Role of pore size and morphology in musculo-skeletal tissue regeneration

Materials Science and Engineering C

Volumn 61, Issue , 2016, Pages 922-939

  Perez, Roman A ^a,b   Mestres, Gemma ^c  

^a Dankook University   (South Korea)

^b BK21 Plus NBM Global Research Center for Regenerative Medicine   (South Korea)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Bone regeneration; Macroporosity; Microporosity; Microstructure; Pore size; Porosity; Rapid prototyping; Scaffold

Indexed keywords

BIOCOMPATIBILITY; BIOMATERIALS; BONE; CELL ADHESION; CELL PROLIFERATION; GENE EXPRESSION; MICROPOROSITY; MICROSTRUCTURE; PORE SIZE; POROSITY; RAPID PROTOTYPING; SCAFFOLDS; SCAFFOLDS (BIOLOGY); TISSUE;

BONE REGENERATION; CELL PENETRATION; CELLULAR ADHESION; INTERCONNECTIVITY; MACRO-POROSITY; NUTRIENT DIFFUSION; PHYSICO-CHEMICALS; PHYSICOCHEMICAL PROPERTY;

TISSUE REGENERATION;

BIOMATERIAL; DRUG CARRIER;

ANIMAL; BONE REGENERATION; CELL ADHESION; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; OSTEOBLAST; PERMEABILITY; PHYSIOLOGY; POROSITY; TISSUE SCAFFOLD; YOUNG MODULUS;

ANIMALS; BIOCOMPATIBLE MATERIALS; BONE REGENERATION; CELL ADHESION; CELL DIFFERENTIATION; DRUG CARRIERS; ELASTIC MODULUS; HUMANS; OSTEOBLASTS; PERMEABILITY; POROSITY; TISSUE SCAFFOLDS;

EID: 84956719629     PISSN: 09284931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.msec.2015.12.087     Document Type: Review

References (164)

