Fabrication and characterization of biomimetic collagen-apatite scaffolds with tunable structures for bone tissue engineering

Acta Biomaterialia

Volumn 9, Issue 7, 2013, Pages 7308-7319

  Xia, Zengmin ^a   Yu, Xiaohua ^a   Jiang, Xi ^b   Brody, Harold D ^a   Rowe, David W ^b   Wei, Mei ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Apatite; Biomimetic; Bone regeneration; Collagen; Freeze drying

Indexed keywords

BIOMIMETIC MATERIALS; BIOMIMETIC PROCESSES; BONE; COLLAGEN; LAMELLAR STRUCTURES; PRECIPITATION (CHEMICAL); SCAFFOLDS (BIOLOGY); SELF ASSEMBLY; TISSUE REGENERATION;

'CURRENT; BONE REGENERATION; BONE REPAIR; BONE TISSUE ENGINEERING; COLLAGEN FIBRES; FABRICATION AND CHARACTERIZATIONS; FREEZE CASTING; FREEZE DRYING; SIMULATED BODY FLUIDS; TUNABLES;

APATITE;

APATITE; COLLAGEN; COLLAGEN FIBER; TISSUE SCAFFOLD;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY FLUID; BONE REGENERATION; BONE REMODELING; BONE TISSUE; CONTROLLED STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSSIFICATION; PRECIPITATION; PRIORITY JOURNAL; SIMULATION; TISSUE ENGINEERING;

EID: 84878304638     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.03.038     Document Type: Article

References (63)

