Effect of Ceramic Scaffold Architectural Parameters on Biological Response

Numerous studies have focused on the optimization of ceramic architectures to fulfill a variety of scaffold functional requirements and improve biological response. Conventional fabrication techniques, however, do not allow for the production of geometrically controlled, reproducible structures and often fail to allow the independent variation of individual geometric parameters. Current developments in additive manufacturing technologies suggest that 3D printing will allow a more controlled and systematic exploration of scaffold architectures. This more direct translation of design into structure requires a pipeline for design-driven optimization. A theoretical framework for systematic design and evaluation of architectural parameters on biological response is presented. Four levels of architecture are considered, namely (1) surface topography, (2) pore size and geometry, (3) porous networks, and (4) macroscopic pore arrangement, including the potential for spatially varied architectures. Studies exploring the effect of various parameters within these levels are reviewed. This framework will hopefully allow uncovering of new relationships between architecture and biological response in a more systematic way as well as inform future refinement of fabrication techniques to fulfill architectural necessities with a consideration of biological implications.

[1]  M Bohner,et al.  Theoretical model to determine the effects of geometrical factors on the resorption of calcium phosphate bone substitutes. , 2004, Biomaterials.

[2]  张兴中,et al.  Positive Effects of High-Temperature Steel Creep Behavior on Continuous Casting Slab , 2012 .

[3]  Dan Sun,et al.  Graded/Gradient Porous Biomaterials , 2009, Materials.

[4]  Rik Huiskes,et al.  A unified theory for osteonal and hemi-osteonal remodeling. , 2008, Bone.

[5]  Scott J Hollister,et al.  Mechanical and in vivo performance of hydroxyapatite implants with controlled architectures. , 2002, Biomaterials.

[6]  K. de Groot Effect of porosity and physicochemical properties on the stability, resorption, and strength of calcium phosphate ceramics. , 1988, Annals of the New York Academy of Sciences.

[7]  D. Brunette Spreading and orientation of epithelial cells on grooved substrata. , 1986, Experimental cell research.

[8]  H. Seitz,et al.  Three-dimensional printing of porous ceramic scaffolds for bone tissue engineering. , 2005, Journal of biomedical materials research. Part B, Applied biomaterials.

[9]  A Tampieri,et al.  Porosity-graded hydroxyapatite ceramics to replace natural bone. , 2001, Biomaterials.

[10]  T J Sims,et al.  Polymer scaffolds fabricated with pore-size gradients as a model for studying the zonal organization within tissue-engineered cartilage constructs. , 2005, Tissue engineering.

[11]  R. Misra,et al.  Biomaterials , 2008 .

[12]  Amy J Wagoner Johnson,et al.  Multiscale osteointegration as a new paradigm for the design of calcium phosphate scaffolds for bone regeneration. , 2010, Biomaterials.

[13]  M. Saxton Two-dimensional continuum percolation threshold for diffusing particles of nonzero radius. , 2010, Biophysical journal.

[14]  R. van Noort,et al.  Osteoblastic differentiation of cultured rat bone marrow cells on hydroxyapatite with different surface topography. , 2003, Dental materials : official publication of the Academy of Dental Materials.

[15]  C. Oakley,et al.  The sequence of alignment of microtubules, focal contacts and actin filaments in fibroblasts spreading on smooth and grooved titanium substrata. , 1993, Journal of cell science.

[16]  F. Beckmann,et al.  The morphology of anisotropic 3D-printed hydroxyapatite scaffolds. , 2008, Biomaterials.

[17]  L. Geris,et al.  A computational model for cell/ECM growth on 3D surfaces using the level set method: a bone tissue engineering case study , 2014, Biomechanics and modeling in mechanobiology.

[18]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

[19]  Davide Carlo Ambrosi,et al.  Stress-Modulated Growth , 2007 .

[20]  A. Leriche,et al.  Synthesis of macroporous β-tricalcium phosphate with controlled porous architectural , 2008 .

[21]  Tadashi Kokubo,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. , 2006, Biomaterials.

[22]  P. Janmey,et al.  Tissue Cells Feel and Respond to the Stiffness of Their Substrate , 2005, Science.

[23]  张静,et al.  Banana Ovate family protein MaOFP1 and MADS-box protein MuMADS1 antagonistically regulated banana fruit ripening , 2015 .

[24]  L. Silvio,et al.  Porosity variation in hydroxyapatite and osteoblast morphology: a scanning electron microscopy study , 2004, Journal of microscopy.

[25]  H. Jinnai,et al.  Surface curvatures of trabecular bone microarchitecture. , 2002, Bone.

[26]  J. M. Garcı́a,et al.  Modelling bone tissue fracture and healing: a review ☆ , 2004 .

[27]  W. Fenchel,et al.  Über Krümmung und Windung geschlossener Raumkurven , 1929 .

