Fibrin matrices: The versatile therapeutic delivery systems

International Journal of Biological Macromolecules

Volumn 81, Issue , 2015, Pages 121-136

  Ahmad, Ejaj ^a   Fatima, Munazza Tamkeen ^a   Hoque, Mehboob ^a   Owais, Mohammad ^a   Saleemuddin, Mohammed ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

Author keywords

Drug delivery; Fibrin microthreads; Fibrinogen; Plasma beads; Plasma microparticle

Indexed keywords

1 (3 DIMETHYLAMINOPROPYL) 3 ETHYLCARBODIIMIDE; ADENOVIRUS VECTOR; ANTIBIOTIC AGENT; ANTINEOPLASTIC AGENT; ATELOCOLLAGEN; BLOOD CLOTTING FACTOR 13; BONE MORPHOGENETIC PROTEIN 2; CANDIDA ALBICANS VACCINE; CARBOPLATIN; CEFOTAXIME; FIBRIN; FIBRIN GLUE; FIBRINOGEN; GALLIC ACID; GENIPIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTARALDEHYDE; GROWTH FACTOR; KERATINOCYTE GROWTH FACTOR; LIPOSOME; MEPACRINE; REAGENT; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; RECOMBINANT EPIDERMAL GROWTH FACTOR; TETRACYCLINE; THROMBIN; TOPOTECAN; DRUG CARRIER;

BONE MARROW DERIVED MONONUCLEAR CELL; CANDIDIASIS; CROSS LINKING; DACRON IMPLANT; DRUG BLOOD LEVEL; DRUG TISSUE LEVEL; ELECTROSPINNING; ENCAPSULATION; EYE TUMOR; FIBRIN CLOT; HEART INFARCTION; HUMAN; HYDROGEL; MESENCHYMAL STEM CELL; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; POLYMERIZATION; PROTEIN DEGRADATION; RETINOBLASTOMA; REVIEW; SCIATIC NERVE INJURY; SEALANT; SEPSIS; SKIN FIBROBLAST; SUSTAINED DRUG RELEASE; TISSUE ENGINEERING; TISSUE REGENERATION; VIRAL GENE THERAPY; WOUND HEALING; ANIMAL; CHEMISTRY; DRUG DELIVERY SYSTEM; PLASMA;

ANIMALS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; FIBRIN; FIBRIN TISSUE ADHESIVE; HUMANS; PLASMA;

EID: 84938857672     PISSN: 01418130     EISSN: 18790003     Source Type: Journal    
DOI: 10.1016/j.ijbiomac.2015.07.054     Document Type: Review

References (176)

1. Podolnikova N.P., Gorkun O.V., Loreth R.M., Yee V.C., Lord S.T., Ugarova T.P. A cluster of basic amino acid residues in the gamma370-381 sequence of fibrinogen comprises a binding site for platelet integrin alpha(IIb)beta3 (glycoprotein IIb/IIIa). Biochemistry 2005, 44:16920-16930.
2. Cheresh D.A. Human endothelial cells synthesize and express an Arg-Gly-Asp-directed adhesion receptor involved in attachment to fibrinogen and von Willebrand factor. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:6471-6475.
3. Gailit J., Clarke C., Newman D., Tonnesen M.G., Mosesson M.W., Clark R.A. Human fibroblasts bind directly to fibrinogen at RGD sites through integrin alpha(v)beta3. Exp. Cell Res. 1997, 232:118-126.
4. Makogonenko E., Tsurupa G., Ingham K., Medved L. Interaction of fibrin(ogen) with fibronectin: further characterization and localization of the fibronectin-binding site. Biochemistry 2002, 41:7907-7913.
5. Podor T.J., Campbell S., Chindemi P., Foulon D.M., Farrell D.H., Walton P.D., Weitz J.I., Peterson C.B. Incorporation of vitronectin into fibrin clots. Evidence for a binding interaction between vitronectin and gamma A/gamma' fibrinogen. J. Biol. Chem. 2002, 277:7520-7528.
6. Bacon-Baguley T., Ogilvie M.L., Gartner T.K., Walz D.A. Thrombospondin binding to specific sequences within the A alpha- and B beta-chains of fibrinogen. J. Biol. Chem. 1990, 265:2317-2323.
7. Sahni A., Odrljin T., Francis C.W. Binding of basic fibroblast growth factor to fibrinogen and fibrin. J. Biol. Chem. 1998, 273:7554-7559.
8. Baird A., Mormede P., Bohlen P. Immunoreactive fibroblast growth factor in cells of peritoneal exudate suggests its identity with macrophage-derived growth factor. Biochem. Biophys. Res. Commun. 1985, 126:358-364.
9. Sahni A., Francis C.W. Vascular endothelial growth factor binds to fibrinogen and fibrin and stimulates endothelial cell proliferation. Blood 2000, 96:3772-3778.
10. O'Kane S., Ferguson M.W. Transforming growth factor beta s and wound healing. Int. J. Biochem. Cell Biol. 1997, 29:63-78.
11. Grainger D.J., Wakefield L., Bethell H.W., Farndale R.W., Metcalfe J.C. Release and activation of platelet latent TGF-beta in blood clots during dissolution with plasmin. Nat. Med. 1995, 1:932-937.
12. Dohan D.M., Choukroun J., Diss A., Dohan S.L., Dohan A.J., Mouhyi J., Gogly B. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: Platelet-related biologic features. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2006, 101:e45-e50.
13. Lustig F., Hoebeke J., Simonson C., Ostergren-Lunden G., Bondjers G., Ruetchi U., Fager G. Processing of PDGF gene products determines interactions with glycosaminoglycans. J. Mol. Recog. 1999, 12:112-120.
