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Frontiers of Materials Science

ISSN 2095-025X

ISSN 2095-0268(Online)

CN 11-5985/TB

Postal Subscription Code 80-974

2018 Impact Factor: 1.701

Front. Mater. Sci.    2021, Vol. 15 Issue (3) : 352-373    https://doi.org/10.1007/s11706-021-0558-4
REVIEW ARTICLE
Porosity parameters in biomaterial science: Definition, impact, and challenges in tissue engineering
Mehdi EBRAHIMI()
Biomedical and Tissue Engineering, Prince Philip Dental Hospital, The University of Hong Kong, Hong Kong, China
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Abstract

Porosity parameters are one of the structural properties of the extracellular microenvironment that have been shown to have a great impact on the cellular phenotype and various biological activities such as diffusion of fluid, initial protein adsorption, permeability, cell penetration and migration, ECM deposition, angiogenesis, and rate and pattern of new tissue formation. The heterogeneity of the study protocols and research methodologies do not allow reliable meta-analysis for definite findings. As such, despite the huge available literature, no generally accepted consensus is defined for the porosity requirements of specific tissue engineering applications. However, based on the biomimetic approach, the biological substitutes should replicate the 3D local microenvironment of the recipient site with matching porosity parameters to best support local cells during tissue regeneration. Ideally, the porosity of biomaterials should mimic the porosity of the substituting natural tissue and match the clinical requirements. Careful analysis of the impact of architectures (i.e., porosity) on biophysical, biochemical, and biological behaviors will support designing smart biomaterials with customized architectural and functional properties that are patient and defect site-specific.

Keywords porosity      pore size      pore geometry      topography      tissue engineering     
Corresponding Author(s): Mehdi EBRAHIMI   
Online First Date: 13 July 2021    Issue Date: 24 September 2021
 Cite this article:   
Mehdi EBRAHIMI. Porosity parameters in biomaterial science: Definition, impact, and challenges in tissue engineering[J]. Front. Mater. Sci., 2021, 15(3): 352-373.
 URL:  
https://academic.hep.com.cn/foms/EN/10.1007/s11706-021-0558-4
https://academic.hep.com.cn/foms/EN/Y2021/V15/I3/352
Fig.1  Stem cell microenvironment and biophysical and biochemical signals that contribute to the regulation of stem cell behaviors. Orange mesh: ECM; Green circle: oxygen molecules; Red triangle: signaling factors from a blood vessel (humoral factors, i.e., hormones); Blue triangle: signaling factors excreted by cells (autocrine and paracrine factors, i.e., growth and differentiation factors); Black lines: cell–cell contact. Cell–ECM interaction also impacts cell behavior. The topography of the ECM substrate can induce differentiation of MSC through the mechanotransduction pathway. This is modulated by integrin activated focal adhesion. This results in alteration of cell morphology due to the contractility of actomyosin fibers that produce cytoskeleton changes. Reproduced and re-formatted with permission from Ref. [3].
Parameter Definition
Open pore Connected pores like tunnels that are accessible by gas, liquid, and particulate suspensions.
Close pore Isolated pores with no connection to the scaffold surface and not contributing to the cell microenvironment but affecting the mechanical properties of the scaffold.
Close porosity Close pore volume/bulk volume.
Open porosity Open pore volume/bulk volume.
Total porosity Total pore volume/bulk volume.
Pore interconnectivity Pore channel that connects different pores and determines the permeability by controlling fluid circulation in the scaffold.
Pore geometry Architectural configuration of pore including its morphology and pore wall.
Pore dimension The mean pore size or diameter.
Pore distribution The spatial arrangement of pore within the scaffold involving pore orientation or alignment.
Pore throat Entrance or the first part of the pore that may act as pore interconnection.
Pore stomach Belly or second part of the pore.
Tab.1  Porosity parameters and the related definitions
Fig.2  Schematic illustration of the pore internal structure demonstrating related porosity parameters in different sections. A — closed pore; B — open pore; C — pore interconnection.
Technique Using Advantages Limitations
Porogen leaching Particulates, fibers, meshes, salt (NaCl), sugar, paraffin, gelatin, ice crystals The amount and size of the porogen can modify the pore size and porosity; a minimal amount of polymer is required. Poor reproducibility; residual porogens; poor pore interconnectivity.
Gas forming Gas generation (i.e., CO2), surface active agents (i.e., tween) No need for leaching step; reduce overall fabrication time. Low initial strength; poor reproducibility; risk of embolism; difficult control of pore connectivity and pore sizes.
Emulsion Oil-water mixtures Allow modification of pore size and percentage. May require a cleaning step; risk of embolism.
Freeze-drying Water freezing+ sublimation Porosity and pore size can be modified by controlling the porosity parameters, polymer/water ratio, and freezing temperature; no need for a further rinsing step. Energy and time-consuming; the parameters need to be controlled to increase scaffold homogeneity.
Templates Positive replica (polymeric foams), negative replica (indirect rapid prototyping) Porosity is determined by the porosity of the template. Very low strength; residuals from the firing step; crystal changes from the firing step; limited pore connectivity; problems with residual solvents.
3D printing Direct rapid prototyping Allows fabrication of a more complex 3D structure with a controlled internal structure. Micro-architecture limited by the particle’s size; applicable to a limited number of polymers due to high temperatures; ceramic scaffold requires sintering to improve on the brittle toughness.
Selective laser sintering Layer-by-layer fusion of a powder bed by laser beam Allows fabrication of complex scaffolds geometries; fast, cost-effective, and does not require the use of any organic solvents. High energy consumed; chance of degradation and decomposition of materials due to heat generation.
Electrospinning A potential difference between a polymeric solution and a collector Simple and cost-effective; generate high surface area and high porosity; possibility to control the diameter of each electrospun fiber. Involvement of toxic organic solvents during fabrication.
Encapsulation Cell entrapment during scaffold gellation Ability to provide immunoshielding for cells; possibility of fabricating injectable forms. The gelation process and encapsulating materials should be biocompatible; difficulty in control of diffusion coefficient to/from cells; lack of internal porous structure.
Tab.2  Manufacturing technique for the generation of pore within substrate biomaterials [8,25?26]
Pore size/µm Cell type Refs.
100–150 human fibroblast [8283]
100–200, 370–400 chondrogenic differentiation [62,8485]
200–450 osteogenic differentiation [44,69,8687]
75–750 (elongated pores) peripheral axon regeneration [88]
20–50 glial and axonal growth [89]
100 transplantation and differentiation of neural stem cells [90]
50–200 smooth muscle cells [91]
<38 microvascular epithelial cells [40]
Tab.3  pore size requirements according to the cell type [40,44,62,69,8291]
Fig.3  (a) The relationship between pore geometry and tissue growth rate. (b) A decrease in proliferation rate as a result of increased microporosity is correlated with a higher differentiation rate.
Fig.4  Classification of the pore system and distribution pattern.
