Skip to main content

Recent Advances in Hemocompatible Polymers for Biomedical Applications

  • Chapter
  • First Online:

Abstract

Blood-material interactions are critical to the success of implantable medical devices that are used in thousands of patients every day. Some common blood-contacting devices include catheters, stents, vascular grafts, heart valve prostheses, and extracorporeal circulation/membrane oxygenation systems. Among other complications, thrombosis and clot formation remains one of the major challenges in clinical application of these devices. The initial biological response of blood to a foreign surface is the rapid adsorption of plasma proteins, which is followed by platelet adhesion and activation, and ultimately thrombus formation. The key factors in clot formation are the chemical and physical nature of the surfaces and their interactions with the blood components, such as platelets and plasma proteins. Despite decades of research, an ideal non-thrombogenic surface is still yet to be identified and clinical use of these blood-contacting devices requires use of anticoagulation agents, increasing the risk of bleeding in patients. In this chapter, we will review some of the current and most promising strategies that have been used over the years to develop polymeric materials with improved hemocompatibility, including highly hydrophilic or hydrophobic surfaces, albumin coated surfaces, zwitterionic polymers, attached endothelial cells, patterned surfaces, immobilized heparin, and nitric oxide (NO) releasing/generating surfaces. We will also discuss some of the important techniques employed (using in vitro and in vivo models) to assess the hemocompatibility of any new material, including the measurement of platelet preservation, platelet and protein adhesion, the effect of flow rates on thrombosis, and the ultimate surface clot area.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

A-A:

Arterio-arterlial

A-V:

Arterio-venous

Alb:

Albumin

Alg:

Sodium alginate

APTT:

Activated partial thromboplastin time

ATRP:

Atom transfer radical polymerization

CysNO:

S-nitrosocysteine

DACA:

Diaminoalkyltrimethoxysilane

DBHD/N2O2 :

Diazeniumdiolated dibutylhexanediamine

DBHD:

N,N′-dibutyl-1,6-hexanediamine

DMHD/N2O2 :

Diazeniumdiolated N,N′-dimethyl-1,6-hexanediamine

DMMSA:

N,N-dimethyl-N-methacryloxyethyl-N-(3-sulfopropyl) ammonium

DMPAMS:

N,N-dimethyl, N-(2-ethyl phosphate ethyl)-aminopropyltrimethyoxysilane

DOS:

Dioctyl sebacate

EC:

Endothelial cells

ECC:

Extracorporeal circulation

GPx:

Glutathione peroxidase

GSH:

Glutathione

GSNO:

S-nitrosoglutathione

HEMA:

2-hydroxyethyl methacrylate

IgG:

Immunoglobulin

LPEI/N2O2 :

Diazeniumdiolated linear polyethylenimine

MDI:

Methylene diphenyl isocyanate

NO:

Nitric oxide

NOgen:

NO-generating

NONOate:

Diazeniumdiolate

NOrel:

NO-releasing

P(PEGDMA):

Poly(poly(ethylene glycol) dimethacrylate)

PAAm:

Polyacrylamides

PDMS:

Poly(dimethylsiloxane)

PEG:

Poly(ethylene glycol)

PEI:

Polyethylenimine

PEGME:

Poly(ethylene glycol) monomethyl ether

PEO:

Poly(ethylene oxide)

PGA:

Polyglycolic acid

PHEMA:

Poly(hydroxyethyl methacrylate)

PLGA:

Poly(lactic-co-glycolic acid)

PMEA:

Poly(2-methoxyethyl acrylate)

PNVP:

Poly(N-vinyl pyrrolidone)

PRP:

Platelet-rich plasma

PS-CO2 :

Carbon dioxide as plasma-treated polystyrene

PTFE:

Polytetrafluoroethylene

PVA:

Poly(vinyl alcohol)

PVC:

Poly(vinyl chloride)

PVMMA:

Poly(vinyl methyl ether-co-malic anhydride)

PVP:

Poly(vinyl pyrrolidone)

RSNO:

S-nitrosothiol

RSSR:

Disulfide

SeCA:

Selenocystamine

SeDPA:

3,3-diselenidedipropionic acid

SNAC:

S-nitroso-N-acetyl-L-cysteine

SNAP:

S-nitroso-N-acetylpenicillamine

SR:

Silicone rubber

vWF:

von Willebrand Factor

References

  1. Ratner, B.D.: The catastrophe revisited: blood compatibility in the 21st century. Biomaterials 28(34), 5144–5147 (2007)

    CAS  Google Scholar 

  2. Colman, R.W.: Mechanisms of thrombus formation and dissolution. Cardiovasc. Pathol. 2(3), 23–31 (1993)

    Google Scholar 

  3. Gorbet, M.B., Sefton, M.V.: Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 25(26), 5681–5703 (2004)

    CAS  Google Scholar 

  4. Dwyer, A.: Surface-treated catheters—a review. In: Seminars in dialysis, pp 542–546. Wiley Online Library (2008)

    Google Scholar 

  5. Ratner, B.D.: Blood compatibility—a perspective. J. Biomater. Sci. Polym. Ed. 11(11), 1107–1119 (2000)

    CAS  Google Scholar 

  6. Gaffney, A.M., Wildhirt, S.M., Griffin, M.J., Annich, G.M., Radomski, M.W.: Extracorporeal life support. BMJ 341 (2010)

    Google Scholar 

  7. Robinson, T.M., Kickler, T.S., Walker, L.K., Ness, P., Bell, W.: Effect of extracorporeal membrane oxygenation on platelets in newborns. Crit. Care Med. 21(7), 1029–1034 (1993)

    CAS  Google Scholar 

  8. Horbett, T.A.: Principles underlying the role of adsorbed plasma proteins in blood interactions with foreign materials. Cardiovasc. Pathol. 2(3), 137–148 (1993)

    Google Scholar 

  9. Schopka, S., Schmid, T., Schmid, C., Lehle, K.: Current strategies in cardiovascular biomaterial functionalization. Materials 3(1), 638–655 (2010)

    CAS  Google Scholar 

  10. Brashm, J., Horbett, T.: Proteins at interfaces: physicochemical and biochemical studies. In: ACS Symposium Series, 1987, p 1. American Chemical Society, Washington, DC

    Google Scholar 

  11. Ikada, Y., Suzuki, M., Tamada, Y.: Polymer surfaces possessing minimal interaction with blood components. In: Polymers as biomaterials, pp 135–147. Springer, Heidelberg (1984)

    Google Scholar 

  12. Nagaoka, S., Mori, Y., Takiuchi, H., Yokota, K., Tanzawa, H., Nishiumi, S.: Interaction between blood components and hydrogels with poly (oxyethylene) chains. In: Polymers as biomaterials, pp 361–374. Springer, Heidelberg (1984)

    Google Scholar 

  13. Jeon, S., Lee, J., Andrade, J., De Gennes, P.: Protein—surface interactions in the presence of polyethylene oxide: I. Simplified Theo. J Colloid Interface Sci 142(1), 149–158 (1991)

    CAS  Google Scholar 

  14. Peppas, N.A., Huang, Y., Torres-Lugo, M., Ward, J.H., Zhang, J.: Physicochemical, foundations and structural design of hydrogels in medicine and biology. Annu. Rev. Biomed. Eng. 2, 9–29 (2000)

    CAS  Google Scholar 

  15. Okada, T., Ikada, Y.: Modification of silicone surface by graft polymerization of acrylamide with corona discharge. Makromol. Chem. 192(8), 1705–1713 (1991)

    CAS  Google Scholar 

  16. Tanaka, M., Hayashi, T., Morita, S.: The roles of water molecules at the biointerface of medical polymers. Polym. J. 45(7), 701–710 (2013)

    CAS  Google Scholar 

  17. Wang, H., Yu, T., Zhao, C., Du, Q.: Improvement of hydrophilicity and blood compatibility on polyethersulfone membrane by adding polyvinylpyrrolidone. Fibers Polym. 10(1), 1–5 (2009)

    Google Scholar 

  18. Hanson, S.R., Harker, L.A., Ratner, B.D., Hoffman, A.: In vivo evaluation of artificial surfaces with a nonhuman primate model of arterial thrombosis. J. Lab. Clin. Med. 95(2), 289–304 (1980)

    CAS  Google Scholar 

  19. Morra, M., Occhiello, E., Garbassi, F.: Surface modification of blood contacting polymers by poly (ethyleneoxide). Clin. Mater. 14(3), 255–265 (1993)

    CAS  Google Scholar 

  20. Kwon, O.H., Nho, Y.C., Park, K.D., Kim, Y.H.: Graft copolymerization of polyethylene glycol methacrylate onto polyethylene film and its blood compatibility. J. Appl. Polym. Sci. 71(4), 631–641 (1999)

