Advances in anti-thrombogenetic strategies of biomaterials_West China Medical Journal

Authors：

LIU Chen ^1,2 , ZHANG Ling ² , FU Ping ² ,  LIU Zhuang ¹

1. School of Chemical Engineering, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Department of Nephrology and Institute of Kidney Diseases, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LIU Zhuang, Email: liuz@scu.edu.cn

Keywords：

Anti-thrombogenetic biomaterials; modification; active substances; endothelialization

DOI：

10.7507/1002-0179.202406160

Video：

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Abstract Full text Figures/Tables Video References Cited by

The presence of thrombus on the surface of blood-contacting biomaterials in clinical practice can significantly impact both the longevity of the biomaterials and the overall survival prognosis of patients. The administration of anticoagulant and antiplatelet medications may heighten the risk of systemic bleeding. Developing biomaterials with anti-thrombogenetic properties and enabling localized anti-thrombosis may offer a solution to these challenges. The development strategies for anti-thrombogenetic biomaterials can be categorized into three main approaches based on the mechanisms of thrombus formation on biomaterial surfaces: altering physical and chemical properties, designing coatings containing or releasing active substances, and promoting endothelialization. However, due to the intricate and interconnected nature of these mechanisms, biomaterials constructed using a single approach may not effectively prevent thrombus formation. The collaborative intervention of various mechanisms can facilitate the development of biomaterials with enhanced blood compatibility.

Citation： LIU Chen, ZHANG Ling, FU Ping, LIU Zhuang. Advances in anti-thrombogenetic strategies of biomaterials. West China Medical Journal, 2024, 39(7): 1028-1035. doi: 10.7507/1002-0179.202406160 Copy