14. Sahni A., Guo M., Sahni S.K., Francis C.W. Interleukin-1beta but not IL-1alpha binds to fibrinogen and fibrin and has enhanced activity in the bound form. Blood 2004, 104:409-414.
15. Higashiyama S., Abraham J.A., Miller J., Fiddes J.C., Klagsbrun M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 1991, 251:936-939.
16. Tsurupa G., Medved L. Identification and characterization of novel tPA- and plasminogen-binding sites within fibrin(ogen) alpha C-domains. Biochemistry 2001, 40:801-808.
17. Wagner O.F., de Vries C., Hohmann C., Veerman H., Pannekoek H. Interaction between plasminogen activator inhibitor type 1 (PAI-1) bound to fibrin and either tissue-type plasminogen activator (t-PA) or urokinase-type plasminogen activator (u-PA). Binding of t-PA/PAI-1 complexes to fibrin mediated by both the finger and the kringle-2 domain of t-PA. J. Clin. Invest. 1989, 84:647-655.
18. Pospisil C.H., Stafford A.R., Fredenburgh J.C., Weitz J.I. Evidence that both exosites on thrombin participate in its high affinity interaction with fibrin. J. Biol. Chem. 2003, 278:21584-21591.
19. Lorand L. Crosslinks in blood: transglutaminase and beyond. FASEB J. 2007, 21:1627-1632.
20. Sierra D.H. Fibrin sealant adhesive systems: a review of their chemistry, material properties and clinical applications. J. Biomater. Appl. 1993, 7:309-352.
21. Bergel S. Ueberwkungen des Fibrins. Dtsch. Wochenschr. 1909, 35:633-665.
22. Pipan C.M., Glasheen W.P., Matthew T.L., Gonias S.L., Hwang L.J., Jane J.A., Spotnitz W.D. Effects of antifibrinolytic agents on the life span of fibrin sealant. J. Surg. Res. 1992, 53:402-407.
23. Alving B.M., Weinstein M.J., Finlayson J.S., Menitove J.E., Fratantoni J.C. Fibrin sealant: summary of a conference on characteristics and clinical uses. Transfusion (Paris) 1995, 35:783-790.
24. Janmey P.A., Winer J.P., Weisel J.W. Fibrin gels and their clinical and bioengineering applications. J. R. Soc. Interface 2009, 6:1-10.
25. Ahmed T.A., Dare E.V., Hincke M. Fibrin: a versatile scaffold for tissue engineering applications. Tissue Eng. B Rev. 2008, 14:199-215.
26. Shaikh F.M., Callanan A., Kavanagh E.G., Burke P.E., Grace P.A., McGloughlin T.M. Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cell. Tissue Organ 2008, 188:333-346.
27. Breen A., O'Brien T., Pandit A. Fibrin as a delivery system for therapeutic drugs and biomolecules. Tissue Eng. B Rev. 2009, 15:201-214.
28. Spicer P.P., Mikos A.G. Fibrin glue as a drug delivery system. J. Control. Release 2010, 148:49-55.
29. Gorodetsky R. The use of fibrin based matrices and fibrin microbeads (FMB) for cell based tissue regeneration. Expert Opin. Biol. Ther. 2008, 8:1831-1846.
30. Ho H.-O., Chen C.-Y. Diffusion characteristics of fibrin films. Int. J. Pharm. 1993, 90:95-104.
31. Kumar T.R., Vasantha Bai M., Krishnan L.K. A freeze-dried fibrin disc as a biodegradable drug release matrix. Biologicals 2004, 32:49-55.
32. Cornwell K.G., Pins G.D. Discrete crosslinked fibrin microthread scaffolds for tissue regeneration. J. Biomed. Mater. Res. A 2007, 82:104-112.
33. Ho H.-O., Hsiao C.-C., Chen C.-Y., Sokoloski T.D., Sheu M.-T. Fibrin based drug delivery systems. II. The preparation and characterization of microbeads. Drug Dev. Ind. Pharm. 1994, 20:535-546.
34. Rejinold N.S., Muthunarayanan M., Deepa N., Chennazhi K.P., Nair S.V., Jayakumar R. Development of novel fibrinogen nanoparticles by two-step co-acervation method. Int. J. Biol. Macromol. 2010, 47:37-43.
35. Praveen G., Sreerekha P.R., Menon D., Nair S.V., Chennazhi K.P. Fibrin nanoconstructs: a novel processing method and their use as controlled delivery agents. Nanotechnology 2012, 23:095102. 10.1088/0957-4484/23/9/095102.
36. Ahmad E., Fatima M.T., Owais M., Saleemuddin M. Beaded plasma clot: a potent sustained-release, drug-delivery system. Ther. Deliv. 2011, 2:573-583.
37. Fatima M.T., Ahmad E., Saleemuddin M. Entrapment in plasma microparticles: a promising strategy for antigen delivery. J. Biomed. Mater. Res. B Appl. Biomater. 2014, 102:1244-1254.
38. Christman K.L., Vardanian A.J., Fang Q., Sievers R.E., Fok H.H., Lee R.J. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 2004, 44:654-660.
39. Okuda M., Uemura Y., Tatsumi N. Quality control material for plasma fibrinogen test produced from purified human fibrinogen. J. Autom. Methods Manag. Chem. 2003, 25:79-85.
40. Berruyer M., Amiral J., Ffrench P., Belleville J., Bastien O., Clerc J., Kassir A., Estanove S., Dechavanne M. Immunization by bovine thrombin used with fibrin glue during cardiovascular operations. Development of thrombin and factor V inhibitors. J. Thorac. Cardiovasc. Surg. 1993, 105:892-897.