1 N Trivedi, J Hollister-Lock, M D Lopez-Avalos, et al.. Increase in β-cell mass in transplanted porcine neonatal pancreatic cell clusters is due to proliferation of β-cells and differentiation of duct cells. Endocrinology, 2001, 142(5): 2115–2122
https://doi.org/10.1210/endo.142.5.8162 pmid: 11316779
2 Y A Mørch, I Donati, B L Strand, et al.. Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules, 2006, 7(5): 1471–1480
https://doi.org/10.1021/bm060010d pmid: 16677028
3 M Ebrahimi. Extracellular matrix: The ideal natural fibrous nanocomposite products. In: A M Inamuddin, A Asiri, Mohammad, eds. Applications of Nanocomposite Materials in Orthopedics. Elsevier, 2019, 263–286
https://doi.org/10.1016/B978-0-12-813740-6.00014-4
4 M S Steinberg. ECM: Its nature, origin and function in cell aggregation. Experimental Cell Research, 1963, 30(2): 257–279
https://doi.org/10.1016/0014-4827(63)90299-4 pmid: 13983727
5 N Mansouri, SamiraBagheri. The influence of topography on tissue engineering perspective. Materials Science and Engineering C, 2016, 61: 906–921
https://doi.org/10.1016/j.msec.2015.12.094 pmid: 26838922
6 A De Arcangelis, E Georges-Labouesse. Integrin and ECM functions: Roles in vertebrate development. Trends in Genetics, 2000, 16(9): 389–395
https://doi.org/10.1016/S0168-9525(00)02074-6 pmid: 10973067
7 G Chen, T Ushida, T Tateishi. Scaffold design for tissue engineering. Macromolecular Bioscience, 2002, 2(2): 67–77
https://doi.org/10.1002/1616-5195(20020201)2:2<67::AID-MABI67>3.0.CO;2-F
8 Q L Loh, C Choong. Three-dimensional scaffolds for tissue engineering applications: Role of porosity and pore size. Tissue Engineering Part B: Reviews, 2013, 19(6): 485–502
https://doi.org/10.1089/ten.teb.2012.0437 pmid: 23672709
9 M Ebrahimi, M G Botelho, S V Dorozhkin. Biphasic calcium phosphates bioceramics (HA/TCP): Concept, physicochemical properties and the impact of standardization of study protocols in biomaterials research. Materials Science and Engineering C, 2017, 71: 1293–1312
https://doi.org/10.1016/j.msec.2016.11.039 pmid: 27987685
10 H Naderi, M M Matin, A R Bahrami. Critical issues in tissue engineering: Biomaterials, cell sources, angiogenesis, and drug delivery systems. Journal of Biomaterials Applications, 2011, 26(4): 383–417
https://doi.org/10.1177/0885328211408946 pmid: 21926148
11 F M Chen, L A Wu, M Zhang, et al.. Homing of endogenous stem/progenitor cells for in situ tissue regeneration: Promises, strategies, and translational perspectives. Biomaterials, 2011, 32(12): 3189–3209
https://doi.org/10.1016/j.biomaterials.2010.12.032 pmid: 21300401
12 B K K Teo, S T Wong, C K Lim, et al.. Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase. ACS Nano, 2013, 7(6): 4785–4798
https://doi.org/10.1021/nn304966z pmid: 23672596
13 R A Pérez, J E Won, J C Knowles, et al.. Naturally and synthetic smart composite biomaterials for tissue regeneration. Advanced Drug Delivery Reviews, 2013, 65(4): 471–496
https://doi.org/10.1016/j.addr.2012.03.009 pmid: 22465488
14 D W Hutmacher. Scaffolds in tissue engineering bone and cartilage. Biomaterials, 2000, 21(24): 2529–2543
https://doi.org/10.1016/S0142-9612(00)00121-6 pmid: 11071603
15 C M Murphy, G P Duffy, A Schindeler, et al.. Effect of collagen–glycosaminoglycan scaffold pore size on matrix mineralization and cellular behavior in different cell types. Journal of Biomedical Materials Research Part A, 2016, 104(1): 291–304
https://doi.org/10.1002/jbm.a.35567 pmid: 26386362
16 M J Dalby, N Gadegaard, R O C Oreffo. Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nature Materials, 2014, 13(6): 558–569
https://doi.org/10.1038/nmat3980 pmid: 24845995
17 R A Marklein, J A Burdick. Controlling stem cell fate with material design. Advanced Materials, 2010, 22(2): 175–189
https://doi.org/10.1002/adma.200901055 pmid: 20217683
18 A J Keung, S Kumar, D V Schaffer. Presentation counts: Microenvironmental regulation of stem cells by biophysical and material cues. Annual Review of Cell and Developmental Biology, 2010, 26(1): 533–556
https://doi.org/10.1146/annurev-cellbio-100109-104042 pmid: 20590452
19 K A Hing, B Annaz, S Saeed, et al.. Microporosity enhances bioactivity of synthetic bone graft substitutes. Journal of Materials Science: Materials in Medicine, 2005, 16(5): 467–475
https://doi.org/10.1007/s10856-005-6988-1 pmid: 15875258
20 R A Perez, G Mestres. Role of pore size and morphology in musculo-skeletal tissue regeneration. Materials Science and Engineering C, 2016, 61: 922–939
https://doi.org/10.1016/j.msec.2015.12.087 pmid: 26838923
21 A L Rosa, M M Beloti, R van Noort. Osteoblastic differentiation of cultured rat bone marrow cells on hydroxyapatite with different surface topography. Dental Materials, 2003, 19(8): 768–772
https://doi.org/10.1016/S0109-5641(03)00024-1 pmid: 14511735
22 P Habibovic, H Yuan, C M van der Valk, et al.. 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials, 2005, 26(17): 3565–3575
https://doi.org/10.1016/j.biomaterials.2004.09.056 pmid: 15621247
23 M Rouahi, O Gallet, E Champion, et al.. Influence of hydroxyapatite microstructure on human bone cell response. Journal of Biomedical Materials Research Part A, 2006, 78A(2): 222–235
https://doi.org/10.1002/jbm.a.30682 pmid: 16628709
24 B Vagaská, L Bacáková, E Filová, et al.. Osteogenic cells on bio-inspired materials for bone tissue engineering. Physiological Research, 2010, 59(3): 309–322
https://doi.org/10.33549/physiolres.931776 pmid: 19681662
25 A Acarregui, A Murua, J L Pedraz, et al.. A perspective on bioactive cell microencapsulation. BioDrugs, 2012, 26(5): 283–301
https://doi.org/10.1007/BF03261887 pmid: 22715813
26 M P Ginebra, M Espanol, E B Montufar, et al.. New processing approaches in calcium phosphate cements and their applications in regenerative medicine. Acta Biomaterialia, 2010, 6(8): 2863–2873
https://doi.org/10.1016/j.actbio.2010.01.036 pmid: 20123046
27 W Y Yeong, C K Chua, K F Leong, et al.. Rapid prototyping in tissue engineering: challenges and potential. Trends in Biotechnology, 2004, 22(12): 643–652
https://doi.org/10.1016/j.tibtech.2004.10.004 pmid: 15542155