1.	Wang Y, Sun X. Reevaluation of lock solutions for central venous catheters in hemodialysis: a narrative review. Ren Fail, 2022, 44(1): 1501-1518.
2.	Ullrich H, Münzel T, Gori T. Coronary stent thrombosis- predictors and prevention. Dtsch Arztebl Int, 2020, 117(18): 320-326.
3.	Teja B, Bosch NA, Diep C, et al. Complication rates of central venous catheters: a systematic review and meta-analysis. JAMA Intern Med, 2024, 184(5): 474-482.
4.	Nilius H, Kaufmann J, Cuker A, et al. Comparative effectiveness and safety of anticoagulants for the treatment of heparin-induced thrombocytopenia. Am J Hematol, 2021, 96(7): 805-815.
5.	Geller AI, Shehab N, Lovegrove MC, et al. Bleeding related to oral anticoagulants: trends in US emergency department visits, 2016-2020. Thromb Res, 2023, 225: 110-115.
6.	Brash JL, Horbett TA, Latour RA, et al. The blood compatibility challenge. Part 2: Protein adsorption phenomena governing blood reactivity. Acta Biomater, 2019, 94: 11-24.
7.	Weber M, Steinle H, Golombek S, et al. Blood-contacting biomaterials: in vitro evaluation of the hemocompatibility. Front Bioeng Biotechnol, 2018, 6: 99.
8.	Jaffer IH, Weitz JI. The blood compatibility challenge. Part 1: Blood-contacting medical devices: the scope of the problem. Acta Biomater, 2019, 94: 2-10.
9.	Visalakshan RM, Macgregor MN, Sasidharan S, et al. Biomaterial surface hydrophobicity-mediated serum protein adsorption and immune responses. ACS Appl Mater Inter, 2019, 11(31): 27615-27623.
10.	Struczyńska M, Firkowska-boden I, Levandovsky N, et al. How crystallographic orientation-induced fibrinogen conformation affects platelet adhesion and activation on TiO₂. Adv Healthc Mater, 2023, 12(13): e2202508.
11.	Sang Y, Roest M, de Laat B, et al. Interplay between platelets and coagulation. Blood Rev, 2021, 46: 100733.
12.	Goel A, Tathireddy H, Wang SH, et al. Targeting the contact pathway of coagulation for the prevention and management of medical device-associated thrombosis. Semin Thromb Hemost, 2023.
13.	Skinner SC, Derebail VK, Poulton CJ, et al. Hemodialysis-related complement and contact pathway activation and cardiovascular risk: a narrative review. Kidney Med, 2021, 3(4): 607-618.
14.	Kourtzelis I, Markiewski MM, Doumas M, et al. Complement anaphylatoxin C5a contributes to hemodialysis-associated thrombosis. Blood, 2010, 116(4): 631-639.
15.	Maitz MF, Martins MCL, Grabow N, et al. The blood compatibility challenge. Part 4: Surface modification for hemocompatible materials: passive and active approaches to guide blood-material interactions. Acta Biomater, 2019, 94: 33-43.
16.	Neubauer K, Zieger B. Endothelial cells and coagulation. Cell Tissue Res, 2022, 387(3): 391-398.
17.	Elwing H, Welin S, Askendal A, et al. A wettability gradient-method for studies of macromolecular interactions at the liquid solid interface. J Colloid Interface Sci, 1987, 119(1): 203-210.
18.	Fan H, Guo Z. Bioinspired surfaces with wettability: biomolecule adhesion behaviors. Biomater Sci, 2020, 8(6): 1502-1535.
19.	Stallard CP, McDonnell KA, Onayemi OD, et al. Evaluation of protein adsorption on atmospheric plasma deposited coatings exhibiting superhydrophilic to superhydrophobic properties. Biointerphases, 2012, 7(1/2/3/4): 31.