1. R.A. Perez, S.-J. Seo, J.-E. Won, E.-J. Lee, J.-H. Jang, J.C. Knowles, and et al. Therapeutically relevant aspects in bone repair and regeneration Mater. Today 2015 10.1016/j.mattod.2015.06.011
2. S.J. Hollister Porous scaffold design for tissue engineering Nat. Mater. 4 2005 518 524 10.1038/nmat1421
3. D.W. Hutmacher Scaffolds in tissue engineering bone and cartilage Biomaterials 21 2000 2529 2543 10.1016/S0142-9612(00)00121-6
4. R.A. Pérez, J.-E. Won, J.C. Knowles, and H.-W. Kim Naturally and synthetic smart composite biomaterials for tissue regeneration Adv. Drug Deliv. Rev. 65 2013 471 496 10.1016/j.addr.2012.03.009
5. Scaffolding in Tissue Engineering 2005 CRC Press (http://books.google.com/books?id=kSczI9Sbq9EC&pgis=1 (accessed July 17, 2014))
6. K. Li, X. Li, G.W. Irwin, and G. He Life System Modeling and Simulation 2007 Springer Berlin Heidelberg Berlin, Heidelberg 10.1007/978-3-540-74771-0
7. K.M. Woo, V.J. Chen, and P.X. Ma Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment J. Biomed. Mater. Res. A 67 2003 531 537 10.1002/jbm.a.10098
8. A. Macchetta, I.G. Turner, and C.R. Bowen Fabrication of HA/TCP scaffolds with a graded and porous structure using a camphene-based freeze-casting method Acta Biomater. 5 2009 1319 1327 10.1016/j.actbio.2008.11.009
9. W. Bonfield Designing porous scaffolds for tissue engineering Philos. Transact. A Math. Phys. Eng. Sci. 364 2006 227 232 10.1098/rsta.2005.1692
10. K. Rechendorff, M.B. Hovgaard, M. Foss, V.P. Zhdanov, and F. Besenbacher Enhancement of protein adsorption induced by surface roughness Langmuir 22 2006 10885 10888 10.1021/la0621923
11. J.Y. Martin, Z. Schwartz, T.W. Hummert, D.M. Schraub, J. Simpson, J. Lankford, and et al. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63) J. Biomed. Mater. Res. 29 1995 389 401 10.1002/jbm.820290314
12. H. Yuan, Z. Yang, Y. Li, X. Zhang, J.D. De Bruijn, and K. De Groot Osteoinduction by calcium phosphate biomaterials J. Mater. Sci. Mater. Med. 9 1998 723 726 (http://www.ncbi.nlm.nih.gov/pubmed/15348929 (accessed June 5, 2014))
13. J. Zhang, D. Barbieri, H. ten Hoopen, J.D. de Bruijn, C.A. van Blitterswijk, and H. Yuan Microporous calcium phosphate ceramics driving osteogenesis through surface architecture J. Biomed. Mater. Res. A 2014 10.1002/jbm.a.35272 (n/a-n/a)
14. A.M.C. Barradas, H. Yuan, C.A. van Blitterswijk, and P. Habibovic Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms Eur. Cell Mater. 21 2011 407 429 (discussion 429. http://www.ncbi.nlm.nih.gov/pubmed/21604242 (accessed June 20, 2014))
15. P. Habibovic, T.M. Sees, M.A. van den Doel, C.A. van Blitterswijk, and K. de Groot Osteoinduction by biomaterials - physicochemical and structural influences J. Biomed. Mater. Res. A 77 2006 747 762 10.1002/jbm.a.30712
16. F. Matassi, A. Botti, L. Sirleo, C. Carulli, and M. Innocenti Porous metal for orthopedics implants Clin. Cases Miner. Bone Metab. 10 2013 111 115 (http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3796997&tool=pmcentrez&rendertype=abstract (accessed October 15, 2015))
17. S. Bose, M. Roy, and A. Bandyopadhyay Recent advances in bone tissue engineering scaffolds Trends Biotechnol. 30 2012 546 554 10.1016/j.tibtech.2012.07.005
18. Tissue Engineering: Roles, Materials, and Applications 2008 Nova Publishers (http://books.google.com/books?id=Aozd7XvWD7MC&pgis=1 (accessed July 7, 2014))
19. C.M. Murphy, M.G. Haugh, and F.J. O'Brien The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering Biomaterials 31 2010 461 466 10.1016/j.biomaterials.2009.09.063
20. R.A. Perez, H.-W. Kim, and M.-P. Ginebra Polymeric additives to enhance the functional properties of calcium phosphate cements J. Tissue Eng. 3 2012 10.1177/2041731412439555 (2041731412439555)
21. P.X. Ma Scaffolds for tissue fabrication Mater. Today. 7 2004 30 40 10.1016/S1369-7021(04)00233-0
22. V.L. Tsang, and S.N. Bhatia Three-dimensional tissue fabrication Adv. Drug Deliv. Rev. 56 2004 1635 1647 10.1016/j.addr.2004.05.001
23. V. Karageorgiou, and D. Kaplan Porosity of 3D biomaterial scaffolds and osteogenesis Biomaterials 26 2005 5474 5491 10.1016/j.biomaterials.2005.02.002
24. F. Krauss Juillerat, U.T. Gonzenbach, P. Elser, A.R. Studart, and L.J. Gauckler Microstructural control of self-setting particle-stabilized ceramic foams J. Am. Ceram. Soc. 94 2011 77 83 10.1111/j.1551-2916.2010.04040.x
25. J.R. Jones, and L.L. Hench Effect of surfactant concentration and composition on the structure and properties of sol-gel-derived bioactive glass foam scaffolds for tissue engineering J. Mater. Sci. 38 2003 3783 3790 10.1023/A:1025988301542
26. Q. Lv, L. Nair, and C.T. Laurencin Fabrication, characterization, and in vitro evaluation of poly(lactic acid glycolic acid)/nano-hydroxyapatite composite microsphere-based scaffolds for bone tissue engineering in rotating bioreactors J. Biomed. Mater. Res. A 91A 2009 679 691 10.1002/jbm.a.32302
27. Q.Z. Chen, I.D. Thompson, and A.R. Boccaccini 45S5 Bioglass®-derived glass-ceramic scaffolds for bone tissue engineering Biomaterials 27 2006 2414 2425 10.1016/j.biomaterials.2005.11.025
28. R. Nazarov, H.-J. Jin, and D.L. Kaplan Porous 3-D scaffolds from regenerated silk fibroin Biomacromolecules 5 2004 718 726 10.1021/bm034327e