28 M Ebrahimi, M Botelho, W Lu, et al.. Integrated approach in designing biphasic nanocomposite collagen/nBCP scaffolds with controlled porosity and permeability for bone tissue engineering. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2020, 108(4): 1738–1753
https://doi.org/10.1002/jbm.b.34518 pmid: 31750983
29 R W Goulet, S A Goldstein, M J Ciarelli, et al.. The relationship between the structural and orthogonal compressive properties of trabecular bone. Journal of Biomechanics, 1994, 27(4): 375–389
https://doi.org/10.1016/0021-9290(94)90014-0 pmid: 8188719
30 V L Tsang, S N Bhatia. Three-dimensional tissue fabrication. Advanced Drug Delivery Reviews, 2004, 56(11): 1635–1647
https://doi.org/10.1016/j.addr.2004.05.001 pmid: 15350293
31 J K Sherwood, S L Riley, R Palazzolo, et al.. A three-dimensional osteochondral composite scaffold for articular cartilage repair. Biomaterials, 2002, 23(24): 4739–4751
https://doi.org/10.1016/S0142-9612(02)00223-5 pmid: 12361612
32 K F Leong, C K Chua, N Sudarmadji, et al.. Engineering functionally graded tissue engineering scaffolds. Journal of the Mechanical Behavior of Biomedical Materials, 2008, 1(2): 140–152
https://doi.org/10.1016/j.jmbbm.2007.11.002 pmid: 19627779
33 S Yang, K F Leong, Z Du, et al.. The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques. Tissue Engineering, 2002, 8(1): 1–11
https://doi.org/10.1089/107632702753503009 pmid: 11886649
34 W Pompe, H Worch, M Epple, et al.. Functionally graded materials for biomedical applications. Materials Science and Engineering A, 2003, 362(1–2): 40–60
https://doi.org/10.1016/S0921-5093(03)00580-X
35 X Miao, D Sun. Graded/gradient porous biomaterials. Materials, 2009, 3(1): 26–47
https://doi.org/10.3390/ma3010026
36 T B F Woodfield, C A Van Blitterswijk, J De Wijn, et al.. Polymer scaffolds fabricated with pore-size gradients as a model for studying the zonal organization within tissue-engineered cartilage constructs. Tissue Engineering, 2005, 11(9–10): 1297–1311
https://doi.org/10.1089/ten.2005.11.1297 pmid: 16259586
37 J V Karpiak, Y Ner, A Almutairi. Density gradient multilayer polymerization for creating complex tissue. Advanced Materials, 2012, 24(11): 1466–1470
https://doi.org/10.1002/adma.201103501 pmid: 22318771
38 Y Zhu, H Wu, S Sun, et al.. Designed composites for mimicking compressive mechanical properties of articular cartilage matrix. Journal of the Mechanical Behavior of Biomedical Materials, 2014, 36: 32–46
https://doi.org/10.1016/j.jmbbm.2014.04.003 pmid: 24793172
39 S H Oh, I K Park, J M Kim, et al.. In vitro and in vivo characteristics of PCL scaffolds with pore size gradient fabricated by a centrifugation method. Biomaterials, 2007, 28(9): 1664–1671
https://doi.org/10.1016/j.biomaterials.2006.11.024 pmid: 17196648
40 I Bružauskaitė, D Bironaitė, E Bagdonas, et al.. Scaffolds and cells for tissue regeneration: Different scaffold pore sizes-different cell effects. Cytotechnology, 2016, 68(3): 355–369
https://doi.org/10.1007/s10616-015-9895-4 pmid: 26091616
41 F Causa, P A Netti, L Ambrosio. A multi-functional scaffold for tissue regeneration: The need to engineer a tissue analogue. Biomaterials, 2007, 28(34): 5093–5099
https://doi.org/10.1016/j.biomaterials.2007.07.030 pmid: 17675151
42 H J Sung, C Meredith, C Johnson, et al.. The effect of scaffold degradation rate on three-dimensional cell growth and angiogenesis. Biomaterials, 2004, 25(26): 5735–5742
https://doi.org/10.1016/j.biomaterials.2004.01.066 pmid: 15147819
43 V Karageorgiou, D Kaplan. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials, 2005, 26(27): 5474–5491
https://doi.org/10.1016/j.biomaterials.2005.02.002 pmid: 15860204
44 S J Hollister. Porous scaffold design for tissue engineering. Nature Materials, 2005, 4(7): 518–524
https://doi.org/10.1038/nmat1421 pmid: 16003400
45 A Macchetta, I G Turner, C R Bowen. Fabrication of HA/TCP scaffolds with a graded and porous structure using a camphene-based freeze-casting method. Acta Biomaterialia, 2009, 5(4): 1319–1327
https://doi.org/10.1016/j.actbio.2008.11.009 pmid: 19112055
46 H A Almeida, P J Bártolo. Topological optimisation of scaffolds for tissue engineering. Procedia Engineering, 2013, 59: 298–306
https://doi.org/10.1016/j.proeng.2013.05.125
47 A Rainer, S M Giannitelli, D Accoto, et al.. Load-adaptive scaffold architecturing: a bioinspired approach to the design of porous additively manufactured scaffolds with optimized mechanical properties. Annals of Biomedical Engineering, 2012, 40(4): 966–975
https://doi.org/10.1007/s10439-011-0465-4 pmid: 22109804
48 A G Mitsak, J M Kemppainen, M T Harris, et al.. Effect of polycaprolactone scaffold permeability on bone regeneration in vivo. Tissue Engineering Part A, 2011, 17(13–14): 1831–1839
https://doi.org/10.1089/ten.tea.2010.0560 pmid: 21395465
49 F J O’Brien, B A Harley, M A Waller, et al.. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technology and Health Care, 2007, 15(1): 3–17
https://doi.org/10.3233/THC-2007-15102 pmid: 17264409
50 P J Emans, E J P Jansen, D van Iersel, et al.. Tissue-engineered constructs: The effect of scaffold architecture in osteochondral repair. Journal of Tissue Engineering and Regenerative Medicine, 2013, 7(9): 751–756
https://doi.org/10.1002/term.1477 pmid: 22438217
51 J X Lu, B Flautre, K Anselme, et al.. Role of interconnections in porous bioceramics on bone recolonization in vitro and in vivo. Journal of Materials Science. Materials in Medicine, 1999, 10(2): 111–120
https://doi.org/10.1023/A:1008973120918 pmid: 15347932
52 B Otsuki, M Takemoto, S Fujibayashi, et al.. Pore throat size and connectivity determine bone and tissue ingrowth into porous implants: Three-dimensional micro-CT based structural analyses of porous bioactive titanium implants. Biomaterials, 2006, 27(35): 5892–5900
https://doi.org/10.1016/j.biomaterials.2006.08.013 pmid: 16945409
53 B Starly, E Yildirim, W Sun. A tracer metric numerical model for predicting tortuosity factors in three-dimensional porous tissue scaffolds. Computer Methods and Programs in Biomedicine, 2007, 87(1): 21–27
https://doi.org/10.1016/j.cmpb.2007.04.003 pmid: 17532090
54 J Hrabe, S Hrabetová, K Segeth. A model of effective diffusion and tortuosity in the extracellular space of the brain. Biophysical Journal, 2004, 87(3): 1606–1617
https://doi.org/10.1529/biophysj.103.039495 pmid: 15345540