41. Banninger H., Hardegger T., Tobler A., Barth A., Schupbach P., Reinhart W., Lammle B., Furlan M. Fibrin glue in surgery: frequent development of inhibitors of bovine thrombin and human factor V. Br. J. Haematol. 1993, 85:528-532.
42. Chapman W.C., Lockstadt H., Singla N., Kafie F.E., Lawson J.H. Phase 2, randomized, double-blind, placebo-controlled, multicenter clinical evaluation of recombinant human thrombin in multiple surgical indications. J. Thromb. Haemost. 2006, 4:2083-2085.
43. Bishop P.D., Lewis K.B., Schultz J., Walker K.M. Comparison of recombinant human thrombin and plasma-derived human alpha-thrombin. Semin. Thromb. Hemost. 2006, 32(Suppl. 1):86-97.
44. Bishop P. Protein characterization of recombinant human thrombin and demonstration of efficacy in models of surgical bleeding. Blood 2003, 102:89b.
45. Cada D.J., Levien T.L., Baker D.E. Prothrombin complex concentrate. Hosp. Pharm. 2013, 48:951-957.
46. Park K.J.H., Lee D.S., Jeong S.W.J.M. Secretory expression of the α-subunit of human coagulation factor XIII in the yeast Pichia pastoris. Biotechnol. Lett. 2002, 24:97-101.
47. Carlson M.A., Calcaterra J., Johanning J.M., Pipinos I.I., Cordes C.M., Velander W.H. A totally recombinant human fibrin sealant. J. Surg. Res. 2014, 187:334-342.
48. Jockenhoevel S., Zund G., Hoerstrup S.P., Chalabi K., Sachweh J.S., Demircan L., Messmer B.J., Turina M. Fibrin gel - advantages of a new scaffold in cardiovascular tissue engineering. Eur. J. Cardiothorac. Surg. 2001, 19:424-430.
49. Mol A., van Lieshout M.I., Dam-de Veen C.G., Neuenschwander S., Hoerstrup S.P., Baaijens F.P., Bouten C.V. Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials 2005, 26:3113-3121.
50. Kjaergard H.K., Weis-Fogh U.S. Important factors influencing the strength of autologous fibrin glue; the fibrin concentration and reaction time - comparison of strength with commercial fibrin glue. Eur. Surg. Res. 1994, 26:273-276.
51. Herbert C.B., Nagaswami C., Bittner G.D., Hubbell J.A., Weisel J.W. Effects of fibrin micromorphology on neurite growth from dorsal root ganglia cultured in three-dimensional fibrin gels. J. Biomed. Mater. Res. 1998, 40:551-559.
52. Rowe S.L., Lee S., Stegemann J.P. Influence of thrombin concentration on the mechanical and morphological properties of cell-seeded fibrin hydrogels. Acta Biomater. 2007, 3:59-67.
53. Breen A., Strappe P., Kumar A., O'Brien T., Pandit A. Optimization of a fibrin scaffold for sustained release of an adenoviral gene vector. J. Biomed. Mater. Res. A 2006, 78:702-708.
54. Oh J.-H., Kim H.-J., Kim T.-I., Baek J.-H., Ryoo H.-M., Woo K.M. The effects of the modulation of the fibronectin-binding capacity of fibrin by thrombin on osteoblast differentiation. Biomaterials 2012, 33:4089-4099.
55. Eyrich D., Wiese H., Maier G., Skodacek D., Appel B., Sarhan H., Tessmar J., Staudenmaier R., Wenzel M.M., Goepferich A., Blunk T. In vitro and in vivo cartilage engineering using a combination of chondrocyte-seeded long-term stable fibrin gels and polycaprolactone-based polyurethane scaffolds. Tissue Eng. 2007, 13:2207-2218.
56. Veklich Y.I., Gorkun O.V., Medved L.V., Nieuwenhuizen W., Weisel J.W. Carboxyl-terminal portions of the alpha chains of fibrinogen and fibrin. Localization by electron microscopy and the effects of isolated alpha C fragments on polymerization. J. Biol. Chem. 1993, 268:13577-13585.
57. Boyce S.T., Holder I.A., Supp A.P., Warden G.D., Greenhalgh D.G. Delivery and activity of antimicrobial drugs released from human fibrin sealant. J. Burn Care Rehabil. 1994, 15:251-255.
58. Woolverton C.J., Fulton J.A., Salstrom S.J., Hayslip J., Haller N.A., Wildroudt M.L., MacPhee M. Tetracycline delivery from fibrin controls peritoneal infection without measurable systemic antibiotic. J. Antimicrob. Chemother. 2001, 48:861-867.
59. Schmoekel H.G., Weber F.E., Schense J.C., Gratz K.W., Schawalder P., Hubbell J.A. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol. Bioeng. 2005, 89:253-262.
60. Campbell P.G., Durham S.K., Hayes J.D., Suwanichkul A., Powell D.R. Insulin-like growth factor-binding protein-3 binds fibrinogen and fibrin. J. Biol. Chem. 1999, 274:30215-30221.
61. Kapoor A.K., Raju S.M. Illustrated medical pharmacology. Tissue Eng. 2013, 13:356.
62. Chung T.W., Yang M.C., Tsai W.J. A fibrin encapsulated liposomes-in-chitosan matrix (FLCM) for delivering water-soluble drugs. Influences of the surface properties of liposomes and the crosslinked fibrin network. Int. J. Pharm. 2006, 311:122-129.
63. Frucht-Perry J., Assil K.K., Ziegler E., Douglas H., Brown S.I., Schanzlin D.J., Weinreb R.N. Fibrin-enmeshed tobramycin liposomes: single application topical therapy of Pseudomonas keratitis. Cornea 1992, 11:393-397.