20.	Wang P, Zhang YL, Fu KL, et al. Zinc-coordinated polydopamine surface with a nanostructure and superhydrophilicity for antibiofouling and antibacterial applications. Mater Adv, 2022, 3(13): 5476-5487.
21.	Chang Y. Designs of zwitterionic polymers. J Polym Res, 2022, 29(7): 286.
22.	Cheng CH, Chen GF, Lin JC. Studies of zwitterionic sulfobetaine functionalized polypropylene surface with or without polyethylene glycol spacer: surface characterization, antibacterial adhesion, and platelet compatibility evaluation. J Biomater Sci Polym Ed, 2020, 31(16): 2060-2077.
23.	Huang KT, Hsieh PS, Dai LG, et al. Complete zwitterionic double network hydrogels with great toughness and resistance against foreign body reaction and thrombus. J Mater Chem B, 2020, 8(33): 7390-7402.
24.	Guo LL, Cheng YF, Ren X, et al. Simultaneous deposition of tannic acid and poly(ethylene glycol) to construct the antifouling polymeric coating on titanium surface. Colloids Surf B Biointerfaces, 2021, 200: 111592.
25.	Perrino C, Lee S, Choi SW, et al. A biomimetic alternative to poly(ethylene glycol) as an antifouling coating: resistance to nonspecific protein adsorption of poly(L-lysine)-graft-dextran. Langmuir, 2008, 24(16): 8850-8856.
26.	Yang W, Xue H, LI W, et al. Pursuing “zero” protein adsorption of poly(carboxybetaine) from undiluted blood serum and plasma. Langmuir, 2009, 25(19): 11911-11916.
27.	Tsai WB, Grunkemeier JM, Horbett TA. Human plasma fibrinogen adsorption and platelet adhesion to polystyrene. J Biomed Mater Res, 1999, 44(2): 130-139.
28.	Yao M, Wei Z, Li J, et al. Microgel reinforced zwitterionic hydrogel coating for blood-contacting biomedical devices. Nat Commun, 2022, 13(1): 5339.
29.	Klee D, Höcker H. Polymers for biomedical applications: improvement of the interface compatibility//Eastmond GC, Höcker H, Klee D. Biomedical applications polymer blends. Advances in polymer science, vol 149. Berlin, Heidelberg: Springer, 1999: 1-57.
30.	Wu XH, Liew YK, Mai CW, et al. Potential of superhydrophobic surface for blood-contacting medical devices. Int J Mol Sci, 2021, 22(7): 3341.
31.	Chen L, Han D, Jiang L. On improving blood compatibility: from bioinspired to synthetic design and fabrication of biointerfacial topography at micro/nano scales. Colloid Surface B, 2011, 85(1): 2-7.
32.	Toes GJ, Van Muiswinkel KW, Van Oeveren W, et al. Superhydrophobic modification fails to improve the performance of small diameter expanded polytetrafluoroethylene vascular grafts. Biomaterials, 2002, 23(1): 255-262.
33.	Betz T, Toepel I, Pfister K, et al. Impact of chronic kidney disease on the outcomes of infrapopliteal venous, and heparin-bonded expanded polytetrafluoroethylene bypass surgeries: a retrospective cohort study. Vasc Med, 2022, 27(1): 55-62.
34.	Milner KR, Snyder AJ, Siedlecki CA. Sub-micron texturing for reducing platelet adhesion to polyurethane biomaterials. J Biomed Mater Res A, 2006, 76(3): 561-570.
35.	Celik N, Sahin F, Ruzi M, et al. Blood repellent superhydrophobic surfaces constructed from nanoparticle-free and biocompatible materials. Colloids Surf B Biointerfaces, 2021, 205: 111864.
