Medical device-induced thrombosis: What causes it and how can we prevent it?

Journal of Thrombosis and Haemostasis

Volumn 13, Issue S1, 2015, Pages S72-S81

  Jaffer, I H ^a   Fredenburgh, J C ^a   Hirsh, J ^a   Weitz, J I ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Catheters; Factor XI; Factor XII; Medical devices; Thrombosis

Indexed keywords

ALBUMIN; ANTICOAGULANT AGENT; ANTITHROMBOCYTIC AGENT; ARGATROBAN; BIOMATERIAL; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12A; CORN TRYPSIN INHIBITOR; DABIGATRAN; ELASTIN; ENOXAPARIN; FIBRINOGEN; FIBRONECTIN; FONDAPARINUX; HEPARIN; HIRUDIN; HIRULOG; MACROGOL; PHOSPHORYLCHOLINE; PROSTACYCLIN; PROSTAGLANDIN E2; PROTEIN C; PYROLYTIC CARBON; RECOMBINANT THROMBOMODULIN; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; WARFARIN; FIBRINOLYTIC AGENT;

CATHETER; CATHETER THROMBOSIS; CLINICAL TRIAL (TOPIC); COMPLEMENT ACTIVATION; CONCENTRATION RESPONSE; CORONARY STENT; DEVICE FAILURE; DRUG EFFECT; DRUG EFFICACY; FIBRIN DEPOSITION; FIBRIN FORMATION; HUMAN; IN VITRO STUDY; LEFT VENTRICULAR ASSIST DEVICE; LEUKOCYTE ADHERENCE; MATERIAL COATING; MECHANICAL HEART VALVE; NONHUMAN; PRIORITY JOURNAL; PROSTHETIC VALVE THROMBOSIS; PROTEIN AGGREGATION; REVIEW; RISK MANAGEMENT; STENT THROMBOSIS; SURFACE CHARGE; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION INHIBITION; THROMBOSIS; THROMBOSIS PREVENTION; ADVERSE EFFECTS; ANIMAL; BLOOD; BLOOD CLOTTING; BLOOD VESSEL PROSTHESIS; CATHETER OBSTRUCTION; CENTRAL VENOUS CATHETER; DRUG EFFECTS; GRAFT OCCLUSION, VASCULAR; HEART ASSIST DEVICE; HEART VALVE PROSTHESIS; PROSTHESES AND ORTHOSES; PROSTHESIS; PROSTHESIS FAILURE; STENT;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; BLOOD VESSEL PROSTHESIS; CATHETER OBSTRUCTION; COATED MATERIALS, BIOCOMPATIBLE; FIBRINOLYTIC AGENTS; GRAFT OCCLUSION, VASCULAR; HEART VALVE PROSTHESIS; HEART-ASSIST DEVICES; HUMANS; PROSTHESES AND IMPLANTS; PROSTHESIS DESIGN; PROSTHESIS FAILURE; STENTS; THROMBOSIS; VASCULAR ACCESS DEVICES;

EID: 84931327017     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12961     Document Type: Review

References (79)

1. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002; 1: 845-67.
2. Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 2005; 11: 1-18.
3. Turbill P, Beugeling T, Poot AA. Proteins involved in the Vroman effect during exposure of human blood plasma to glass and polyethylene. Biomaterials 1996; 17: 1279-87.
4. Ortega-Vinuesa JL, Tengvall P, Walivaara B, Lundstrom I. Stagnant versus dynamic conditions: a comparative adsorption study of blood proteins. Biomaterials 1998; 19: 251-62.
5. Haynes CA, Norde W. Globular proteins at solid/liquid interfaces. Colloids Surf, B 1994; 2: 517-66.
6. Gorbet MB, Sefton MV. Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 2004; 25: 5681-703.
7. Savage B, Ruggeri ZM. Selective recognition of adhesive sites in surface-bound fibrinogen by glycoprotein IIb-IIIa on nonactivated platelets. J Biol Chem 1991; 266: 11227-33.
