ISO 10993-4 is an international standard describing the methods of testing of medical devices for interactions with blood for regulatory purpose. The complexity of blood responses to biomaterial surfaces and the variability of blood functions in different individuals and species pose difficulties in standardisation. Moreover, in vivo or in vitro testing, as well as the clinical relevance of certain findings, is still matter of debate. This review deals with the major remaining problems, including a brief explanation of surface interactions with blood, the current ISO 10993 requirements for testing, and the role of in vitro test models. The literature is reviewed on anticoagulation, shear rate, blood-air interfaces, incubation time, and the importance of evaluation of the surface area after blood contact. Two test categories deserve further attention: complement and platelet function, including the effects on platelets from adhesion proteins, venipuncture, and animal derived- blood. The material properties, hydrophilicity, and roughness, as well as reference materials, are discussed. Finally this review calls for completing the acceptance criteria in the ISO standard based on a panel of test results. 1. Introduction Application of biomaterials in direct blood contact results in activation of the blood coagulation system and in an inflammatory reaction. These responses of blood are due to the natural response of the host defence mechanism against foreign surfaces. Inadequate control by natural inhibitors results in pathological processes, such as microthrombi generation or thrombosis, bleeding complications, haemodynamic instability, fever, edema, and organ damage. These adverse events become manifest during prolonged and intensive foreign material contact with vascular implants and extracorporeal blood circulation [1–7]. Despite their small surface area, coronary stents impose an ongoing risk for thrombosis by 1% per year [8]. A major difference between blood contacting and tissue implants is that blood might continue to be activated, despite a covering layer of proteins and cells, whereas implants in tissue become encapsulated and thus neutralised within weeks. It is hard to speculate on a direct relation with haemocompatibility, but consensus exists about the important role of poor haemocompatibility in direct and sustained adverse reactions. This review will deal with some of the remaining important practical aspects and problems of haemocompatibility testing. Adequate positive reference materials are warranted and acceptance criteria for all aspects
References
[1]
S. Westaby, “Organ dysfunction after cardiopulmonary bypass. A systemic inflammatory reaction initiated by the extracorporeal circuit,” Intensive Care Medicine, vol. 13, no. 2, pp. 89–95, 1987.
[2]
J. Butler, G. M. Rocker, and S. Westaby, “Inflammatory response to cardiopulmonary bypass,” Annals of Thoracic Surgery, vol. 55, no. 2, pp. 552–559, 1993.
[3]
E. Fransen, J. Maessen, M. Dentener, N. Senden, G. Geskes, and W. Buurman, “Systemic inflammation present in patients undergoing CABG without extracorporeal circulation,” Chest, vol. 113, no. 5, pp. 1290–1295, 1998.
[4]
P. Bruins, H. te Velthuis, A. P. Yazdanbakhsh et al., “Activation of the complement system during and after cardiopulmonary bypass surgery: postsurgery activation involves c-reactive protein and is associated with postoperative arrhythmia,” Circulation, vol. 96, no. 10, pp. 3542–3548, 1997.
[5]
B. Nilsson, O. Korsgren, J. D. Lambris, and K. N. Ekdahl, “Can cells and biomaterials in therapeutic medicine be shielded from innate immune recognition?” Trends in Immunology, vol. 31, no. 1, pp. 32–38, 2010.
[6]
J. K. Kirklin, S. Westaby, and E. H. Blackstone, “Complement and the damaging effects of cardiopulmonary bypass,” Journal of Thoracic and Cardiovascular Surgery, vol. 86, no. 6, pp. 845–857, 1983.
[7]
J. K. Kirklin, “Prospects for understanding and eliminating the deleterious effects of cardiopulmonary bypass,” Annals of Thoracic Surgery, vol. 51, no. 4, pp. 529–531, 1991.
[8]
G. De Luca, M. T. Dirksen, C. Spaulding et al., “Drug-Eluting Stent in Primary Angioplasty (DESERT) Cooperation. Drug-eluting vs bare-metal stents in primary angioplasty: a pooled patient-level meta-analysis of randomized trials,” Archives of Internal Medicine, vol. 172, no. 8, pp. 611–621, 2012.
[9]
E. F. Mammen, “Contact activation: the interaction of clotting, fibrinolytic, kinin and complement systems,” Biomedical Progress, vol. 2, pp. 31–34, 1990.
[10]
L. Vroman, “The life of an artificial device in contact with blood: initial events and their effect on its final state,” Bulletin of the New York Academy of Medicine, vol. 64, no. 4, pp. 352–357, 1988.
[11]
L. F. Brass, “The biochemistry of platelet activation,” in Hematology. Basic Principles and Practice, R. Hoffman, E. I. Benz, S. J. Shattil, B. Furie, and H. J. Cohen, Eds., pp. 1176–1197, Churchill Livingstone, New York, NY, USA, 1991.
[12]
H. S. Bassiouny, R. H. Song, H. Kocharyan, E. Kins, S. Glagov, and T. W. Wakefield, “Low flow enhances platelet activation after acute experimental arterial injury,” Journal of Vascular Surgery, vol. 27, no. 5, pp. 910–918, 1998.
[13]
O. Moen, K. H？g？sen, E. Fosse et al., “Attenuation of changes in leukocyte surface markers and complement activation with heparin-coated cardiopulmonary bypass,” Annals of Thoracic Surgery, vol. 63, no. 1, pp. 105–111, 1997.
[14]
S. Wan, J. L. Leclerc, and J. L. Vincent, “Inflammatory response to cardiopulmonary bypass: mechanisms involved and possible therapeutic strategies,” Chest, vol. 112, no. 3, pp. 676–692, 1997.
[15]
“ISO 10993 Biological evaluation of medical devices—Part 4: selection of tests for interactions with blood,” December 2002.
[16]
Medical dictionary 2012.
[17]
P. D. Goodman, E. T. Barlow, P. M. Crapo, S. F. Mohammad, and K. A. Solen, “Computational model of device-induced thrombosis and thromboembolism,” Annals of Biomedical Engineering, vol. 33, no. 6, pp. 780–797, 2005.