29. P. Gentile, M. Mattioli-Belmonte, V. Chiono, C. Ferretti, F. Baino, C. Tonda-Turo, and et al. Bioactive glass/polymer composite scaffolds mimicking bone tissue J. Biomed. Mater. Res. A 100A 2012 2654 2667 10.1002/jbm.a.34205
30. S. del Valle, N. Miño, F. Muñoz, A. González, J.A. Planell, and M.-P. Ginebra In vivo evaluation of an injectable macroporous calcium phosphate cement J. Mater. Sci. Mater. Med. 18 2007 353 361 10.1007/s10856-006-0700-y
31. P. Chen, J. Tao, S. Zhu, Y. Cai, Q. Mao, D. Yu, and et al. Radially oriented collagen scaffold with SDF-1 promotes osteochondral repair by facilitating cell homing Biomaterials 39 2015 114 123 10.1016/j.biomaterials.2014.10.049
32. W.J. Li, C.T. Laurencin, E.J. Caterson, R.S. Tuan, and F.K. Ko Electrospun nanofibrous structure: a novel scaffold for tissue engineering J. Biomed. Mater. Res. 60 2002 613 621 10.1002/jbm.10167
33. J.L. Simon, E.D. Rekow, V.P. Thompson, H. Beam, J.L. Ricci, and J.R. Parsons MicroCT analysis of hydroxyapatite bone repair scaffolds created via three-dimensional printing for evaluating the effects of scaffold architecture on bone ingrowth J. Biomed. Mater. Res. A 85A 2008 371 377 10.1002/jbm.a.31484
34. A. Salerno, E. Di Maio, S. Iannace, and P.A. Netti Tailoring the pore structure of PCL scaffolds for tissue engineering prepared via gas foaming of multi-phase blends J. Porous. Mater. 19 2011 181 188 10.1007/s10934-011-9458-9
35. B.-H. Yoon, Y.-H. Koh, C.-S. Park, and H.-E. Kim Generation of large pore channels for bone tissue engineering using camphene-based freeze casting J. Am. Ceram. Soc. 90 2007 1744 1752 10.1111/j.1551-2916.2007.01670.x
36. S.-M. Lien, L.-Y. Ko, and T.-J. Huang Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering Acta Biomater. 5 2009 670 679 10.1016/j.actbio.2008.09.020
37. P.X. Ma, and J.W. Choi Biodegradable polymer scaffolds with well-defined interconnected spherical pore network Tissue Eng. 7 2001 23 33 10.1089/107632701300003269
38. Q. Hou, D.W. Grijpma, and J. Feijen Preparation of interconnected highly porous polymeric structures by a replication and freeze-drying process J. Biomed. Mater. Res. B Appl. Biomater. 67 2003 732 740 10.1002/jbm.b.10066
39. J. Zhang, L. Wu, D. Jing, and J. Ding A comparative study of porous scaffolds with cubic and spherical macropores Polymer 46 2005 4979 4985 10.1016/j.polymer.2005.02.120
40. L.J. White, V. Hutter, H. Tai, S.M. Howdle, and K.M. Shakesheff The effect of processing variables on morphological and mechanical properties of supercritical CO2 foamed scaffolds for tissue engineering Acta Biomater. 8 2012 61 71 10.1016/j.actbio.2011.07.032
41. F. Baino, and C. Vitale-Brovarone Mechanical properties and reliability of glass-ceramic foam scaffolds for bone repair Mater. Lett. 118 2014 27 30 10.1016/j.matlet.2013.12.037
42. Q. Chen, F. Baino, S. Spriano, N.M. Pugno, and C. Vitale-Brovarone Modelling of the strength-porosity relationship in glass-ceramic foam scaffolds for bone repair J. Eur. Ceram. Soc. 34 2014 2663 2673 10.1016/j.jeurceramsoc.2013.11.041
43. A. Dejaco, V.S. Komlev, J. Jaroszewicz, W. Swieszkowski, and C. Hellmich Micro CT-based multiscale elasticity of double-porous (pre-cracked) hydroxyapatite granules for regenerative medicine J. Biomech. 45 2012 1068 1075 10.1016/j.jbiomech.2011.12.026
44. D. Taylor, J.G. Hazenberg, and T.C. Lee The cellular transducer in damage-stimulated bone remodelling: a theoretical investigation using fracture mechanics J. Theor. Biol. 225 2003 65 75 10.1016/S0022-5193(03)00222-4
45. J.-S. Lee, H. Do Cha, J.-H. Shim, J.W. Jung, J.Y. Kim, and D.-W. Cho Effect of pore architecture and stacking direction on mechanical properties of solid freeform fabrication-based scaffold for bone tissue engineering J. Biomed. Mater. Res. A 100 2012 1846 1853 10.1002/jbm.a.34149
46. T. Serra, J.A. Planell, and M. Navarro High-resolution PLA-based composite scaffolds via 3-D printing technology Acta Biomater. 9 2013 5521 5530 10.1016/j.actbio.2012.10.041
47. M. Yeo, C.G. Simon, and G. Kim Effects of offset values of solid freeform fabricated PCL-β-TCP scaffolds on mechanical properties and cellular activities in bone tissue regeneration J. Mater. Chem. 22 2012 21636 10.1039/c2jm31165h
48. C. Wu, Y. Luo, G. Cuniberti, Y. Xiao, and M. Gelinsky Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability Acta Biomater. 7 2011 2644 2650 10.1016/j.actbio.2011.03.009
49. K.-W. Lee, S. Wang, L. Lu, E. Jabbari, B.L. Currier, and M.J. Yaszemski Fabrication and characterization of poly(propylene fumarate) scaffolds with controlled pore structures using 3-dimensional printing and injection molding Tissue Eng. 12 2006 2801 2811 10.1089/ten.2006.12.2801
50. J.M. Sobral, S.G. Caridade, R.A. Sousa, J.F. Mano, and R.L. Reis Three-dimensional plotted scaffolds with controlled pore size gradients: effect of scaffold geometry on mechanical performance and cell seeding efficiency Acta Biomater. 7 2011 1009 1018 10.1016/j.actbio.2010.11.003
51. J. Wu, Q. Zhao, J. Sun, and Q. Zhou Preparation of poly(ethylene glycol) aligned porous cryogels using a unidirectional freezing technique Soft Matter 8 2012 3620 10.1039/c2sm07411g