8. Tsai WB, Grunkemeier JM, Horbett TA. Human plasma fibrinogen adsorption and platelet adhesion to polystyrene. J Biomed Mater Res 1999; 44: 130-9.
9. Tsai WB, Grunkemeier JM, McFarland CD, Horbett TA. Platelet adhesion to polystyrene-based surfaces preadsorbed with plasmas selectively depleted in fibrinogen, fibronectin, vitronectin, or von Willebrand's factor. J Biomed Mater Res 2002; 60: 348-59.
10. Lee JH, Lee HB. Platelet adhesion onto wettability gradient surfaces in the absence and presence of plasma proteins. J Biomed Mater Res 1998; 41: 304-11.
11. Yayapour N, Nygren H. Interactions between whole blood and hydrophilic or hydrophobic glass surfaces: kinetics of cell adhesion. Colloids Surf, B 1999; 15: 127-38.
12. Loike JD, Sodeik B, Cao L, Leucona S, Weitz JI, Detmers PA, Wright SD, Silverstein SC. CD11c/CD18 on neutrophils recognizes a domain at the N terminus of the A alpha chain of fibrinogen. Proc Natl Acad Sci USA 1991; 88: 1044-8.
13. Wright SD, Weitz JI, Huang AJ, Levin SM, Silverstein SC, Loike JD. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc Natl Acad Sci USA 1988; 85: 7734-8.
14. Morley DJ, Feuerstein IA. Adhesion of polymorphonuclear leukocytes to protein-coated and platelet adherent surfaces. Thromb Haemost 1989; 62: 1023-8.
15. Kazatchkine MD, Carreno MP. Activation of the complement system at the interface between blood and artificial surfaces. Biomaterials 1988; 9: 30-5.
16. Bowers VM, Fisher LR, Francis GW, Williams KL. A micromechanical technique for monitoring cell-substrate adhesiveness: measurements of the strength of red blood cell adhesion to glass and polymer test surfaces. J Biomed Mater Res 1989; 23: 1453-73.
17. Yau JW, Stafford AR, Liao P, Fredenburgh JC, Roberts R, Weitz JI. Mechanism of catheter thrombosis: comparison of the antithrombotic activities of fondaparinux, enoxaparin, and heparin in vitro and in vivo. Blood 2011; 118: 6667-74.
18. Yau JW, Stafford AR, Liao P, Fredenburgh JC, Roberts R, Brash JL, Weitz JI. Corn trypsin inhibitor coating attenuates the prothrombotic properties of catheters in vitro and in vivo. Acta Biomater 2012; 8: 4092-100.
19. Yau JW, Liao P, Fredenburgh JC, Stafford AR, Revenko AS, Monia BP, Weitz JI. Selective depletion of factor XI or factor XII with antisense oligonucleotides attenuates catheter thrombosis in rabbits. Blood 2014; 123: 2102-7.
20. Larsson M, Rayzman V, Nolte MW, Nickel KF, Bjorkqvist J, Jamsa A, Hardy MP, Fries M, Schmidbauer S, Hedenqvist P, Broome M, Pragst I, Dickneite G, Wilson MJ, Nash AD, Panousis C, Renne T. A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci Transl Med 2014; 6: 222ra17.
21. Matafonov A, Leung PY, Gailani AE, Grach SL, Puy C, Cheng Q, Sun MF, McCarty OJ, Tucker EI, Kataoka H, Renne T, Morrissey JH, Gruber A, Gailani D. Factor XII inhibition reduces thrombus formation in a primate thrombosis model. Blood 2014; 123: 1739-46.
22. Crosby JR, Marzec U, Revenko AS, Zhao C, Gao D, Matafonov A, Gailani D, MacLeod AR, Tucker EI, Gruber A, Hanson SR, Monia BP. Antithrombotic effect of antisense factor XI oligonucleotide treatment in primates. Arterioscler Thromb Vasc Biol 2013; 33: 1670-8.