55 J M Zalc, S C Reyes, E Iglesia. The effects of diffusion mechanism and void structure on transport rates and tortuosity factors in complex porous structures. Chemical Engineering Science, 2004, 59(14): 2947–2960
https://doi.org/10.1016/j.ces.2004.04.028
56 E A Botchwey, M A Dupree, S R Pollack, et al.. Tissue engineered bone: Measurement of nutrient transport in three-dimensional matrices. Journal of Biomedical Materials Research Part A, 2003, 67A(1): 357–367
https://doi.org/10.1002/jbm.a.10111 pmid: 14517896
57 M M C G Silva, L A Cyster, J J A Barry, et al.. The effect of anisotropic architecture on cell and tissue infiltration into tissue engineering scaffolds. Biomaterials, 2006, 27(35): 5909–5917
https://doi.org/10.1016/j.biomaterials.2006.08.010 pmid: 16949666
58 B Dorj, J E Won, O Purevdorj, et al.. A novel therapeutic design of microporous-structured biopolymer scaffolds for drug loading and delivery. Acta Biomaterialia, 2014, 10(3): 1238–1250
https://doi.org/10.1016/j.actbio.2013.11.002 pmid: 24239677
59 M Nikkhah, F Edalat, S Manoucheri, et al.. Engineering microscale topographies to control the cell–substrate interface. Biomaterials, 2012, 33(21): 5230–5246
https://doi.org/10.1016/j.biomaterials.2012.03.079 pmid: 22521491
60 S M Lien, L Y Ko, T J Huang. Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering. Acta Biomaterialia, 2009, 5(2): 670–679
https://doi.org/10.1016/j.actbio.2008.09.020 pmid: 18951858
61 C M Murphy, F J O’Brien. Understanding the effect of mean pore size on cell activity in collagen-glycosaminoglycan scaffolds. Cell Adhesion & Migration, 2010, 4(3): 377–381
https://doi.org/10.4161/cam.4.3.11747 pmid: 20421733
62 Y Zhao, K Tan, Y Zhou, et al.. A combinatorial variation in surface chemistry and pore size of three-dimensional porous poly(ε-caprolactone) scaffolds modulates the behaviors of mesenchymal stem cells. Materials Science and Engineering C, 2016, 59: 193–202
https://doi.org/10.1016/j.msec.2015.10.017 pmid: 26652364
63 S Nehrer, H A Breinan, A Ramappa, et al.. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials, 1997, 18(11): 769–776
https://doi.org/10.1016/S0142-9612(97)00001-X pmid: 9177854
64 J J Klawitter, J G Bagwell, A M Weinstein, et al.. An evaluation of bone growth into porous high density polyethylene. Journal of Biomedical Materials Research, 1976, 10(2): 311–323
https://doi.org/10.1002/jbm.820100212 pmid: 1254618
65 P Y Huri, B A Ozilgen, D L Hutton, et al.. Scaffold pore size modulates in vitro osteogenesis of human adipose-derived stem/stromal cells. Biomedical Materials, 2014, 9(4): 045003
https://doi.org/10.1088/1748-6041/9/4/045003 pmid: 24945873
66 L G Sicchieri, G E Crippa, P T de Oliveira, et al.. Pore size regulates cell and tissue interactions with PLGA-CaP scaffolds used for bone engineering. Journal of Tissue Engineering and Regenerative Medicine, 2012, 6(2): 155–162
https://doi.org/10.1002/term.422 pmid: 21446054
67 S Kujala, J Ryhänen, A Danilov, et al.. Effect of porosity on the osteointegration and bone ingrowth of a weight-bearing nickel-titanium bone graft substitute. Biomaterials, 2003, 24(25): 4691–4697
https://doi.org/10.1016/S0142-9612(03)00359-4 pmid: 12951012
68 T H Kim, S H Oh, E B Kwon, et al.. In vitro evaluation of osteogenesis and myogenesis from adipose-derived stem cells in a pore size gradient scaffold. Macromolecular Research, 2013, 21(8): 878–885
https://doi.org/10.1007/s13233-013-1099-1
69 C M Murphy, M G Haugh, 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, 2010, 31(3): 461–466
https://doi.org/10.1016/j.biomaterials.2009.09.063 pmid: 19819008
70 T C Lim, K S Chian, 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. Journal of Biomedical Materials Research Part A, 2010, 94A(4): 1303‒1311
https://doi.org/10.1002/jbm.a.32747
71 J W Lee, G Ahn, J Y Kim, et al.. Evaluating cell proliferation based on internal pore size and 3D scaffold architecture fabricated using solid freeform fabrication technology. Journal of Materials Science: Materials in Medicine, 2010, 21(12): 3195–3205
https://doi.org/10.1007/s10856-010-4173-7 pmid: 20981473
72 T Mygind, M Stiehler, A Baatrup, et al.. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials, 2007, 28(6): 1036–1047
https://doi.org/10.1016/j.biomaterials.2006.10.003 pmid: 17081601
73 E Tsuruga, H Takita, H Itoh, et al.. Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. Journal of Biochemistry, 1997, 121(2): 317–324
https://doi.org/10.1093/oxfordjournals.jbchem.a021589 pmid: 9089406
74 S M M Roosa, J M Kemppainen, E N Moffitt, et al.. The pore size of polycaprolactone scaffolds has limited influence on bone regeneration in an in vivo model. Journal of Biomedical Materials Research Part A, 2010, 92A(1): 359–368
https://doi.org/10.1002/jbm.a.32381 pmid: 19189391
75 S F Hulbert, F A Young, R S Mathews, et al.. Potential of ceramic materials as permanently implantable skeletal prostheses. Journal of Biomedical Materials Research, 1970, 4(3): 433–456
https://doi.org/10.1002/jbm.820040309 pmid: 5469185
76 F A Akin, H Zreiqat, S Jordan, et al.. Preparation and analysis of macroporous TiO2 films on Ti surfaces for bone-tissue implants. Journal of Biomedical Materials Research, 2001, 57(4): 588–596
https://doi.org/10.1002/1097-4636(20011215)57:4<588::AID-JBM1206>3.0.CO;2-Y pmid: 11553890
77 G Akay, M A Birch, M A Bokhari. Microcellular polyHIPE polymer supports osteoblast growth and bone formation in vitro. Biomaterials, 2004, 25(18): 3991–4000
https://doi.org/10.1016/j.biomaterials.2003.10.086 pmid: 15046889
78 M C von Doernberg, B von Rechenberg, M Bohner, et al.. In vivo behavior of calcium phosphate scaffolds with four different pore sizes. Biomaterials, 2006, 27(30): 5186–5198
https://doi.org/10.1016/j.biomaterials.2006.05.051 pmid: 16790273
79 A I Itälä, H O Ylänen, C Ekholm, et al.. Pore diameter of more than 100 microm is not requisite for bone ingrowth in rabbits. Journal of Biomedical Materials Research, 2001, 58(6): 679–683
https://doi.org/10.1002/jbm.1069 pmid: 11745521
80 S Sánchez-Salcedo, D Arcos, M Vallet-Regí. Upgrading calcium phosphate scaffolds for tissue engineering applications. Key Engineering Materials, 2008, 377: 19–42