36.	Montgomerie Z, Popat KC. Improved hemocompatibility and reduced bacterial adhesion on superhydrophobic titania nanoflower surfaces. Mater Sci Eng C Mater Biol Appl, 2021, 119: 111503.
37.	Yun GT, Jung WB, Oh MS, et al. Springtail-inspired superomniphobic surface with extreme pressure resistance. Sci Adv, 2018, 4(8): eaat4978.
38.	Leslie DC, Waterhouse A, Berthet JB, et al. A bioinspired omniphobic surface coating on medical devices prevents thrombosis and biofouling. Nat Biotechnol, 2014, 32(11): 1134-1140.
39.	Roberts TR, Choi JH, Wendorff DS, et al. Tethered liquid perfluorocarbon coating for 72 hour heparin-free extracorporeal life support. ASAIO J, 2021, 67(7): 798-808.
40.	Kuten Pella O, Hornyák I, Horváthy D, et al. Albumin as a biomaterial and therapeutic agent in regenerative medicine. Int J Mol Sci, 2022, 23(18): 10557.
41.	Subramanian A. Corrigendum to “Evaluation of the real-time protein adsorption kinetics on albumin-binding surfaces by dynamic in situ spectroscopic ellipsometry” [TSF 520 (2012) 2200–2207]. Thin Solid Films, 2012, 520(19): 6334.
42.	Gonçalves IC, Martins MC, Barbosa MA, et al. Protein adsorption and clotting time of pHEMA hydrogels modified with C18 ligands to adsorb albumin selectively and reversibly. Biomaterials, 2009, 30(29): 5541-5551.
43.	Freitas SC, Maia S, Figueiredo AC, et al. Selective albumin-binding surfaces modified with a thrombin-inhibiting peptide. Acta Biomater, 2014, 10(3): 1227-1237.
44.	Sivaraman B, Latour RA. Time-dependent conformational changes in adsorbed albumin and its effect on platelet adhesion. Langmuir, 2012, 28(5): 2745-2752.
45.	Marois Y, Chakfé N, Guidoin R, et al. An albumin-coated polyester arterial graft: in vivo assessment of biocompatibility and healing characteristics. Biomaterials, 1996, 17(1): 3-14.
46.	Kudo FA, Nishibe T, Miyazaki K, et al. Albumin-coated knitted dacron aortic prosthses. Study of postoperative inflammatory reactions. Int Angiol, 2002, 21(3): 214-217.
47.	Li R, Li Y, Bai Y, et al. Achieving superior anticoagulation of endothelial membrane mimetic coating by heparin grafting at zwitterionic biocompatible interfaces. Int J Biol Macromol, 2024, 257(Pt 1): 128574.
48.	Zhang Y, Man J, Liu J, et al. Construction of the mussel-inspired PDAM/lysine/heparin composite coating combining multiple anticoagulant strategies. ACS Appl Mater Interfaces, 2023, 15(23): 27719-27731.
49.	Zhang M, Chan CHH, Pauls JP, et al. Investigation of heparin-loaded poly(ethylene glycol)-based hydrogels as anti-thrombogenic surface coatings for extracorporeal membrane oxygenation. J Mater Chem B, 2022, 10(26): 4974-4983.
50.	Özdemir M, Taydas O, Danisan G, et al. Comparison of the complications and long-term results of heparin-coated and non-heparin-coated symmetric-tip hemodialysis catheters. J Vasc Access, 2023: 11297298231202536.
51.	Clark TWI, Jacobs D, Charles HW, et al. Comparison of heparin-coated and conventional split-tip hemodialysis catheters. Cardiovasc Interv Radiol, 2009, 32(4): 703-706.
52.	Jain G, Allon M, Saddekni S, et al. Does heparin coating improve patency or reduce infection of tunneled dialysis catheters?. Clin J Am Soc Nephrol, 2009, 4(11): 1787-1790.