23. Tucker EI, Marzec UM, White TC, Hurst S, Rugonyi S, McCarty OJT, Gailani D, Gruber A, Hanson SR. Prevention of vascular graft occlusion and thrombus-associated thrombin generation by inhibition of factor XI. Blood 2009; 113: 936-44.
24. Johnson RJ. Complement activation during extracorporeal therapy: biochemistry, cell biology and clinical relevance. Nephrol Dial Transplant 1994; 9 (Suppl. 2): 36-45.
25. Kazatchkine MD, Haeffner-Cavaillon N. Mechanisms and consequences of complement activation during hemodialysis. Adv Exp Med Biol 1989; 260: 19-26.
26. Krisinger MJ, Goebeler V, Lu Z, Meixner SC, Myles T, Pryzdial ELG, Conway EM. Thrombin generates previously unidentified C5 products that support the terminal complement activation pathway. Blood 2012; 120: 1717-25.
27. Amara U, Rittirsch D, Flierl M, Bruckner U, Klos A, Gebhard F, Lambris JD, Huber-Lang M. Interaction between the coagulation and complement system. In: Lambris JD, ed. Current Topics in Complement II. New York, USA: Springer, 2008: 68-76.
28. Bluestein D, Girdhar G, Einav S, Slepian MJ. Device thrombogenicity emulation: a novel methodology for optimizing the thromboresistance of cardiovascular devices. J Biomech 2013; 46: 338-44.
29. Andrade JD, Hlady V. Protein adsorption and materials biocompatibility: a tutorial review and suggested hypotheses. Biopolymers/Non-Exclusion HPLC. Berlin, Heidelberg: Springer, 1986: 1-63.
30. Lee JH, Lee HB, Andrade JD. Blood compatibility of polyethylene oxide surfaces. Prog Polym Sci 1995; 20: 1043-79.
31. Kim S, Lee R, Oster H, Coleman D, Andrade J, Lentz D, Olsen D. Platelet Adhesion to polymer surfaces. Trans Am Soc Artif Intern Organs 1974; 20: 449-55.
32. Park K, Mosher DF, Cooper SL. Acute surface-induced thrombosis in the canine ex vivo model: importance of protein composition of the initial monolayer and platelet activation. J Biomed Mater Res 1986; 20: 589-612.
33. Kang I-K, Kwon BK, Lee JH, Lee HB. Immobilization of proteins on poly(methyl methacrylate) films. Biomaterials 1993; 14: 787-92.
34. Nelson KD, Eisenbaumer R, Pomerantz M, Eberhart RC. High affinity polyethylene oxide for improved biocompatibility. ASAIO J 1996; 42: M884-9.
35. Eberhart RC, Munro MS, Frautschi JR, Lubin M, Clubb FJ, Miller CW, Sevastianov VI. Influence of endogenous albumin binding on blood-material Interactionsa. Ann N Y Acad Sci 1987; 516: 78-95.
36. ® arterial prostheses. Biomaterials 1989; 10: 147-55.
37. Al-Khaffaf H, Charlesworth D. Albumin-coated vascular prostheses: a five-year follow-up. J Vasc Surg 1996; 23: 686-90.
38. Kudo FA, Nishibe T, Miyazaki K, Flores J, Yasuda K. Albumin-coated knitted Dacron aortic prosthses. Study of postoperative inflammatory reactions. Int Angiol 2002; 21: 214-7.
39. Marois Y, Chakfé N, Guidoin R, Duhamel RC, Roy R, Marois M, King MW, Douville Y. An albumin-coated polyester arterial graft: in vivo assessment of biocompatibility and healing characteristics. Biomaterials 1996; 17: 3-14.
