Heparin-chitosan-coated acellular bone matrix enhances perfusion of blood and vascularization in bone tissue engineering scaffolds

Tissue Engineering - Part A

Volumn 17, Issue 19-20, 2011, Pages 2369-2378

  Sun, Xin Jun ^a,b   Peng, Wei ^a,c   Yang, Zai Liang ^a   Ren, Ming Liang ^a   Zhang, Shi Chang ^a   Zhang, Wei Guo ^d   Zhang, Lian Yang ^d   Xiao, Kai ^a   Wang, Zheng Guo ^a   Zhang, Bo ^a   Wang, Jin ^d  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b 89th Hospital of PLA   (China)

^c 309TH HOSPITAL OF PLA   (China)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; BONE; CHITOSAN; COATINGS; COMPUTERIZED TOMOGRAPHY; POLYSACCHARIDES; TISSUE; TOMOGRAPHY;

ACTIVATED PARTIAL THROMBOPLASTIN TIME; ANTI-COAGULATION; ANTICOAGULATION PROPERTIES; BLOOD PERFUSION; BLOOD SUPPLY; BONE DEFECT MODELS; BONE MATRIX; BONE TISSUE ENGINEERING; COATING PROCESS; COMPUTED TOMOGRAPHY; DECELLULARIZED; EXTRACELLULAR BONE MATRICES; HEMOCOMPATIBILITY; HISTOLOGICAL EXAMINATION; IN-VITRO; IN-VIVO; LAYER-BY-LAYERS; PERFUSION IMAGING; SURFACE-MODIFIED; THICK-TISSUE; TISSUE SUBSTITUTE; VASCULARIZATION; WASTE PRODUCTS;

SCAFFOLDS (BIOLOGY);

ORYCTOLAGUS CUNICULUS;

BIOMATERIAL; CHITOSAN; HEPARIN; TISSUE SCAFFOLD;

ANGIOGENESIS; ANIMAL; ARTICLE; BONE MATRIX; CHEMISTRY; DRUG EFFECT; IMPLANT; METHODOLOGY; PATHOLOGY; PERFUSION; RABBIT; SWINE; TIME; TISSUE ENGINEERING; ULTRASTRUCTURE; VASCULARIZATION; X RAY PHOTOELECTRON SPECTROSCOPY;

ANIMALS; BONE MATRIX; CHITOSAN; COATED MATERIALS, BIOCOMPATIBLE; HEPARIN; IMPLANTS, EXPERIMENTAL; NEOVASCULARIZATION, PHYSIOLOGIC; PERFUSION; PHOTOELECTRON SPECTROSCOPY; RABBITS; SUS SCROFA; TIME FACTORS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 80053096411     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2011.0027     Document Type: Article

References (52)