https://doi.org/10.4028/www.scientific.net/KEM.377.19
81 S J Simske, R A Ayers, T A Bateman. Porous materials for bone engineering. Materials Science Forum, 1997, 250: 151–182
https://doi.org/10.4028/www.scientific.net/MSF.250.151
82 H J Kim, U J Kim, G Vunjak-Novakovic, et al.. Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells. Biomaterials, 2005, 26(21): 4442–4452
https://doi.org/10.1016/j.biomaterials.2004.11.013 pmid: 15701373
83 B B Mandal, S C Kundu. Cell proliferation and migration in silk fibroin 3D scaffolds. Biomaterials, 2009, 30(15): 2956–2965
https://doi.org/10.1016/j.biomaterials.2009.02.006 pmid: 19249094
84 S H Oh, T H Kim, G I Im, et al.. Investigation of pore size effect on chondrogenic differentiation of adipose stem cells using a pore size gradient scaffold. Biomacromolecules, 2010, 11(8): 1948–1955
https://doi.org/10.1021/bm100199m pmid: 20690707
85 P Duan, Z Pan, L Cao, et al.. The effects of pore size in bilayered poly(lactide-co-glycolide) scaffolds on restoring osteochondral defects in rabbits. Journal of Biomedical Materials Research Part A, 2014, 102(1): 180–192
https://doi.org/10.1002/jbm.a.34683 pmid: 23637068
86 A Penk, Y Förster, H A Scheidt, et al.. The pore size of PLGA bone implants determines the de novo formation of bone tissue in tibial head defects in rats. Magnetic Resonance in Medicine, 2013, 70(4): 925–935
https://doi.org/10.1002/mrm.24541 pmid: 23165861
87 F M Klenke, Y Liu, H Yuan, et al.. Impact of pore size on the vascularization and osseointegration of ceramic bone substitutes in vivo. Journal of Biomedical Materials Research Part A, 2008, 85A(3): 777–786
https://doi.org/10.1002/jbm.a.31559 pmid: 17896777
88 T Hausner, R Schmidhammer, S Zandieh, et al.. Nerve regeneration using tubular scaffolds from biodegradable polyurethane. Acta Neurochirurgica Supplementum, 2007, 100: 69–72
https://doi.org/10.1007/978-3-211-72958-8_15 pmid: 17985549
89 A Bozkurt, R Deumens, C Beckmann, et al.. In vitro cell alignment obtained with a Schwann cell enriched microstructured nerve guide with longitudinal guidance channels. Biomaterials, 2009, 30(2): 169–179
https://doi.org/10.1016/j.biomaterials.2008.09.017 pmid: 18922575
90 N Yuan, W Tian, L Sun, et al.. Neural stem cell transplantation in a double-layer collagen membrane with unequal pore sizes for spinal cord injury repair. Neural Regeneration Research, 2014, 9(10): 1014–1019
https://doi.org/10.4103/1673-5374.133160 pmid: 25206753
91 M Lee, B M Wu, J C Y Dunn. Effect of scaffold architecture and pore size on smooth muscle cell growth. Journal of Biomedical Materials Research Part A, 2008, 87A(4): 1010–1016
https://doi.org/10.1002/jbm.a.31816 pmid: 18257081
92 B A C Harley, H D Kim, M H Zaman, et al.. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophysical Journal, 2008, 95(8): 4013–4024
https://doi.org/10.1529/biophysj.107.122598 pmid: 18621811
93 I V Yannas. Tissue regeneration by use of collagen–glycosaminoglycan copolymers. Clinical Materials, 1992, 9(3–4): 179–187
https://doi.org/10.1016/0267-6605(92)90098-E pmid: 10149968
94 T Knight, J Basu, E A Rivera, et al.. Fabrication of a multi-layer three-dimensional scaffold with controlled porous micro-architecture for application in small intestine tissue engineering. Cell Adhesion & Migration, 2013, 7(3): 267–274
https://doi.org/10.4161/cam.24351 pmid: 23563499
95 G C Reilly, A J Engler. Intrinsic extracellular matrix properties regulate stem cell differentiation. Journal of Biomechanics, 2010, 43(1): 55–62
https://doi.org/10.1016/j.jbiomech.2009.09.009 pmid: 19800626
96 B A Harley, J H Leung, E C C M Silva, et al.. Mechanical characterization of collagen-glycosaminoglycan scaffolds. Acta Biomaterialia, 2007, 3(4): 463–474
https://doi.org/10.1016/j.actbio.2006.12.009 pmid: 17349829
97 M Y Kim, D J Li, L K Pham, et al.. Microfabrication of high-resolution porous membranes for cell culture. Journal of Membrane Science, 2014, 452: 460–469
https://doi.org/10.1016/j.memsci.2013.11.034 pmid: 24567663
98 H I Chang, Y Wang. Cell responses to surface and architecture of tissue engineering scaffolds. In: Eberli D, ed. Regenerative Medicine and Tissue Engineering: Cells and Biomaterials.Croatia: InTech, 2011, 569–588
99 S R Peyton, Z I Kalcioglu, J C Cohen, et al.. Marrow-derived stem cell motility in 3D synthetic scaffold is governed by geometry along with adhesivity and stiffness. Biotechnology and Bioengineering, 2011, 108(5): 1181–1193
https://doi.org/10.1002/bit.23027 pmid: 21449030
100 M Zhang, D Methot, V Poppa, et al.. Cardiomyocyte grafting for cardiac repair: Graft cell death and anti-death strategies. Journal of Molecular and Cellular Cardiology, 2001, 33(5): 907–921
https://doi.org/10.1006/jmcc.2001.1367 pmid: 11343414
101 J S Lee, H D Cha, J H Shim, et al.. Effect of pore architecture and stacking direction on mechanical properties of solid freeform fabrication-based scaffold for bone tissue engineering. Journal of Biomedical Materials Research Part A, 2012, 100A(7): 1846–1853
https://doi.org/10.1002/jbm.a.34149 pmid: 22488723
102 A Phadke, Y S Hwang, S H Kim, et al.. Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells. European Cells & Materials, 2013, 25: 114–129
https://doi.org/10.22203/eCM.v025a08 pmid: 23329467
103 X Liu, M N Rahaman, Q Fu. Bone regeneration in strong porous bioactive glass (13–93) scaffolds with an oriented microstructure implanted in rat calvarial defects. Acta Biomaterialia, 2013, 9(1): 4889–4898
https://doi.org/10.1016/j.actbio.2012.08.029 pmid: 22922251
104 Q Fu, M N Rahaman, B S Bal, et al.. In vitro cellular response to hydroxyapatite scaffolds with oriented pore architectures. Materials Science and Engineering C, 2009, 29(7): 2147–2153
https://doi.org/10.1016/j.msec.2009.04.016
105 K M Brouwer, W F Daamen, N van Lochem, et al.. Construction and in vivo evaluation of a dual layered collagenous scaffold with a radial pore structure for repair of the diaphragm. Acta Biomaterialia, 2013, 9(6): 6844–6851
https://doi.org/10.1016/j.actbio.2013.03.003 pmid: 23499986
106 E S Sanzana, M Navarro, M P Ginebra, et al.. Role of porosity and pore architecture in the in vivo bone regeneration capacity of biodegradable glass scaffolds. Journal of Biomedical Materials Research Part A, 2014, 102(6): 1767–1773
