123. Ju L, Dong J, Cruz MA, Zhu C. The N-terminal flanking region of the A1 domain regulates the force-dependent binding of von Willebrand factor to platelet glycoprotein Ibα. J Biol Chem 2013; 288: 32289-301.
124. Lam WA, Chaudhuri O, Crow A, Webster KD, Li T-D, Kita A, Huang J, Fletcher DA. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat Mater 2011; 10: 61-6.