53.	Sobhiyeh M, Bagherhosseini N. Comparison of patency of heparin-coated with non-heparin coated catheters in patients under hemodialysis: a randomized clinical trial. Med Sci, 2019, 23(96): 191-194.
54.	Kasirajan K. Outcomes after heparin-induced thrombocytopenia in patients with Propaten vascular grafts. Ann Vasc Surg, 2012, 26(6): 802-808.
55.	Zhang Y, Zhao Q, Li W, et al. Substrate independent liquid phase epitaxy of HKUST-1 as anticoagulant and antimicrobial coating. Adv Mater Interfaces, 2020, 7(12): 1902011.
56.	Bakola V, Karagkiozaki V, Tsiapla AR, et al. Dipyridamole-loaded biodegradable PLA nanoplatforms as coatings for cardiovascular stents. Nanotechnology, 2018, 29(27): 275101.
57.	Zheng Z, Li X, Dai X, et al. Surface functionalization of anticoagulation and anti-nonspecific adsorption with recombinant hirudin modification. Biomater Adv, 2022, 135: 212741.
58.	Wakai IY, Wang Q, Zhao J, et al. Surface modification of polycarbonate urethane by grafting polyethylene glycol and bivalirudin drug for improving hemocompatibility. Polym Adv Technol, 2023, 34(2): 531-538.
59.	Lukovic D, Nyolczas N, Hemetsberger R, et al. Human recombinant activated protein C-coated stent for the prevention of restenosis in porcine coronary arteries. J Mater Sci Mater, Med, 2015, 26(10): 241.
60.	Chandiwal A, Zaman FS, Mast AE, et al. Factor Xa inhibition by immobilized recombinant tissue factor pathway inhibitor. J Biomater Sci Polym Ed, 2006, 17(9): 1025-1037.
61.	Kaplan MA, Sergienko KV, Kolmakova AA, et al. Development of a biocompatible PLGA polymers capable to release thrombolytic enzyme prourokinase. J Biomater Sci Polym Ed, 2020, 31(11): 1405-1420.
62.	Yau JW, Teoh H, Verma S. Endothelial cell control of thrombosis. BMC Cardiovasc Disord, 2015, 15: 130.
63.	Figueiredo C, Eicke D, Yuzefovych Y, et al. Low immunogenic endothelial cells endothelialize the left ventricular assist device. Sci Rep, 2019, 9(1): 11318.
64.	Govindarajan T, Shandas R. Microgrooves encourage endothelial cell adhesion and organization on shape-memory polymer surfaces. Acs Appl Bio Mater, 2019, 2(5): 1897-1906.
65.	Bedair TM, Min IJ, Park W, et al. Covalent immobilization of fibroblast-derived matrix on metallic stent for expeditious re-endothelialization. J Ind Eng Chem, 2019, 70: 385-393.
66.	Munisso MC, Yamaoka T. Peptide with endothelial cell affinity and antiplatelet adhesion property to improve hemocompatibility of blood-contacting biomaterials. Pept Sci, 2019, 111(5): e24114.
67.	Hou YC, Li JA, Zhu SJ, et al. Tailoring of cardiovascular stent material surface by immobilizing exosomes for better pro-endothelialization function. Colloids Surf B Biointerfaces, 2020, 189: 110831.
68.	Royer C, Guay-begin AA, Chanseau C, et al. Bioactive micropatterning of biomaterials for induction of endothelial progenitor cell differentiation: acceleration of in situ endothelialization. J Biomed Mater Res A, 2020, 108(7): 1479-1492.
69.	Avci-Adali M, Ziemer G, Wendel HP. Induction of EPC homing on biofunctionalized vascular grafts for rapid in vivo self-endothelialization--a review of current strategies. Biotechnol Adv, 2010, 28(1): 119-129.