64. Royce S.M., Askari M., Marra K.G. Incorporation of polymer microspheres within fibrin scaffolds for the controlled delivery of FGF-1. J. Biomater. Sci. Polym. Ed. 2004, 15:1327-1336.
65. Wang S.S., Yang M.C., Chung T.W. Liposomes/chitosan scaffold/human fibrin gel composite systems for delivering hydrophilic drugs - release behaviors of tirofiban in vitro. Drug Deliv. 2008, 15:149-157.
66. Grassl E.D., Oegema T.R., Tranquillo R.T. A fibrin-based arterial media equivalent. J. Biomed. Mater. Res. A 2003, 66:550-561.
67. Wozniak G. Fibrin sealants in supporting surgical techniques: the importance of individual components. Cardiovasc. Surg. 2003, 11(Suppl. 1):17-21.
68. Dare E.V., Griffith M., Poitras P., Kaupp J.A., Waldman S.D., Carlsson D.J., Dervin G., Mayoux C., Hincke M.T. Genipin cross-linked fibrin hydrogels for in vitro human articular cartilage tissue-engineered regeneration. Cell Tissue Organs 2009, 190:313-325.
69. Sell S.A., Francis M.P., Garg K., McClure M.J., Simpson D.G., Bowlin G.L. Cross-linking methods of electrospun fibrinogen scaffolds for tissue engineering applications. Biomed. Mater. 2008, 3:045001.
70. McManus M.C., Boland E.D., Koo H.P., Barnes C.P., Pawlowski K.J., Wnek G.E., Simpson D.G., Bowlin G.L. Mechanical properties of electrospun fibrinogen structures. Acta Biomater. 2006, 2:19-28.
71. Gough J.E., Scotchford C.A., Downes S. Cytotoxicity of glutaraldehyde crosslinked collagen/poly(vinyl alcohol) films is by the mechanism of apoptosis. J. Biomed. Mater. Res. 2002, 61:121-130.
72. Osathanon T., Giachelli C.M., Somerman M.J. Immobilization of alkaline phosphatase on microporous nanofibrous fibrin scaffolds for bone tissue engineering. Biomaterials 2009, 30:4513-4521.
73. Beduschi R., Beduschi M.C., Wojno K.J., Jhung M., Williams A.L., Wolf J.S. Antifibrinolytic additives to fibrin glue for laparoscopic wound closure in urinary tract. J. Endourol. 1999, 13:283-287.
74. Buchta C., Hedrich H.C., Macher M., Hocker P., Redl H. Biochemical characterization of autologous fibrin sealants produced by CryoSeal and Vivostat in comparison to the homologous fibrin sealant product Tissucol/Tisseel. Biomaterials 2005, 26:6233-6241.
75. Ahmed T.A., Griffith M., Hincke M. Characterization and inhibition of fibrin hydrogel-degrading enzymes during development of tissue engineering scaffolds. Tissue Eng. 2007, 13:1469-1477.
76. Ye Q., Zund G., Benedikt P., Jockenhoevel S., Hoerstrup S.P., Sakyama S., Hubbell J.A., Turina M. Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering. Eur. J. Cardiothorac. Surg. 2000, 17:587-591.
77. Marx G., Mou X. Characterizing fibrin glue performance as modulated by heparin, aprotinin, and factor XIII. J. Lab. Clin. Med. 2002, 140:152-160.
78. Lorentz K.M., Kontos S., Frey P., Hubbell J.A. Engineered aprotinin for improved stability of fibrin biomaterials. Biomaterials 2011, 32:430-438.
79. Sakiyama-Elbert S.E., Hubbell J.A. Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J. Control. Release 2000, 69:149-158.
80. Sakiyama-Elbert S.E., Hubbell J.A. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J. Control. Release 2000, 65:389-402.
81. Redl H., Schlag G., Stanek G., Hirschl A., Seelich T. In vitro properties of mixtures of fibrin seal and antibiotics. Biomaterials 1983, 4:29-32.
82. Deyerling W., Haverich A., Potel J., Hetzer R. A suspension of fibrin glue and antibiotic for local treatment of mycotic aneurysms in endocarditis - an experimental study. Thorac. Cardiovasc. Surg. 1984, 32:369-372.
83. Zilch H., Lambiris E. The sustained release of cefotaxim from a fibrin-cefotaxim compound in treatment of osteitis. Pharmacokinetic study and clinical results. Arch. Orthop. Trauma. Surg. 1986, 106:36-41.
84. Haverich A., Frimpong-Boateng K., Wahlers T., Schafers H.J. Pericardial flap-plasty for protection of the tracheal anastomosis in heart-lung transplantation. J. Card. Surg. 1989, 4:136-139.
85. Kram H.B., del Junco T., Clark S.R., Ocampo H.P., Shoemaker W.C. Techniques of splenic preservation using fibrin glue. J. Trauma 1990, 30:97-101.
86. Ney A.L., Kelly P.H., Tsukayama D.T., Bubrick M.P. Fibrin glue-antibiotic suspension in the prevention of prosthetic graft infection. J. Trauma 1990, 30:1000-1005.
87. Karck M., Siclari F., Wahlig H., Sperling U., Schmid C., Haverich A. Pretreatment of prosthetic valve sewing-ring with the antibiotic/fibrin sealant compound as a prophylactic tool against prosthetic valve endocarditis. Eur. J. Cardiothorac. Surg. 1990, 4:142-146.
88. Greco F., de Palma L., Spagnolo N., Rossi A., Specchia N., Gigante A. Fibrin-antibiotic mixtures: an in vitro study assessing the possibility of using a biologic carrier for local drug delivery. J. Biomed. Mater. Res. 1991, 25:39-51.