    CAS  Google Scholar 

  21. Balakrishnan, B., Kumar, D., Yoshida, Y., Jayakrishnan, A.: Chemical modification of poly (vinyl chloride) resin using poly (ethylene glycol) to improve blood compatibility. Biomaterials 26(17), 3495–3502 (2005)

    CAS  Google Scholar 

  22. Amiji, M.M.: Synthesis of anionic poly(ethylene glycol) derivative for chitosan surface modification in blood-contacting applications. Carbohydr. Polym. 32(3–4), 193–199 (1997)

    CAS  Google Scholar 

  23. Wang, J., Pan, C.J., Huang, N., Sun, H., Yang, P., Leng, Y.X., Chen, J.Y., Wan, G.J., Chu, P.K.: Surface characterization and blood compatibility of poly(ethylene terephthalate) modified by plasma surface grafting. Surf. Coat. Technol. 196(1–3), 307–311 (2005)

    CAS  Google Scholar 

  24. Okner, R., Domb, A.J., Mandler, D.: Electrochemically deposited poly(ethylene glycol)-based sol–gel thin films on stainless steel stents. New J. Chem. 33(7), 1596–1604 (2009)

    CAS  Google Scholar 

  25. Nho, Y.C., Kwon, O.H.: Blood compatibility of AAc, HEMA, and PEGMA-grafted cellulose film. Radiat. Phys. Chem. 66(4), 299–307 (2003)

    CAS  Google Scholar 

  26. Li, M., Neoh, K.G., Xu, L.Q., Wang, R., Kang, E.T., Lau, T., Olszyna, D.P., Chiong, E.: Surface modification of silicone for biomedical applications requiring long-term antibacterial, antifouling, and hemocompatible properties. Langmuir 28(47), 16408–16422 (2012)

    CAS  Google Scholar 

  27. Jin, J., Jiang, W., Yin, J.H., Ji, X.L., Stagnaro, P.: Plasma proteins adsorption mechanism on polyethylene-grafted poly(ethylene glycol) surface by quartz crystal microbalance with dissipation. Langmuir 29(22), 6624–6633 (2013)

    CAS  Google Scholar 

  28. Chung, C.W., Kim, H.W., Kim, Y.B., Rhee, Y.H.: Poly(ethylene glycol)-grafted poly(3-hydroxyundecenoate) networks for enhanced blood compatibility. Int. J. Biol. Macromol. 32(1–2), 17–22 (2003)

    CAS  Google Scholar 

  29. Chiag, Y.C., Chang, Y., Chen, W.Y., Ruaan, R.C.: Biofouling resistance of ultrafiltration membranes controlled by surface self-assembled coating with PEGylated copolymers. Langmuir 28(2), 1399–1407 (2012)

    CAS  Google Scholar 

  30. Bajpai, A.K.: Blood protein adsorption onto a polymeric biomaterial of polyethylene glycol and poly[(2-hydroxyethyl methacrylate)-co-acrylonitrile] and evaluation of in vitro blood compatibility. Polym. Int. 54(2), 304–315 (2005)

    CAS  Google Scholar 

  31. Alibeik, S., Zhu, S., Brash, J.L.: Surface modification with PEG and hirudin for protein resistance and thrombin neutralization in blood contact. Colloids Surf. B 81(2), 389–396 (2010)

    CAS  Google Scholar 

  32. Harris, J.M.: Poly (ethylene glycol) chemistry: biotechnical and biomedical applications. Springer, Heidelberg (1992)

    Google Scholar 

  33. Llanos, G.R., Sefton, M.V.: Immobilization of poly (ethylene glycol) onto a poly (vinyl alcohol) hydrogel: 2. Evaluation of thrombogenicity. J. Biomed. Mater. Res. 27(11), 1383–1391 (1993)

    CAS  Google Scholar 

  34. Lee, J.H., Lee, H.B.: Platelet adhesion onto wettability gradient surfaces in the absence and presence of plasma proteins. J. Biomed. Mater. Res. 41(2), 304–311 (1998)

    CAS  Google Scholar 

  35. Sefton, M., Gemmell, C., Gorbet, M. Nonthrombogenic treatments and strategies. Biomaterials Science: An Introduction to Materials in Medicine, pp. 456–470. Elsevier, New York (2004)

    Google Scholar 

  36. Tanaka, M., Motomura, T., Kawada, M., Anzai, T., Yuu, K., Shiroya, T., Shimura, K., Onishi, M., Akira, M.: Blood compatible aspects of poly(2-methoxyethylacrylate) (PMEA)—relationship between protein adsorption and platelet adhesion on PMEA surface. Biomaterials 21(14), 1471–1481 (2000)

    CAS  Google Scholar 

  37. Nydegger, U., Rieben, R., Lämmle, B.: Biocompatibility in transfusion medicine. Transfus. Sci. 17(4), 481–488 (1996)

    CAS  Google Scholar 

  38. Kolobow, T., Stool, E., Weathersby, P., Pierce, J., Hayano, F., Suaudeau, J.: Superior blood compatibility of silicone rubber free of silica filler in the membrane lung. ASAIO Trans. 20, 269 (1974)

    Google Scholar 

  39. Szycher, M.: Biostability of polyurethane elastomers: a critical review. J. Biomater. Appl. 3(2), 297–402 (1988)

    CAS  Google Scholar 

  40. Lassen, B., Malmsten, M.: Structure of protein layers during competitive adsorption. J. Colloid Interface Sci. 180(2), 339–349 (1996)

    CAS  Google Scholar 

  41. Sivaraman, B., Fears, K.P., Latour, R.A.: Investigation of the effects of surface chemistry and solution concentration on the conformation of adsorbed proteins using an improved circular dichroism method. Langmuir 25(5), 3050–3056 (2009)

    CAS  Google Scholar 

  42. Cozzens, D., Luk, A., Ojha, U., Ruths, M., Faust, R.: Surface characterization and protein interactions of segmented polyisobutylene-based thermoplastic polyurethanes. Langmuir 27(23), 14160–14168 (2011)

    CAS  Google Scholar 

  43. Bahulekar, R., Tamura, N., Ito, S., Kodama, M.: Platelet adhesion and complement activation studies on poly (N-alkyl mono and disubstituted) acrylamide derivatives. Biomaterials 20(4), 357–362 (1999)

    CAS  Google Scholar 

  44. Matsuda, T., Ito, S.: Surface coating of hydrophilic-hydrophobic block co-polymers on a poly (acrylonitrile) haemodialyser reduces platelet adhesion and its transmembrane stimulation. Biomaterials 15(6), 417–422 (1994)

    CAS  Google Scholar 

  45. Hoffman, A.S., Cohn, D., Hanson, S.R., Harker, L.A., Horbett, T.A., Ratner, B.D., Reynolds, L.O.: Application of radiation-grafted hydrogels as blood-contacting biomaterials. Radiat. Phys. Chem. 22(1), 267–283 (1983)

    CAS  Google Scholar 

  46. Khorasani, M., Mirzadeh, H.: In vitro blood compatibility of modified PDMS surfaces as superhydrophobic and superhydrophilic materials. J. Appl. Polym. Sci. 91(3), 2042–2047 (2004)

    CAS  Google Scholar 

  47. Okubo, M., Hattori, H.: Competitive adsorption of fibrinogen and albumin onto polymer microspheres having hydrophilic/hydrophobic heterogeneous surface structures. Colloid Polym. Sci. 271(12), 1157–1164 (1993)

    CAS  Google Scholar 

  48. Klose, T., Welzel, P.B., Werner, C.: Protein adsorption from flowing solutions on pure and maleic acid copolymer modified glass particles. Colloids Surf., B 51(1), 1–9 (2006)

    CAS  Google Scholar 

  49. Sefton, M.V., Gemmell, C.H., Gorbet, M.B.: What really is blood compatibility? J. Biomater. Sci. Polym. Ed. 11(11), 1165–1182 (2000)

    CAS  Google Scholar 

  50. Andrade, J., Hlady, V.: Protein adsorption and materials biocompatibility: a tutorial review and suggested hypotheses. In: Biopolymers/Non-Exclusion HPLC, pp 1–63. Springer, Heidelberg (1986)

    Google Scholar 

  51. Kottke-Marchant, K., Anderson, J.M., Umemura, Y., Marchant, R.E.: Effect of albumin coating on the in vitro blood compatibility of Dacron® arterial prostheses. Biomaterials 10(3), 147–155 (1989)

    CAS  Google Scholar 

  52. Guidoin, R., Snyder, R., Martin, L., Botzko, K., Marois, M., Awad, J., King, M., Domurado, D., Bedros, M., Gosselin, C.: Albumin coating of a knitted polyester arterial prosthesis: an alternative to preclotting. Ann. Thorac. Surg. 37(6), 457–465 (1984)