52. A. Arora, A. Kothari, and D.S. Katti Pore orientation mediated control of mechanical behavior of scaffolds and its application in cartilage-mimetic scaffold design J. Mech. Behav. Biomed. Mater. 51 2015 169 183 10.1016/j.jmbbm.2015.06.033
53. S. Jia, L. Liu, W. Pan, G. Meng, C. Duan, L. Zhang, and et al. Oriented cartilage extracellular matrix-derived scaffold for cartilage tissue engineering J. Biosci. Bioeng. 113 2012 647 653 10.1016/j.jbiosc.2011.12.009
54. J.M. Cordell, M.L. Vogl, and A.J. Wagoner Johnson The influence of micropore size on the mechanical properties of bulk hydroxyapatite and hydroxyapatite scaffolds J. Mech. Behav. Biomed. Mater. 2 2009 560 570 10.1016/j.jmbbm.2009.01.009
55. S. Fiorilli, F. Baino, V. Cauda, M. Crepaldi, C. Vitale-Brovarone, D. Demarchi, and et al. Electrophoretic deposition of mesoporous bioactive glass on glass-ceramic foam scaffolds for bone tissue engineering J. Mater. Sci. Mater. Med. 26 2015 21 10.1007/s10856-014-5346-6
56. C. Vitale-Brovarone, F. Baino, M. Miola, R. Mortera, B. Onida, and E. Verné Glass-ceramic scaffolds containing silica mesophases for bone grafting and drug delivery J. Mater. Sci. Mater. Med. 20 2009 809 820 10.1007/s10856-008-3635-7
57. J.W. Lee, G. Ahn, J.Y. Kim, and D.-W. Cho Evaluating cell proliferation based on internal pore size and 3D scaffold architecture fabricated using solid freeform fabrication technology J. Mater. Sci. Mater. Med. 21 2010 3195 3205 10.1007/s10856-010-4173-7
58. T.C. Lim, K.S. Chian, and K.F. Leong Cryogenic prototyping of chitosan scaffolds with controlled micro and macro architecture and their effect on in vivo neo-vascularization and cellular infiltration J. Biomed. Mater. Res. A 94 2010 1303 1311 10.1002/jbm.a.32747
59. 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 10.1016/j.biomaterials.2004.02.052
60. T. Mygind, M. Stiehler, A. Baatrup, H. Li, X. Zou, A. Flyvbjerg, and et al. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds Biomaterials 28 2007 1036 1047 10.1016/j.biomaterials.2006.10.003
61. G.-I. Im, J.-Y. Ko, and J.H. Lee Chondrogenesis of adipose stem cells in a porous polymer scaffold: influence of the pore size Cell Transplant. 21 2012 2397 2405 10.3727/096368912X638865
62. S. Yamane, N. Iwasaki, Y. Kasahara, K. Harada, T. Majima, K. Monde, and et al. Effect of pore size on in vitro cartilage formation using chitosan-based hyaluronic acid hybrid polymer fibers J. Biomed. Mater. Res. A 81 2007 586 593 10.1002/jbm.a.31095
63. D.J. Griffon, M.R. Sedighi, D.V. Schaeffer, J.A. Eurell, and A.L. Johnson Chitosan scaffolds: interconnective pore size and cartilage engineering Acta Biomater. 2 2006 313 320 10.1016/j.actbio.2005.12.007
64. C.G. Jeong, and S.J. Hollister Mechanical and biochemical assessments of three-dimensional poly(1,8-octanediol-co-citrate) scaffold pore shape and permeability effects on in vitro chondrogenesis using primary chondrocytes Tissue Eng. A 16 2010 3759 3768 10.1089/ten.TEA.2010.0103
65. S.H. Oh, I.K. Park, J.M. Kim, and J.H. Lee In vitro and in vivo characteristics of PCL scaffolds with pore size gradient fabricated by a centrifugation method Biomaterials 28 2007 1664 1671 10.1016/j.biomaterials.2006.11.024
66. S.H. Oh, T.H. Kim, G. Il Im, and J.H. Lee Investigation of pore size effect on chondrogenic differentiation of adipose stem cells using a pore size gradient scaffold Biomacromolecules 11 2010 1948 1955 10.1021/bm100199m
67. S. Park, G. Kim, Y.C. Jeon, Y. Koh, and W. Kim 3D polycaprolactone scaffolds with controlled pore structure using a rapid prototyping system J. Mater. Sci. Mater. Med. 20 2009 229 234 10.1007/s10856-008-3573-4
68. J.X. Lu, B. Flautre, K. Anselme, P. Hardouin, A. Gallur, M. Descamps, and et al. Role of interconnections in porous bioceramics on bone recolonization in vitro and in vivo J. Mater. Sci. Mater. Med. 10 1999 111 120 (http://www.ncbi.nlm.nih.gov/pubmed/15347932 (accessed June 20, 2014))
69. F.P.W. Melchels, A.M.C. Barradas, C.A. van Blitterswijk, J. de Boer, J. Feijen, and D.W. Grijpma Effects of the architecture of tissue engineering scaffolds on cell seeding and culturing Acta Biomater. 6 2010 4208 4217 10.1016/j.actbio.2010.06.012
70. J.M. Kemppainen, and S.J. Hollister Differential effects of designed scaffold permeability on chondrogenesis by chondrocytes and bone marrow stromal cells Biomaterials 31 2010 279 287 10.1016/j.biomaterials.2009.09.041
71. A. Phadke, Y. Hwang, S.H. Kim, S.H. Kim, T. Yamaguchi, K. Masuda, and et al. Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells Eur. Cell Mater. 25 2013 114 128 (discussion 128-9. http://www.ncbi.nlm.nih.gov/pubmed/23329467 (accessed June 20, 2014))
72. Q. Fu, M.N. Rahaman, B.S. Bal, and R.F. Brown In vitro cellular response to hydroxyapatite scaffolds with oriented pore architectures Mater. Sci. Eng. C 29 2009 2147 2153 10.1016/j.msec.2009.04.016
73. S.R. Caliari, and B.A.C. Harley The effect of anisotropic collagen-GAG scaffolds and growth factor supplementation on tendon cell recruitment, alignment, and metabolic activity Biomaterials 32 2011 5330 5340 10.1016/j.biomaterials.2011.04.021