40. Kim YH, Lee CW, Hong MK, Park SW, Tahk SJ, Yang JY, Saito S, Santoso T, Quan L, Ge J, Weissman NJ, Lansky AJ, Mintz GS, Park SJ. Randomized comparison of carbon ion-implanted stent versus bare metal stent in coronary artery disease: the Asian Pacific Multicenter Arthos Stent Study (PASS) trial. Am Heart J 2005; 149: 336-41.
41. Sick PB, Brosteanu O, Ulrich M, Thiele H, Niebauer J, Busch I, Schuler G. Prospective randomized comparison of early and late results of a carbonized stent versus a high-grade stainless steel stent of identical design: the Prevention of Recurrent Venous Thromboembolism (PREVENT) trial. Am Heart J 2005; 149: 681-8.
42. Sick PB, Gelbrich G, Kalnins U, Erglis A, Bonan R, Aengevaeren W, Elsner D, Lauer B, Woinke M, Brosteanu O, Schuler G. Comparison of early and late results of a Carbofilm-coated stent versus a pure high-grade stainless steel stent (the Carbostent-Trial). Am J Cardiol 2004; 93: 1351-6.
43. Chang Chung Y, Hong Chiu Y, Wei Wu Y, Tai Tao Y. Self-assembled biomimetic monolayers using phospholipid-containing disulfides. Biomaterials 2005; 26: 2313-24.
44. Feng W, Zhu S, Ishihara K, Brash JL. Adsorption of fibrinogen and lysozyme on silicon grafted with Poly(2-methacryloyloxyethyl phosphorylcholine) via surface-initiated atom transfer radical polymerization. Langmuir 2005; 21: 5980-7.
45. Jordan SW, Faucher KM, Caves JM, Apkarian RP, Rele SS, Sun X-L, Hanson SR, Chaikof EL. Fabrication of a phospholipid membrane-mimetic film on the luminal surface of an ePTFE vascular graft. Biomaterials 2006; 27: 3473-81.
46. Lewis AL, Tolhurst LA, Stratford PW. Analysis of a phosphorylcholine-based polymer coating on a coronary stent pre- and post-implantation. Biomaterials 2002; 23: 1697-706.
47. Kuiper KKJ, Robinson KA, Chronos NAF, Cui J, Palmer SJ, Nordrehaug JE. Phosphorylcholine-coated metallic stents in rabbit iliac and porcine coronary arteries. Scand Cardiovasc J 1998; 32: 261-8.
48. Galli M, Bartorelli A, Bedogni F, DeCesare N, Klugmann S, Maiello L, Miccoli F, Moccetti T, Onofri M, Paolillo V, Pirisi R, Presbitero P, Sganzerla P, Viecca M, Zerboni S, Lanteri G. Italian BiodivYsio open registry (BiodivYsio PC-coated stent): study of clinical outcomes of the implant of a PC-coated coronary stent. J Invasive Cardiol 2000; 12: 452-8.
49. Trabbic-Carlson K, Setton LA, Chilkoti A. Swelling and mechanical behaviors of chemically cross-linked hydrogels of elastin-like polypeptides. Biomacromolecules 2003; 4: 572-80.
50. McPherson DT, Morrow C, Minehan DS, Wu J, Hunter E, Urry DW. Production and purification of a recombinant elastomeric polypeptide, G-(VPGVG)19-VPGV, from Escherichia coli. Biotechnol Prog 1992; 8: 347-52.
51. Nagapudi K, Brinkman WT, Leisen J, Thomas BS, Wright ER, Haller C, Wu X, Apkarian RP, Conticello VP, Chaikof EL. Protein-based thermoplastic elastomers. Macromolecules 2004; 38: 345-54.
52. DeFife KM, Shive MS, Hagen KM, Clapper DL, Anderson JM. Effects of photochemically immobilized polymer coatings on protein adsorption, cell adhesion, and the foreign body reaction to silicone rubber. J Biomed Mater Res 1999; 44: 298-307.