https://doi.org/10.1002/jbm.a.34845 pmid: 23813739
107 P Yilgor, R A Sousa, R L Reis, et al.. 3D plotted PCL scaffolds for stem cell based bone tissue engineering. Macromolecular Symposia, 2008, 269(1): 92–99
https://doi.org/10.1002/masy.200850911
108 C G Jeong, 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 Engineering Part A, 2010, 16(12): 3759–3768
https://doi.org/10.1089/ten.tea.2010.0103 pmid: 20666604
109 C M Bidan, K P Kommareddy, M Rumpler, et al.. Geometry as a factor for tissue growth: Towards shape optimization of tissue engineering scaffolds. Advanced Healthcare Materials, 2013, 2(1): 186–194
https://doi.org/10.1002/adhm.201200159 pmid: 23184876
110 G C Jr Engelmayr, G D Papworth, S C Watkins, et al.. Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. Journal of Biomechanics, 2006, 39(10): 1819–1831
https://doi.org/10.1016/j.jbiomech.2005.05.020 pmid: 16043186
111 C M Nelson, R P Jean, J L Tan, et al.. Emergent patterns of growth controlled by multicellular form and mechanics. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(33): 11594–11599
https://doi.org/10.1073/pnas.0502575102 pmid: 16049098
112 M Rumpler, A Woesz, J W C Dunlop, et al.. The effect of geometry on three-dimensional tissue growth. Journal of the Royal Society: Interface, 2008, 5(27): 1173–1180
https://doi.org/10.1098/rsif.2008.0064 pmid: 18348957
113 A Scarano, M Degidi, V Perrotti, et al.. Experimental evaluation in rabbits of the effects of thread concavities in bone formation with different titanium implant surfaces. Clinical Implant Dentistry and Related Research, 2014, 16(4): 572–581
https://doi.org/10.1111/cid.12033 pmid: 23305450
114 U Ripamonti, L C Roden, L F Renton. Osteoinductive hydroxyapatite-coated titanium implants. Biomaterials, 2012, 33(15): 3813–3823
https://doi.org/10.1016/j.biomaterials.2012.01.050 pmid: 22364700
115 A A Zadpoor. Bone tissue regeneration: The role of scaffold geometry. Biomaterials Science, 2015, 3(2): 231–245
https://doi.org/10.1039/C4BM00291A pmid: 26218114
116 F P W Melchels, B Tonnarelli, A L Olivares, et al.. The influence of the scaffold design on the distribution of adhering cells after perfusion cell seeding. Biomaterials, 2011, 32(11): 2878–2884
https://doi.org/10.1016/j.biomaterials.2011.01.023 pmid: 21288567
117 J Wu, Q Zhao, J Sun, et al.. Preparation of poly(ethylene glycol) aligned porous cryogels using a unidirectional freezing technique. Soft Matter, 2012, 8(13): 3620
https://doi.org/10.1039/c2sm07411g
118 S Jia, L Liu, W Pan, et al.. Oriented cartilage extracellular matrix-derived scaffold for cartilage tissue engineering. Journal of Bioscience and Bioengineering, 2012, 113(5): 647–653
https://doi.org/10.1016/j.jbiosc.2011.12.009 pmid: 22265894
119 A Arora, A Kothari, D S Katti. Pore orientation mediated control of mechanical behavior of scaffolds and its application in cartilage-mimetic scaffold design. Journal of the Mechanical Behavior of Biomedical Materials, 2015, 51: 169–183
https://doi.org/10.1016/j.jmbbm.2015.06.033 pmid: 26256472
120 J M Sobral, S G Caridade, R A Sousa, et al.. Three-dimensional plotted scaffolds with controlled pore size gradients: Effect of scaffold geometry on mechanical performance and cell seeding efficiency. Acta Biomaterialia, 2011, 7(3): 1009–1018
https://doi.org/10.1016/j.actbio.2010.11.003 pmid: 21056125
121 A Salerno, D Guarnieri, M Iannone, et al.. Effect of micro- and macroporosity of bone tissue three-dimensional poly(ε-caprolactone) scaffold on human mesenchymal stem cells invasion, proliferation, and differentiation in vitro. Tissue Engineering Part A, 2010, 16(8): 2661–2673
https://doi.org/10.1089/ten.tea.2009.0494 pmid: 20687813
122 S W Choi, Y Zhang, Y Xia. Three-dimensional scaffolds for tissue engineering: The importance of uniformity in pore size and structure. Langmuir, 2010, 26(24): 19001–19006
https://doi.org/10.1021/la104206h pmid: 21090781
123 H A Declercq, T Desmet, P Dubruel, et al.. The role of scaffold architecture and composition on the bone formation by adipose-derived stem cells. Tissue Engineering Part A, 2014, 20(1–2): 434–444
https://doi.org/10.1089/ten.tea.2013.0179 pmid: 23998529
124 K A Hing. Bioceramic bone graft substitutes: Influence of porosity and chemistry. International Journal of Applied Ceramic Technology, 2005, 2(3): 184–199
https://doi.org/10.1111/j.1744-7402.2005.02020.x
125 P Chen, J Tao, S Zhu, et al.. Radially oriented collagen scaffold with SDF-1 promotes osteochondral repair by facilitating cell homing. Biomaterials, 2015, 39: 114–123
https://doi.org/10.1016/j.biomaterials.2014.10.049 pmid: 25477178
126 E L W de Mulder, G Hannink, N Verdonschot, et al.. Effect of polyurethane scaffold architecture on ingrowth speed and collagen orientation in a subcutaneous rat pocket model. Biomedical Materials, 2013, 8(2): 025004
https://doi.org/10.1088/1748-6041/8/2/025004 pmid: 23385628
127 J Lee, S Shanbhag, N A Kotov. Inverted colloidal crystals as three-dimensional microenvironments for cellular co-cultures. Journal of Materials Chemistry, 2006, 16(35): 3558
https://doi.org/10.1039/b605797g
128 W T Godbey, B S S Hindy, M E Sherman, et al.. A novel use of centrifugal force for cell seeding into porous scaffolds. Biomaterials, 2004, 25(14): 2799–2805
https://doi.org/10.1016/j.biomaterials.2003.09.056 pmid: 14962558
129 J R Mauney, J Blumberg, M Pirun, et al.. Osteogenic differentiation of human bone marrow stromal cells on partially demineralized bone scaffolds in vitro. Tissue Engineering, 2004, 10(1–2): 81–92
https://doi.org/10.1089/107632704322791727 pmid: 15009933
130 A Nieponice, L Soletti, J Guan, et al.. Development of a tissue-engineered vascular graft combining a biodegradable scaffold, muscle-derived stem cells and a rotational vacuum seeding technique. Biomaterials, 2008, 29(7): 825–833
https://doi.org/10.1016/j.biomaterials.2007.10.044 pmid: 18035412
131 H Liu, K Roy. Biomimetic three-dimensional cultures significantly increase hematopoietic differentiation efficacy of embryonic stem cells. Tissue Engineering, 2005, 11(1–2): 319–330
https://doi.org/10.1089/ten.2005.11.319 pmid: 15738685
132 L Meinel, R Fajardo, S Hofmann, et al.. Silk implants for the healing of critical size bone defects. Bone, 2005, 37(5): 688–698