74. P. Yilgor, R.A. Sousa, R.L. Reis, N. Hasirci, and V. Hasirci 3D plotted PCL scaffolds for stem cell based bone tissue engineering Macromol. Symp. 269 2008 92 99 10.1002/masy.200850911
75. F. O'Brien Influence of freezing rate on pore structure in freeze-dried collagen-GAG scaffolds Biomaterials 25 2004 1077 1086 10.1016/S0142-9612(03)00630-6
76. A. Salerno, D. Guarnieri, M. Iannone, S. Zeppetelli, and P.A. Netti Effect of micro- and macroporosity of bone tissue three-dimensional-poly(epsilon-caprolactone) scaffold on human mesenchymal stem cells invasion, proliferation, and differentiation in vitro Tissue Eng. A 16 2010 2661 2673 10.1089/ten.tea.2009.0494
77. S.-W. Choi, Y. Zhang, and Y. Xia Three-dimensional scaffolds for tissue engineering: the importance of uniformity in pore size and structure Langmuir 26 2010 19001 19006 10.1021/la104206h
78. H.A. Declercq, T. Desmet, P. Dubruel, and M.J. Cornelissen The role of scaffold architecture and composition on the bone formation by adipose-derived stem cells Tissue Eng. A 20 2014 434 444 10.1089/ten.TEA.2013.0179
79. T.B.F. Woodfield, C.A. Van Blitterswijk, J. De Wijn, T.J. Sims, A.P. Hollander, and J. Riesle Polymer scaffolds fabricated with pore-size gradients as a model for studying the zonal organization within tissue-engineered cartilage constructs Tissue Eng. 11 2005 1297 1311 10.1089/ten.2005.11.1297
80. A. Penk, Y. Förster, H.A. Scheidt, A. Nimptsch, M.C. Hacker, M. Schulz-Siegmund, and et al. The pore size of PLGA bone implants determines the de novo formation of bone tissue in tibial head defects in rats Magn. Reson. Med. 70 2013 925 935 10.1002/mrm.24541
81. 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. A 85 2008 777 786 10.1002/jbm.a.31559
82. P. Duan, Z. Pan, L. Cao, Y. He, H. Wang, Z. Qu, and et al. The effects of pore size in bilayered poly(lactide-co-glycolide) scaffolds on restoring osteochondral defects in rabbits J. Biomed. Mater. Res. A 2013 10.1002/jbm.a.34683
83. M. Belicchi, R. Cancedda, A. Cedola, F. Fiori, M. Gavina, A. Giuliani, and et al. Some applications of nanotechnologies in stem cells research Mater. Sci. Eng. B 165 2009 139 147 10.1016/j.mseb.2009.09.018
84. J.R. Jones, G. Poologasundarampillai, R.C. Atwood, D. Bernard, and P.D. Lee Non-destructive quantitative 3D analysis for the optimisation of tissue scaffolds Biomaterials 28 2007 1404 1413 10.1016/j.biomaterials.2006.11.014
85. C. Renghini, A. Giuliani, S. Mazzoni, F. Brun, E. Larsson, F. Baino, and et al. Microstructural characterization and in vitro bioactivity of porous glass-ceramic scaffolds for bone regeneration by synchrotron radiation X-ray microtomography J. Eur. Ceram. Soc. 33 2013 1553 1565 10.1016/j.jeurceramsoc.2012.10.016
86. S. Kujala, J. Ryhänen, A. Danilov, and J. Tuukkanen Effect of porosity on the osteointegration and bone ingrowth of a weight-bearing nickel-titanium bone graft substitute Biomaterials 24 2003 4691 4697 (http://www.ncbi.nlm.nih.gov/pubmed/12951012 (accessed June 20, 2014))
87. O. Gauthier, J.M. Bouler, E. Aguado, P. Pilet, and G. Daculsi Macroporous biphasic calcium phosphate ceramics: influence of macropore diameter and macroporosity percentage on bone ingrowth Biomaterials. 19 1998 133 139 (http://www.ncbi.nlm.nih.gov/pubmed/9678860 (accessed June 5, 2014))
88. J.L. Simon, S. Michna, J.A. Lewis, E.D. Rekow, V.P. Thompson, J.E. Smay, and et al. In vivo bone response to 3D periodic hydroxyapatite scaffolds assembled by direct ink writing J. Biomed. Mater. Res. A 83 2007 747 758 10.1002/jbm.a.31329
89. A.I. Itälä, H.O. Ylänen, C. Ekholm, K.H. Karlsson, and H.T. Aro Pore diameter of more than 100 microm is not requisite for bone ingrowth in rabbits J. Biomed. Mater. Res. 58 2001 679 683 (http://www.ncbi.nlm.nih.gov/pubmed/11745521 (accessed June 20, 2014))
90. M.-C. von Doernberg, B. von Rechenberg, M. Bohner, S. Grünenfelder, G.H. van Lenthe, R. Müller, and et al. In vivo behavior of calcium phosphate scaffolds with four different pore sizes Biomaterials 27 2006 5186 5198 10.1016/j.biomaterials.2006.05.051
91. S.M.M. Roosa, J.M. Kemppainen, E.N. Moffitt, P.H. Krebsbach, and S.J. Hollister The pore size of polycaprolactone scaffolds has limited influence on bone regeneration in an in vivo model J. Biomed. Mater. Res. A 92 2010 359 368 10.1002/jbm.a.32381
92. R.A. Perez, S.-J. Seo, J.-E. Won, E.-J. Lee, J.-H. Jang, J.C. Knowles, and et al. Therapeutically relevant aspects in bone repair and regeneration Mater. Today 2015 10.1016/j.mattod.2015.06.011
93. R.A. Perez, J.-H. Kim, J.O. Buitrago, I.B. Wall, and H.-W. Kim Novel therapeutic core-shell hydrogel scaffolds with sequential delivery of cobalt and bone morphogenetic protein-2 for synergistic bone regeneration Acta Biomater. 23 2015 295 308 10.1016/j.actbio.2015.06.002
94. A. Hoppe, N.S. Güldal, and A.R. Boccaccini A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics Biomaterials 32 2011 2757 2774 10.1016/j.biomaterials.2011.01.004
95. V. Mourino, J.P. Cattalini, and Boccaccini Metallic ions as therapeutic agents in tissue engineering scaffolds: an overview of their biological applications and strategies for new developments J. R. Soc. Interface 9 2012 401 419 10.1098/rsif.2011.0611