89. Kram H.B., Bansal M., Timberlake O., Shoemaker W.C. Antibacterial effects of fibrin glue-antibiotic mixtures. J. Surg. Res. 1991, 50:175-178.
90. Haverich A., Hirt S., Karck M., Siclari F., Wahlig H. Prevention of graft infection by bonding of gentamycin to Dacron prostheses. J. Vasc. Surg. 1992, 15:187-193.
91. van der Ham A.C., Kort W.J., Weijma I.M., van den Ingh H.F., Jeekel H. Effect of antibiotics in fibrin sealant on healing colonic anastomoses in the rat. Br. J. Surg. 1992, 79:525-528.
92. Osada T., Yamamura K., Yano K., Fujimoto K., Mizuno K., Sakurai T., Nabeshima T. Distribution and serum concentration of sisomicin released from fibrin glue-sealed dacron graft in the rat and human. J. Biomed. Mater. Res. 2000, 52:53-57.
93. Watanabe G., Haverich A., Speier R., Dresler C., Borst H.G. Surgical treatment of active infective endocarditis with paravalvular involvement. J. Thorac. Cardiovasc. Surg. 1994, 107:171-177.
94. Tsourvakas S., Hatzigrigoris P., Tsibinos A., Kanellakopoulou K., Giamarellou H., Dounis E. Pharmacokinetic study of fibrin clot-ciprofloxacin complex: an in vitro and in vivo experimental investigation. Arch. Orthop. Trauma Surg. 1995, 114:295-297.
95. Thompson D.F., Davis T.W. The addition of antibiotics to fibrin glue. South. Med. J. 1997, 90:681-684.
96. Park M.S., Kim Y.B. Sustained release of antibiotic from a fibrin-gelatin-antibiotic mixture. Laryngoscope 1997, 107:1378-1381.
97. Itokazu M., Yamamoto K., Yang W.Y., Aoki T., Kato N., Watanabe K. The sustained release of antibiotic from freeze-dried fibrin-antibiotic compound and efficacies in a rat model of osteomyelitis. Infection 1997, 25:359-363.
98. Marone P., Monzillo V., Segu C., Antoniazzi E. Antibiotic-impregnated fibrin glue in ocular surgery: in vitro antibacterial activity. Ophthalmologica 1999, 213:12-15.
99. Kara S., Arikan S., Ersan I., Taskiran Comez A. Simplified technique for sealing corneal perforations using a fibrin glue-assisted amniotic membrane transplant-plug. Case Rep. Ophthalmol. Med. 2014, 2014:351534.
100. Ozaki S., Saito A., Nakaminami H., Ono M., Noguchi N., Motomura N. Comprehensive evaluation of fibrin glue as a local drug-delivery system-efficacy and safety of sustained release of vancomycin by fibrin glue against local methicillin-resistant Staphylococcus aureus infection. J. Artif. Organs 2014, 17:42-49.
101. Fujimoto K., Yamamura K., Osada T., Hayashi T., Nabeshima T., Matsushita M., Nishikimi N., Sakurai T., Nimura Y. Subcutaneous tissue distribution of vancomycin from a fibrin glue/Dacron graft carrier. J. Biomed. Mater. Res. 1997, 36:564-567.
102. Hou T., Xu J., Li Q., Feng J., Zen L. In vitro evaluation of a fibrin gel antibiotic delivery system containing mesenchymal stem cells and vancomycin alginate beads for treating bone infections and facilitating bone formation. Tissue Eng. A 2008, 14:1173-1182.
103. Alphonsa B.M., Kumar P.T.S., Praveen G., Biswas R., Chennazhi K.P., Jayakumar R. Antimicrobial drugs encapsulated in fibrin nanoparticles for treating microbial infested wounds. Pharm. Res. 2014, 31:1338-1351. 10.1007/s11095-013-1254-6.
104. Brajtburg J., Elberg S., Bolard J., Kobayashi G.S., Levy R.A., Ostlund R.E., Schlessinger D., Medoff G. Interaction of plasma proteins and lipoproteins with amphotericin B. J. Infect. Dis. 1984, 149:986-997.
105. Bekersky I., Fielding R.M., Dressler D.E., Lee J.W., Buell D.N., Walsh T.J. Plasma protein binding of amphotericin B and pharmacokinetics of bound versus unbound amphotericin B after administration of intravenous liposomal amphotericin B (AmBisome) and amphotericin B deoxycholate. Antimicrob. Agent Chemother. 2002, 46:834-840.
106. Trombi L., Mattii L., Pacini S., D'Alessandro D., Battolla B., Orciuolo E., Buda G., Fazzi R., Galimberti S., Petrini M. Human autologous plasma-derived clot as a biological scaffold for mesenchymal stem cells in treatment of orthopedic healing. J. Orthop. Res. 2008, 26:176-183.
107. Vedakumari W.S., Sastry T.P. Physiologically clotted fibrin - preparation and characterization for tissue engineering and drug delivery applications. Biologicals 2014, 42:277-284.
108. Tripthi P.S., Rao S.G., Bhat P. Platelet-rich fibrin (PRF) gel as a medium for local drug delivery of metronidazole. Int. J. Adv. Health Sci. 2014, 1:113-122.
109. Kitazawa H., Sato H., Adachi I., Masuko Y., Horikoshi I. Microdialysis assessment of fibrin glue containing sodium alginate for local delivery of doxorubicin in tumor-bearing rats. Biol. Pharm. Bull. 1997, 20:278-281.
110. Yoshida H., Yamaoka Y., Shinoyama M., Kamiya A. Novel drug delivery system using autologous fibrin glue--release properties of anti-cancer drugs. Biol. Pharm. Bull. 2000, 23:371-374.