53. Woodhouse KA, Klement P, Chen V, Gorbet MB, Keeley FW, Stahl R, Fromstein JD, Bellingham CM. Investigation of recombinant human elastin polypeptides as non-thrombogenic coatings. Biomaterials 2004; 25: 4543-53.
54. Jordan SW, Haller CA, Sallach RE, Apkarian RP, Hanson SR, Chaikof EL. The effect of a recombinant elastin-mimetic coating of an ePTFE prosthesis on acute thrombogenicity in a baboon arteriovenous shunt. Biomaterials 2007; 28: 1191-7.
55. MacEwan SR, Chilkoti A. Applications of elastin-like polypeptides in drug delivery. J Control Release 2014; 190: 314-30.
56. Alibeik S, Zhu S, Yau JW, Weitz JI, Brash JL. Surface modification with polyethylene glycol-corn trypsin inhibitor conjugate to inhibit the contact factor pathway on blood-contacting surfaces. Acta Biomater 2011; 7: 4177-86.
57. Alibeik S, Zhu S, Yau JW, Weitz JI, Brash JL. Modification of polyurethane with polyethylene glycol-corn trypsin inhibitor for inhibition of factor XIIa in blood contact. J Biomater Sci Polym Ed 2011; 23: 1981-93.
58. Alibeik S, Zhu S, Yau JW, Weitz JI, Brash JL. Dual surface modification with PEG and corn trypsin inhibitor: effect of PEG:CTI ratio on protein resistance and anticoagulant properties. J Biomed Mater Res A 2012; 100: 856-62.
59. Klement P, Du YJ, Berry LR, Tressel P, Chan AK. Chronic performance of polyurethane catheters covalently coated with ATH complex: a rabbit jugular vein model. Biomaterials 2006; 27: 5107-17.
60. Vrolix MC, Legrand VM, Reiber JH, Grollier G, Schalij MJ, Brunel P, Martinez-Elbal L, Gomez-Recio M, Bar FW, Bertrand ME, Colombo A, Brachman J. Heparin-coated Wiktor stents in human coronary arteries (MENTOR trial). MENTOR Trial Investigators. Am J Cardiol 2000; 86: 385-9.
61. Wohrle J, Al-Khayer E, Grotzinger U, Schindler C, Kochs M, Hombach V, Hoher M. Comparison of the heparin coated vs the uncoated Jostent-no influence on restenosis or clinical outcome. Eur Heart J 2001; 22: 1808-16.
62. Edmunds LH Jr, Colman RW. Thrombin during cardiopulmonary bypass. Ann Thorac Surg 2006; 82: 2315-22.
63. Liu T, Liu Y, Chen Y, Liu S, Maitz MF, Wang X, Zhang K, Wang J, Wang Y, Chen J, Huang N. Immobilization of heparin/poly-(L)-lysine nanoparticles on dopamine-coated surface to create a heparin density gradient for selective direction of platelet and vascular cells behavior. Acta Biomater 2014; 10: 1940-54.
64. Deng J, Liu X, Ma L, Cheng C, Shi W, Nie C, Zhao C. Heparin-mimicking multilayer coating on polymeric membrane via LbL assembly of cyclodextrin-based supramolecules. ACS Appl Mater Interfaces 2014; 6: 21603-14.
65. Gao W, Lin T, Li T, Yu M, Hu X, Duan D. Sodium alginate/heparin composites on PVC surfaces inhibit the thrombosis and platelet adhesion: applications in cardiac surgery. Int J Clin Exp Med 2013; 6: 259-68.
66. Nakayama Y, Yamaoka S, Yamanami M, Fujiwara M, Uechi M, Takamizawa K, Ishibashi-Ueda H, Nakamichi M, Uchida K, Watanabe T, Kanda K, Yaku H. Water-soluble argatroban for antithrombogenic surface coating of tissue-engineered cardiovascular tissues. J Biomed Mater Res, Part B 2011; 99B: 420-30.