96. B. Feng, Z. Jinkang, W. Zhen, L. Jianxi, C. Jiang, L. Jian, and et al. The effect of pore size on tissue ingrowth and neovascularization in porous bioceramics of controlled architecture in vivo Biomed. Mater. 6 2011 015007 10.1088/1748-6041/6/1/015007
97. A.G. Mitsak, J.M. Kemppainen, M.T. Harris, and S.J. Hollister Effect of polycaprolactone scaffold permeability on bone regeneration in vivo Tissue Eng. A 17 2011 1831 1839 10.1089/ten.TEA.2010.0560
98. J.P. Li, P. Habibovic, M. van den Doel, C.E. Wilson, J.R. de Wijn, C.A. van Blitterswijk, and et al. Bone ingrowth in porous titanium implants produced by 3D fiber deposition Biomaterials 28 2007 2810 2820 10.1016/j.biomaterials.2007.02.020
99. P.J. Emans, E.J.P. Jansen, D. van Iersel, T.J.M. Welting, T.B.F. Woodfield, S.K. Bulstra, and et al. Tissue-engineered constructs: the effect of scaffold architecture in osteochondral repair J. Tissue Eng. Regen. Med. 7 2013 751 756 10.1002/term.1477
100. K.M. Brouwer, W.F. Daamen, N. van Lochem, D. Reijnen, R.M.H. Wijnen, and T.H. van Kuppevelt Construction and in vivo evaluation of a dual layered collagenous scaffold with a radial pore structure for repair of the diaphragm Acta Biomater. 9 2013 6844 6851 10.1016/j.actbio.2013.03.003
101. E.L.W. de Mulder, G. Hannink, N. Verdonschot, and P. Buma Effect of polyurethane scaffold architecture on ingrowth speed and collagen orientation in a subcutaneous rat pocket model Biomed. Mater. 8 2013 025004 10.1088/1748-6041/8/2/025004
102. T.M.G. Chu, D.G. Orton, S.J. Hollister, S.E. Feinberg, and J.W. Halloran Mechanical and in vivo performance of hydroxyapatite implants with controlled architectures Biomaterials 23 2002 1283 1293 http://www.ncbi.nlm.nih.gov/pubmed/11808536 (accessed September 3, 2015)
103. E.L.W. de Mulder, G. Hannink, T.H. van Kuppevelt, W.F. Daamen, and P. Buma Similar hyaline-like cartilage repair of osteochondral defects in rabbits using isotropic and anisotropic collagen scaffolds Tissue Eng. A 20 2014 635 645 10.1089/ten.TEA.2013.0083
104. E.S. Sanzana, M. Navarro, M.-P. Ginebra, J.A. Planell, A.C. Ojeda, and H.A. Montecinos Role of porosity and pore architecture in the in vivo bone regeneration capacity of biodegradable glass scaffolds J. Biomed. Mater. Res. A 102 2014 1767 1773 10.1002/jbm.a.34845
105. X. Liu, M.N. Rahaman, and Q. Fu Bone regeneration in strong porous bioactive glass (13-93) scaffolds with an oriented microstructure implanted in rat calvarial defects Acta Biomater. 9 2013 4889 4898 10.1016/j.actbio.2012.08.029
106. K.A. Hing Bioceramic bone graft substitutes: Influence of porosity and chemistry Int. J. Appl. Ceram. Technol. 2 2005 184 199 10.1111/j.1744-7402.2005.02020.x
107. D.D. Deligianni, N.D. Katsala, P.G. Koutsoukos, and Y.F. Missirlis Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength Biomaterials 22 2001 87 96
108. X.D. Zhu, H.J. Zhang, H.S. Fan, W. Li, and X.D. Zhang Effect of phase composition and microstructure of calcium phosphate ceramic particles on protein adsorption Acta Biomater. 6 2010 1536 1541 10.1016/j.actbio.2009.10.032
109. A.L. Rosa, M.M. Beloti, and R. van Noort Osteoblastic differentiation of cultured rat bone marrow cells on hydroxyapatite with different surface topography Dent. Mater. 19 2003 768 772 10.1016/S0109-5641(03)00024-1
110. M. Espanol, R.A. Perez, E.B. Montufar, C. Marichal, A. Sacco, and M.P. Ginebra Intrinsic porosity of calcium phosphate cements and its significance for drug delivery and tissue engineering applications Acta Biomater. 5 2009 2752 2762 10.1016/j.actbio.2009.03.011
111. Y. Wang, E. Bella, C.S.D. Lee, C. Migliaresi, L. Pelcastre, Z. Schwartz, and et al. The synergistic effects of 3-D porous silk fibroin matrix scaffold properties and hydrodynamic environment in cartilage tissue regeneration Biomaterials 31 2010 4672 4681 10.1016/j.biomaterials.2010.02.006
112. A. Mittal, P. Negi, K. Garkhal, S. Verma, and N. Kumar Integration of porosity and bio-functionalization to form a 3D scaffold: cell culture studies and in vitro degradation Biomed. Mater. 5 2010 045001 10.1088/1748-6041/5/4/045001
113. S. Yoshida, K. Hagiwara, T. Hasebe, and a. Hotta Surface modification of polymers by plasma treatments for the enhancement of biocompatibility and controlled drug release Surf. Coat. Technol. 233 2013 99 107 10.1016/j.surfcoat.2013.02.042
114. N.R. Washburn, K.M. Yamada, C.G. Simon, S.B. Kennedy, and E.J. Amis High-throughput investigation of osteoblast response to polymer crystallinity: influence of nanometer-scale roughness on proliferation Biomaterials 25 2004 1215 1224 10.1016/j.biomaterials.2003.08.043
115. N.E. Vrana, A. Dupret, C. Coraux, D. Vautier, C. Debry, and P. Lavalle Hybrid titanium/biodegradable polymer implants with an hierarchical pore structure as a means to control selective cell movement PLoS ONE 6 2011 e20480 10.1371/journal.pone.0020480
116. U. Ripamonti Bone induction in nonhuman primates. An experimental study on the baboon Clin. Orthop. Relat. Res. 284-94 1991 http://www.ncbi.nlm.nih.gov/pubmed/1864050 (accessed June 20, 2014)