[18]
L. J. Wurzinger, P. Blasberg, F. Horii, and H. Schmid-Sch？bein, “A stagnation point flow technique to measure platelet adhesion onto polymer films from native blood—a technical report,” Thrombosis Research, vol. 44, no. 3, pp. 401–406, 1986.
[19]
V. I. Sevastianov and V. M. Parfeev, “Fatigue and hemocompatibility of polymer materials,” Artificial Organs, vol. 11, no. 1, pp. 20–25, 1987.
[20]
M. Dadsetan, H. Mirzadeh, N. Sharifi-Sanjani, and P. Salehian, “In vitro studies of platelet adhesion on laser-treated polyethylene terephtalate surface,” Journal of Biomedical Materials Research, vol. 54, no. 4, pp. 540–546, 2001.
[21]
N. Huang, P. Yang, Y. X. Leng et al., “Hemocompatibility of titanium oxide films,” Biomaterials, vol. 24, no. 13, pp. 2177–2187, 2003.
[22]
E. Bodnar, “The Medtronic Parallel valve and the lessons learned,” The Journal of Heart Valve Disease, vol. 5, no. 6, pp. 572–573, 1996.
[23]
C. T. Salerno, J. Droel, and R. W. Bianco, “Current state of in vivo preclinical heart valve evaluation,” Journal of Heart Valve Disease, vol. 7, no. 2, pp. 158–162, 1998.
[24]
F. Maillet, M. D. Kazatchkine, and D. Glotz, “Heparin prevents formation of the human C3 amplification convertase by inhibiting the binding site for B on C3b,” Molecular Immunology, vol. 20, no. 12, pp. 1401–1404, 1983.
[25]
R. Kopp, R. Bensberg, A. Kashefi, K. Mottaghy, R. Rossaint, and R. Kuhlen, “Effect of hirudin versus heparin on hemocompatibility of blood contacting biomaterials: an in vitro study,” International Journal of Artificial Organs, vol. 28, no. 12, pp. 1272–1277, 2005.
[26]
H. Yang, A. Reheman, P. Chen et al., “Fibrinogen and von willebrand factor-independent platelet aggregation in vitro and in vivo,” Journal of Thrombosis and Haemostasis, vol. 4, no. 10, pp. 2230–2237, 2006.
[27]
J. K. Unger, C. Haltern, B. Dohmen, and R. Rossaint, “Influence of different heparin concentrations on the results of in vitro investigations in plasmaseparation technology using capillary membrane filters,” Artificial Organs, vol. 27, no. 7, pp. 649–657, 2003.
[28]
M. Motomiya and T. Karino, “Flow patterns in the human carotid artery bifurcation,” Stroke, vol. 15, no. 1, pp. 50–56, 1984.
[29]
Y. C. Fung, Biomechanics. Circulation, Springer, New York, NY, USA, 2nd edition, 1977.
[30]
C. G. Caro, J. M. Fitz-Gerald, and R. C. Schroter, “Atheroma and arterial wall shear. Observation, correlation and proposal of a shear dependent mass transfer mechanism for atherogenesis,” Proceedings of the Royal Society of London. Series B, vol. 177, no. 46, pp. 109–159, 1971.
[31]
U. Kessler, T. Grau, F. Gronchi et al., “Comparison of porcine and human coagulation by thrombelastometry,” Thrombosis Research, vol. 128, pp. 477–482, 2011.
[32]
A. Kamiya and T. Togawa, “Adaptive regulation of wall shear stress to flow change in the canine carotid artery,” The American Journal of Physiology, vol. 239, no. 1, pp. H14–21, 1980.
[33]
A. P. Yoganathan, “Cardiac valve prostheses,” in The Biomedical Engineering Handbook, J. D. Bronzino, Ed., pp. 1847–1870, CRC Press, Boca Raton, Fla, USA, 1995.
[34]
K. H. Keller, “The dynamics of the interaction of cells with surfaces,” in Interaction of the Blood With Natural and Artificial Surfaces, E. W. Salzman, Ed., pp. 119–138, Dekker, New York, NY, USA, 1981.
[35]
G. H. Anderson, J. D. Hellums, J. L. Moake, and C. P. Alfrey Jr., “Platelet lysis and aggregation in shear fields,” Blood Cells, vol. 4, no. 3, pp. 499–507, 1978.
[36]
B. M. Yun, J. Wu, H. A. Simon et al., “A numerical investigation of blood damage in the hinge area of aortic bileaflet mechanical heart valves during the leakage phase,” Annals of Biomedical Engineering, vol. 40, no. 7, pp. 1468–1485, 2012.
[37]
J. J. Wentzel, R. Krams, J. C. H. Schuurbiers et al., “Relationship between neointimal thickness and shear stress after wallstent implantation in human coronary arteries,” Circulation, vol. 103, no. 13, pp. 1740–1745, 2001.
[38]
D. S. De Wachter, P. R. Verdonck, R. F. Verhoeven, and R. O. Hombrouckx, “Red cell injury assessed in a numeric model of a peripheral dialysis needle,” ASAIO Journal, vol. 42, no. 5, pp. M524–M529, 1996.
[39]
J. R. O'Brien, “Shear-induced platelet aggregation,” The Lancet, vol. 335, no. 8691, pp. 711–713, 1990.
[40]
J. L. Moake, N. A. Turner, N. A. Stathopoulos, L. Nolasco, and J. D. Hellums, “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, vol. 71, no. 5, pp. 1366–1374, 1988.
[41]
P. Tandon and S. L. Diamond, “Hydrodynamic effects and receptor interactions of platelets and their aggregates in linear shear flow,” Biophysical Journal, vol. 73, no. 5, pp. 2819–2835, 1997.
[42]
A. Bonnefoy, Q. Liu, C. Legrand, and M. M. Frojmovic, “Efficiency of platelet adhesion to fibrinogen depends on both cell activation and flow,” Biophysical Journal, vol. 78, no. 6, pp. 2834–2843, 2000.
