Image-based analysis and simulation of the effect of platelet storage temperature on clot mechanics under uniaxial strain

Ayres CE, Jha BS, Meredith H, Bowman JR, Bowlin GL, Henderson SC, Simpson DG (2008) Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach. J Biomater Sci Polym Ed 19:603–621. https://doi.org/10.1163/156856208784089643 Ban E, Barocas VH, Shephard MS, Picu RC (2016) Softening in random networks of non-identical beams. J Mech Phys Solids 87:38–50. https://doi.org/10.1016/j.jmps.2015.11.001 Baradet TC, Haselgrove JC, Weisel JW (1995) Three-dimensional reconstruction of fibrin clot networks from stereoscopic intermediate voltage electron microscope images and analysis of branching. Biophys J 68:1551–1560. https://doi.org/10.1016/S0006-3495(95)80327-9 Berhan L, Sastry AM (2003) On modeling bonds in fused, porous networks: 3d simulations of fibrous–particulate joints. J Compos Mater 37:715–740. https://doi.org/10.1177/002199803029725 Brown AEX, Litvinov RI, Discher DE, Purohit PK, Weisel JW (2009) Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325:741–744. https://doi.org/10.1126/science.1172484 Campbell RA, Overmyer KA, Bagnell CR, Wolberg AS (2008) Cellular procoagulant activity dictates clot structure and stability as a function of distance from the cell surface. Arterioscler Thromb Vasc Biol 28:2247–2254. https://doi.org/10.1161/ATVBAHA.108.176008 Campbell RA, Overmyer KA, Selzman CH, Sheridan BC, Wolberg AS (2009) Contributions of extravascular and intravascular cells to fibrin network formation, structure, and stability. Blood 114:4886–4896. https://doi.org/10.1182/blood-2009-06-228940 Campbell RA, Aleman M, Gray LD, Falvo MR, Wolberg AS (2010) Flow profoundly influences fibrin network structure: implications for fibrin formation and clot stability in haemostasis. Thromb Haemost 104:1281–1284. https://doi.org/10.1160/TH10-07-0442 Collet J-P, Shuman H, Ledger RE, Lee S, Weisel JW (2005) The elasticity of an individual fibrin fiber in a clot. Proc Natl Acad Sci USA 102:9133–9137. https://doi.org/10.1073/pnas.0504120102 Costalat V, Lobotesis K, Machi P, Mourand I, Maldonado I, Heroum C, Vendrell JF, Milhaud D, Riquelme C, Bonafé A, Arquizan C (2012) Prognostic factors related to clinical outcome following thrombectomy in ischemic stroke (RECOST study). 50 patients prospective study. Eur J Radiol 81:4075–4082. https://doi.org/10.1016/j.ejrad.2012.07.012 D’Amore A, Stella JA, Wagner WR, Sacks MS (2010) Characterization of the complete fiber network topology of planar fibrous tissues and scaffolds. Biomaterials 31:5345–5354. https://doi.org/10.1016/j.biomaterials.2010.03.052 D’Amore A, Amoroso N, Gottardi R, Hobson C, Carruthers C, Watkins S, Wagner WR, Sacks MS (2014) From single fiber to macro-level mechanics: a structural finite-element model for elastomeric fibrous biomaterials. J Mech Behav Biomed Mater 39:146–161. https://doi.org/10.1016/j.jmbbm.2014.07.016 Dulińska I, Targosz M, Strojny W, Lekka M, Czuba P, Balwierz W, Szymoński M (2006) Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J Biochem Biophys Methods 66:1–11. https://doi.org/10.1016/j.jbbm.2005.11.003 Duong H, Wu B, Tawil B (2009) Modulation of 3D fibrin matrix stiffness by intrinsic fibrinogen–thrombin compositions and by extrinsic cellular activity. Tissue Eng Part A 15:1865–1876. https://doi.org/10.1089/ten.tea.2008.0319 Eng W (2018) Nonlinear stiffness and viscoelasticity of inhibitor-treated blood clots by tensile testing. Master’s thesis, San Jose State University, San Jose, CA, USA Eng W, Kim M, Ramasubramanian A, Lee S-JJ (2018) A modular test platform for micromechanical tensile testing of soft biomaterials. Presented at the ASME 2018 international mechanical engineering congress and exposition, American Society of Mechanical Engineers, pp V003T04A030–V003T04A030. https://doi.org/10.1115/IMECE2018-87259 Heussinger C, Frey E (2007) Role of architecture in the elastic response of semiflexible polymer and fiber networks. Phys Rev E Stat Nonlinear Soft