67. Wyers MC, Phaneuf MD, Rzucidlo EM, Contreras MA, LoGerfo FW, Quist WC. In vivo assessment of a novel dacron surface with covalently bound recombinant hirudin. Cardiovasc Pathol 1999; 8: 153-9.
68. Lu L, Li Q-L, Maitz MF, Chen J-L, Huang N. Immobilization of the direct thrombin inhibitor-bivalirudin on 316L stainless steel via polydopamine and the resulting effects on hemocompatibility in vitro. J Biomed Mater Res, Part A 2012; 100A: 2421-30.
69. Yeh HY, Lin JC. Bioactivity and platelet adhesion study of a human thrombomodulin-immobilized nitinol surface. J Biomater Sci Polym Ed 2009; 20: 807-19.
70. Li JM, Singh MJ, Nelson PR, Hendricks GM, Itani M, Rohrer MJ, Cutler BS. Immobilization of human thrombomodulin to expanded polytetrafluoroethylene. J Surg Res 2002; 105: 200-8.
71. Sperling C, Salchert K, Streller U, Werner C. Covalently immobilized thrombomodulin inhibits coagulation and complement activation of artificial surfaces in vitro. Biomaterials 2004; 25: 5101-13.
72. Mehta SR, Boden WE, Eikelboom JW, Flather M, Steg PG, Avezum A, Afzal R, Piegas LS, Faxon DP, Widimsky P, Budaj A, Chrolavicius S, Rupprecht HJ, Jolly S, Granger CB, Fox KA, Bassand JP, Yusuf S. Antithrombotic therapy with fondaparinux in relation to interventional management strategy in patients with ST- and non-ST-segment elevation acute coronary syndromes: an individual patient-level combined analysis of the Fifth and Sixth Organization to Assess Strategies in Ischemic Syndromes (OASIS 5 and 6) randomized trials. Circulation 2008; 118: 2038-46.
73. Mehta SR, Granger CB, Eikelboom JW, Bassand J-P, Wallentin L, Faxon DP, Peters RJG, Budaj A, Afzal R, Chrolavicius S, Fox KAA, Yusuf S. Efficacy and safety of fondaparinux versus enoxaparin in patients with acute coronary syndromes undergoing percutaneous coronary intervention: results from the OASIS-5 trial. J Am Coll Cardiol 2007; 50: 1742-51.
74. Eikelboom JW, Connolly SJ, Brueckmann M, Granger CB, Kappetein AP, Mack MJ, Blatchford J, Devenny K, Friedman J, Guiver K, Harper R, Khder Y, Lobmeyer MT, Maas H, Voigt J-U, Simoons ML, Werf FVD. Dabigatran versus warfarin in patients with mechanical heart valves. N Engl J Med 2013; 369: 1206-14.
75. Yau JW, Liao P, Fredenburgh JC, Roberts RS, Weitz JI. Only high levels of dabigatran attenuate catheter thrombosis in vitro and in rabbits. Thromb Haemost 2014; 112: 79-86.
76. Leyh RG, Fischer S, Ruhparwar A, Haverich A. Anticoagulation for prosthetic heart valves during pregnancy: is low-molecular-weight heparin an alternative? Eur J Cardiothorac Surg 2002; 21: 577-9.
77. Chan W, Anand S, Ginsberg JS. Anticoagulation of pregnant women with mechanical heart valves: a systematic review of the literature. Arch Intern Med 2000; 160: 191-6.
78. Bane CE Jr, Gailani D. Factor XI as a target for antithrombotic therapy. Drug Discov Today 2014; 19: 1454-8.
79. Büller HR, Bethune C, Bhanot S, Gailani D, Monia BP, Raskob GE, Segers A, Verhamme P, Weitz JI. Factor XI antisense oligonucleotide for prevention of venous thrombosis. N Engl J Med 2015; 372: 232-40.