[43]
B. Sivaraman and R. A. Latour, “The relationship between platelet adhesion on surfaces and the structure versus the amount of adsorbed fibrinogen,” Biomaterials, vol. 31, no. 5, pp. 832–839, 2010.
[44]
S. Casalino, E. Stelian, E. Novelli et al., “Reduced transfusion requirements with a closed cardiopulmonary bypass system,” Journal of Cardiovascular Surgery, vol. 49, no. 3, pp. 363–369, 2008.
[45]
D. Paparella, G. Scrascia, C. Rotunno et al., “A biocompatible cardiopulmonary bypass strategy to reduce hemostatic and inflammatory alterations: a randomized controlled trial,” Journal of Cardiothoracic and Vascular Anesthesia, vol. 26, no. 4, pp. 557–562, 2012.
[46]
T. Ohata, M. Mitsuno, M. Yamamura et al., “Minimal cardiopulmonary bypass attenuates neutrophil activation and cytokine release in coronary artery bypass grafting,” Journal of Artificial Organs, vol. 10, no. 2, pp. 92–95, 2007.
[47]
C. A. Skrabal, G. Steinhoff, and A. Liebold, “Minimizing cardiopulmonary bypass attenuates myocardial damage after cardiac surgery,” ASAIO Journal, vol. 53, no. 1, pp. 32–35, 2007.
[48]
J. Gong, R. Larsson, K. N. Ekdahl, T. E. Mollnes, U. Nilsson, and B. Nilsson, “Tubing loops as a model for cardiopulmonary bypass circuits: both the biomaterial and the blood-gas phase interfaces induce complement activation in an in vivo model,” Journal of Clinical Immunology, vol. 16, no. 4, pp. 222–229, 1996.
[49]
A. B. Chandler, “In vitro thrombotic coagulation of blood: a method for producing a thrombus,” Laboratory Investigation, vol. 7, pp. 110–116, 1958.
[50]
G. Tepe, J. Schmehl, H. P. Wendel et al., “Reduced thrombogenicity of nitinol stents—in vitro evaluation of different surface modifications and coatings,” Biomaterials, vol. 27, no. 4, pp. 643–650, 2006.
[51]
T. Thorsen, H. Klausen, R. T. Lie, and H. Holmsen, “Bubble-induced aggregation of platelets: effects of gas species, proteins, and decompression,” Undersea & Hyperbaric Medicine, vol. 20, no. 2, pp. 101–119, 1993.
[52]
S. Ritz-Timme, N. Eckelt, E. Schmidtke, and H. Thomsen, “Genesis and diagnostic value of leukocyte and platelet accumulations around “air bubbles” in blood after venous air embolism,” International Journal of Legal Medicine, vol. 111, no. 1, pp. 22–26, 1998.
[53]
R. Miller, V. B. Fainerman, R. Wüstneck, J. Kr？gel, and D. V. Trukhin, “Characterisation of the initial period of protein adsorption by dynamic surface tension measurements using different drop techniques,” Colloids and Surfaces A, vol. 131, no. 1–3, pp. 225–230, 1998.
[54]
C. Gómez-Suárez, H. J. Busscher, and H. C. van der Mei, “Analysis of bacterial detachment from substratum surfaces by the passage of air-liquid interfaces,” Applied and Environmental Microbiology, vol. 67, no. 6, pp. 2531–2537, 2001.
[55]
J. Wang, Y. Zheng, F. Q. Nie, J. Zhai, and L. Jiang, “Air bubble bursting effect of lotus leaf,” Langmuir, vol. 25, no. 24, pp. 14129–14134, 2009.
[56]
Z. H. Wu, H. B. Chen, Y. M. Dong et al., “Cleaning using nanobubbles: defouling by electrochemical generation of bubbles,” Journal of Colloid and Interface Science, vol. 328, no. 1, pp. 10–14, 2008.
[57]
A. Agarwal, W. J. Ng, and Y. Liu, “Principle and applications of microbubble and nanobubble technology for water treatment,” Chemosphere, vol. 84, no. 9, pp. 1175–1180, 2011.
[58]
M. Gosling, J. Golledge, R. J. Turner, and J. T. Powell, “Arterial flow conditions downregulate thrombomodulin on saphenous vein endothelium,” Circulation, vol. 99, no. 8, pp. 1047–1053, 1999.
[59]
S. H. J. Monnink, A. J. van Boven, H. O. J. Peels et al., “Silicon-carbide coated coronary stents have low platelet and leukocyte adhesion during platelet activation,” Journal of Investigative Medicine, vol. 47, no. 6, pp. 304–310, 1999.
[60]
K. Gutensohn, C. Beythien, J. Bau et al., “In vitro analyses of diamond-like carbon coated stents: reduction of metal ion release, platelet activation, and thrombogenicity,” Thrombosis Research, vol. 99, no. 6, pp. 577–585, 2000.
[61]
G. Amoroso, A. J. van Boven, C. Volkers, H. J. G. M. Crijns, and W. van Oeveren, “Multilink stent promotes less platelet and leukocyte adhesion than a traditional stainless steel stent: an in vitro experimental study,” Journal of Investigative Medicine, vol. 49, no. 3, pp. 265–272, 2001.
[62]
K. Münch, M. F. Wolf, P. Gruffaz et al., “Use of simple and complex in vitro models for multiparameter characterization of human blood-material/device interactions,” Journal of Biomaterials Science, Polymer Edition, vol. 11, no. 11, pp. 1147–1163, 2000.
[63]
W. van Oeveren, I. F. Tielliu, and J. deHart, “Comparison of modified Chandler, roller pump, and ball valve circulation models for in vitro testing in high blood flow conditions: application in thrombogenicity testing of different materials for vascular applications,” International Journal of Biomaterials, vol. 2012, Article ID 673163, 7 pages, 2012.
[64]
X. M. Zhao, Y. P. Wu, H. X. Cai, et al., “The influence of the pulsatility of the blood flow on the extent of platelet adhesion,” Thrombosis Research, vol. 121, no. 6, pp. 821–825, 2008.