1. Langer, R., and Vacanti, J.P. Tissue engineering. Science 260, 920, 1993.
2. Marcacci, M., Kon, E., Moukhachev, V., Lavroukov, A., Kutepov, S., Quarto, R., et al. Stem cells associated with macroporous bioceramics for long bone repair: 6 to 7 year outcome of a pilot clinical study. Tissue Eng 13, 947, 2007.
3. Zhang, Z.Y., Teoh, S.H., Chong, M.S., Lee, E.S., Tan, L.G., Mattar, C.N., et al. Neo-vascularization and bone formation mediated by fetal mesenchymal stem cell tissue-engineered bone grafts in critical-size femoral defects. Biomaterials 31, 608, 2010.
4. Buma, P., Schreurs, W., and Verdonschot, N. Skeletal tissue engineering from in vitro studies to large animal models. Biomaterials 25, 1487, 2004.
5. Nomi, M., Atala, A., Coppi, P.D., and Soker, S. Principals of neovascularization for tissue engineering. Mol Aspects Med 23, 463, 2002.
6. Cassell, O.C., Hofer, S.O., Morrison, W.A., and Knight, K.R. Vascularisation of tissue engineered grafts: the regulation of angiogenesis in reconstructive surgery and in disease states. Br J Plast Surg 55, 603, 2002.
7. Shastri, V.P. Future of regenerative medicine: challenges and hurdles. Artif Organs 30, 828, 2006.
8. Laschke, M.W., Harder, Y., Amon, M., Martin, I., Farhadi, J., Ring, A., et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng 12, 2093, 2006.
9. Vogler, E.A., and Siedlecki, C.A. Contact activation of blood-plasma coagulation. Biomaterials 30, 1857, 2009.
10. Tadashi Sasagawa, Tatsuya Shimizu, Sachiko Sekiya, Yuji Haraguchi, and Masayuki Yamato. Design of prevascularized three-dimensional cell-dense tissues using a cell sheet stacking manipulation technology. Biomaterials 31, 1646, 2010.
11. Ratner, B.D. The catastrophe revisited: blood compatibility in the 21st century. Biomaterials 28, 5144, 2007.
12. McFadden, E.P., Stabile, E., Regar, E., Cheneau, E., Ong, A.T., Kinnaird, T., et al. Late thrombosis in drug-eluting coronary stents after discontinuation of antiplatelet therapy. Lancet 364, 1519, 2004.
13. Serruys, P.W., Emanuelsson, H., van der Giessen, W., Lunn, A.C., Kiemeney, F., Macaya, C., et al. Heparin-coated Palmaz-Schatz stents in human coronary arteries: early outcome of the Benestent-II pilot study. Circulation 93, 412, 1996.
14. Serruys, P.W., van Hout, B., Bonnier, H., Legrand, V., Garcia, E., Macaya, C., et al. Randomised comparison of implantation of heparin coated stents with balloon angioplasty in selected patients with coronary artery disease (Bene-stent II). Lancet 352, 673, 1998.
15. Chen, H., Chen, Y., Sheardown, H., and Brook, M.A. Immobilization of heparin on a silicone surface through a heterobifunctional PEG spacer. Biomaterials 26, 7418, 2005.
16. Liu, Q., Ding, J., Mante, F.K., Wunder, S., and Baran, G.R. The role of surface functional groups in calcium phosphate nucleation on titanium foil: a self-assembled monolayer technique. Biomaterials 23, 3103, 2002.
17. Fu, J.H., Ji, J., Yuan, W.Y., and Shen, J.C. Construction of anti-adhesive and antibacterial multilayer films via layer-bylayer assembly of heparin and chitosan. Biomaterials 26, 6684, 2005.
18. Meng, S., Liu, Z., Shen, L., Guo, Z., Chou, L.L., Zhong, W., et al. The effect of a laye-by-layer chitosan-heparin coating on the endothelialization and coagulation properties of a coronary stent system. Biomaterials 30, 2276, 2009.
19. Christensen, K., Larsson, R., Emanuelsson, H.K., Elgue, G., and Larsson, A. Heparin coating of the stent graft-effects on platelets, coagulation and complement activation. Biomaterials 22, 349, 2001.
20. Chen, J.L., Li, Q.L., Chen, J.Y., Chen, C., and Huang, N. Improving blood-compatibility of titanium by coating collagen-heparin multilayers. Appl Surf Sci 255, 6894, 2009.
21. Pike, D.B., Cai, S., Pomraning, K.R., Firpo, M.A., Fisher, R.J., Shu, X.Z., et al. Heparin regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF. Biomaterials 27, 5242, 2006.
22. Yang Zhilu, Wang Jin, Luo Rifang, and Manfred F. Maitz. The covalent immobilization of heparin to pulsed-plasma polymeric allylamine films on 316L stainless steel and the resulting effects on hemocompatibility. Biomaterials 31, 2072, 2010.
23. Rouwkema, J., de Boer, J., and Van Blitterswijk, C.A. Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. Tissue Eng 12, 2685, 2006.
24. Yuan, J., Cui, L., Zhang, W.J., Liu, W., and Cao, Y. Repair of canine mandibular bone defects with bone marrow stromal cells and porous b-tricalcium phosphate. Biomaterials 28, 1005, 2007.
25. Qiang, C., Zailiang, Y., Shijin, S., et al. Adipose-derived stem cells modified genetically in vivo promote reconstruction of bone defects. Cytotherapy 12, 831, 2010.
26. Gorbet, M.B., and Sefton, M.V. Biomaterial associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 25, 5681, 2004.