    CAS  Google Scholar 

  53. Bos, G.W., Scharenborg, N.M., Poot, A.A., Engbers, G.H., Beugeling, T., Van Aken, W.G., Feijen, J.: Blood compatibility of surfaces with immobilized albumin–heparin conjugate and effect of endothelial cell seeding on platelet adhesion. J. Biomed. Mater. Res. 47(3), 279–291 (1999)

    CAS  Google Scholar 

  54. Mohammad, S., Olsen, D.: Immobilized albumin-immunoglobulin G for improved hemocompatibility of biopolymers. ASAIO J. 35(3), 384–387 (1989)

    CAS  Google Scholar 

  55. Hoffman, A., Schmer, G., Harris, C., Kraft, W.: Covalent binding of biomolecules to radiation-grafted hydrogels on inert polymer surfaces. ASAIO J. 18(1), 10–16 (1972)

    CAS  Google Scholar 

  56. Mikhalovska, L.I., Santin, M., Denyer, S.P., Lloyd, A.W., Teer, D.G., Field, S., Mikhalovsky, S.V.: Fibrinogen adsorption and platelet adhesion to metal and carbon coatings. Thromb. Haemost. 92(11), 1032–1039 (2004)

    CAS  Google Scholar 

  57. Dion, I., Roques, X., Baquey, H., Baudet, E., Basse Cathalinat, B., More, N.: Hemocompatibility of diamond-like carbon coating. Bio-Med. Mater. Eng. 3(1), 51–55 (1993)

    CAS  Google Scholar 

  58. Sivaraman, B., Latour, R.A.: The adherence of platelets to adsorbed albumin by receptor-mediated recognition of binding sites exposed by adsorption-induced unfolding. Biomaterials 31(6), 1036–1044 (2010)

    CAS  Google Scholar 

  59. Sivaraman, B., Latour, R.A.: Delineating the roles of the GPIIb/IIIa and GP-Ib-IX-V platelet receptors in mediating platelet adhesion to adsorbed fibrinogen and albumin. Biomaterials 32(23), 5365–5370 (2011)

    CAS  Google Scholar 

  60. Oyane, A., Ishizone, T., Uchida, M., Furukawa, K., Ushida, T., Yokoyama, H.: Spontaneous formation of blood-compatible surfaces on hydrophobic polymers: Surface enrichment of a block copolymer with a water-soluble block. Adv Mater 17(19), 2329–2332 (2005)

    CAS  Google Scholar 

  61. Okano, T., Aoyagi, T., Kataoka, K., Abe, K., Sakurai, Y., Shimada, M., Shinohara, I.: Hydrophilic-hydrophobic microdomain surfaces having an ability to suppress platelet aggregation and their in vitro antithrombogenicity. J. Biomed. Mater. Res. 20(7), 919–927 (1986)

    CAS  Google Scholar 

  62. Okano, T., Nishiyama, S., Shinohara, I., Akaike, T., Sakurai, Y., Kataoka, K., Tsuruta, T.: Effect of hydrophilic and hydrophobic microdomains on mode of interaction between block polymer and blood platelets. J. Biomed. Mater. Res. 15(3), 393–402 (1981)

    CAS  Google Scholar 

  63. Sato, H., Nakajima, A., Hayashi, T., Chen, G.W., Noishiki, Y.: Microheterophase structure, permeability, and biocompatibility of A-B-A triblock copolymer membranes composed of poly (γ-ethyl L-glutamate) as the A component and polybutadiene as the B component. J. Biomed. Mater. Res. 19(9), 1135–1155 (1985)

    CAS  Google Scholar 

  64. Nojiri, C., Okano, T., Jacobs, H.A., Park, K.D., Mohammad, S.F., Olsen, D.B., Kim, S.W.: Blood compatibility of PEO grafted polyurethane and HEMA/styrene block copolymer surfaces. J. Biomed. Mater. Res. 24(9), 1151–1171 (1990)

    CAS  Google Scholar 

  65. Takahara, A., Tashita, J.-I., Kajiyama, T., Takayanagi, M., Macknight, W.J.: Microphase separated structure and blood compatibility of segmented poly (urethaneureas) with different diamines in the hard segment. Polymer 26(7), 978–986 (1985)

    CAS  Google Scholar 

  66. Takahara, A., Tashita, J.-I., Kajiyama, T., Takayanagi, M., Macknight, W.J.: Microphase separated structure, surface composition and blood compatibility of segmented poly (urethaneureas) with various soft segment components. Polymer 26(7), 987–996 (1985)

    CAS  Google Scholar 

  67. Sasaki, T., Ratner, B.D., Hoffman, A.S.: Radiation-induced co-graft polymerization of 2-hydroxyethyl methacrylate and ethyl methacrylate onto silicone rubber films. In: Abstracts of Papers of ACS. ACS, Washington, DC, Jan 1975

    Google Scholar 

  68. Okano, T., Uruno, M., Sugiyama, N., Shimada, M., Shinohara, I., Kataoka, K., Sakurai, Y.: Suppression of platelet activity on microdomain surfaces of 2-hydroxyethyl methacrylate-polyether block copolymers. J. Biomed. Mater. Res. 20(7), 1035–1047 (1986)

    CAS  Google Scholar 

  69. Lewis, K.B., Ratner, B.D.: Observation of surface rearrangement of polymers using ESCA. J. Colloid Interface Sci. 159(1), 77–85 (1993)

    CAS  Google Scholar 

  70. Chen, H., Zhang, Z., Chen, Y., Brook, M.A., Sheardown, H.: Protein repellant silicone surfaces by covalent immobilization of poly (ethylene oxide). Biomaterials 26(15), 2391–2399 (2005)

    CAS  Google Scholar 

  71. Shen, M., Martinson, L., Wagner, M.S., Castner, D.G., Ratner, B.D., Horbett, T.A.: PEO-like plasma polymerized tetraglyme surface interactions with leukocytes and proteins: in vitro and in vivo studies. J. Biomater. Sci. Polym. Ed. 13(4), 367–390 (2002)

    CAS  Google Scholar 

  72. Fushimi, F., Nakayama, M., Nishimura, K., Hiyoshi, T.: Platelet adhesion, contact phase coagulation activation, and C5a generation of polyethylene glycol acid-grafted high flux cellulosic membrane with varieties of grafting amounts. Artif. Organs 22(10), 821–826 (1998)

    CAS  Google Scholar 

  73. Gorbet, M.B., Sefton, M.V.: Leukocyte activation and leukocyte procoagulant activities after blood contact with polystyrene and polyethylene glycol–immobilized polystyrene beads. J. Lab. Clin. Med. 137(5), 345–355 (2001)

    CAS  Google Scholar 

  74. Hansson, K.M., Tosatti, S., Isaksson, J., Wetterö, J., Textor, M., Lindahl, T.L., Tengvall, P.: Whole blood coagulation on protein adsorption-resistant PEG and peptide functionalised PEG-coated titanium surfaces. Biomaterials 26(8), 861–872 (2005)

    CAS  Google Scholar 

  75. Suggs, L.J., Shive, M.S., Garcia, C.A., Anderson, J.M., Mikos, A.G.: In vitro cytotoxicity and in vivo biocompatibility of poly (propylene fumarate-co-ethylene glycol) hydrogels. J. Biomed. Mater. Res. 46(1), 22–32 (1999)

    CAS  Google Scholar 

  76. Gombotz, W.R., Guanghui, W., Horbett, T.A., Hoffman, A.S.: Protein adsorption to poly (ethylene oxide) surfaces. J. Biomed. Mater. Res. 25(12), 1547–1562 (1991)

    CAS  Google Scholar 

  77. Norde, W., Gage, D.: Interaction of bovine serum albumin and human blood plasma with PEO-tethered surfaces: influence of PEO chain length, grafting density, and temperature. Langmuir 20(10), 4162–4167 (2004)

    CAS  Google Scholar 

  78. Kizhakkedathu, J.N., Janzen, J., Le, Y., Kainthan, R.K., Brooks, D.E.: Poly (oligo (ethylene glycol) acrylamide) brushes by surface initiated polymerization: effect of macromonomer chain length on brush growth and protein adsorption from blood plasma. Langmuir 25(6), 3794–3801 (2009)

    CAS  Google Scholar 

  79. Lai, B.F., Creagh, A.L., Janzen, J., Haynes, C.A., Brooks, D.E., Kizhakkedathu, J.N.: The induction of thrombus generation on nanostructured neutral polymer brush surfaces. Biomaterials 31(26), 6710–6718 (2010)