[65]
J. S. Cho, K. Ouriel, J. A. DeWeese, R. M. Green, G. Y. Chen, and J. Stoughton, “Thrombus formation on polytetrafluoroethylene surfaces: the importance of von Willebrand factor,” Cardiovascular Surgery, vol. 3, no. 6, pp. 645–651, 1995.
[66]
H. M. M. van Beusekom, D. M. Whelan, S. H. Hofma et al., “Long-term endothelial dysfunction is more pronounced after stenting than after balloon angioplasty in porcine coronary arteries,” Journal of the American College of Cardiology, vol. 32, no. 4, pp. 1109–1117, 1998.
[67]
P. K. Shah, “Plaque disruption and coronary thrombosis: new insight into pathogenesis and prevention,” Clinical Cardiology, vol. 20, no. 12, pp. II38–II44, 1997.
[68]
R. G. Mason, W. H. Zucker, and B. A. Shinoda, “Study of the reactions of blood with artificial surfaces. Use of the thrombogenerator,” Laboratory Investigation, vol. 31, no. 2, pp. 143–155, 1974.
[69]
C. Mrowietz, R. P. Franke, U. T. Seyfert, J. W. Park, and F. Jung, “Haemocompatibility of polymer-coated stainless steel stents as compared to uncoated stents,” Clinical Hemorheology and Microcirculation, vol. 32, no. 2, pp. 89–103, 2005.
[70]
M. K. Pangburn and H. J. Muller-Eberhard, “The C3 convertase of the alternative pathway of human complement. Enzymic properties of the bimolecular proteinase,” Biochemical Journal, vol. 235, no. 3, pp. 723–730, 1986.
[71]
K. N. J. Stevens, Y. B. J. Aldenhoff, F. H. van der Veen, J. G. Maessen, and L. H. Koole, “Bioengineering of improved biomaterials coatings for extracorporeal circulation requires extended observation of blood-biomaterial interaction under flow,” Journal of Biomedicine and Biotechnology, vol. 2007, Article ID 29464, 10 pages, 2007.
[72]
N. Nurdin, P. Fran？ois, Y. Mugnier et al., “Haemocompatibility evaluation of DLC- and SiC-coated surfaces,” European Cells and Materials, vol. 5, pp. 17–28, 2003.
[73]
D. Jovanovic, G. E. Engels, J. A. Plantinga et al., “Novel polyurethanes with interconnected porous structure induce in vivo tissue remodeling and accompanied vascularization,” Journal of Biomedical Materials Research Part A, vol. 95, no. 1, pp. 198–208, 2010.
[74]
M. F. Meek, K. Jansen, R. Steendam, W. van Oeveren, P. B. van Wachem, and M. J. A. van Luyn, “In vitro degradation and biocompatibility of poly(DL-lactide-ε-caprolactone) nerve guides,” Journal of Biomedical Materials Research Part A, vol. 68, no. 1, pp. 43–51, 2004.
[75]
N. Ferraz, D. O. Carlsson, J. Hong et al., “Haemocompatibility and ion exchange capability of nanocellulose polypyrrole membranes intended for blood purification. C3a en C5-9,” Journal of the Royal Society Interface, vol. 9, no. 73, pp. 1943–1955, 2012.
[76]
A. Sokolov, B. C. Hellerud, A. Pharo, E. A. Johannessen, and T. E. Mollnes, “Complement activation by candidate biomaterials of an implantable microfabricated medical device,” Journal of Biomedical Materials Research Part B, vol. 98, no. 2, pp. 323–329, 2011.
[77]
G. Bergseth, J. D. Lambris, T. E. Mollnes, and K. T. Lappegrd, “Artificial surface-induced inflammation relies on complement factor 5: proof from a deficient person,” Annals of Thoracic Surgery, vol. 91, no. 2, pp. 527–533, 2011.
[78]
L. Muthusubramaniam, R. Lowe, W. H. Fissell et al., “Hemocompatibility of silicon-based substrates for biomedical implant applications,” Annals of Biomedical Engineering, vol. 39, no. 4, pp. 1296–1305, 2011.
[79]
A. Erlenk？tter, P. Endres, B. Nederlof, C. Hornig, and J. Vienken, “Score model for the evaluation of dialysis membrane hemocompatibility,” Artificial Organs, vol. 32, no. 12, pp. 962–969, 2008.
[80]
S. Sinn, T. Scheuermann, S. Deichelbohrer, G. Ziemer, and H. P. Wendel, “A novel in vitro model for preclinical testing of the hemocompatibility of intravascular stents according to ISO 10993-4,” Journal of Materials Science: Materials in Medicine, vol. 22, no. 6, pp. 1521–1528, 2011.
[81]
D. Rittirsch, H. Redl, and M. Huber-Lang, “Role of complement in multiorgan failure,” Clinical and Developmental Immunology, vol. 2012, Article ID 962927, 10 pages, 2012.
[82]
R. S. Hotchkiss and I. E. Karl, “The pathophysiology and treatment of sepsis,” The New England Journal of Medicine, vol. 348, no. 2, pp. 138–150, 2003.
[83]
R. S. Hotchkiss, P. E. Swanson, B. D. Freeman et al., “Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction,” Critical Care Medicine, vol. 27, no. 7, pp. 1230–1251, 1999.
[84]
T. Goya, T. Morisaki, and M. Torisu, “Immunologic assessment of host defense impairment in patients with septic multiple organ failure: relationship between complement activation and changes in neutrophil function,” Surgery, vol. 115, no. 2, pp. 145–155, 1994.
[85]
C. L. Sprung, D. R. Schultz, and E. Marcial, “Complement activation in septic shock patients,” Critical Care Medicine, vol. 14, no. 6, pp. 525–528, 1986.
[86]
J. Charchaflieh, J. Wei, G. Labaze, et al., “The role of complement system in septic shock,” Clinical and Developmental Immunology, vol. 2012, Article ID 407324, 8 pages, 2012.
[87]
Y. M. Bilgin, A. Brand, S. P. Berger, M. R. Daha, and A. Roos, “Mannose-binding lectin is involved in multiple organ dysfunction syndrome after cardiac surgery: effects of blood transfusions,” Transfusion, vol. 48, no. 4, pp. 601–608, 2008.