27. Tseng, P.Y., Rele, S.S., Sun, X.L., and Chaikof, E.L. Membrane mimetic films containing thrombomodulin and heparin inhibit tissue factor induced thrombin generation in a flow model. Biomaterials 27, 2637, 2006.
28. Werner, C., Maitz, M.F., and Sperling, C. Current strategies towards hemocompatible coatings. J Mater Chem 17, 3376, 2007.
29. Takada, T., Katagiri, T., Ifuku, M., et al. Sulfated polysaccharides enhance the biological activities of bone morphogenetic proteins. J Biol Chem 278, 43229, 2003.
30. Robinson, D.E., Marson, A., Short, R.D., Buttle, D.J., Day, A.J., Parry, K.L., et al. Surface gradient of functional heparin. Adv Mater 20, 1166, 2008.
31. Vrolix, M.C.M., Legrand, V.M., Reiber, J.H.C., Grollier, G., Schalij, M.J., Brunel, P., et al. Heparin coated Wiktor stents in human coronary arteries (MENTOR trial). Am J Cardiol 86, 385, 2000.
32. Chen, H., Chen, Y., Sheardown, H., and Brook, M.A. Immobilization of heparin on a silicone surface through a heterobifunctional PEG spacer. Biomaterials 26, 7418, 2005.
33. Liu, Q., Ding, J., Mante, F.K., Wunder, S., and Baran, G.R. The role of surface functional groups in calcium phosphate nucleation on titanium foil: a self-assembled monolayer technique. Biomaterials 23, 3103, 2002.
34. Fu, J.H., Ji, J., Yuan, W.Y., and Shen, J.C. Construction of anti-adhesive and antibacterial multilayer films via layer-bylayer assembly of heparin and chitosan. Biomaterials 26, 6684, 2005.
35. Meng Sheng, Liu Zongjun, and Shen Li. The effect of a layerby-layer chitosan heparin coating on the endothelialization and coagulation properties of a coronary stent system. Biomaterials 30, 2276, 2009.
36. Jiang, T., Khan, Y., Nair, L.S., Abdel-Fattah, W.I., and Laurencin, C.T. Functionalization of chitosan/poly(lactic acid-glycolic acid) sintered microsphere scaffolds via surface heparinization for bone tissue engineering. J Biomed Mater Res A 93, 1193, 2010.
37. Fu, J.H., Ji, J., Yuan, W.Y., and Shen, J.C. Construction of anti-adhesive and antibacterial multilayer films via layer-bylayer assembly of heparin and chitosan. Biomaterials 26, 6684, 2005.
38. Takahashi, S., Kaneda, H., Tanaka, S., Miyashita, Y., Shiono, T., Taketani, Y., et al Late angiographic stent thrombosis after sirolimus-eluting stent implantation.Circulation 71, 226, 2007.
39. Tsai, A.G., Johnson, P.C., and Intaglietta, M. Oxygen gradients in the microcirculation. Physiol Rev 83, 933, 2003.
40. Muschler, G.F., Nakamoto, C., and Griffith, L.G. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am 86-A, 1541, 2004.
41. Peter R. Hoskins. Simulation and validation of arterial ultrasound imaging and blood flow. Ultrasound Med Biol 34, 693, 2008.
42. Bolland, B.J.R.F., Kanczler, J.M., Dunlop, D.G., and Oreffo, R.O.C. Development of in vivo mCT evaluation of neovascularisation in tissue engineered bone constructs. Bone 43, 195, 2008.
43. Antonella Bisio, Sara Guglieri, Marta Frigerio, Giangiacomo Torri, Elena Vismara, Umberto Cornelli, Donata Bensi, Sergio Gonellad, and Luigi De Ambrosi. Controlled g-ray irradiation of heparin generates oligosaccharides enriched in highly sulfated sequences. Carbohydrate Polymers 55, 101, 2004.
44. Dam, A.M., Gazsó , E.G., Kaewpila, S., and Maschek, I. Radiation sterilization dose calculation for heparin and aprotinin based on ISO Method 1. Int J Pharm 121, 245, 1995.
45. Nobuhiko Miyazawa, Ali Syed Arbab, Takako Umeda, and Iwao Akiyama. Perfusion CT investigation of chronic internal carotid artery occlusion: comparison with SPECT. Clin Neurol Neurosurg 108, 11, 2005.
46. Daisuke Takenaka, Yoshiharu Ohnoa, Hisanobu Koyama, Munenobu Nogami, and Yumiko Onishi. Co-registered perfusion SPECT/CT: utility for prediction of improved postoperative outcome in lung volume reduction surgery candidates. Eur J Radiol 74, 465, 2010.
47. Hong Zhao, Jingshan Gong, Yan Wang, Zuoquan Zhang, and Peixin Qin. Renal hemodynamic changes with aging: a preliminary study using CT perfusion in the healthy elderly. Clin Imaging 34, 247, 2010.
48. Andreas K̈ amena, Florian Streitparth, Christian Grieser, Lukas Lehmkuhl, et al. Dynamic perfusion CT: optimizing the temporal resolution for the calculation of perfusion CT parameters in stroke patients. Eur J Radiol 64, 111, 2007.
49. Lisa Tang, Ghassan Hamarneh, and Anna Celler. Validation of mutual information based registration of CT and bone SPECT images in dual isotope studies. Computer Methods Programs Biomed 92, 173, 2008.
50. Gillard, J.H., Antoun, N.M., Burnet, N.G., and Pickard, J.D. Reproducibility of quantitative CT perfusion imaging. Br J Radiol 74, 552, 2001.
51. Roberts, H.C., Dillon, W.P., and Smith, W.S. Dynamic CT perfusion to assess the effect of carotid revascularization in chronic cerebral ischemia. Am J Neuroradiol 21, 421, 2000.
52. Young Han Lee,Woocheol Kwon, Myung Soon Kim, Young Ju Kim, and Myeong Sub Lee. Lung perfusion CT: the differentiation of cavitary mass. Eur J Radiol 73, 59, 2010.