1. Wang Y, Sun X. Reevaluation of lock solutions for central venous catheters in hemodialysis: a narrative review. Ren Fail, 2022, 44(1): 1501-1518.
2. Ullrich H, Münzel T, Gori T. Coronary stent thrombosis- predictors and prevention. Dtsch Arztebl Int, 2020, 117(18): 320-326.
3. Teja B, Bosch NA, Diep C, et al. Complication rates of central venous catheters: a systematic review and meta-analysis. JAMA Intern Med, 2024, 184(5): 474-482.
4. Nilius H, Kaufmann J, Cuker A, et al. Comparative effectiveness and safety of anticoagulants for the treatment of heparin-induced thrombocytopenia. Am J Hematol, 2021, 96(7): 805-815.
5. Geller AI, Shehab N, Lovegrove MC, et al. Bleeding related to oral anticoagulants: trends in US emergency department visits, 2016-2020. Thromb Res, 2023, 225: 110-115.
6. Brash JL, Horbett TA, Latour RA, et al. The blood compatibility challenge. Part 2: Protein adsorption phenomena governing blood reactivity. Acta Biomater, 2019, 94: 11-24.
7. Weber M, Steinle H, Golombek S, et al. Blood-contacting biomaterials: in vitro evaluation of the hemocompatibility. Front Bioeng Biotechnol, 2018, 6: 99.
8. Jaffer IH, Weitz JI. The blood compatibility challenge. Part 1: Blood-contacting medical devices: the scope of the problem. Acta Biomater, 2019, 94: 2-10.
9. Visalakshan RM, Macgregor MN, Sasidharan S, et al. Biomaterial surface hydrophobicity-mediated serum protein adsorption and immune responses. ACS Appl Mater Inter, 2019, 11(31): 27615-27623.
10. Struczyńska M, Firkowska-boden I, Levandovsky N, et al. How crystallographic orientation-induced fibrinogen conformation affects platelet adhesion and activation on TiO₂. Adv Healthc Mater, 2023, 12(13): e2202508.
11. Sang Y, Roest M, de Laat B, et al. Interplay between platelets and coagulation. Blood Rev, 2021, 46: 100733.
12. Goel A, Tathireddy H, Wang SH, et al. Targeting the contact pathway of coagulation for the prevention and management of medical device-associated thrombosis. Semin Thromb Hemost, 2023.
13. Skinner SC, Derebail VK, Poulton CJ, et al. Hemodialysis-related complement and contact pathway activation and cardiovascular risk: a narrative review. Kidney Med, 2021, 3(4): 607-618.
14. Kourtzelis I, Markiewski MM, Doumas M, et al. Complement anaphylatoxin C5a contributes to hemodialysis-associated thrombosis. Blood, 2010, 116(4): 631-639.
15. Maitz MF, Martins MCL, Grabow N, et al. The blood compatibility challenge. Part 4: Surface modification for hemocompatible materials: passive and active approaches to guide blood-material interactions. Acta Biomater, 2019, 94: 33-43.
16. Neubauer K, Zieger B. Endothelial cells and coagulation. Cell Tissue Res, 2022, 387(3): 391-398.
17. Elwing H, Welin S, Askendal A, et al. A wettability gradient-method for studies of macromolecular interactions at the liquid solid interface. J Colloid Interface Sci, 1987, 119(1): 203-210.
18. Fan H, Guo Z. Bioinspired surfaces with wettability: biomolecule adhesion behaviors. Biomater Sci, 2020, 8(6): 1502-1535.
19. Stallard CP, McDonnell KA, Onayemi OD, et al. Evaluation of protein adsorption on atmospheric plasma deposited coatings exhibiting superhydrophilic to superhydrophobic properties. Biointerphases, 2012, 7(1/2/3/4): 31.
20. Wang P, Zhang YL, Fu KL, et al. Zinc-coordinated polydopamine surface with a nanostructure and superhydrophilicity for antibiofouling and antibacterial applications. Mater Adv, 2022, 3(13): 5476-5487.
21. Chang Y. Designs of zwitterionic polymers. J Polym Res, 2022, 29(7): 286.
22. Cheng CH, Chen GF, Lin JC. Studies of zwitterionic sulfobetaine functionalized polypropylene surface with or without polyethylene glycol spacer: surface characterization, antibacterial adhesion, and platelet compatibility evaluation. J Biomater Sci Polym Ed, 2020, 31(16): 2060-2077.
23. Huang KT, Hsieh PS, Dai LG, et al. Complete zwitterionic double network hydrogels with great toughness and resistance against foreign body reaction and thrombus. J Mater Chem B, 2020, 8(33): 7390-7402.
24. Guo LL, Cheng YF, Ren X, et al. Simultaneous deposition of tannic acid and poly(ethylene glycol) to construct the antifouling polymeric coating on titanium surface. Colloids Surf B Biointerfaces, 2021, 200: 111592.