[88]
P. F. Stahel, M. C. Morganti-Kossmann, and T. Kossmann, “The role of the complement system in traumatic brain injury,” Brain Research Reviews, vol. 27, no. 3, pp. 243–256, 1998.
[89]
N. J. Lynch, C. L. Willis, C. C. Nolan et al., “Microglial activation and increased synthesis of complement component C1q precedes blood-brain barrier dysfunction in rats,” Molecular Immunology, vol. 40, no. 10, pp. 709–716, 2004.
[90]
M. Bosmann and P. A. Ward, “Role of C3, C5 and anaphylatoxin receptors in acute lung injury and in sepsis,” Advances in Experimental Medicine and Biology, vol. 946, pp. 147–159, 2012.
[91]
J. S. Solomkin, L. A. Cotta, and P. S. Satoh, “Complement activation and clearance in acute illness and injury: evidence for C5a as a cell-directed mediator of the adult respiratory distress syndrome in man,” Surgery, vol. 97, no. 6, pp. 668–678, 1985.
[92]
P. F. Langlois and M. S. Gawryl, “Accentuated formation of the terminal C5b-9 complement complex in patient plasma precedes development of the adult respiratory distress syndrome,” American Review of Respiratory Disease, vol. 138, no. 2, pp. 368–375, 1988.
[93]
G. Zilow, J. A. Sturm, U. Rother, and M. Kirschfink, “Complement activation and the prognostic value of C3a in patients at risk of adult respiratory distress syndrome,” Clinical and Experimental Immunology, vol. 79, no. 2, pp. 151–157, 1990.
[94]
P. F. Weinberg, M. A. Matthay, and R. O. Webster, “Biologically active products of complement and acute lung injury in patients with the sepsis syndrome,” American Review of Respiratory Disease, vol. 130, no. 5, pp. 791–796, 1984.
[95]
E. Fosse, J. Pillgram-Larsen, J. L. Svennevig et al., “Complement activation in injured patients occurs immediately and is dependent on the severity of the trauma,” Injury, vol. 29, no. 7, pp. 509–514, 1998.
[96]
G. Atefi, F. S. Zetoune, T. J. Herron et al., “Complement dependency of cardiomyocyte release of mediators during sepsis,” FASEB Journal, vol. 25, no. 7, pp. 2500–2508, 2011.
[97]
R. J. Levy, D. A. Piel, P. D. Acton et al., “Evidence of myocardial hibernation in the septic heart,” Critical Care Medicine, vol. 33, no. 12, pp. 2752–2756, 2005.
[98]
J. M. Thurman, M. S. Lucia, D. Ljubanovic, and V. M. Holers, “Acute tubular necrosis is characterized by activation of the alternative pathway of complement,” Kidney International, vol. 67, no. 2, pp. 524–530, 2005.
[99]
G. Smedegard, L. Cui, and T. E. Hugli, “Endotoxin-induced shock in the rat. A role for C5a,” American Journal of Pathology, vol. 135, no. 3, pp. 489–497, 1989.
[100]
Z. Tang, B. Lu, E. Hatch, S. H. Sacks, and N. S. Sheerin, “C3a mediates epithelial-to-mesenchymal transition in proteinuric nephropathy,” Journal of the American Society of Nephrology, vol. 20, no. 3, pp. 593–603, 2009.
[101]
S. Gando, T. Kameue, N. Matsuda et al., “Combined activation of coagulation and inflammation has an important role in multiple organ dysfunction and poor outcome after severe trauma,” Thrombosis and Haemostasis, vol. 88, no. 6, pp. 943–949, 2002.
[102]
M. Levi, E. De Jonge, and T. van der Poll, “New treatment strategies for disseminated intravascular coagulation based on current understanding of the pathophysiology,” Annals of Medicine, vol. 36, no. 1, pp. 41–49, 2004.
[103]
E. Abraham, “Coagulation abnormalities in acute lung injury and sepsis,” American Journal of Respiratory Cell and Molecular Biology, vol. 22, no. 4, pp. 401–404, 2000.
[104]
C. T. Esmon, “The impact of the inflammatory response on coagulation,” Thrombosis Research, vol. 114, no. 5-6, pp. 321–327, 2004.
[105]
C. E. Bamberg, C. R. Mackay, H. Lee et al., “The C5a receptor (C5aR) C5L2 is a modulator of C5aR-mediated signal transduction,” Journal of Biological Chemistry, vol. 285, no. 10, pp. 7633–7644, 2010.
[106]
Q. Zhu, L. Chen, P. Zhu et al., “Preparation of PNIPAM-g-P (NIPAM-co-St) microspheres and their blood compatibility,” Colloids and Surfaces B, vol. 104, pp. 61–65, 2012.
[107]
F. Jung, S. Braune, and A. Lendlein, “Haemocompatibility testing of biomaterials using human platelets,” Clinical Hemorheology and Microcirculation, vol. 53, pp. 97–115, 2013.
[108]
R. E. Baier and R. C. Dutton, “Initial events in interactions of blood with a foreign surface,” Journal of Biomedical Materials Research, vol. 3, no. 1, pp. 191–206, 1969.
[109]
B. Seifert, B. Hiebl, and F. Jung, “Interaction of platelets with body foreign surfaces,” Series on Biomechanics, vol. 25, pp. 140–146, 2010.
[110]
U. T. Seyfert and F. Jung, “Criteria and principles of in vitro hemocompatibility testing according to the ISO 10993(4),” Infusionstherapie und Transfusionsmedizin, vol. 27, no. 6, pp. 317–322, 2000.
[111]
R. P. Zahedi, U. Lewandrowski, J. Wiesner et al., “Phosphoproteome of resting human platelets,” Journal of Proteome Research, vol. 7, no. 2, pp. 526–534, 2008.
[112]
L. Senzel, D. V. Gnatenko, and W. F. Bahou, “The platelet proteome,” Current Opinion in Hematology, vol. 16, no. 5, pp. 329–333, 2009.