117. C. Klein, K. de Groot, W. Chen, Y. Li, and X. Zhang Osseous substance formation induced in porous calcium phosphate ceramics in soft tissues Biomaterials 15 1994 31 34 http://www.ncbi.nlm.nih.gov/pubmed/8161654 (accessed June 20, 2014)
118. H. Yamasaki, and H. Sakai Osteogenic response to porous hydroxyapatite ceramics under the skin of dogs Biomaterials 13 1992 308 312 http://www.ncbi.nlm.nih.gov/pubmed/1318086 (accessed June 20, 2014)
119. M.P. Lutolf, and J.a. Hubbell Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering Nat. Biotechnol. 23 2005 47 55 10.1038/nbt1055
120. a. Howe, a.E. Aplin, S.K. Alahari, and R.L. Juliano Integrin signaling and cell growth control Curr. Opin. Cell Biol. 10 1998 220 231
121. F.G. Giancotti Integrin signaling Science 285 80- 1999 1028 1033 10.1126/science.285.5430.1028
122. G. Wei, and P.X. Ma Partially nanofibrous architecture of 3D tissue engineering scaffolds Biomaterials 30 2009 6426 6434 10.1016/j.biomaterials.2009.08.012
123. J. Wang, H. Zhang, X. Zhu, H. Fan, Y. Fan, and X. Zhang Dynamic competitive adsorption of bone-related proteins on calcium phosphate ceramic particles with different phase composition and microstructure J. Biomed. Mater. Res. B Appl. Biomater. 101 2013 1069 1077 10.1002/jbm.b.32917
124. R.A. Perez, S. Del Valle, G. Altankov, and M.-P. Ginebra Porous hydroxyapatite and gelatin/hydroxyapatite microspheres obtained by calcium phosphate cement emulsion J. Biomed. Mater. Res. B Appl. Biomater. 97 2011 156 166 10.1002/jbm.b.31798
125. R.A. Perez, G. Altankov, E. Jorge-Herrero, and M.P. Ginebra Micro- and nanostructured hydroxyapatite-collagen microcarriers for bone tissue-engineering applications J. Tissue Eng. Regen. Med. 7 2013 353 361 10.1002/term.530
126. R.A. Perez, T.-H. Kim, M. Kim, J.-H. Jang, M.-P. Ginebra, and H.-W. Kim Calcium phosphate cements loaded with basic fibroblast growth factor: delivery and in vitro cell response J. Biomed. Mater. Res. A 101 2013 923 931 10.1002/jbm.a.34390
127. M. Espanol, I. Casals, S. Lamtahri, M.-T. Valderas, and M.-P. Ginebra Assessment of protein entrapment in hydroxyapatite scaffolds by size exclusion chromatography Biointerphases 7 2012 37 10.1007/s13758-012-0037-7
128. W. Cao, and L.L. Hench Bioactive materials Ceram. Int. 22 1996 493 507 10.1016/0272-8842(95)00126-3
129. J. De Groot Carriers that concentrate native bone morphogenetic protein in vivo Tissue Eng. 4 1998 337 341
130. P. Habibovic, H. Yuan, C.M. van der Valk, G. Meijer, C.A. van Blitterswijk, and K. de Groot 3D microenvironment as essential element for osteoinduction by biomaterials Biomaterials 26 2005 3565 3575 10.1016/j.biomaterials.2004.09.056
131. R.Z. LeGeros Calcium phosphate-based osteoinductive materials Chem. Rev. 108 2008 4742 4753 10.1021/cr800427g
132. M.S. Lord, M. Foss, and F. Besenbacher Influence of nanoscale surface topography on protein adsorption and cellular response Nano Today 5 2010 66 78 10.1016/j.nantod.2010.01.001
133. C. Dai, H. Guo, J. Lu, J. Shi, J. Wei, and C. Liu Osteogenic evaluation of calcium/magnesium-doped mesoporous silica scaffold with incorporation of rhBMP-2 by synchrotron radiation-based μCT Biomaterials 32 2011 8506 8517 10.1016/j.biomaterials.2011.07.090
134. C. Wu, W. Fan, J. Chang, and Y. Xiao Mesoporous bioactive glass scaffolds for efficient delivery of vascular endothelial growth factor J. Biomater. Appl. 28 2013 367 374 10.1177/0885328212453635
135. Y.F. Zhao, S.C.J. Loo, Y.Z. Chen, F.Y.C. Boey, and J. Ma In situ SAXRD study of sol-gel induced well-ordered mesoporous bioglasses for drug delivery J. Biomed. Mater. Res. A 85 2008 1032 1042 10.1002/jbm.a.31545
136. J.G. Dellinger, J.A.C. Eurell, and R.D. Jamison Bone response to 3D periodic hydroxyapatite scaffolds with and without tailored microporosity to deliver bone morphogenetic protein 2 J. Biomed. Mater. Res. Part A 76A 2006 366 376 10.1002/jbm.a.30523
137. J.R. Woodard, A.J. Hilldore, S.K. Lan, C.J. Park, A.W. Morgan, J.A.C. Eurell, and et al. The mechanical properties and osteoconductivity of hydroxyapatite bone scaffolds with multi-scale porosity Biomaterials 28 2007 45 54 10.1016/j.biomaterials.2006.08.021
138. B. Dorj, J.-E. Won, O. Purevdorj, K.D. Patel, J.-H. Kim, E.-J. Lee, and et al. A novel therapeutic design of microporous-structured biopolymer scaffolds for drug loading and delivery Acta Biomater. 10 2014 1238 1250 10.1016/j.actbio.2013.11.002
139. R.A. Perez, A. El-Fiqi, J.-H. Park, T.-H. Kim, J.-H. Kim, and H.-W. Kim Therapeutic bioactive microcarriers: co-delivery of growth factors and stem cells for bone tissue engineering Acta Biomater. 10 2014 520 530 10.1016/j.actbio.2013.09.042
140. S. Radin, T. Chen, and P. Ducheyne The controlled release of drugs from emulsified, sol gel processed silica microspheres Biomaterials 30 2009 850 858 10.1016/j.biomaterials.2008.09.066
141. S. Kwon, R.K. Singh, R.A. Perez, E.A. Abou Neel, H.-W. Kim, and W. Chrzanowski Silica-based mesoporous nanoparticles for controlled drug delivery J. Tissue Eng. 4 2013 10.1177/2041731413503357 (2041731413503357)
142. R.A. Perez, and M.-P. Ginebra Injectable collagen/α-tricalcium phosphate cement: collagen-mineral phase interactions and cell response J. Mater. Sci. Mater. Med. 2012 10.1007/s10856-012-4799-8