25. Perrino C, Lee S, Choi SW, et al. A biomimetic alternative to poly(ethylene glycol) as an antifouling coating: resistance to nonspecific protein adsorption of poly(L-lysine)-graft-dextran. Langmuir, 2008, 24(16): 8850-8856.
26. Yang W, Xue H, LI W, et al. Pursuing “zero” protein adsorption of poly(carboxybetaine) from undiluted blood serum and plasma. Langmuir, 2009, 25(19): 11911-11916.
27. Tsai WB, Grunkemeier JM, Horbett TA. Human plasma fibrinogen adsorption and platelet adhesion to polystyrene. J Biomed Mater Res, 1999, 44(2): 130-139.
28. Yao M, Wei Z, Li J, et al. Microgel reinforced zwitterionic hydrogel coating for blood-contacting biomedical devices. Nat Commun, 2022, 13(1): 5339.
29. Klee D, Höcker H. Polymers for biomedical applications: improvement of the interface compatibility//Eastmond GC, Höcker H, Klee D. Biomedical applications polymer blends. Advances in polymer science, vol 149. Berlin, Heidelberg: Springer, 1999: 1-57.
30. Wu XH, Liew YK, Mai CW, et al. Potential of superhydrophobic surface for blood-contacting medical devices. Int J Mol Sci, 2021, 22(7): 3341.
31. Chen L, Han D, Jiang L. On improving blood compatibility: from bioinspired to synthetic design and fabrication of biointerfacial topography at micro/nano scales. Colloid Surface B, 2011, 85(1): 2-7.
32. Toes GJ, Van Muiswinkel KW, Van Oeveren W, et al. Superhydrophobic modification fails to improve the performance of small diameter expanded polytetrafluoroethylene vascular grafts. Biomaterials, 2002, 23(1): 255-262.
33. Betz T, Toepel I, Pfister K, et al. Impact of chronic kidney disease on the outcomes of infrapopliteal venous, and heparin-bonded expanded polytetrafluoroethylene bypass surgeries: a retrospective cohort study. Vasc Med, 2022, 27(1): 55-62.
34. Milner KR, Snyder AJ, Siedlecki CA. Sub-micron texturing for reducing platelet adhesion to polyurethane biomaterials. J Biomed Mater Res A, 2006, 76(3): 561-570.
35. Celik N, Sahin F, Ruzi M, et al. Blood repellent superhydrophobic surfaces constructed from nanoparticle-free and biocompatible materials. Colloids Surf B Biointerfaces, 2021, 205: 111864.
36. Montgomerie Z, Popat KC. Improved hemocompatibility and reduced bacterial adhesion on superhydrophobic titania nanoflower surfaces. Mater Sci Eng C Mater Biol Appl, 2021, 119: 111503.
37. Yun GT, Jung WB, Oh MS, et al. Springtail-inspired superomniphobic surface with extreme pressure resistance. Sci Adv, 2018, 4(8): eaat4978.
38. Leslie DC, Waterhouse A, Berthet JB, et al. A bioinspired omniphobic surface coating on medical devices prevents thrombosis and biofouling. Nat Biotechnol, 2014, 32(11): 1134-1140.
39. Roberts TR, Choi JH, Wendorff DS, et al. Tethered liquid perfluorocarbon coating for 72 hour heparin-free extracorporeal life support. ASAIO J, 2021, 67(7): 798-808.
40. Kuten Pella O, Hornyák I, Horváthy D, et al. Albumin as a biomaterial and therapeutic agent in regenerative medicine. Int J Mol Sci, 2022, 23(18): 10557.
41. Subramanian A. Corrigendum to “Evaluation of the real-time protein adsorption kinetics on albumin-binding surfaces by dynamic in situ spectroscopic ellipsometry” [TSF 520 (2012) 2200–2207]. Thin Solid Films, 2012, 520(19): 6334.
42. Gonçalves IC, Martins MC, Barbosa MA, et al. Protein adsorption and clotting time of pHEMA hydrogels modified with C18 ligands to adsorb albumin selectively and reversibly. Biomaterials, 2009, 30(29): 5541-5551.
43. Freitas SC, Maia S, Figueiredo AC, et al. Selective albumin-binding surfaces modified with a thrombin-inhibiting peptide. Acta Biomater, 2014, 10(3): 1227-1237.
44. Sivaraman B, Latour RA. Time-dependent conformational changes in adsorbed albumin and its effect on platelet adhesion. Langmuir, 2012, 28(5): 2745-2752.
45. Marois Y, Chakfé N, Guidoin R, et al. An albumin-coated polyester arterial graft: in vivo assessment of biocompatibility and healing characteristics. Biomaterials, 1996, 17(1): 3-14.
46. Kudo FA, Nishibe T, Miyazaki K, et al. Albumin-coated knitted dacron aortic prosthses. Study of postoperative inflammatory reactions. Int Angiol, 2002, 21(3): 214-217.
47. Li R, Li Y, Bai Y, et al. Achieving superior anticoagulation of endothelial membrane mimetic coating by heparin grafting at zwitterionic biocompatible interfaces. Int J Biol Macromol, 2024, 257(Pt 1): 128574.