[113]
B. Savage, E. Saldívar, and Z. M. Ruggeri, “Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor,” Cell, vol. 84, no. 2, pp. 289–297, 1996.
[114]
B. Sivaraman and R. A. Latour, “Delineating the roles of the GPIIb/IIIa and GP-Ib-IX-V platelet receptors in mediating platelet adhesion to adsorbed fibrinogen and albumin,” Biomaterials, vol. 32, no. 23, pp. 5365–5370, 2011.
[115]
M. Auton, C. Zhu, and M. A. Cruz, “The mechanism of VWF-mediated platelet GPIbα binding,” Biophysical Journal, vol. 99, no. 4, pp. 1192–1201, 2010.
[116]
S. J. Shattil, M. H. Ginsberg, and J. S. Brugge, “Adhesive signaling in platelets,” Current Opinion in Cell Biology, vol. 6, no. 5, pp. 695–704, 1994.
[117]
J. G. White, “Anatomy and structural organization of the platelet,” in Hemostasis and Thrombosis: Basic Principles and Clinical Practice, R. W. Colman, J. Hirsh, V. J. Marder, and E. W. Salzman, Eds., pp. 397–413, Lippincott, Philadelphia, Pa, USA, 1994.
[118]
G. V. R. Born and P. D. Richardson, “Activation time of blood platelets,” Journal of Membrane Biology, vol. 57, no. 2, pp. 87–90, 1980.
[119]
J. E. B. Fox, “The platelet cytoskeleton,” Thrombosis and Haemostasis, vol. 70, no. 6, pp. 884–893, 1993.
[120]
F. Misselwitz, V. L. Leytin, and V. S. Repin, “Effect of metabolic inhibitors on platelet attachment, spreading and aggregation on collagen-coated surfaces,” Thrombosis Research, vol. 46, no. 2, pp. 233–240, 1987.
[121]
S. Braune, M. Lange, K. Richau et al., “Interaction of thrombocytes with poly(ether imide): the influence of processing,” Clinical Hemorheology and Microcirculation, vol. 46, no. 2-3, pp. 239–250, 2010.
[122]
B. D. Ratner, “The catastrophe revisited: blood compatibility in the 21st century,” Biomaterials, vol. 28, no. 34, pp. 5144–5147, 2007.
[123]
P. Thevenot, W. Hu, and L. Tang, “Surface chemistry influences implant biocompatibility,” Current Topics in Medicinal Chemistry, vol. 8, no. 4, pp. 270–280, 2008.
[124]
D. R. Schmidt, H. Waldeck, and W. J. Kao, “Protein adsorption to biomaterials,” in Biological Interactions on Materials Surfaces, D. A. Puelo and R. Bizios, Eds., pp. 2–18, Springer, New York, NY, USA, 2009.
[125]
J. J. Sixma and P. G. De Groot, “Regulation of platelet adhesion to the vessel wall,” Annals of the New York Academy of Sciences, vol. 714, pp. 190–199, 1994.
[126]
G. M. Annich, J. P. Meinhardt, K. A. Mowery et al., “Reduced platelet activation and thrombosis in extracorporeal circuits coated with nitric oxide release polymers,” Critical Care Medicine, vol. 28, no. 4, pp. 915–920, 2000.
[127]
M. H. Schoenfisch, K. A. Mowery, M. V. Rader, N. Baliga, J. A. Wahr, and M. E. Meyerhoff, “Improving the thromboresistivity of chemical sensors via nitric oxide release: fabrication and in vivo evaluation of NO-releasing oxygen-sensing catheters,” Analytical Chemistry, vol. 72, no. 6, pp. 1119–1126, 2000.
[128]
H. Zhang, G. M. Annich, J. Miskulin et al., “Nitric oxide releasing silicone rubbers with improved blood compatibility: preparation, characterization, and in vivo evaluation,” Biomaterials, vol. 23, no. 6, pp. 1485–1494, 2002.
[129]
J. Feng and E. L. Chaikof, “Reconstitution of thrombomodulin into polymerizable phospholipid vesicles,” Polymer Preprints, vol. 41, no. 2, pp. 16–17, 2000.
[130]
C. H. Bamford, I. P. Middleton, K. G. Al-Lamee, and J. J. Paprotny, “Modification of biomaterials to improve blood compatibility,” International Journal of Artificial Organs, vol. 15, no. 2, pp. 71–78, 1992.
[131]
S. Curry, H. Mandelkow, P. Brick, and N. Franks, “Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites,” Nature Structural Biology, vol. 5, no. 9, pp. 827–835, 1998.
[132]
W. B. Tsai, J. M. Grunkemeier, and T. A. Horbett, “Variations in the ability of adsorbed fibrinogen to mediate platelet adhesion to polystyrene-based materials: a multivariate statistical analysis of antibody binding to the platelet binding sites of fibrinogen,” Journal of Biomedical Materials Research Part A, vol. 67, no. 4, pp. 1255–1268, 2003.
[133]
D. J. Cziperle, K. A. Joyce, C. W. Tattersall et al., “Albumin impregnated vascular grafts: albumin resorption and tissue reactions,” Journal of Cardiovascular Surgery, vol. 33, no. 4, pp. 407–414, 1992.
[134]
K. Kottke-Marchant, J. M. Anderson, Y. Umemura, and R. E. Marchant, “Effect of albumin coating on the in vitro blood compatibility of Dacron arterial prostheses,” Biomaterials, vol. 10, no. 3, pp. 147–155, 1989.
[135]
Y. Marois, N. Chakfé, R. Guidoin et al., “An albumin-coated polyester arterial graft: in vivo assessment of biocompatibility and healing characteristics,” Biomaterials, vol. 17, no. 1, pp. 3–14, 1996.
[136]
R. W. Colman, “Mechanisms of thrombus formation and dissolution,” Cardiovascular Pathology, vol. 2, pp. 23S–31S, 1993.
[137]
S. C. Makrides and U. S. Ryan, “Overview of the endothelium,” in Thrombosis and Hemorrhage, J. Loscalzo, A. I. Schafer, and editors, Eds., pp. 295–306, Williams & Wilkins, Baltimore, MD, USA, 2nd edition, 1998.