111. Simpson A.E., Gilbert J.A., Rudnick D.E., Geroski D.H., Aaberg T.M., Edelhauser H.F. Transscleral diffusion of carboplatin: an in vitro and in vivo study. Arch. Ophthalmol. 2002, 120:1069-1074.
112. Van Quill K.R., Dioguardi P.K., Tong C.T., Gilbert J.A., Aaberg T.M., Grossniklaus H.E., Edelhauser H.F., O'Brien J.M. Subconjunctival carboplatin in fibrin sealant in the treatment of transgenic murine retinoblastoma. Ophthalmology 2005, 112:1151-1158.
113. Tsui J.Y., Dalgard C., Van Quill K.R., Lee L., Grossniklaus H.E., Edelhauser H.F., O'Brien J.M. Subconjunctival topotecan in fibrin sealant in the treatment of transgenic murine retinoblastoma. Invest. Ophthalmol. Vis. Sci. 2008, 49:490-496.
114. Martino M.M., Briquez P.S., Ranga A., Lutolf M.P., Hubbell J.A. Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc. Nat. Acad. Sci. U. S. A. 2013, 110:4563-4568.
115. Linhardt R.J. Heparin; an important drug enters its seventh decade. Chem. Ind. 1991, 2:45-50.
116. Capila I., Linhardt R.J. Heparin-protein interactions. Angew. Chem. 2002, 41:391-412.
117. Willerth S.M., Rader A., Sakiyama-Elbert S.E. The effect of controlled growth factor delivery on embryonic stem cell differentiation inside fibrin scaffolds. Stem Cell Res. 2008, 1:205-218.
118. Wood M.D., Sakiyama-Elbert S.E. Release rate controls biological activity of nerve growth factor released from fibrin matrices containing affinity-based delivery systems. J. Biomed. Mater. Res. A 2008, 84:300-312.
119. Wood M.D., Moore A.M., Hunter D.A., Tuffaha S., Borschel G.H., Mackinnon S.E., Sakiyama-Elbert S.E. Affinity-based release of glial-derived neurotrophic factor from fibrin matrices enhances sciatic nerve regeneration. Acta Biomater. 2009, 5:959-968.
120. Arrighi I., Mark S., Alvisi M., von Rechenberg B., Hubbell J.A., Schense J.C. Bone healing induced by local delivery of an engineered parathyroid hormone prodrug. Biomaterials 2009, 30:1763-1771.
121. Zhao W., Han Q., Lin H., Gao Y., Sun W., Zhao Y., Wang B., Chen B., Xiao Z., Dai J. Improved neovascularization and wound repair by targeting human basic fibroblast growth factor (bFGF) to fibrin. J. Mol. Med. (Berl.) 2008, 86:1127-1138.
122. Morton T.J., Furst W., van Griensven M., Redl H. Controlled release of substances bound to fibrin-anchors or of DNA. Drug Deliv. 2009, 16:102-107.
123. Machadoa E.G., Issa J.P., Figueiredo F.A., Santos G.R., Galdeanoa E.A., Alves M.C., Chacona E.L., Ferreira Junior R.S., Barravierac B., Cunha M.R. A new heterologous fibrin sealant as scaffold to recombinant human bone morphogenetic protein-2 (rhBMP-2) and natural latex proteins for the repair of tibial bone defects. Acta Histochem. 2015, 117:288-296.
124. Barros L.C., Ferreira R.S., Barraviera S.R., Stolf H.O., Thomazini-Santos I.A., Mendes-Giannini M.J., Toscano E., Barraviera B. A new fibrin sealant from Crotalus durissus terrificus Venom: applications in medicine. J. Toxicol. Environ. Health B: Crit. Rev. 2009, 12:553-571.
125. Periyathambi P., Vedakumari W.S., Baskar S.K., Bojja S., Sastry T.P. Osteogenic potency of magnetic fibrin nanoparticles - a novel perspective in bone tissue engineering. Mater. Lett. 2015, 139:108-111.
126. Soon A.S., Stabenfeldt S.E., Brown W.E., Barker T.H. Engineering fibrin matrices: the engagement of polymerization pockets through fibrin knob technology for the delivery and retention of therapeutic proteins. Biomaterials 2010, 31:1944-1954.
127. Meyenburg S., Lilie H., Panzner S., Rudolph R. Fibrin encapsulated liposomes as protein delivery system. Studies on the in vitro release behavior. J. Control. Release 2000, 69:159-168.
128. Zhou W., Zhao M., Zhao Y., Mou Y. A fibrin gel loaded with chitosan nanoparticles for local delivery of rhEGF: preparation and in vitro release studies. J. Mater. Sci. Mater. Med. 2011, 22:1221-1230.
129. Caplice N.M., Clover A.J.P. Fibrin as a delivery system in wound healing tissue engineering applications. J. Control. Release 2014, 196:1-8.
130. Baldwin S.L., Bertholet S., Reese V.A., Ching L.K., Reed S.G., Coler R.N. The importance of adjuvant formulation in the development of a tuberculosis vaccine. J. Immunol. 2012, 188:2189-2197.
131. Orr M.T., Fox C.B., Baldwin S.L., Sivananthan S.J., Lucas E., Lin S., Phan T., Moon J.J., Vedvick T.S., Reed S.G., Coler R.N. Adjuvant formulation structure and composition are critical for the development of an effective vaccine against tuberculosis. J. Control. Release 2013, 172:190-200.
132. Oyewumi M.O., Kumar A., Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert. Rev. Vaccines 2010, 9:1095-1107.
133. Ahmad E., Fatima M.T., Saleemuddin M., Owais M. Plasma beads loaded with Candida albicans cytosolic proteins impart protection against the fungal infection in BALB/c mice. Vaccine 2012, 30:6851-6858.