1. C. Du, F.Z. Cui, W. Zhang, Q.L. Feng, X.D. Zhu, and K. de Groot Formation of calcium phosphate/collagen composites through mineralization of collagen matrix J Biomed Mater Res 50 2000 518 527
2. S. Yunoki, H. Sugiura, T. Ikoma, E. Kondo, K. Yasuda, and J. Tanaka Effects of increased collagen-matrix density on the mechanical properties and in absorbability of hydroxyapatite-collagen composites as artificial bone materials J Biomed Mater Res, Part B: App Biomater 6 2011 015012
3. A. Akkouch, Z. Zhang, and M. Rouabhi A novel collagen/hydroxyapatite/ poly(lactide-co-e-caprolactone) biodegradable and bioactive 3D porous scaffold for bone regeneration J Biomed Mater Res, Part A 96 2011 693 704
4. I. Tcacencu, and M. Wendel Collagen-hydroxyapatite composite enhances regeneration of calvaria bone defects in young rats but postpones the regeneration of calvaria bone in aged rats J Mater Sci Mater Med 19 2008 2015 2021
5. A. Matsuura, T. Kubo, K. Doi, K. Hayashi, K. Morita, and R. Yokota Bone formation ability of carbonate apatite-collagen scaffolds with different carbonate contents Dent Mater J 28 2009 234 242
6. Y.S. Pek, S. Gao, M.S. Arshad, and Leck.K.J. Ying Porous collagen-apatite nanocomposite foams as bone regeneration scaffolds Biomaterials 29 2008 4300 4305
7. A.A. Al-Munajjed, N.A. Plunkett, J.P. Gleeson, T. Weber, C. Jungreuthmayer, and T. Levingstone Development of a biomimetic collagen-hydroxyapatite scaffold for bone tissue engineering using a SBF immersion technique J Biomed Mater Res, Part B App Biomater 90 2009 584 591
8. A.A. Al-Munajjed, J.P. Gleeson, and F.J. O'Brien Development of a collagen calcium-phosphate scaffold as a novel bone graft substitute Stud Health Technol Inf 133 2008 11 20
9. M. Kikuchi, S. Itohv, S. Ichinose, K. Shinomiya, and J. Tanaka Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo Biomaterials 22 2001 1705 1711
10. A. Ficai, E. Andronescu, G. Voicu, C. Ghitulica, B.S. Vasile, and D. Ficai Self-assembled collagen/hydroxyapatite composite materials J Chem Eng 160 2010 794 800
11. M. Gelinsky, P.B. Welzel, P. Simon, A. Bernhardt, and U. König Porous three-dimensional scaffolds made of mineralised collagen: preparation and properties of a biomimetic nanocomposite material for tissue engineering of bone J Chem Eng 137 2008 84 96
12. H. Nitzsche, A. Lochmann, H. Metz, A. Hauser, F. Syrowatka, and E. Hempel Fabrication and characterization of a biomimetic composite scaffold for bone defect repair J Biomed Mater Res, Part A 94 2010 298 307
13. W. Zhang, S.S. Liao, and F.Z. Cui Hierarchical self-sssembly of nano-fibrils in mineralized collagen Chem Mater 15 2003 3221 3226
14. Y. Liu, N. Li, Y. Qi, L. Dai, T.E. Bryan, and J. Mao Intrafibrillar collagen mineralization produced by biomimetic hierarchical nanoapatite assembly Adv Mater 23 2011 975 980
15. N. Nassif, F. Gobeaux, J. Seto, E. Belaminie, J. Seto, and P. Davidson Self-assembled collagen/apatite matrix with bone-like hierarchy Chem Mater 22 2010 3307 3309
16. J.H. Song, H.E. Kim, and H.W. Kim Collagen-apatite nanocomposite membranes for guided bone regeneration J Biomed Mater Res, Part B App Biomater 83 2007 248 257
17. F. Peng, J.R. Olsen, M.T. Shaw, and M. Wei Influence of pre-treatment on the surface characteristics of PLLA fibers and subsequent hydroxyapatite coating J Biomed Mater Res, Part B App Biomater 88 2009 220 229
18. L. Ma, C. Gao, Z. Mao, J. Zhou, and J. Shen Enhanced biological stability of collagen porous scaffolds by using amino acids as novel cross-linking bridges Biomaterials 25 2004 2997 3004
19. S. Tang, S.M. Vickers, H.P. Hsu, and M. Spector Fabrication and characterization of porous hyaluronic acid-collagen composite scaffolds J Biomed Mater Res, Part A 82 2007 323 335
20. L. Ma, C. Gao, Z. Mao, J. Zhou, J. Shen, and X. Hu Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering Biomaterials 24 2003 4833 4841