[138]
M. C. Frost, M. M. Reynolds, and M. E. Meyerhoff, “Polymers incorporating nitric oxide releasing/generating substances for improved biocompatibility of blood-contacting medical devices,” Biomaterials, vol. 26, no. 14, pp. 1685–1693, 2005.
[139]
K. Breddin, H. Grun, H. J. Krzywanek, and W. P. Schremmer, “On the measurement of spontaneous platelet aggregation. The platelet aggregation test III. Methods and first clinical results,” Thrombosis and Haemostasis, vol. 35, no. 3, pp. 669–691, 1976.
[140]
M. G. Cohen, J. S. Rossi, J. Garbarino et al., “Insights into the inhibition of platelet activation by omega-3 polyunsaturated fatty acids: beyond aspirin and clopidogrel,” Thrombosis Research, vol. 128, pp. 335–340, 2011.
[141]
F. Jung, C. Wischke, and A. Lendlein, “Degradable, multifunctional cardiovascular implants: challenges and hurdles,” MRS Bulletin, vol. 35, no. 8, pp. 607–613, 2010.
[142]
R. Bach, F. Jung, I. Kohsiek et al., “Factors affecting the restenosis rate after percutaneous transluminal coronary angioplasty,” Thrombosis Research, vol. 74, no. 1, pp. S55–S67, 1994.
[143]
C. Tamburrelli, F. Gianfagna, M. D'Imperio et al., “Postprandial cell inflammatory response to a standardised fatty meal in subjects at different degree of cardiovascular risk,” Thrombosis and Haemostasis, vol. 107, no. 3, pp. 530–537, 2012.
[144]
A. Ahmed, R. A. Khan, M. K. Azim et al., “Effect of natural honey on human platelets and blood coagulation proteins,” Pakistan Journal of Pharmaceutical Sciences, vol. 24, no. 3, pp. 389–397, 2011.
[145]
R. Bach, U. Schmidt, F. Jung et al., “Effects of fish oil capsules in two dosages on blood pressure, platelet functions, haemorheological and clinical chemistry parameters in apparently healthy subjects,” Annals of Nutrition and Metabolism, vol. 33, no. 6, pp. 359–367, 1989.
[146]
S. Bhaskar and A. A. Rauf, “Modulatory effect of coffee on platelet function,” Indian Journal of Physiology and Pharmacology, vol. 54, no. 2, pp. 141–148, 2010.
[147]
A. K. Dutta-Roy, L. Crosbie, and M. J. Gordon, “Effects of tomato extract on human platelet aggregation in vitro,” Platelets, vol. 12, no. 4, pp. 218–227, 2001.
[148]
L. Fernández-Murga, J. J. Tarín, M. A. García-Perez, and A. Cano, “The impact of chocolate on cardiovascular health,” Maturitas, vol. 69, no. 4, pp. 312–321, 2011.
[149]
W. R. Patterson and J. H. Cissik, “A comparison of human and canine platelet fatty acid composition,” Comparative Biochemistry and Physiology Part B, vol. 99, no. 1, pp. 147–150, 1991.
[150]
W. R. Patterson and J. H. Cissik, “A comparison of human and porcine platelet fatty acid composition,” Comparative Biochemistry and Physiology Part B, vol. 101, no. 4, pp. 645–649, 1992.
[151]
L. du Plessis, A. J. Botha, and K. Stevens, “Ultrastructure of buffalo, Syncerus caffer, platelets: comparison with bovine and human platelets,” Journal of Morphology, vol. 229, no. 3, pp. 309–314, 1996.
[152]
E. F. Grabowski, P. Didisheim, and J. C. Lewis, “Platelet adhesion to foreign surfaces under controlled conditions of whole blood flow: human vs rabbit, dog, calf, sheep, pig, macaque, and baboon,” Transactions of the American Society for Artificial Organs, vol. 23, pp. 141–151, 1977.
[153]
L. K. Jennings, M. M. White, and T. D. Mandrell, “Interspecies comparison of platelet aggregation, LIBS expression and clot retraction: observed differences in GPIIb-IIIa functional activity,” Thrombosis and Haemostasis, vol. 74, no. 6, pp. 1551–1556, 1995.
[154]
P. Swier, S. F. Mohammad, D. B. Olsen, and W. J. Kolff, “A comparison of the antiplatelet effect of aspirin on human and bovine platelets,” ASAIO Transactions, vol. 35, no. 3, pp. 205–208, 1989.
[155]
D. R. Gross, “Thromboembolic phenomena and the use of the pig as an appropriate animal model for research on cardiovascular devices,” International Journal of Artificial Organs, vol. 20, no. 4, pp. 195–203, 1997.
[156]
M. J. Zurbano, B. Fusté, G. Arderiu, G. Escolar, A. Ordinas, and M. Díaz-Ricart, “Differences and similarities in tyrosine phosphorylation of proteins in platelets from human and pig species,” Journal of Thrombosis and Haemostasis, vol. 1, no. 11, pp. 2411–2418, 2003.
[157]
R. E. Baier, “Adhesion in the biologic environment,” Biomaterials, Medical Devices & Artificial Organs, vol. 12, pp. 33–59, 1984.
[158]
M. F. Harmand and F. Briquet, “In vitro comparative evaluation under static conditions of the hemocompatibility of four types of tubing for cardiopulmonary bypass,” Biomaterials, vol. 20, no. 17, pp. 1561–1571, 1999.
[159]
W. B. Tsai, J. M. Grunkemeier, and T. A. Horbett, “Human plasma fibrinogen adsorption and platelet adhesion to polystyrene,” Journal of Biomedical Materials Research, vol. 44, no. 2, pp. 30–39, 1999.
[160]
T. G. Ruardy, J. M. Schakenraad, H. C. van der Mei, and H. J. Busscher, “Preparation and characterization of chemical gradient surfaces and their application for the study of cellular interaction phenomena,” Surface Science Reports, vol. 29, no. 1, pp. 1–30, 1997.