Matter Phys 75:011917. https://doi.org/10.1103/PhysRevE.75.011917 Höök P, Brito-Robinson T, Kim O, Narciso C, Goodson HV, Weisel JW, Alber MS, Zartman JJ (2017) Whole blood clot optical clearing for nondestructive 3D imaging and quantitative analysis. Biomed Opt Express 8:3671–3686. https://doi.org/10.1364/BOE.8.003671 Hotaling NA, Bharti K, Kriel H, Simon CG Jr (2015) DiameterJ: a validated open source nanofiber diameter measurement tool. Biomaterials 61:327–338. https://doi.org/10.1016/j.biomaterials.2015.05.015 Jansen KA, Licup AJ, Sharma A, Rens R, MacKintosh FC, Koenderink GH (2018) The role of network architecture in collagen mechanics. Biophys J 114:2665–2678. https://doi.org/10.1016/j.bpj.2018.04.043 Kim E, Kim OV, Machlus KR, Liu X, Kupaev T, Lioi J, Wolberg AS, Chen DZ, Rosen ED, Xu Z, Alber M (2011) Correlation between fibrin network structure and mechanical properties: an experimental and computational analysis. Soft Matter 7:4983–4992. https://doi.org/10.1039/C0SM01528H Kim OV, Litvinov RI, Alber MS, Weisel JW (2017) Quantitative structural mechanobiology of platelet-driven blood clot contraction. Nat Commun 8:1274. https://doi.org/10.1038/s41467-017-00885-x Krasokha N, Theisen W, Reese S, Mordasini P, Brekenfeld C, Gralla J, Slotboom J, Schrott G, Monstadt H (2010) Mechanical properties of blood clots—a new test method. Materialwissenschaft Werkstofftechnik 41:1019–1024 Kulachenko A, Uesaka T (2012) Direct simulations of fiber network deformation and failure. Mech Mater 51:1–14. https://doi.org/10.1016/j.mechmat.2012.03.010 Lai VK, Lake SP, Frey CR, Tranquillo RT, Barocas VH (2012) Mechanical behavior of collagen-fibrin co-gels reflects transition from series to parallel interactions with increasing collagen content. J Biomech Eng 134:011004. https://doi.org/10.1115/1.4005544 Lever J, Krzywinski M, Altman N (2017) Points of significance: principal component analysis. Nat Methods 14:641–642. https://doi.org/10.1038/nmeth.4346 Li W, Sigley J, Pieters M, Helms CC, Nagaswami C, Weisel JW, Guthold M (2016) Fibrin fiber stiffness is strongly affected by fiber diameter, but not by fibrinogen glycation. Biophys J 110:1400–1410. https://doi.org/10.1016/j.bpj.2016.02.021 Li W, Lucioni T, Li R, Bonin K, Cho SS, Guthold M (2017) Stretching single fibrin fibers hampers their lysis. Acta Biomater 60:264–274. https://doi.org/10.1016/j.actbio.2017.07.037 Lippi G, Favaloro EJ (2018) Venous and arterial thromboses: two sides of the same coin? Semin Thromb Hemost 44:239–248. https://doi.org/10.1055/s-0037-1607202 Liu W, Jawerth LM, Sparks EA, Falvo MR, Hantgan RR, Superfine R, Lord ST, Guthold M (2006) Fibrin fibers have extraordinary extensibility and elasticity. Science 313:634. https://doi.org/10.1126/science.1127317 Matsumoto T, Sasaki J-I, Alsberg E, Egusa H, Yatani H, Sohmura T (2007) Three-dimensional cell and tissue patterning in a strained fibrin gel system. PLoS ONE 2:e1211. https://doi.org/10.1371/journal.pone.0001211 Mehta BP, Nogueira RG (2012) Should clot composition affect choice of endovascular therapy? Neurology 79:S63–S67. https://doi.org/10.1212/WNL.0b013e3182695859 Moreno-Arotzena O, Meier J, del Amo C, García-Aznar J (2015) Characterization of fibrin and collagen gels for engineering wound healing models. Materials 8:1636–1651. https://doi.org/10.3390/ma8041636 Nair PM, Pandya SG, Dallo SF, Reddoch KM, Montgomery RK, Pidcoke HF, Cap AP, Ramasubramanian AK (2017) Platelets stored at 4 °C contribute to superior clot properties compared to current standard-of-care through fibrin-crosslinking. Br J Haematol 178:119–129. https://doi.org/10.1111/bjh.14751 Oval Profile Plot [WWW Document] (n.d.) https://imagej.nih.gov/ij/plugins/oval-profile.html. Accessed 1 Dec 2019 Parazzi V, Lazzari L, Rebulla P (2010) Platelet gel from cord blood: a novel tool for tissue engineering. Platelets 21:549–554. https://doi.org/10.3109/09537104.2010.514626 Peter Selinger: Potrace [WWW Document] (n.d.) http://potrace.sourceforge.net/. Accessed 1 Dec 2019 Picu RC (2011) Mechanics of random fiber networks—a review. Soft Matter 7:6768–6785. https://doi.org/10.1039/C1SM05022B Pidcoke HF, Spinella PC, Ramasubramanian AK, Strandenes G, Hervig T, Ness PM, Cap AP (2014) Refrigerated platelets for the treatment of acute bleeding: a review of the literature and reexamination of current standards. Shock 41(Suppl 1):51–53. https://doi.org/10.1097/SHK.0000000000000078 Piechocka IK, Bacabac RG, Potters M, Mackintosh FC, Koenderink GH (2010) Structural hierarchy governs fibrin gel mechanics. Biophys J 98:2281–2289. https://doi.org/10.1016/j.bpj.2010.01.040 Reddoch KM, Pidcoke HF, Montgomery RK, Fedyk CG, Aden JK, Ramasubramanian AK, Cap AP (2014) Hemostatic function of apheresis platelets stored at 4°C and 22°C. Shock 41(Suppl 1):54–61. https://doi.org/10.1097/SHK.0000000000000082 Reddoch-Cardenas KM, Bynum JA, Meledeo MA, Nair PM, Wu X, Darlington DN, Ramasubramanian AK, Cap AP (2018) Cold-stored platelets: a product with function optimized for hemorrhage control. Transfus Apher Sci. https://doi.org/10.1016/j.transci.2018.12.012 Rowe SL, Lee S, Stegemann JP (2007) Influence of thrombin concentration on the mechanical and morphological properties of cell-seeded fibrin hydrogels. Acta Biomater 3:59–67. https://doi.org/10.1016/j.actbio.2006.08.006 Ryan EA, Mockros LF, Weisel JW, Lorand L (1999) Structural origins of fibrin clot rheology. Biophys J 77:2813–2826. https://doi.org/10.1016/S0006-3495(99)77113-4 Schwarz Henriques S, Sandmann R, Strate A, Köster S (2012) Force field evolution during human blood platelet activation. J Cell Sci 125:3914–3920. https://doi.org/10.1242/jcs.108126 Shlens J (2014) A tutorial on principal component analysis. arXiv:1404.1100v1 Sprouse LR 2nd, Peeters P, Bosiers M (2005) The capture of visible debris by distal cerebral protection filters during carotid artery stenting: is it predictable? J Vasc Surg 41:950–955. https://doi.org/10.1016/j.jvs.2005.02.048 Stein AM, Vader DA, Jawerth LM, Weitz DA, Sander LM (2008) An algorithm for extracting the network geometry of three-dimensional collagen gels. J Microsc 232:463–475. https://doi.org/10.1111/j.1365-2818.2008.02141.x Taylor SE, Cao T, Talauliker PM, Lifshitz J (2013) Objective morphological quantification of microscopic images using a fast Fourier transform (FFT) analysis. Curr Protoc Essent Lab Tech 95:9.5.1–9.5.12. https://doi.org/10.1002/9780470089941.et0905s07 Todo A, Minaeian A, Sahni R, Chao KH (2013) Incidence and outcome of procedural distal emboli using the Penumbra thrombectomy for acute stroke. J Neurointerv Surg 5:135–138. https://doi.org/10.1136/neurintsurg-2011-010216 Undas A, Ariëns RAS (2011) Fibrin clot structure and function. Arterioscler Thromb Vasc Biol. https://doi.org/10.1161/atvbaha.111.230631 Varjú I, Sótonyi P, Machovich R, Szabó L, Tenekedjiev K, Silva MMCG, Longstaff C, Kolev K (2011) Hindered dissolution of fibrin formed under mechanical stress. J Thromb Haemost 9:979–986. https://doi.org/10.1111/j.1538-7836.2011.04203.x Weisel JW, Litvinov RI (2017) Fibrin formation, structure and properties. In: Parry DAD, Squire J (eds) Fibrous proteins: structures and mechanisms, subcellular biochemistry. Springer, Cham, pp 405–456. https://doi.org/10.1007/978-3-319-49674-0_13 Wen Q, Basu A, Winer JP, Yodh A, Janmey PA (2007) Local and global deformations in a strain-stiffening fibrin gel. New J Phys 9:428–428. https://doi.org/10.1088/1367-2630/9/11/428 Wen Q, Basu A, Janmey PA, Yodh AG (2012) Non-affine deformations in polymer hydrogels. Soft Matter 8:8039–8049. https://doi.org/10.1039/c2sm25364j Yang M, Yu Y, Walsh WR, Yang J-L, Baker L, Lennox AF, Crowe PJ, Varcoe RL (2016) A microscopic and biomarker evaluation of embolic filter debris collected during carotid artery stenting. J Endovasc Ther 23:275–284. https://doi.org/10.1177/1526602816628284 Žagar G, Onck PR, van der Giessen E (2015) Two fundamental mechanisms govern the stiffening of cross-linked networks. Biophys J 108:1470–1479. https://doi.org/10.1016/j.bpj.2015.02.015