    CAS  Google Scholar 

  80. Thierry, B., Merhi, Y., Silver, J., Tabrizian, M.: Biodegradable membrane-covered stent from chitosan-based polymers. J. Biomed. Mater. Res. A 75(3), 556–566 (2005)

    Google Scholar 

  81. Wright, M.J., Woodrow, G., Umpleby, S., Hull, S., Brownjohn, A.M., Turney, J.H.: Low thrombogenicity of polyethylene glycol–grafted cellulose membranes does not influence heparin requirements in hemodialysis. Am. J. Kidney Dis. 34(1), 36–42 (1999)

    CAS  Google Scholar 

  82. Sirolli, V., Di Stante, S., Stuard, S., Di Liberato, L., Amoroso, L., Cappelli, P., Bonomini, M.: Biocompatibility and functional performance of a polyethylene glycol acid-grafted cellulosic membrane for hemodialysis. Int. J. Artif. Organs 23(6), 356–364 (2000)

    CAS  Google Scholar 

  83. Cao, L., Sukavaneshvar, S., Ratner, B.D., Horbett, T.A.: Glow discharge plasma treatment of polyethylene tubing with tetraglyme results in ultralow fibrinogen adsorption and greatly reduced platelet adhesion. J. Biomed. Mater. Res. A 79(4), 788–803 (2006)

    Google Scholar 

  84. Rodriguez-Emmenegger, C., Brynda, E., Riedel, T., Houska, M., Šubr, V., Alles, A.B., Hasan, E., Gautrot, J.E., Huck, W.T.: Polymer brushes showing non-fouling in blood plasma challenge the currently accepted design of protein resistant surfaces. Macromol. Rapid Commun. 32(13), 952–957 (2011)

    CAS  Google Scholar 

  85. Herring, M.B., Compton, R., Legrand, D.R., Gardner, A.L.: Endothelial cell seeding in the management of vascular thrombosis. Semin. Thromb. Hemost. 15(2), 200–205 (1989)

    Google Scholar 

  86. Williams, S.K., Rose, D.G., Jarrell, B.E.: Microvascular endothelial cell sodding of ePTFE vascular grafts: improved patency and stability of the cellular lining. J. Biomed. Mater. Res. 28(2), 203–212 (1994)

    CAS  Google Scholar 

  87. Zilla, P., Deutsch, M., Meinhart, J., Puschmann, R., Eberl, T., Minar, E., Dudczak, R., Lugmaier, H., Schmidt, P., Noszian, I.: Clinical in vitro endothelialization of femoropopliteal bypass grafts: an actuarial follow-up over three years. J. Vasc. Surg. 19(3), 540–548 (1994)

    CAS  Google Scholar 

  88. Kutryk, M., van Dortmont, L., de Crom, R., van der Kamp, A., Verdouw, P., van der Giessen, W.: Seeding of intravascular stents by the xenotransplantation of genetically modified endothelial cells. Semin. Interv. Cardiol. 3(3-4), 217–220 (1998)

    Google Scholar 

  89. Zünd, G., Hoerstrup, S.P., Schoeberlein, A., Lachat, M., Uhlschmid, G., Vogt, P.R., Turina, M.: Tissue engineering: a new approach in cardiovascular surgery; seeding of human fibroblasts followed by human endothelial cells on resorbable mesh. Eur. J. Cardiothorac. Surg. 13(2), 160–164 (1998)

    Google Scholar 

  90. Taite, L.J., Yang, P., Jun, H.-W., West, J.L.: Nitric oxide-releasing polyurethane–PEG copolymer containing the YIGSR peptide promotes endothelialization with decreased platelet adhesion. J. Biomed. Mater. Res. B Appl. Biomater. 84(1), 108–116 (2008)

    Google Scholar 

  91. L’heureux, N., Pâquet, S., Labbé, R., Germain, L., Auger, F.A.: A completely biological tissue-engineered human blood vessel. FASEB J 12(1), 47–56 (1998)

    Google Scholar 

  92. Kawamoto, Y., Nakao, A., Ito, Y., Wada, N., Kaibara, M.: Endothelial cells on plasma-treated segmented-polyurethane: adhesion strength, antithrombogenicity and cultivation in tubes. J. Mater. Sci. Mater. Med. 8(9), 551–557 (1997)

    CAS  Google Scholar 

  93. Li, J., Ding, M., Fu, Q., Tan, H., Xie, X., Zhong, Y.: A novel strategy to graft RGD peptide on biomaterials surfaces for endothelization of small-diamater vascular grafts and tissue engineering blood vessel. J. Mater. Sci. Mater. Med. 19(7), 2595–2603 (2008)

    CAS  Google Scholar 

  94. Yin, M., Yuan, Y., Liu, C., Wang, J.: Development of mussel adhesive polypeptide mimics coating for in-situ inducing re-endothelialization of intravascular stent devices. Biomaterials 30(14), 2764–2773 (2009)

    CAS  Google Scholar 

  95. Jiang, S., Cao, Z.: Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Adv. Mater. 22(9), 920–932 (2010)

    CAS  Google Scholar 

  96. Wu, L., Guo, Z., Meng, S., Zhong, W., Du, Q., Chou, L.L.: Synthesis of a zwitterionic silane and its application in the surface modification of silicon-based material surfaces for improved hemocompatibility. ACS Appl. Mater. Interfaces 2(10), 2781–2788 (2010)

    CAS  Google Scholar 

  97. Zhang, Z., Chen, S., Chang, Y., Jiang, S.: Surface grafted sulfobetaine polymers via atom transfer radical polymerization as superlow fouling coatings. J. Phys. Chem. B 110(22), 10799–10804 (2006)

    CAS  Google Scholar 

  98. Ishihara, K., Nomura, H., Mihara, T., Kurita, K., Iwasaki, Y., Nakabayashi, N.: Why do phospholipid polymers reduce protein adsorption? J. Biomed. Mater. Res. 39(2), 323–330 (1998)

    CAS  Google Scholar 

  99. Holmlin, R.E., Chen, X., Chapman, R.G., Takayama, S., Whitesides, G.M.: Zwitterionic SAMs that resist nonspecific adsorption of protein from aqueous buffer. Langmuir 17(9), 2841–2850 (2001)

    CAS  Google Scholar 

  100. Jiang, Y., Rongbing, B., Ling, T., Jian, S., Sicong, L.: Blood compatibility of polyurethane surface grafted copolymerization with sulfobetaine monomer. Colloids Surf. B Biointerfaces 36(1), 27–33 (2004)

    CAS  Google Scholar 

  101. Min, D.Y., Li, Z.Z., Shen, J., Lin, S.C.: Research and synthesis of organosilicon nonthrombogenic materials containing sulfobetaine group. Colloids Surf. B Biointerfaces 79(2), 415–420 (2010)

    CAS  Google Scholar 

  102. Yuan, J., Lin, S., Shen, J.: Enhanced blood compatibility of polyurethane functionalized with sulfobetaine. Colloids Surf. B Biointerfaces 66(1), 90–95 (2008)

    CAS  Google Scholar 

  103. West, S.L., Salvage, J.P., Lobb, E.J., Armes, S.P., Billingham, N.C., Lewis, A.L., Hanlon, G.W., Lloyd, A.W.: The biocompatibility of crosslinkable copolymer coatings containing sulfobetaines and phosphobetaines. Biomaterials 25(7–8), 1195–1204 (2004)

    CAS  Google Scholar 

  104. Lobb, E.J., Ma, I., Billingham, N.C., Armes, S.P., Lewis, A.L.: Facile synthesis of well-defined, biocompatible phosphorylcholine-based methacrylate copolymers via atom transfer radical polymerization at 20 C. J. Am. Chem. Soc. 123(32), 7913–7914 (2001)

    CAS  Google Scholar 

  105. Ma, H., Hyun, J., Stiller, P., Chilkoti, A.: “Non-fouling” oligo(ethylene glycol)- functionalized polymer brushes synthesized by surface-initiated atom transfer radical polymerization. Adv. Mater. 16(4), 338–341 (2004)

    CAS  Google Scholar 

  106. Zhang, Z., Zhang, M., Chen, S., Horbett, T.A., Ratner, B.D., Jiang, S.: Blood compatibility of surfaces with superlow protein adsorption. Biomaterials 29(32), 4285–4291 (2008)

    CAS  Google Scholar 

  107. Yuan, J., Zhang, J., Zhou, J., Yuan, Y., Shen, J., Lin, S.: Platelet adhesion onto segmented polyurethane surfaces modified by carboxybetaine. J. Biomater. Sci. Polym. Ed. 14(12), 1339–1349 (2003)