[161]
V. Karagkiozaki, S. Logothetidis, S. Lousinian, and G. Giannoglou, “Impact of surface electric properties of carbon-based thin films on platelets activation for nano-medical and nano-sensing applications,” International Journal of Nanomedicine, vol. 3, no. 4, pp. 461–469, 2008.
[162]
J. M. Schmehl, C. Harder, H. P. Wendel, C. D. Claussen, and G. Tepe, “Silicon carbide coating of nitinol stents to increase antithrombogenic properties and reduce nickel release,” Cardiovascular Revascularization Medicine, vol. 9, no. 4, pp. 255–262, 2008.
[163]
B. R. Alevriadou, J. L. Moake, N. A. Turner et al., “Real-time analysis of shear-dependent thrombus formation and its blockade by inhibitors of von Willebrand factor binding to platelets,” Blood, vol. 81, no. 5, pp. 1263–1276, 1993.
[164]
S. Beumer, H. F. G. Heijnen, M. J. W. Ijsseldijk, E. Orlando, P. G. De Groot, and J. J. Sixma, “Platelet adhesion to fibronectin in flow: the importance of von Willebrand factor and glycoprotein Ib,” Blood, vol. 86, no. 9, pp. 3452–3460, 1995.
[165]
J. M. Grunkemeier, W. B. Tsai, M. R. Alexander, D. G. Castner, and T. A. Horbett, “Platelet adhesion and procoagulant activity induced by contact with radiofrequency glow discharge polymers: roles of adsorbed fibrinogen and vWF,” Journal of Biomedical Materials Research, vol. 51, pp. 669–679, 2000.
[166]
J. K. Chesnutt and H. C. Han, “Tortuosity triggers platelet activation and thrombus formation in microvessels,” Journal of Biomechanical Engineering, vol. 133, no. 12, Article ID 121004, 2011.
[167]
H. T. Spijker, R. Bos, H. J. Busscher, R. Graaff, and W. van Oeveren, “Adhesion of blood platelets under flow to wettability gradient polyethylene surfaces made in a shielded gas plasma,” Journal of Adhesion Science and Technology, vol. 16, no. 13, pp. 1703–1713, 2002.
[168]
C. J. Jen, L. I. Hui-Mei, J. S. Wang, H. I. Chen, and S. Usami, “Flow-induced detachment of adherent platelets from fibrinogen-coated surface,” American Journal of Physiology, vol. 270, no. 1, pp. H160–H166, 1996.
[169]
H. T. Spijker, R. Bos, H. J. Busscher, T. G. van Kooten, and W. van Oeveren, “Platelet adhesion and activation on a shielded plasma gradient prepared on polyethylene,” Biomaterials, vol. 23, no. 3, pp. 757–766, 2002.
[170]
A. L. Bailly, A. Lautier, A. Laurent et al., “Thrombosis of angiographic catheters in humans: experimental study,” International Journal of Artificial Organs, vol. 22, no. 10, pp. 690–700, 1999.
[171]
W. Zingg, A. W. Neumann, A. B. Strong, and D. R. Absolom, “Effect of surface roughness on platelet adhesion under static and under flow conditions,” Canadian Journal of Surgery, vol. 25, no. 1, pp. 16–19, 1982.
[172]
W. Zingg, A. W. Neumann, and A. B. Strong, “Platelet adhesion to smooth and rough hydrophobic and hydrophilic surfaces under conditions of static exposure and laminar flow,” Biomaterials, vol. 2, no. 3, pp. 156–158, 1981.
[173]
N. Tsunoda, K. I. Kokubo, K. Sakai, M. Fukuda, M. Myazaki, and T. Hiyohi, “Surface roughness of cellulose hollow fiber dialysis membranes and platelet adhesion,” ASAIO Journal, vol. 45, no. 5, pp. 418–423, 1999.
[174]
J. F. Hecker and R. O. Edwards, “Effects of roughness on the thrombogenicity of a plastic,” Journal of Biomedical Materials Research, vol. 15, no. 1, pp. 1–7, 1981.
[175]
M. F. Maitz, M. T. Pham, E. Wieser, and I. Tsyganov, “Blood compatibility of titanium oxides with various crystal structure and element doping,” Journal of Biomaterials Applications, vol. 17, no. 4, pp. 303–319, 2003.
[176]
T. Zhao, Y. Li, Y. Gao, Y. Xiang, H. Chen, and T. Zhang, “Hemocompatibility investigation of the NiTi alloy implanted with tantalum,” Journal of Materials Science. Materials in Medicine, vol. 22, no. 10, pp. 2311–2318, 2011.
[177]
M. C. Bélanger and Y. Marois, “Hemocompatibility, biocompatibility, inflammatory and in vivo studies of primary reference materials low-density polyethylene and polydimethylsiloxane: a review,” Journal of Biomedical Materials Research, vol. 58, no. 5, pp. 467–477, 2001.
[178]
D. Motlagh, J. Allen, R. Hoshi, J. Yang, K. Lui, and G. Ameer, “Hemocompatibility evaluation of poly(diol citrate) in vitro for vascular tissue engineering,” Journal of Biomedical Materials Research Part A, vol. 82, no. 4, pp. 907–916, 2007.
[179]
M. Fischer, C. P. Baptista, I. C. Gon？alves et al., “The effect of octadecyl chain immobilization on the hemocompatibility of poly (2-hydroxyethyl methacrylate),” Biomaterials, vol. 33, pp. 7677–7685, 2012.
[180]
U. Streller, C. Sperling, H. übner J, R. Hanke, and C. Werner, “Design and evaluation of novel blood incubation systems for in vitro hemocompatibilityassessment of planar solid surfaces,” Journal of Biomedical Materials Research Part B, vol. 66, pp. 379–390, 2003.
[181]
T. T. Schug, A. Janesick, B. Blumberg, and J. J. Heindel, “Endocrine disrupting chemicals and disease susceptibility,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 127, pp. 204–215, 2011.