143. R.A. Perez, and H.-W. Kim Core-shell designed scaffolds of alginate/alpha-tricalcium phosphate for the loading and delivery of biological proteins J. Biomed. Mater. Res. A 101 2013 1103 1112 10.1002/jbm.a.34406
144. D. Pastorino, C. Canal, and M.-P. Ginebra Drug delivery from injectable calcium phosphate foams by tailoring the macroporosity-drug interaction Acta Biomater. 12 2015 250 259 10.1016/j.actbio.2014.10.031
145. M.-P.P. Ginebra, C. Canal, M. Espanol, D. Pastorino, and E.B. Montufar Calcium phosphate cements as drug delivery materials Adv. Drug Deliv. Rev. 64 2012 1090 1110 10.1016/j.addr.2012.01.008
146. M.P. Ginebra, M. Espanol, E.B. Montufar, R.A. Perez, and G. Mestres New processing approaches in calcium phosphate cements and their applications in regenerative medicine Acta Biomater. 6 2010 2863 2873 10.1016/j.actbio.2010.01.036
147. S.J. Lee, J.S. Choi, K.S. Park, G. Khang, Y.M. Lee, and H.B. Lee Response of MG63 osteoblast-like cells onto polycarbonate membrane surfaces with different micropore sizes Biomaterials 25 2004 4699 4707 10.1016/j.biomaterials.2003.11.034
148. Q. Zhang, Y. Jiang, Y. Zhang, Z. Ye, W. Tan, and M. Lang Effect of porosity on long-term degradation of poly (ε-caprolactone) scaffolds and their cellular response Polym. Degrad. Stab. 98 2013 209 218 10.1016/j.polymdegradstab.2012.10.008
149. Y. Takahashi, and Y. Tabata Effect of the fiber diameter and porosity of non-woven PET fabrics on the osteogenic differentiation of mesenchymal stem cells J. Biomater. Sci. Polym. Ed. 15 2004 41 57 http://www.ncbi.nlm.nih.gov/pubmed/15027842 (accessed June 20, 2014)
150. J. Rnjak-Kovacina, S.G. Wise, Z. Li, P.K.M. Maitz, C.J. Young, Y. Wang, and et al. Tailoring the porosity and pore size of electrospun synthetic human elastin scaffolds for dermal tissue engineering Biomaterials 32 2011 6729 6736 10.1016/j.biomaterials.2011.05.065
151. 2 films on Ti surfaces for bone-tissue implants J. Biomed. Mater. Res. 57 2001 588 596 http://www.ncbi.nlm.nih.gov/pubmed/11553890 (accessed June 20, 2014)
152. J. Isaac, J.-C. Hornez, D. Jian, M. Descamps, P. Hardouin, and D. Magne Beta-TCP microporosity decreases the viability and osteoblast differentiation of human bone marrow stromal cells J. Biomed. Mater. Res. A 86 2008 386 393 10.1002/jbm.a.31644
153. P. Kasten, I. Beyen, P. Niemeyer, R. Luginbühl, M. Bohner, and W. Richter Porosity and pore size of beta-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: an in vitro and in vivo study Acta Biomater. 4 2008 1904 1915 10.1016/j.actbio.2008.05.017
154. Y. Wan, Y. Wang, Z. Liu, X. Qu, B. Han, J. Bei, and et al. Adhesion and proliferation of OCT-1 osteoblast-like cells on micro- and nano-scale topography structured poly(L-lactide) Biomaterials 26 2005 4453 4459 10.1016/j.biomaterials.2004.11.016
155. K. Anselme, M. Bigerelle, B. Noel, E. Dufresne, D. Judas, a. Iost, and et al. Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses J. Biomed. Mater. Res. 49 2000 155 166 10.1002/(SICI)1097-4636(200002)49:2<155::AID-JBM2>3.0.CO;2-J
156. K. Anselme, P. Linez, M. Bigerelle, D. Le Maguer, A. Le Maguer, P. Hardouin, and et al. The relative influence of the topography and chemistry of TiAl6V4 surfaces on osteoblastic cell behaviour Biomaterials 21 2000 1567 1577
157. J. Lincks, B.D. Boyan, C.R. Blanchard, C.H. Lohmann, Y. Liu, D.L. Cochran, and et al. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition Biomater. Silver Jubil. Compend. 19 2006 147 160 10.1016/B978-008045154-1.50019-8
158. R.A. Gittens, T. McLachlan, R. Olivares-Navarrete, Y. Cai, S. Berner, R. Tannenbaum, and et al. The effects of combined micron-/submicron-scale surface roughness and nanoscale features on cell proliferation and differentiation Biomaterials 32 2011 3395 3403 10.1016/j.biomaterials.2011.01.029
159. G. Zhao, A.L. Raines, M. Wieland, Z. Schwartz, and B.D. Boyan Requirement for both micron- and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography Biomaterials 28 2007 2821 2829 10.1016/j.biomaterials.2007.02.024
160. X. Zhu, J. Chen, L. Scheideler, R. Reichl, and J. Geis-Gerstorfer Effects of topography and composition of titanium surface oxides on osteoblast responses Biomaterials 25 2004 4087 4103 10.1016/j.biomaterials.2003.11.011
161. R. Ikeda, H. Fujioka, I. Nagura, T. Kokubu, N. Toyokawa, A. Inui, and et al. The effect of porosity and mechanical property of a synthetic polymer scaffold on repair of osteochondral defects Int. Orthop. 33 2009 821 828 10.1007/s00264-008-0532-0
162. K.A. Hing, B. Annaz, S. Saeed, P.A. Revell, and T. Buckland Microporosity enhances bioactivity of synthetic bone graft substitutes J. Mater. Sci. Mater. Med. 16 2005 467 475 10.1007/s10856-005-6988-1
163. B.J. Story, W.R. Wagner, D.M. Gaisser, S.D. Cook, and A.M. Rust-Dawicki In vivo performance of a modified CSTi dental implant coating Int. J. Oral Maxillofac. Implants 13 1998 749 757 (http://www.ncbi.nlm.nih.gov/pubmed/9857585 (accessed June 20, 2014))
164. C. Knabe, C. Koch, A. Rack, and M. Stiller Effect of beta-tricalcium phosphate particles with varying porosity on osteogenesis after sinus floor augmentation in humans Biomaterials 29 2008 2249 2258 10.1016/j.biomaterials.2008.01.026