134. Vedakumari W.S., Prabu P., Babu S.C., Sastry T.P. Fibrin nanoparticles as possible vehicles for drug delivery. Biochim. Biophys. Acta 2013, 1830:4244-4253.
135. Andree C., Voigt M., Wenger A., Erichsen T., Bittner K., Schaefer D., Walgenbach K.J., Borges J., Horch R.E., Eriksson E., Stark G.B. Plasmid gene delivery to human keratinocytes through a fibrin-mediated transfection system. Tissue Eng. 2001, 7:757-766.
136. Gelse K., von der Mark K., Aigner T., Park J., Schneider H. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum. 2003, 48:430-441.
137. Breen A., Mc Redmond G., Dockery P., O'Brien T., Pandit A. Assessment of wound healing in the alloxan-induced diabetic rabbit ear model. J. Invest. Surg. 2008, 21:261-269.
138. Kulkarni M.M., Greiser U., O'Brien T., Pandit A. A temporal gene delivery system based on fibrin microspheres. Mol. Pharm. 2011, 8:439-446.
139. Escamez M.J., Carretero M., Garcia M., Martinez-Santamaria L., Mirones I., Duarte B., Holguin A., Garcia E., Garcia V., Meana A., Jorcano J.L., Larcher F., Del Rio M. Assessment of optimal virus-mediated growth factor gene delivery for human cutaneous wound healing enhancement. J. Invest. Dermatol. 2008, 128:1565-1575.
140. des Rieux A., Shikanov A., Shea L.D. Fibrin hydrogels for non-viral vector delivery in vitro. J. Control. Release 2009, 136:148-154.
141. Lee T.C., Ho J.T., Hung K.S., Chen W.F., Chung Y.H., Yang Y.L. Bone morphogenetic protein gene therapy using a fibrin scaffold for a rabbit spinal-fusion experiment. Neurosurgery 2006, 58:373-380. discussion 373-380.
142. Rice J.J., Martino M.M., De Laporte L., Tortelli F., Briquez P.S., Hubbell J.A. Engineering the regenerative microenvironment with biomaterials. Adv. Healthc. Mater. 2013, 2:57-71.
143. Mosesson M.W. Fibrinogen and fibrin polymerization and functions. Blood Coagul. Fibrinolysis 1999, 10(Suppl. 1):S45-S48.
144. Cox S., Cole M., Tawil B. Behavior of human dermal fibroblasts in three-dimensional fibrin clots: dependence on fibrinogen and thrombin concentration. Tissue Eng. 2004, 10:942-954.
145. Ho W., Tawil B., Dunn J.C., Wu B.M. The behavior of human mesenchymal stem cells in 3D fibrin clots: dependence on fibrinogen concentration and clot structure. Tissue Eng. 2006, 12:1587-1595.
146. Mana M., Cole M., Cox S., Tawil B. Human U937 monocyte behavior and protein expression on various formulations of three-dimensional fibrin clots. Wound Repair Regen. 2006, 14:72-80.
147. Trombi L., D'Alessandro D., Pacini S., Fiorentino B., Scarpellini M., Fazzi R., Galimberti S., Guazzini S., Petrini M. Good manufacturing practice-grade fibrin gel is useful as a scaffold for human mesenchymal stromal cells and supports in vitro osteogenic differentiation. Transfusion (Paris) 2008, 48:2246-2251.
148. Proulx M.K., Carey S.P., Ditroia L.M., Jones C.M., Fakharzadeh M., Guyette J.P., Clement A.L., Orr R.G., Rolle M.W., Pins G.D., Gaudette G.R. Fibrin microthreads support mesenchymal stem cell growth while maintaining differentiation potential. J. Biomed. Mater. Res. A 2011, 96:301-312.
149. Gorodetsky R., Clark R.A., An J., Gailit J., Levdansky L., Vexler A., Berman E., Marx G. Fibrin microbeads (FMB) as biodegradable carriers for culturing cells and for accelerating wound healing. J. Invest. Dermatol. 1999, 112:866-872.
150. Horch R.E., Bannasch H., Kopp J., Andree C., Stark G.B. Single-cell suspensions of cultured human keratinocytes in fibrin-glue reconstitute the epidermis. Cell Transpl. 1998, 7:309-317.
151. Hankemeier S., van Griensven M., Ezechieli M., Barkhausen T., Austin M., Jagodzinski M., Meller R., Bosch U., Krettek C., Zeichen J. Tissue engineering of tendons and ligaments by human bone marrow stromal cells in a liquid fibrin matrix in immunodeficient rats: results of a histologic study. Arch. Orthop. Trauma Surg. 2007, 127:815-821.
152. Chong A.K., Ang A.D., Goh J.C., Hui J.H., Lim A.Y., Lee E.H., Lim B.H. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model. J. Bone Joint. Surg. Am. 2007, 89:74-81.
153. Visser L.C., Arnoczky S.P., Caballero O., Egerbacher M. Platelet-rich fibrin constructs elute higher concentrations of transforming growth factor-β1 and increase tendon cell proliferation over time when compared to blood clots: a comparative in vitro analysis. Vet. Surg. 2010, 39:811-817.
154. Shim G., Im S., Lee S., Park J.Y., Kim J., Jin H., Lee S., Im I., Kim D.D., Kim S.W., Lee T.J., Eom J.S., Yi T.G., Song S.U., Byun Y., Oh Y.K. Enhanced survival of transplanted human adipose-derived stem cells by co-delivery with liposomal apoptosome inhibitor in fibrin gel matrix. Eur. J. Pharm. Biopharm. 2013, 85:673-681.