    CAS  Google Scholar 

  108. Kitano, H., Tada, S., Mori, T., Takaha, K., Gemmei-Ide, M., Tanaka, M., Fukuda, M., Yokoyama, Y.: Correlation between the structure of water in the vicinity of carboxybetaine polymers and their blood-compatibility. Langmuir 21(25), 11932–11940 (2005)

    CAS  Google Scholar 

  109. Lee, B., Shin, H.-S., Park, K., Han, D.: Surface grafting of blood compatible zwitterionic poly(ethylene glycol) on diamond-like carbon-coated stent. J. Mater. Sci. Mater. Med. 22(3), 507–514 (2011)

    CAS  Google Scholar 

  110. Yuan, Y., Ai, F., Zang, X., Zhuang, W., Shen, J., Lin, S.: Polyurethane vascular catheter surface grafted with zwitterionic sulfobetaine monomer activated by ozone. Colloids Surf. B Biointerfaces 35(1), 1–5 (2004)

    CAS  Google Scholar 

  111. Galli, M., Sommariva, L., Prati, F., Zerboni, S., Politi, A., Bonatti, R., Mameli, S., Butti, E., Pagano, A., Ferrari, G.: Acute and mid-term results of phosphorylcholine-coated stents in primary coronary stenting for acute myocardial infarction. Catheter Cardiovasc. Interv. 53(2), 182–187 (2001)

    CAS  Google Scholar 

  112. Lewis, A., Tolhurst, L., Stratford, P.: Analysis of a phosphorylcholine-based polymer coating on a coronary stent pre-and post-implantation. Biomaterials 23(7), 1697–1706 (2002)

    CAS  Google Scholar 

  113. Rabenstein, D.L.: Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 19(3), 312–331 (2002)

    CAS  Google Scholar 

  114. Hylton, D.M., Shalaby, S.W., Latour, R.A.: Direct correlation between adsorption-induced changes in protein structure and platelet adhesion. J Biomed. Mater. Res. A 73A(3), 349–358 (2005)

    CAS  Google Scholar 

  115. Ayres, N., Holt, D., Jones, C., Corum, L., Grainger, D.: Polymer brushes containing sulfonated sugar repeat units: synthesis, characterization, and in vitro testing of blood coagulation activation. J. Polym. Sci., Part A: Polym. Chem. 46(23), 7713–7724 (2008)

    CAS  Google Scholar 

  116. Kidane, A.G., Salacinski, H., Tiwari, A., Bruckdorfer, K.R., Seifalian, A.M.: Anticoagulant and antiplatelet agents: their clinical and device application (s) together with usages to engineer surfaces. Biomacromolecules 5(3), 798–813 (2004)

    CAS  Google Scholar 

  117. Sakiyama-Elbert, S.E.: Incorporation of heparin into biomaterials. Acta Biomater. 10(4), 1581–1587 (2013)

    Google Scholar 

  118. Wan Kim, S., Jacobs, H.: Design of nonthrombogenic polymer surfaces for blood-contacting medical devices. Blood Purif. 14(5), 357–372 (1996)

    Google Scholar 

  119. Larm, O., Larsson, R., Olsson, P.: A new non-thrombogenic surface prepared by selective covalent binding of heparin via a modified reducing terminal residue. Biomater. Med. Devices Artif. Organs 11(2–3), 161–173 (1983)

    CAS  Google Scholar 

  120. Michanetzis, G., Katsala, N., Missirlis, Y.: Comparison of haemocompatibility improvement of four polymeric biomaterials by two heparinization techniques. Biomaterials 24(4), 677–688 (2003)

    CAS  Google Scholar 

  121. Miyara, H., Harumiya, N., Mori, Y., Tanzawa, H.: A new antithrombogenic heparinized polymer. J. Biomed. Mater. Res. 11(2), 251–265 (1977)

    Google Scholar 

  122. Goddard, J.M., Hotchkiss, J.H.: Polymer surface modification for the attachment of bioactive compounds. Prog. Polym. Sci. 32(7), 698–725 (2007)

    CAS  Google Scholar 

  123. Engbers, G.H., Feijen, J.: Current techniques to improve the blood compatibility of biomaterial surfaces. Int. J. Artif. Organs 14(4), 199–215 (1991)

    CAS  Google Scholar 

  124. Gölander, C., Arwin, H., Eriksson, J., Lundstrom, I., Larsson, R.: Heparin surface film formation through adsorption of colloidal particles studied by ellipsometry and scanning electron microscopy. Colloids Surf. 5(1), 1–16 (1982)

    Google Scholar 

  125. Seifert, B., Romaniuk, P., Groth, T.: Bioresorbable, heparinized polymers for stent coating: in vitro studies on heparinization efficiency, maintenance of anticoagulant properties and improvement of stent haemocompatibility. J. Mater. Sci. Mater. Med. 7(8), 465–469 (1996)

    CAS  Google Scholar 

  126. Bamford, C., Al-Lamee, K.: Studies in polymer surface modification and grafting for biomedical uses: 2. Application to arterial blood filters and oxygenators. Polymer 37(22), 4885–4889 (1996)

    CAS  Google Scholar 

  127. Byun, Y., Jacobs, H.A., Kim, S.W.: Heparin surface immobilization through hydrophilic spacers: thrombin and antithrombin III binding kinetics. J. Biomater. Sci. Polym. Ed. 6(1), 1–13 (1994)

    CAS  Google Scholar 

  128. Park, K.D., Okano, T., Nojiri, C., Kim, S.W.: Heparin immobilization onto segmented polyurethaneurea surfaces—effect of hydrophilic spacers. J. Biomed. Mater. Res. 22(11), 977–992 (1988)

    CAS  Google Scholar 

  129. Arnander, C., Bagger-Sjoebaeck, D., Frebelius, S., Larsson, R., Swedenborg, J.: Long-term stability in vivo of a thromboresistant heparinized surface. Biomaterials 8(6), 496–499 (1987)

    CAS  Google Scholar 

  130. Vroman, L.: The life of an artificial device in contact with blood: initial events and their effect on its final state. Bull. N. Y. Acad. Med. 64(4), 352 (1988)

    CAS  Google Scholar 

  131. Wendel, H.P., Ziemer, G.: Coating-techniques to improve the hemocompatibility of artificial devices used for extracorporeal circulation. Eur. J. Cardiothorac. Surg. 16(3), 342–350 (1999)

    CAS  Google Scholar 

  132. Keuren, J.F., Wielders, S.J., Willems, G.M., Morra, M., Lindhout, T.: Fibrinogen adsorption, platelet adhesion and thrombin generation at heparinized surfaces exposed to flowing blood. Thromb. Haemost. 87(4), 742–747 (2002)

    CAS  Google Scholar 

  133. Weber, N., Wendel, H.P., Ziemer, G.: Hemocompatibility of heparin-coated surfaces and the role of selective plasma protein adsorption. Biomaterials 23(2), 429–439 (2002)

    CAS  Google Scholar 

  134. Sperling, C., Houska, M., Brynda, E., Streller, U., Werner, C.: In vitro hemocompatibility of albumin–heparin multilayer coatings on polyethersulfone prepared by the layer-by-layer technique. J. Biomed. Mater. Res. A 76(4), 681–689 (2006)

    Google Scholar 

  135. Werner, C., Maitz, M.F., Sperling, C.: Current strategies towards hemocompatible coatings. J. Mater. Chem. 17(32), 3376–3384 (2007)

    CAS  Google Scholar 

  136. Vaughn, M.W.: Estimation of nitric oxide production and reaction rates in tissue by use of a mathematical model. Am. J. Physiol. Heart Circ. Physiol. 274(6), H2163–H2176 (1998)

    CAS  Google Scholar 

  137. Frost, M.C., Reynolds, M.M., Meyerhoff, M.E.: Polymers incorporating nitric oxide releasing/generating substances for improved biocompatibility of blood-contacting medical devices. Biomaterials 26(14), 1685–1693 (2005)

    CAS  Google Scholar 

  138. Seabra, A.B., Marcato, P.D., De Paula, L.B., Durán, N.: New strategy for controlled release of nitric oxide. J. Nano. Res. 20, 61–67 (2012)

    CAS  Google Scholar 

  139. Riccio, D.A., Schoenfisch, M.H.: Nitric oxide release: Part I. Macromol. Scaffolds. Chem. Soc. Rev. 41(10), 3731–3741 (2012)

    CAS  Google Scholar 

  140. Kim, J., Saravanakumar, G., Choi, H.W., Park, D., Kim, W.J.: A platform for nitric oxide delivery. J. Mater. Chem. B Mater. Biol. Med. 2, 341–356 (2014)