https://doi.org/10.1016/j.bone.2005.06.010 pmid: 16140599
133 B S Chang, C K Lee, K S Hong, et al.. Osteoconduction at porous hydroxyapatite with various pore configurations. Biomaterials, 2000, 21(12): 1291–1298
https://doi.org/10.1016/S0142-9612(00)00030-2 pmid: 10811311
134 M I Gariboldi, S M Best. Effect of ceramic scaffold architectural parameters on biological response. Frontiers in Bioengineering and Biotechnology, 2015, 3: 151
https://doi.org/10.3389/fbioe.2015.00151 pmid: 26501056
135 M S Lord, M Foss, F Besenbacher. Influence of nanoscale surface topography on protein adsorption and cellular response. Nano Today, 2010, 5(1): 66–78
https://doi.org/10.1016/j.nantod.2010.01.001
136 B Annaz, K A Hing, M Kayser, et al.. Porosity variation in hydroxyapatite and osteoblast morphology: A scanning electron microscopy study. Journal of Microscopy, 2004, 215(Pt 1): 100–110
https://doi.org/10.1111/j.0022-2720.2004.01354.x pmid: 15230881
137 D D Deligianni, N D Katsala, P G Koutsoukos, et al.. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials, 2001, 22(1): 87–96
https://doi.org/10.1016/S0142-9612(00)00174-5 pmid: 11085388
138 A Bignon, J Chouteau, J Chevalier, et al.. Effect of micro- and macroporosity of bone substitutes on their mechanical properties and cellular response. Journal of Materials Science: Materials in Medicine, 2003, 14(12): 1089–1097
https://doi.org/10.1023/B:JMSM.0000004006.90399.b4 pmid: 15348502
139 G Zhao, A L Raines, M Wieland, et al.. Requirement for both micron- and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography. Biomaterials, 2007, 28(18): 2821–2829
https://doi.org/10.1016/j.biomaterials.2007.02.024 pmid: 17368532
140 K Anselme, P Linez, M Bigerelle, et al.. The relative influence of the topography and chemistry of TiAl6V4 surfaces on osteoblastic cell behaviour. Biomaterials, 2000, 21(15): 1567–1577
https://doi.org/10.1016/S0142-9612(00)00042-9 pmid: 10885729
141 K Anselme, M Bigerelle, B Noel, et al.. Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. Journal of Biomedical Materials Research, 2000, 49(2): 155–166
https://doi.org/10.1002/(SICI)1097-4636(200002)49:2<155::AID-JBM2>3.0.CO;2-J pmid: 10571901
142 J Isaac, J C Hornez, D Jian, et al.. β-TCP microporosity decreases the viability and osteoblast differentiation of human bone marrow stromal cells. Journal of Biomedical Materials Research Part A, 2008, 86A(2): 386–393
https://doi.org/10.1002/jbm.a.31644 pmid: 17969032
143 Y Takahashi, Y Tabata. Effect of the fiber diameter and porosity of non-woven PET fabrics on the osteogenic differentiation of mesenchymal stem cells. Journal of Biomaterials Science: Polymer Edition, 2004, 15(1): 41–57
https://doi.org/10.1163/156856204322752228 pmid: 15027842
144 P Kasten, I Beyen, P Niemeyer, et al.. Porosity and pore size of β-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: An in vitro and in vivo study. Acta Biomaterialia, 2008, 4(6): 1904–1915
https://doi.org/10.1016/j.actbio.2008.05.017 pmid: 18571999
145 J Malmström, E Adolfsson, A Arvidsson, et al.. Bone response inside free-form fabricated macroporous hydroxyapatite scaffolds with and without an open microporosity. Clinical Implant Dentistry and Related Research, 2007, 9(2): 79–88
https://doi.org/10.1111/j.1708-8208.2007.00031.x pmid: 17535331
146 D D Deligianni, N D Katsala, P G Koutsoukos, et al.. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials, 2001, 22(1): 87–96
https://doi.org/10.1016/S0142-9612(00)00174-5 pmid: 11085388
147 S W S Laurie, L B Kaban, J B Mulliken, et al.. Donor-site morbidity after harvesting rib and iliac bone. Plastic and Reconstructive Surgery, 1984, 73(6): 933–938
https://doi.org/10.1097/00006534-198406000-00014 pmid: 6374708
148 S Ruijtenberg, S van den Heuvel. Coordinating cell proliferation and differentiation: Antagonism between cell cycle regulators and cell type-specific gene expression. Cell Cycle, 2016, 15(2): 196–212
https://doi.org/10.1080/15384101.2015.1120925 pmid: 26825227
149 A Satyanarayana, P Kaldis. Mammalian cell-cycle regulation: Several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene, 2009, 28(33): 2925–2939
https://doi.org/10.1038/onc.2009.170 pmid: 19561645
150 B Boward, T Wu, S Dalton. Control of cell fate through cell cycle and pluripotency networks. Stem Cells, 2016, 34(6): 1427–1436
https://doi.org/10.1002/stem.2345 pmid: 26889666
151 J Cao, M Spielmann, X Qiu, et al.. The single-cell transcriptional landscape of mammalian organogenesis. Nature, 2019, 566(7745): 496–502
https://doi.org/10.1038/s41586-019-0969-x pmid: 30787437
152 D H Kim, S B Khatau, Y Feng, et al.. Actin cap associated focal adhesions and their distinct role in cellular mechanosensing. Scientific Reports, 2012, 2(1): 555
https://doi.org/10.1038/srep00555 pmid: 22870384
153 R P Martins, J D Finan, F Guilak, et al.. Mechanical regulation of nuclear structure and function. Annual Review of Biomedical Engineering, 2012, 14(1): 431–455
https://doi.org/10.1146/annurev-bioeng-071910-124638 pmid: 22655599
154 S Dupont, L Morsut, M Aragona, et al.. Role of YAP/TAZ in mechanotransduction. Nature, 2011, 474(7350): 179–183
https://doi.org/10.1038/nature10137 pmid: 21654799
155 G Halder, S Dupont, S Piccolo. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nature Reviews: Molecular Cell Biology, 2012, 13(9): 591–600
https://doi.org/10.1038/nrm3416 pmid: 22895435
156 R Janoštiak, A C Pataki, J Brábek, et al.. Mechanosensors in integrin signaling: The emerging role of p130Cas. European Journal of Cell Biology, 2014, 93(10–12): 445–454
https://doi.org/10.1016/j.ejcb.2014.07.002 pmid: 25062607
157 J Zhang, D Barbieri, H ten Hoopen, et al.. Microporous calcium phosphate ceramics driving osteogenesis through surface architecture. Journal of Biomedical Materials Research Part A, 2015, 103(3): 1188–1199
https://doi.org/10.1002/jbm.a.35272 pmid: 25044678
158 P Habibovic, T M Sees, M A van den Doel, et al.. Osteoinduction by biomaterials: Physicochemical and structural influences. Journal of Biomedical Materials Research Part A, 2006, 77A(4): 747–762
https://doi.org/10.1002/jbm.a.30712 pmid: 16557498