155. Löndahl M., Tarnow L., Karlsmark T., Lundquist R., Nielsen A.M., Michelsen M., Nilsson A., Zakrzewski M., Jörgensen B. Use of an autologous leucocyte and platelet-rich fibrin patch on hard-to-heal DFUs: a pilot study. J. Wound Care 2015, 24:172-178.
156. Falanga V., Iwamoto S., Chartier M., Yufit T., Butmarc J., Kouttab N., Shrayer D., Carson P. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 2007, 13:1299-1312.
157. Torio-Padron N., Borges J., Momeni A., Mueller M.C., Tegtmeier F.T., Stark G.B. Implantation of VEGF transfected preadipocytes improves vascularization of fibrin implants on the cylinder chorioallantoic membrane (CAM) model. Minim. Invasive Ther. Allied Technol. 2007, 16:155-162.
158. Dare E.V., Vascotto S.G., Carlsson D., Hincke M.T., Griffith M. Differentiation of a fibrin gel encapsulated chondrogenic cell line. Int. J. Artif. Organs 2007, 30:619-627.
159. Ryu J.H., Kim I.K., Cho S.W., Cho M.C., Hwang K.K., Piao H., Piao S., Lim S.H., Hong Y.S., Choi C.Y., Yoo K.J., Kim B.S. Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 2005, 26:319-326.
160. Gwak S.J., Choi D., Paik S.S., Lee E.Y., Lees K.S., Kim B.S. Stable hepatocyte transplantation using fibrin matrix. Biotechnol. Lett. 2004, 26:505-508.
161. Beattie G.M., Montgomery A.M., Lopez A.D., Hao E., Perez B., Just M.L., Lakey J.R., Hart M.E., Hayek A. A novel approach to increase human islet cell mass while preserving beta-cell function. Diabetes 2002, 51:3435-3439.
162. Andrades P., Asiedu C., Rodriguez C., Goodwin K.J., McCarn J., Thomas J.M. Subcutaneous pancreatic islet transplantation using fibrin glue as a carrier. Transpl. Proc. 2007, 39:191-192.
163. Najjar M., Manzoli V., Villa C., Martino M.M., Molano R.D., Torrente Y., Pileggi A., Inverardi L., Ricordi C., Hubbell J.A., Tomei A.A. Fibrin gels engineered with pro-angiogenic growth factors promote engraftment of pancreatic islets in extrahepatic sites in mice. Biotechnol. Bioeng. 2015, 10.1002/bit.25589.
164. Ahmed T.A.E., Ringuette R., Wallace V.A., Griffith M. Autologous fibrin glue as an encapsulating scaffold for delivery of retinal progenitor cells. Front. Bioeng. Biotechnol. 2014, 10.3389/fbioe.2014.00085.
165. Cummings C.L., Gawlitta D., Nerem R.M., Stegemann J.P. Properties of engineered vascular constructs made from collagen, fibrin, and collagen-fibrin mixtures. Biomaterials 2004, 25:3699-3706.
166. Perka C., Schultz O., Lindenhayn K., Spitzer R.S., Muschik M., Sittinger M., Burmester G.R. Joint cartilage repair with transplantation of embryonic chondrocytes embedded in collagen-fibrin matrices. Clin. Exp. Rheumatol. 2000, 18:13-22.
167. Perka C., Spitzer R.S., Lindenhayn K., Sittinger M., Schultz O. Matrix-mixed culture: new methodology for chondrocyte culture and preparation of cartilage transplants. J. Biomed. Mater. Res. 2000, 49:305-311.
168. Park S.H., Park S.R., Chung S.I., Pai K.S., Min B.H. Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif. Organs 2005, 29:838-845.
169. Aper T., Teebken O.E., Steinhoff G., Haverich A. Use of a fibrin preparation in the engineering of a vascular graft model. Eur. J. Vasc. Endovasc. Surg. 2004, 28:296-302.
170. Alaminos M., Del Carmen Sanchez-Quevedo M., Munoz-Avila J.I., Serrano D., Medialdea S., Carreras I., Campos A. Construction of a complete rabbit cornea substitute using a fibrin-agarose scaffold. Invest. Ophthalmol. Vis. Sci. 2006, 47:3311-3317.
171. Kim B.S., Kim H.J., Choi J.G., You H.K., Lee J. The effects of fibrinogen concentration on fibrin/atelocollagen composite gel: an in vitro and in vivo study in rabbit calvarial bone defect. Clin. Oral Implants Res. 2014.
172. Snyder T.N., Madhavan K., Intrator M., Dregalla R.C., Park D. A fibrin/hyaluronic acid hydrogel for the delivery of mesenchymal stem cells and potential for articular cartilage repair. J. Biol. Eng. 2014, 8:10.
173. Akiyama H. Control of chondrogenesis by the transcription factor Sox9. Mod. Rheumatol. Jpn. Rheum. Assoc. 2008, 18:213-219.
174. Ahearne M., Kelly D.J. A comparison of fibrin, agarose and gellan gum hydrogels as carriers of stem cells and growth factor delivery microspheres for cartilage regeneration. Biomed. Mater. 2013, 8. 035004 (10pp). 10.1088/1748-6041/8/3/035004.
175. Yang H.S., La W.G., Cho Y.M., Shin W., Yeo G.D., Kim B.S. Comparison between heparin-conjugated fibrin and collagen sponge as bone morphogenetic protein-2 carriers for bone regeneration. Exp. Mol. Med. 2013, 44:350-355.
176. Feng X., Clark R.A., Galanakis D., Tonnesen M.G. Fibrin and collagen differentially regulate human dermal microvascular endothelial cell integrins: stabilization of alphav/beta3 mRNA by fibrin1. J. Invest. Dermatol. 1999, 113:913-919.