    CAS  Google Scholar 

  141. Jen, M.C., Serrano, M.C., Van Lith, R., Ameer, G.A.: Polymer-based nitric oxide therapies: recent insights for biomedical applications. Adv. Funct. Mater. 22(2), 239–260 (2012)

    CAS  Google Scholar 

  142. Halpenny, G.M., Mascharak, P.K.: Emerging antimicrobial applications of nitric oxide (NO) and NO-releasing materials. Anti-Infect. Agents Med. Chem. 9(4), 187–197 (2010)

    CAS  Google Scholar 

  143. Eroy-Reveles, A.A., Mascharak, P.K.: Nitric oxide-donating materials and their potential in pharmacological applications for site-specific nitric oxide delivery. Future Med. Chem. 1(8), 1497–1507 (2009)

    CAS  Google Scholar 

  144. Carpenter, A.W., Schoenfisch, M.H.: Nitric oxide release: Part II. Ther. Appl. Chem. Soc. Rev. 41(10), 3742–3752 (2012)

    CAS  Google Scholar 

  145. Mowery, K.A., Schoenfisch, M.H., Saavedra, J.E., Keefer, L.K., Meyerhoff, M.E.: Preparation and characterization of hydrophobic polymeric films that are thromboresistant via nitric oxide release. Biomaterials 21(1), 9–21 (2000)

    CAS  Google Scholar 

  146. Skrzypchak, A.M., Lafayette, N.G., Bartlett, R.H., Zhou, Z., Frost, M.C., Meyerhoff, M.E., Reynolds, M.M., Annich, G.M.: Effect of varying nitric oxide release to prevent platelet consumption and preserve platelet function in an in vivo model of extracorporeal circulation. Perfusion 22(3), 193–200 (2007)

    Google Scholar 

  147. Batchelor, M.M., Reoma, S.L., Fleser, P.S., Nuthakki, V.K., Callahan, R.E., Shanley, C.J., Politis, J.K., Elmore, J., Merz, S.I., Meyerhoff, M.E.: More lipophilic dialkyldiamine-based diazeniumdiolates: synthesis, characterization, and application in preparing thromboresistant nitric oxide release polymeric coatings. J. Med. Chem. 46(24), 5153–5161 (2003)

    CAS  Google Scholar 

  148. Fleser, P.S., Nuthakki, V.K., Malinzak, L.E., Callahan, R.E., Seymour, M.L., Reynolds, M.M., Merz, S.I., Meyerhoff, M.E., Bendick, P.J., Zelenock, G.B., Shanley, C.J.: Nitric oxide-releasing biopolymers inhibit thrombus formation in a sheep model of artcriovenous bridge grafts. J. Vasc. Surg. 40(4), 803–811 (2004)

    Google Scholar 

  149. Smith, D.J., Chakravarthy, D., Pulfer, S., Simmons, M.L., Hrabie, J.A., Citro, M.L., Saavedra, J.E., Davies, K.M., Hutsell, T.C., Mooradian, D.L., Hanson, S.R., Keefer, L.K.: Nitric oxide-releasing polymers containing the [N(O)NO]- group. J. Med. Chem. 39(5), 1148–1156 (1996)

    CAS  Google Scholar 

  150. Annich, G.M., Meinhardt, J.P., Mowery, K.A., Ashton, B.A., Merz, S.I., Hirschl, R.B., Meyerhoff, M.E., Bartlett, R.H.: Reduced platelet activation and thrombosis in extracorporeal circuits coated with nitric oxide release polymers. Crit. Care Med. 28(4), 915–920 (2000)

    CAS  Google Scholar 

  151. Zhang, H., Annich, G.M., Miskulin, J., Osterholzer, K., Merz, S.I., Bartlett, R.H., Meyerhoff, M.E.: Nitric oxide releasing silicone rubbers with improved blood compatibility: preparation, characterization, and in vivo evaluation. Biomaterials 23(6), 1485–1494 (2002)

    CAS  Google Scholar 

  152. Marxer, S.M., Rothrock, A.R., Nablo, B.J., Robbins, M.E., Schoenfisch, M.H.: Preparation of nitric oxide (NO)-releasing sol-gels for biomaterial applications. Chem. Mater. 15(22), 4193–4199 (2003)

    CAS  Google Scholar 

  153. Nablo, B.J., Schoenfisch, M.H.: In vitro cytotoxicity of nitric oxide-releasing sol-gel derived materials. Biomaterials 26(21), 4405–4415 (2005)

    CAS  Google Scholar 

  154. Hetrick, E.M., Schoenfisch, M.H.: Antibacterial nitric oxide-releasing xerogels: Cell viability and parallel plate flow cell adhesion studies. Biomaterials 28(11), 1948–1956 (2007)

    CAS  Google Scholar 

  155. Koh, A., Carpenter, A.W., Slomberg, D.L., Schoenfisch, M.H.: Nitric oxide-releasing silica nanoparticle-doped polyurethane electrospun fibers. ACS Appl. Mater. Interfaces 5(16), 7956–7964 (2013)

    CAS  Google Scholar 

  156. Koh, A., Riccio, D.A., Sun, B., Carpenter, A.W., Nichols, S.P., Schoenfisch, M.H.: Fabrication of nitric oxide-releasing polyurethane glucose sensor membranes. Biosens. Bioelectron. 28(1), 17–24 (2011)

    CAS  Google Scholar 

  157. Shin, J.H., Metzger, S.K., Schoenfisch, M.H.: Synthesis of nitric oxide-releasing silica nanoparticles. J. Am. Chem. Soc. 129(15), 4612–4619 (2007)

    CAS  Google Scholar 

  158. Shin, J.H., Schoenfisch, M.H.: Inorganic/organic hybrid silica nanoparticles as a nitric oxide delivery scaffold. Chem. Mater. 20(1), 239–249 (2008)

    CAS  Google Scholar 

  159. Lu, Y., Sun, B., Li, C.H., Schoenfisch, M.H.: Structurally diverse nitric oxide-releasing poly(propylene imine) dendrimers. Chem. Mater. 23(18), 4227–4233 (2011)

    CAS  Google Scholar 

  160. Stasko, N.A., Schoenfisch, M.H.: Dendrimers as a scaffold for nitric oxide release. J. Am. Chem. Soc. 128(25), 8265–8271 (2006)

    CAS  Google Scholar 

  161. Sun, B., Slomberg, D.L., Chudasama, S.L., Lu, Y., Schoenfisch, M.H.: Nitric oxide-releasing dendrimers as antibacterial agents. Biomacromolecules 13(10), 3343–3354 (2012)

    CAS  Google Scholar 

  162. Lantvit, S.M., Barrett, B.J., Reynolds, M.M.: Nitric oxide releasing material adsorbs more fibrinogen. J. Biomed. Mater. Res. A 101(11), 3201–3210 (2013)

    Google Scholar 

  163. Wu, Y., Zhou, Z., Meyerhoff, M.E.: In vitro platelet adhesion on polymeric surfaces with varying fluxes of continuous nitric oxide release. J. Biomed. Mater. Res. A 81(4), 956–963 (2007)

    Google Scholar 

  164. Major, T.C., Brant, D.O., Reynolds, M.M., Bartlett, R.H., Meyerhoff, M.E., Handa, H., Annich, G.M.: The attenuation of platelet and monocyte activation in a rabbit model of extracorporeal circulation by a nitric oxide releasing polymer. Biomaterials 31(10), 2736–2745 (2010)

    CAS  Google Scholar 

  165. Handa, H., Brisbois, E.J., Major, T.C., Refahiyat, L., Amoako, K.A., Annich, G.M., Bartlett, R.H., Meyerhoff, M.E.: In vitro and in vivo study of sustained nitric oxide release coating using diazeniumdiolate-doped poly(vinyl chloride) matrix with poly(lactide-co-glycolide) additive. J. Mater. Chem. B Mater. Biol. Med. 1(29), 3578–3587 (2013)

    CAS  Google Scholar 

  166. Handa, H., Major, T.C., Brisbois, E.J., Amoako, K.A., Meyerhoff, M.E., Bartlett, R.H.: Hemocompatibility comparison of biomedical grade polymers using rabbit thrombogenicity model for preparing nonthrombogenic nitric oxide releasing surfaces. J. Mater. Chem. B Mater. Biol. Med. 2(8), 1059–1067 (2014)

    CAS  Google Scholar 

  167. Al-Sa’doni, H., Ferro, A.: S-nitrosothiols: a class of nitric oxide-donor drugs. Clin. Sci. 98(5), 507–520 (2000)

    Google Scholar 

  168. Hogg, N.: Biological chemistry and clinical potential of S-nitrosothiols. Free Radical Biol. Med. 28(10), 1478–1486 (2000)