159 K Rechendorff, M B Hovgaard, M Foss, et al.. Enhancement of protein adsorption induced by surface roughness. Langmuir, 2006, 22(26): 10885–10888
https://doi.org/10.1021/la0621923 pmid: 17154557
160 I O Smith, X H Liu, L A Smith, et al.. Nanostructured polymer scaffolds for tissue engineering and regenerative medicine. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechno-logy, 2009, 1(2): 226–236
https://doi.org/10.1002/wnan.26 pmid: 20049793
161 X Liu, P X Ma. Polymeric scaffolds for bone tissue engineering. Annals of Biomedical Engineering, 2004, 32(3): 477–486
https://doi.org/10.1023/B:ABME.0000017544.36001.8e pmid: 15095822
162 S Li, J R De Wijn, J Li, et al.. Macroporous biphasic calcium phosphate scaffold with high permeability/porosity ratio. Tissue Engineering, 2003, 9(3): 535–548
https://doi.org/10.1089/107632703322066714 pmid: 12857421
163 Y Li, S T Yang. Effects of three-dimensional scaffolds on cell organization and tissue development. Biotechnology and Bioprocess Engineering; BBE, 2001, 6(5): 311–325
https://doi.org/10.1007/BF02932999
164 R A Perez, J H Kim, J O Buitrago, et al.. Novel therapeutic core–shell hydrogel scaffolds with sequential delivery of cobalt and bone morphogenetic protein-2 for synergistic bone regeneration. Acta Biomaterialia, 2015, 23: 295–308
https://doi.org/10.1016/j.actbio.2015.06.002 pmid: 26054564
165 R A Perez, S J Seo, J E Won, et al.. Therapeutically relevant aspects in bone repair and regeneration. Materials Today, 2015, 18(10): 573–589
https://doi.org/10.1016/j.mattod.2015.06.011
166 O Oliviero, M Ventre, P A Netti. Functional porous hydrogels to study angiogenesis under the effect of controlled release of vascular endothelial growth factor. Acta Biomaterialia, 2012, 8(9): 3294–3301
https://doi.org/10.1016/j.actbio.2012.05.019 pmid: 22641106
167 A Artel, H Mehdizadeh, Y C Chiu, et al.. An agent-based model for the investigation of neovascularization within porous scaffolds. Tissue Engineering Part A, 2011, 17(17–18): 2133–2141
https://doi.org/10.1089/ten.tea.2010.0571 pmid: 21513462
168 Y Kuboki, Q M Jin, H Takita. Geometry of carriers controlling phenotypic expression in BMP-induced osteogenesis and chondrogenesis. Journal of Bone and Joint Surgery: American Volume, 2001, 83A(Suppl 1): S105–S115
https://doi.org/10.2106/00004623-200100002-00005 pmid: 11314788
169 B Feng, Z Jinkang, W Zhen, et al.. The effect of pore size on tissue ingrowth and neovascularization in porous bioceramics of controlled architecture in vivo. Biomedical Materials, 2011, 6(1): 015007
https://doi.org/10.1088/1748-6041/6/1/015007 pmid: 21206002
170 V Mouriño, J P Cattalini, A R Boccaccini. Metallic ions as therapeutic agents in tissue engineering scaffolds: An overview of their biological applications and strategies for new developments. Journal of the Royal Society: Interface, 2012, 9(68): 401–419
https://doi.org/10.1098/rsif.2011.0611 pmid: 22158843
171 H Yamasaki, H Sakai. Osteogenic response to porous hydroxyapatite ceramics under the skin of dogs. Biomaterials, 1992, 13(5): 308–312
https://doi.org/10.1016/0142-9612(92)90054-R pmid: 1318086
172 C Klein, K de Groot, W Chen, et al.. Osseous substance formation induced in porous calcium phosphate ceramics in soft tissues. Biomaterials, 1994, 15(1): 31–34
https://doi.org/10.1016/0142-9612(94)90193-7 pmid: 8161654
173 U Ripamonti. Bone induction in nonhuman primates. An experimental study on the baboon. Clinical Orthopaedics and Related Research, 1991, (269): 284–294
pmid: 1864050
174 L Wang, B Zhang, C Bao, et al.. Ectopic osteoid and bone formation by three calcium-phosphate ceramics in rats, rabbits and dogs. PLoS One, 2014, 9(9): e107044
https://doi.org/10.1371/journal.pone.0107044 pmid: 25229501
175 R Z LeGeros. Calcium phosphate-based osteoinductive materials. Chemical Reviews, 2008, 108(11): 4742–4753
https://doi.org/10.1021/cr800427g pmid: 19006399
176 M P Lutolf, J A Hubbell. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nature Biotechnology, 2005, 23(1): 47–55
https://doi.org/10.1038/nbt1055 pmid: 15637621
177 G Wei, P X Ma. Partially nanofibrous architecture of 3D tissue engineering scaffolds. Biomaterials, 2009, 30(32): 6426–6434
https://doi.org/10.1016/j.biomaterials.2009.08.012 pmid: 19699518
178 H Yuan, H Fernandes, P Habibovic, et al.. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(31): 13614–13619
https://doi.org/10.1073/pnas.1003600107 pmid: 20643969
179 U Ripamonti. The morphogenesis of bone in replicas of porous hydroxyapatite obtained from conversion of calcium carbonate exoskeletons of coral. The Journal of Bone and Joint Surgery: American Volume, 1991, 73(5): 692–703
https://doi.org/10.2106/00004623-199173050-00007 pmid: 1675218
180 M Espanol, R A Perez, E B Montufar, et al.. Intrinsic porosity of calcium phosphate cements and its significance for drug delivery and tissue engineering applications. Acta Biomaterialia, 2009, 5(7): 2752–2762
https://doi.org/10.1016/j.actbio.2009.03.011 pmid: 19357005
181 A M C Barradas, H Yuan, C A van Blitterswijk, et al.. Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. European Cells & Materials, 2011, 21: 407–429, discussion 429
https://doi.org/10.22203/eCM.v021a31 pmid: 21604242
182 A Hoppe, N S Güldal, A R Boccaccini. A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials, 2011, 32(11): 2757–2774
https://doi.org/10.1016/j.biomaterials.2011.01.004 pmid: 21292319
183 P Y Wang, L R Clements, H Thissen, et al.. High-throughput characterisation of osteogenic differentiation of human mesenchymal stem cells using pore size gradients on porous alumina. Biomaterials Science, 2013, 1(9): 924–932
https://doi.org/10.1039/c3bm60026b pmid: 32481961
184 A Papadimitropoulos, S A Riboldi, B Tonnarelli, et al.. A collagen network phase improves cell seeding of open-pore structure scaffolds under perfusion. Journal of Tissue Engineering and Regenerative Medicine, 2013, 7(3): 183–191
https://doi.org/10.1002/term.506 pmid: 22095721
185 M Bohner, F Baumgart. Theoretical model to determine the effects of geometrical factors on the resorption of calcium phosphate bone substitutes. Biomaterials, 2004, 25(17): 3569–3582
https://doi.org/10.1016/j.biomaterials.2003.10.032 pmid: 15020131
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