48. Zhang Y, Man J, Liu J, et al. Construction of the mussel-inspired PDAM/lysine/heparin composite coating combining multiple anticoagulant strategies. ACS Appl Mater Interfaces, 2023, 15(23): 27719-27731.
49. Zhang M, Chan CHH, Pauls JP, et al. Investigation of heparin-loaded poly(ethylene glycol)-based hydrogels as anti-thrombogenic surface coatings for extracorporeal membrane oxygenation. J Mater Chem B, 2022, 10(26): 4974-4983.
50. Özdemir M, Taydas O, Danisan G, et al. Comparison of the complications and long-term results of heparin-coated and non-heparin-coated symmetric-tip hemodialysis catheters. J Vasc Access, 2023: 11297298231202536.
51. Clark TWI, Jacobs D, Charles HW, et al. Comparison of heparin-coated and conventional split-tip hemodialysis catheters. Cardiovasc Interv Radiol, 2009, 32(4): 703-706.
52. Jain G, Allon M, Saddekni S, et al. Does heparin coating improve patency or reduce infection of tunneled dialysis catheters?. Clin J Am Soc Nephrol, 2009, 4(11): 1787-1790.
53. Sobhiyeh M, Bagherhosseini N. Comparison of patency of heparin-coated with non-heparin coated catheters in patients under hemodialysis: a randomized clinical trial. Med Sci, 2019, 23(96): 191-194.
54. Kasirajan K. Outcomes after heparin-induced thrombocytopenia in patients with Propaten vascular grafts. Ann Vasc Surg, 2012, 26(6): 802-808.
55. Zhang Y, Zhao Q, Li W, et al. Substrate independent liquid phase epitaxy of HKUST-1 as anticoagulant and antimicrobial coating. Adv Mater Interfaces, 2020, 7(12): 1902011.
56. Bakola V, Karagkiozaki V, Tsiapla AR, et al. Dipyridamole-loaded biodegradable PLA nanoplatforms as coatings for cardiovascular stents. Nanotechnology, 2018, 29(27): 275101.
57. Zheng Z, Li X, Dai X, et al. Surface functionalization of anticoagulation and anti-nonspecific adsorption with recombinant hirudin modification. Biomater Adv, 2022, 135: 212741.
58. Wakai IY, Wang Q, Zhao J, et al. Surface modification of polycarbonate urethane by grafting polyethylene glycol and bivalirudin drug for improving hemocompatibility. Polym Adv Technol, 2023, 34(2): 531-538.
59. Lukovic D, Nyolczas N, Hemetsberger R, et al. Human recombinant activated protein C-coated stent for the prevention of restenosis in porcine coronary arteries. J Mater Sci Mater, Med, 2015, 26(10): 241.
60. Chandiwal A, Zaman FS, Mast AE, et al. Factor Xa inhibition by immobilized recombinant tissue factor pathway inhibitor. J Biomater Sci Polym Ed, 2006, 17(9): 1025-1037.
61. Kaplan MA, Sergienko KV, Kolmakova AA, et al. Development of a biocompatible PLGA polymers capable to release thrombolytic enzyme prourokinase. J Biomater Sci Polym Ed, 2020, 31(11): 1405-1420.
62. Yau JW, Teoh H, Verma S. Endothelial cell control of thrombosis. BMC Cardiovasc Disord, 2015, 15: 130.
63. Figueiredo C, Eicke D, Yuzefovych Y, et al. Low immunogenic endothelial cells endothelialize the left ventricular assist device. Sci Rep, 2019, 9(1): 11318.
64. Govindarajan T, Shandas R. Microgrooves encourage endothelial cell adhesion and organization on shape-memory polymer surfaces. Acs Appl Bio Mater, 2019, 2(5): 1897-1906.
65. Bedair TM, Min IJ, Park W, et al. Covalent immobilization of fibroblast-derived matrix on metallic stent for expeditious re-endothelialization. J Ind Eng Chem, 2019, 70: 385-393.
66. Munisso MC, Yamaoka T. Peptide with endothelial cell affinity and antiplatelet adhesion property to improve hemocompatibility of blood-contacting biomaterials. Pept Sci, 2019, 111(5): e24114.
67. Hou YC, Li JA, Zhu SJ, et al. Tailoring of cardiovascular stent material surface by immobilizing exosomes for better pro-endothelialization function. Colloids Surf B Biointerfaces, 2020, 189: 110831.
68. Royer C, Guay-begin AA, Chanseau C, et al. Bioactive micropatterning of biomaterials for induction of endothelial progenitor cell differentiation: acceleration of in situ endothelialization. J Biomed Mater Res A, 2020, 108(7): 1479-1492.
69. Avci-Adali M, Ziemer G, Wendel HP. Induction of EPC homing on biofunctionalized vascular grafts for rapid in vivo self-endothelialization--a review of current strategies. Biotechnol Adv, 2010, 28(1): 119-129.

West China Medical Journal

Advances in anti-thrombogenetic strategies of biomaterials

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