    CAS  Google Scholar 

  169. Hogg, N., Singh, R.J., Kalyanaraman, B.: The role of glutathione in the transport and catabolism of nitric oxide. FEBS Lett. 382(3), 223–228 (1996)

    CAS  Google Scholar 

  170. Langford, E.J., Brown, A.S., Wainwright, R.J., Debelder, A.J., Thomas, M.R., Smith, R.E.A., Radomski, M.W., Martin, J.F., Moncada, S.: Inhibition of platelet activity by S-nitrosoglutathione during coronary angioplasty. Lancet 344(8935), 1458–1460 (1994)

    CAS  Google Scholar 

  171. Radomski, M.W., Rees, D.D., Dutra, A., Moncada, S.: S-nitroso-glutathione inhibits platelet activation in vitro and in vivo. Br. J. Pharmacol. 107(3), 745–749 (1992)

    CAS  Google Scholar 

  172. Salas, E., Moro, M.A., Askew, S., Hodson, H.F., Butler, A.R., Radomski, M.W., Moncada, S.: Comparative pharmacology of analogues of S-nitroso-N-acetyl-DL-penicillamine on human platelets. Br. J. Pharmacol. 112(4), 1071–1076 (1994)

    CAS  Google Scholar 

  173. De Souza, G.F.P., Yokoyama-Yasunaka, J.K.U., Seabra, A.B., Miguel, D.C., De Oliveira, M.G., Uliana, S.R.B.: Leishmanicidal activity of primary S-nitrosothiols against Leishmania major and Leishmania amazonensis: implications for the treatment of cutaneous leishmaniasis. Nitric Oxide 15(3), 209–216 (2006)

    Google Scholar 

  174. Salas, E., Langford, E.J., Marrinan, M.T., Martin, J.F., Moncada, S., De Belder, A.J.: S-nitrosoglutathione inhibits platelet activation and deposition in coronary artery saphenous vein grafts in vitro and in vivo. Heart 80(2), 146–150 (1998)

    CAS  Google Scholar 

  175. Albert, J., Daleskog, M., Wallen, N.H.: A comparison of the antiplatelet effect of S-nitrosoglutathione in whole blood and platelet-rich plasma. Thromb. Res. 102(2), 161–165 (2001)

    CAS  Google Scholar 

  176. Ricardo, K.F.S., Shishido, S.M., De Oliveira, M.G., Krieger, M.H.: Characterization of the hypotensive effect of S-nitroso-N-acetylcysteine in normotensive and hypertensive conscious rats. Nitric Oxide-Biol. Ch 7(1), 57–66 (2002)

    CAS  Google Scholar 

  177. Dicks, A.P., Swift, H.R., Williams, D.L.H., Butler, A.R., Al-Sa’doni, H.H., Cox, B.G.: Identification of Cu + as the effective reagent in nitric oxide formation from S-nitrosothiols (RSNO). J. Chem. Soc. Perkin Trans. 2, 481–487 (1996)

    Google Scholar 

  178. Sexton, D.J., Muruganandam, A., Mckenney, D.J., Mutus, B.: Visible light photochemical release of nitric oxide from S-nitrosoglutathione: potential photochemotherapeutic applications. Photochem. Photobiol. 59(4), 463–467 (1994)

    CAS  Google Scholar 

  179. Wood, P.D., Mutus, B., Redmond, R.W.: The mechanism of photochemical release of nitric oxide from S-nitrosoglutathione. Photochem. Photobiol. 64(3), 518–524 (1996)

    CAS  Google Scholar 

  180. Frost, M.C., Meyerhoff, M.E.: Controlled photoinitiated release of nitric oxide from polymer films containing S-Nitroso-N-acetyl-dl-penicillamine derivatized fumed silica filler. J. Am. Chem. Soc. 126(5), 1348–1349 (2004)

    CAS  Google Scholar 

  181. Shishido, S.L.M., Seabra, A.B., Loh, W., Ganzarolli De Oliveira, M.: Thermal and photochemical nitric oxide release from S-nitrosothiols incorporated in Pluronic F127 gel: potential uses for local and controlled nitric oxide release. Biomaterials 24(20), 3543–3553 (2003)

    CAS  Google Scholar 

  182. Seabra, A.B., De Oliveira, M.G.: Poly(vinyl alcohol) and poly(vinyl pyrrolidone) blended films for local nitric oxide release. Biomaterials 25(17), 3773–3782 (2004)

    CAS  Google Scholar 

  183. Seabra, A.B., De Souza, G.F.P., Da Rocha, L.L., Eberlin, M.N., De Oliveira, M.G.: S-nitrosoglutathione incorporated in poly(ethylene glycol) matrix: potential use for topical nitric oxide delivery. Nitric Oxide-Biol. Ch 11(3), 263–272 (2004)

    Google Scholar 

  184. Seabra, A.B., Da Rocha, L.L., Eberlin, M.N., De Oliveira, M.G.: Solid films of blended poly(vinyl alcohol)/poly(vinyl pyrrolidone) for topical S-nitrosoglutathione and nitric oxide release. J. Pharm. Sci. 94(5), 994–1003 (2005)

    CAS  Google Scholar 

  185. Simoes, M., De Oliveira, M.G.: Poly(vinyl alcohol) films for topical delivery of S-Nitrosoglutathione: effect of freezing-thawing on the diffusion properties. J. Biomed. Mater. Res. B Appl. Biomater. 93B(2), 416–424 (2010)

    CAS  Google Scholar 

  186. Brisbois, E.J., Handa, H., Major, T.C., Bartlett, R.H., Meyerhoff, M.E.: Long-term nitric oxide release and elevated temperature stability with S-nitroso-N-acetylpenicillamine (SNAP)-doped Elast-eon E2As polymer. Biomaterials 34(28), 6957–6966 (2013)

    CAS  Google Scholar 

  187. Joslin, J.M., Lantvit, S.M., Reynolds, M.M.: Nitric oxide releasing tygon materials: studies in donor leaching and localized nitric oxide release at a polymer-buffer interface. ACS Appl. Mater. Interfaces 5(19), 9285–9294 (2013)

    CAS  Google Scholar 

  188. Riccio, D.A., Dobmeier, K.P., Hetrick, E.M., Privett, B.J., Paul, H.S., Schoenfisch, M.H.: Nitric oxide-releasing S-nitrosothiol-modified xerogels. Biomaterials 30(27), 4494–4502 (2009)

    CAS  Google Scholar 

  189. Riccio, D.A., Coneski, P.N., Nichols, S.P., Broadnax, A.D., Schoenfisch, M.H.: Photoinitiated nitric oxide-releasing tertiary S-Nitrosothiol-modified xerogels. ACS Appl. Mater. Interfaces 4(2), 796–804 (2012)

    CAS  Google Scholar 

  190. Coneski, P.N., Schoenfisch, M.H.: Synthesis of nitric oxide-releasing polyurethanes with S-nitrosothiol-containing hard and soft segments. Polym Chem. 2(4), 906–913 (2011)

    CAS  Google Scholar 

  191. Frost, M.C., Meyerhoff, M.E.: Synthesis, characterization, and controlled nitric oxide release from S-nitrosothiol-derivatized fumed silica polymer filler particles. J. Biomed. Mater. Res. A 72A(4), 409–419 (2005)

    CAS  Google Scholar 

  192. Coneski, P.N., Rao, K.S., Schoenfisch, M.H.: Degradable nitric oxide-releasing biomaterials via post-polymerization functionalization of cross-linked polyesters. Biomacromolecules 11(11), 3208–3215 (2010)

    CAS  Google Scholar 

  193. Damodaran, V.B., Place, L.W., Kipper, M.J., Reynolds, M.M.: Enzymatically degradable nitric oxide releasing S-nitrosated dextran thiomers for biomedical applications. J. Mater. Chem. 22, 23038–23048 (2012)

    CAS  Google Scholar 

  194. Damodaran, V.B., Reynolds, M.M.: Biodegradable S-nitrosothiol tethered multiblock polymer for nitric oxide delivery. J. Mater. Chem. 21, 5870–5872 (2011)

    CAS  Google Scholar 

  195. Damodaran, V.B., Joslin, J.M., Wold, K.A., Lantvit, S.M., Reynolds, M.M.: S-Nitrosated biodegradable polymers for biomedical applications: synthesis, characterization and impact of thiol structure on the physicochemical properties. J. Mater. Chem. 22, 5990–6001 (2012)

    CAS  Google Scholar 

  196. Seabra, A.B., Martins, D., Simoes, M., Da Silva, R., Brocchi, M., De Oliveira, M.G.: Antibacterial nitric oxide-releasing polyester for the coating of blood-contacting artificial materials. Artif. Organs 34(7), E204–E214 (2010)