21. J.M. Holzwarth, and P.X. Ma Biomimetic nanofibrous scaffolds for bone tissue engineering Biomaterials 32 36 2011 9622 9629
22. H. Qu, and M. Wei The effect of temperature and initial pH on biomimetic apatite coating J Biomed Mater Res, Part B App Biomater 87 2008 204 212
23. H. Qu, and M. Wei Improvement of adhesive strength of biomimetically coated titanium implants J Biomed Mater Res, Part B App Biomater 84 2008 436 443
24. Y. Zhang, G. Zhang, and M. Wei Controlling the biodegradation rate of magnesium using biomimetic apatite coating J Biomed Mater Res, Part B App Biomater 89 2009 408 414
25. H. Qu, Z. Xia, D. Knecht, and M. Wei Synthesis of dense collagen/apatite composites using a biomimetic method J Am Ceram Soc 91 2008 3211 3215
26. Z. Xia, X. Yu, and M. Wei Biomimetic collagen/apatite coating formation on Ti6Al4V substrates J Biomed Mater Res, Part B App Biomater 100 3 2012 871 881
27. U.G.K. Wegst, M. Schecter, A.E. Donius, and P.M. Hunger Biomaterials by freeze casting Philos Trans R Soc A 368 2010 2099 2121
28. H. Zhang, I. Hussain, M. Brust, M.F. Butler, S.P. Rannard, and A.I. Cooper Aligned two- and three-dimensional structures by directional freezing of polymers and nanoparticles Nat Mater 4 2005 787 793
29. S. Zmora, R. Glicklis, and S. Cohen Tailoring the pore architecture in 3-D alginate scaffolds by controlling the freezing regime during fabrication Biomaterials 23 2002 4087 4094
30. N. Bhardwaj, Q.T. Nguyen, A.C. Chen, D.L. Kaplan, R.L. Sah, and S.C. Kundu Potential of 3-D tissue constructs engineered from bovine chondrocytes/silk fibroin-chitosan for in vitro cartilage tissue engineering Biomaterials 32 2011 5773 5781
31. C. Xu, P. Su, X. Chen, Y. Meng, W. Yu, and A. Xiang Biocompatibility and osteogenesis of biomimetic bioglass-collagen-phosphatidylserine composite scaffolds for bone tissue engineering Biomaterials 32 2011 1051 1058
32. K.A. Faraj, T.H.V. Kuppevel, and W.F. Daamen Construction of collagen scaffolds that mimic the three-dimensional architecture of specific tissues Tissue Eng 13 2007 2387 2394
33. B.P. Kanungo, E. Silva, K.V. Van Vliet, and L.J. Gibson Characterization of mineralized collagen-glycosaminoglycan scaffolds for bone regeneration Acta Biomater 4 2008 490 503
34. F.J. O'Brien, B.A. Harley, I.V. Yannas, and L.J. Gibson Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds Biomaterials 25 2004 1077 1086
35. F.J. O'Brien, B.A. Harley, I.V. Yannas, and L.J. Gibson The effect of pore size on cell adhesion in collagen-GAG scaffolds Biomaterials 26 2005 433 441
36. M.G. Haugh, C.M. Murphy, and F.J. O'Brien Novel freeze-drying methods to produce a range of collagen-glycosaminoglycan scaffolds with tailored mean pore sizes Tissue Eng C 16 2010 887 894
37. J.I. Dawson, D.A. Wahl, S.A. Lanham, J.M. Kanczler, J.T. Czernuszka, and R.O.C. Oreffo Development of specific collagen scaffolds to support the osteogenic and chondrogenic differentiation of human bone marrow stromal cells Biomaterials 29 2008 3105 3116
38. A.K. Lynn, S.M. Best, R.E. Cameron, B.A. Harley, I.V. Yannas, and L.J. Gibson Design of a multiphase osteochondral scaffold. I. Control of chemical composition J Biomed Mater Res, Part A 92 2010 1057 1065
39. X. Yu, L. Wang, F. Peng, X. Jiang, Z. Xia, and J. Huang The effect of fresh bone marrow cells on reconstruction of mouse calvarial defect combined with calvarial osteoprogenitor cells and collagen-apatite scaffold J Tissue Eng Regen Med 2012 10.1002/term.1490
40. H. Schoof, L. Bruns, A. Fischer, I. Heschel, and G. Rau Dendritic ice morphology in unidirectionally solidified collagen suspensions J Crystal Growth 209 2000 122 129
41. S. Deville, E. Saiz, R.K. Nalla, and A.P. Tomsia Freezing as a path to build complex composites Science 311 2006 515 518
42. S. Deville, E. Saiz, and A.P. Tomsia Freeze casting of hydroxyapatite scaffolds for bone tissue engineering Biomaterials 27 2006 5480 5489
43. H. Schoof, J. Apel, I. Heschel, and G. Rau Control of pore structure and size in freeze-dried collagen sponges J Biomed Mater Res 58 2001 352 357
44. S. Yunoki, T. Ikoma, A. Tsuchiya, A. Monkawa, K. Ohta, and S. Sotome Fabrication and mechanical and tissue ingrowth properties of unidirectionally porous hydroxyapatite/collagen composite J Biomed Mater Res, Part B App Biomater 80 2007 166 173
45. N. Rajan, J. Habermehl, M.F. Coté, C.J. Doillon, and D. Mantovani Preparation of ready-to-use, storable and reconstituted type I collagen from rat tail tendon for tissue engineering applications Nat Protoc 1 2007 2753 2758
46. Y. Wang, Y. Liu, K. Buhl, and D. Rowe Comparison of the action of transient and continuous PTH on primary osteoblast cultures expressing differentiation stage-specific GFP J Biomed Mater Res 20 2005 5 14
47. L. Wang, Y. Liu, Z. Kalajzic, X. Jiang, and D.W. Rowe Heterogeneity of engrafted bone-lining cells after systemic and local transplantation Blood 106 2005 3650 3657
48. X. Jiang, Z. Kalajzic, P. Maye, A. Braut, J. Bellizzi, and M. Mina Histological analysis of GFP expression in murine bone J Histochem Cytochem 53 2005 593 602
49. F. Barrere, C.A. van Blitterswijk, K. de Groot, and P. Layrolle Influence of ionic strength and carbonate on the Ca-P coating formation from SBF×5 solution Biomaterials 23 2002 1921 1930
50. X. Liu, L.A. Smith, J. Hu, and P.X. Ma Biomimetic nanofibrous gelatin/apatite composite scaffolds for bone tissue engineering Biomaterials 30 2009 2252 2258
51. C. Liu, Z. Han, and J.T. Czernuszka Gradient collagen/nanohydroxyapatite composite scaffold: development and characterization Acta Biomater 5 2009 661 669
52. S. Deville, E. Maire, G. Bernard-Granger, A. Lasalle, A. Bogner, and C. Gauthler Metastable and unstable cellular solidification of colloidal suspensions Nat Mater 8 2009 966 972
53. S.S.L. Peppin, and J.S. Wettlaufer Experimental verification of morphological instability in freezing aqueous colloidal suspensions Phys Rev Lett 100 2008 238301 238304
54. S. Deville Freeze-casting of porous ceramics: a review of current achievements and issues Adv Eng Mater 10 2008 155 169
55. S.S.L. Peppin, A. Majumdar, and J.S. Wettlaufer Morphological instability of a non-equilibrium ice-colloid interface Proc R Soc A 466 2010 177 194
56. J.Y. Rho, L. Kuhn-Spearing, and P. Zioupos Mechanical properties and the hierarchical structure of bone Med Eng Phys 20 1998 92 101
57. K. Whang, K.E. Healy, D.R. Elenz, E.K. Nam, D.C. Tsai, and C.H. Thomas Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture Tissue Eng 5 1 1999 35 51
58. V. Karageorgiou, and D. Kaplan Porosity of 3D biomaterial scaffolds and osteogenesis Biomaterials 26 27 2005 5474 5491
59. A. Penk, Y. Förster, H.A. Scheidt, A. Nimptsch, M.C. Hacker, and M. Schulz-Siegmund The pore size of PLGA bone implants determines the de novo formation of bone tissue in tibial head defects in rats Magn Reson Med 2012 10.1002/mrm.24541
60. M.H. Mankani, S. Afghani, J. Franco, M. Launey, S. Marshall, and G.W. Marshall Lamellar spacing in cuboid hydroxyapatite scaffolds regulates bone formation by human bone marrow stromal cells Tissue Eng A 17 11-12 2011 1615 1623
61. B. Feng, Z. Jinkang, W. Zhen, L. Jianxi, C. Jiang, and L. Jian The effect of pore size on tissue ingrowth and neovascularization in porous bioceramics of controlled architecture in vivo J Biomed Mater Res, Part B App Biomater 6 1 2011 015007
62. F.M. Klenke, Y. Liu, H. Yuan, E.B. Hunziker, K.A. Siebenrock, and W. Hofstetter Impact of pore size on the vascularization and osseointegration of ceramic bone substitutes in vivo J Biomed Mater Res, Part A 85 3 2008 777 786
63. A. Ardizzoni Osteocyte lacunar size-lamellar thickness relationships in human secondary osteons J Biomed Mater Res 28 2 2001 215 219