    CAS  Google Scholar 

  197. Seabra, A.B., Da Silva, R., De Souza, G.F.P., De Oliveira, M.G.: Antithrombogenic polynitrosated polyester/poly(methyl methacrylate) blend for the coating of blood-contacting surfaces. Artif. Organs 32(4), 262–267 (2008)

    CAS  Google Scholar 

  198. Li, Y., Lee, P.I.: Controlled nitric oxide delivery platform based on S-nitrosothiol conjugated interpolymer complexes for diabetic wound healing. Mol. Pharm. 7(1), 254–266 (2009)

    Google Scholar 

  199. Gierke, G.E., Nielsen, M., Frost, M.C.: S-Nitroso- N -acetyl-D-penicillamine covalently linked to polydimethylsiloxane (SNAP–PDMS) for use as a controlled photoinitiated nitric oxide release polymer. Sci. Technol. Adv. Mat. 12(5), 055007 (2011)

    Google Scholar 

  200. Stasko, N.A., Fischer, T.H., Schoenfisch, M.H.: S-Nitrosothiol-modified dendrimers as nitric oxide delivery vehicles. Biomacromolecules 9(3), 834–841 (2008)

    CAS  Google Scholar 

  201. Riccio, D.A., Nugent, J.L., Schoenfisch, M.H.: Stober synthesis of nitric oxide-releasing S-Nitrosothiol-modified silica particles. Chem. Mater. 23(7), 1727–1735 (2011)

    CAS  Google Scholar 

  202. Duan, X., Lewis, R.S.: Improved haemocompatibility of cysteine-modified polymers via endogenous nitric oxide. Biomaterials 23(4), 1197–1203 (2002)

    CAS  Google Scholar 

  203. Gappa-Fahlenkamp, H., Lewis, R.S.: Improved hemocompatibility of poly(ethylene terephthalate) modified with various thiol-containing groups. Biomaterials 26(17), 3479–3485 (2005)

    CAS  Google Scholar 

  204. Oh, B.K., Meyerhoff, M.E.: Spontaneous Catalytic Generation of Nitric Oxide from S-Nitrosothiols at the Surface of Polymer Films Doped with Lipophilic Copper(II) Complex. J. Am. Chem. Soc. 125(32), 9552–9553 (2003)

    CAS  Google Scholar 

  205. Oh, B.K., Meyerhoff, M.E.: Catalytic generation of nitric oxide from nitrite at the interface of polymeric films doped with lipophilic Cu (II)-complex: a potential route to the preparation of thromboresistant coatings. Biomaterials 25(2), 283–293 (2004)

    CAS  Google Scholar 

  206. Hwang, S., Meyerhoff, M.E.: Polyurethane with tethered copper (II)–cyclen complex: preparation, characterization and catalytic generation of nitric oxide from S-nitrosothiols. Biomaterials 29(16), 2443–2452 (2008)

    CAS  Google Scholar 

  207. Puiu, S.C., Zhou, Z., White, C.C., Neubauer, L.J., Zhang, Z., Lange, L.E., Mansfield, J.A., Meyerhoff, M.E., Reynolds, M.M.: Metal ion-mediated nitric oxide generation from polyurethanes via covalently linked copper(II)-cyclen moieties. J. Biomed. Mater. Res. Part B Appl. Biomater. 91B(1), 203–212 (2009)

    CAS  Google Scholar 

  208. Major, T.C., Brant, D.O., Burney, C.P., Amoako, K.A., Annich, G.M., Meyerhoff, M.E., Handa, H., Bartlett, R.H.: The hemocompatibility of a nitric oxide generating polymer that catalyzes S-nitrosothiol decomposition in an extracorporeal circulation model. Biomaterials 32(26), 5957–5969 (2011)

    CAS  Google Scholar 

  209. Mugesh, G., Singh, H.B.: Synthetic organoselenium compounds as antioxidants: glutathione peroxidase activity. Chem. Soc. Rev. 29(5), 347–357 (2000)

    CAS  Google Scholar 

  210. Hou, Y., Guo, Z., Li, J., Wang, P.G.: Seleno compounds and glutathione peroxidase catalyzed decomposition of S-nitrosothiols. Biochem. Biophys. Res. Commun. 228(1), 88–93 (1996)

    CAS  Google Scholar 

  211. Yang, J., Welby, J.L., Meyerhoff, M.E.: Generic nitric oxide (NO) generating surface by immobilizing organoselenium species via layer-by-layer assembly. Langmuir 24(18), 10265–10272 (2008)

    CAS  Google Scholar 

  212. Cha, W., Meyerhoff, M.E.: Catalytic generation of nitric oxide from S-nitrosothiols using immobilized organoselenium species. Biomaterials 28(1), 19–27 (2007)

    CAS  Google Scholar 

  213. Cai, W., Wu, J., Xi, C., Ashe Iii, A.J., Meyerhoff, M.E.: Carboxyl-ebselen-based layer-by-layer films as potential antithrombotic and antimicrobial coatings. Biomaterials 32(31), 7774–7784 (2011)

    CAS  Google Scholar 

  214. Reynolds, M.M., Frost, M.C., Meyerhoff, M.E.: Nitric oxide-releasing hydrophobic polymers: preparation, characterization, and potential biomedical applications. Free Radical Biol. Med. 37(7), 926–936 (2004)

    CAS  Google Scholar 

  215. Sefton, M.V., Gemmell, C.H., Gorbet, M.B.: What really is blood compatibility? J. Biomat. Sci-Polym. E 11(11), 1165–1182 (2000)

    CAS  Google Scholar 

  216. Lemm, W., Unger, V., Bucherl, E.S.: Blood compatibility of polymers: in vitro and in vivo tests. Med. Biol. Eng. Comput. 18(4), 521–526 (1980)

    CAS  Google Scholar 

  217. Kirkpatrick, C., Mittermayer, C.: Theoretical and practical aspects of testing potential biomaterials in vitro. J. Mater. Sci. Mater. Med. 1(1), 9–13 (1990)

    Google Scholar 

  218. Sefton, M.V.: Perspective on hemocompatibility testing. J. Biomed. Mater. Res. 55(4), 445–446 (2001)

    CAS  Google Scholar 

  219. Seyfert, U.T., Biehl, V., Schenk, J.: In vitro hemocompatibility testing of biomaterials according to the ISO 10993-4. Biomol. Eng. 19(2), 91–96 (2002)

    CAS  Google Scholar 

  220. Braune, S., Grunze, M., Straub, A., Jung, F.: Are there sufficient standards for the in vitro hemocompatibility testing of biomaterials? Biointerphases 8(1), 1–9 (2013)

    Google Scholar 

  221. Ratner, B.D.: Evaluation of the blood compatibility of synthetic polymers: consensus and significance. Contemporary Biomaterials: Material and Host Response, Clinical Applications, New Technology and Legal Aspects, pp. 193–204. Noyes Publications, Park Ridge (1984)

    Google Scholar 

  222. Hanson, S.R., Ratner, B.: Evaluation of blood-materials interactions. In: Biomaterials science: an introduction to materials in medicine, pp. 367–378. San Diego (2004)

    Google Scholar 

  223. Ratner, B.D., Horbett, T.A.: Chapter II.3.5—Evaluation of blood–materials interactions. In: Ratner BD, Hoffman AS, Schoen FJ, Lemons JE (eds) Biomaterials Science (Third Edition), pp. 617–634. Academic Press, Waltham (2013)

    Google Scholar 

  224. Sefton, M.V., Sawyer, A., Gorbet, M., Black, J.P., Cheng, E., Gemmell, C., Pottinger-Cooper, E.: Does surface chemistry affect thrombogenicity of surface modified polymers? J. Biomed. Mater. Res. 55(4), 447–459 (2001)

    CAS  Google Scholar 

  225. Gristina, A.G.: Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 237, 1588–1595 (1987)

    CAS  Google Scholar 

  226. Tzoneva, R., Heuchel, M., Groth, T., Altankov, G., Albrecht, W., Paul, D.: Fibrinogen adsorption and platelet interactions on polymer membranes. J. Biomater. Sci. Polym. Ed. 13(9), 1033–1050 (2002)

    CAS  Google Scholar 

  227. Haycox, C.L., Ratner, B.D.: In vitro platelet interactions in whole human blood exposed to biomaterial surfaces: Insights on blood compatibility. J. Biomed. Mater. Res. 27(9), 1181–1193 (1993)

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark E. Meyerhoff .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Brisbois, E.J., Handa, H., Meyerhoff, M.E. (2015). Recent Advances in Hemocompatible Polymers for Biomedical Applications. In: Puoci, F. (eds) Advanced Polymers in Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-12478-0_16

Download citation

Publish with us

Policies and ethics