[28]  Binil Starly,et al.  A tracer metric numerical model for predicting tortuosity factors in three-dimensional porous tissue scaffolds , 2007, Comput. Methods Programs Biomed..

[29]  Ralph Müller,et al.  Control of in vitro tissue-engineered bone-like structures using human mesenchymal stem cells and porous silk scaffolds. , 2007, Biomaterials.

[30]  A. Husmann,et al.  Understanding anisotropy and architecture in ice-templated biopolymer scaffolds. , 2014, Materials science & engineering. C, Materials for biological applications.

[31]  Lorenz Holzer,et al.  Contradicting Geometrical Concepts in Pore Size Analysis Attained with Electron Microscopy and Mercury Intrusion , 2008 .

[32]  P. Thomsen,et al.  Bone response inside free-form fabricated macroporous hydroxyapatite scaffolds with and without an open microporosity. , 2007, Clinical implant dentistry and related research.

[33]  Philip Kollmannsberger,et al.  How Linear Tension Converts to Curvature: Geometric Control of Bone Tissue Growth , 2012, PloS one.

[34]  Simon C Watkins,et al.  Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. , 2006, Journal of biomechanics.

[35]  W. Soboyejo,et al.  An investigation of the initial attachment and orientation of osteoblast-like cells on laser grooved Ti-6Al-4V surfaces , 2009 .

[36]  Huipin Yuan,et al.  3D microenvironment as essential element for osteoinduction by biomaterials. , 2005, Biomaterials.

[37]  A. Piattelli,et al.  Experimental evaluation in rabbits of the effects of thread concavities in bone formation with different titanium implant surfaces. , 2014, Clinical implant dentistry and related research.

[38]  B. Bal,et al.  Proliferation and function of MC3T3-E1 cells on freeze-cast hydroxyapatite scaffolds with oriented pore architectures , 2009, Journal of materials science. Materials in medicine.

[39]  S. Milz,et al.  Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing , 2005, Journal of materials science. Materials in medicine.

[40]  Michel Labouesse,et al.  A tension-induced mechanotransduction pathway promotes epithelial morphogenesis , 2011, Nature.

[41]  S F Hulbert,et al.  Potential of ceramic materials as permanently implantable skeletal prostheses. , 1970, Journal of biomedical materials research.

[42]  H. Takita,et al.  Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. , 1997, Journal of biochemistry.

[43]  M. Awano,et al.  Preparation of NiO–YSZ tubular support with radially aligned pore channels , 2003 .

[44]  J. Lu,et al.  Role of interconnections in porous bioceramics on bone recolonization in vitro and in vivo , 1999, Journal of materials science. Materials in medicine.

[45]  A. Bandyopadhyay,et al.  Micromachined Si channel width and tortuosity on human osteoblast cell attachment and proliferation , 2010 .

[46]  Peter Greil,et al.  Mechanical properties and in vitro cell compatibility of hydroxyapatite ceramics with graded pore structure. , 2002, Biomaterials.

[47]  Dietmar W. Hutmacher,et al.  Scaffold design and fabrication technologies for engineering tissues — state of the art and future perspectives , 2001, Journal of biomaterials science. Polymer edition.

[48]  O. Lee,et al.  Matrix stiffness regulation of integrin‐mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[49]  Paul Roschger,et al.  Towards bone replacement materials from calcium phosphates via rapid prototyping and ceramic gelcasting , 2005 .

[50]  Eduardo Saiz,et al.  Architectural Control of Freeze‐Cast Ceramics Through Additives and Templating , 2009, 1710.04095.

[51]  Savio L-Y Woo,et al.  Cell orientation determines the alignment of cell-produced collagenous matrix. , 2003, Journal of biomechanics.

[52]  Karel Segeth,et al.  A model of effective diffusion and tortuosity in the extracellular space of the brain. , 2004, Biophysical journal.

[53]  L E Lanyon,et al.  The influence of mechanical function on the development and remodeling of the tibia. An experimental study in sheep. , 1979, The Journal of bone and joint surgery. American volume.

[54]  K. Shakesheff,et al.  The effect of anisotropic architecture on cell and tissue infiltration into tissue engineering scaffolds. , 2006, Biomaterials.

[55]  Enrique Iglesia,et al.  The effects of diffusion mechanism and void structure on transport rates and tortuosity factors in complex porous structures , 2004 .

[56]  J Tramper,et al.  The effect of PEGT/PBT scaffold architecture on oxygen gradients in tissue engineered cartilaginous constructs. , 2004, Biomaterials.

[57]  Amir A Zadpoor,et al.  Bone tissue regeneration: the role of scaffold geometry. , 2015, Biomaterials science.

[58]  J. Lewis,et al.  Concentrated hydroxyapatite inks for direct-write assembly of 3-D periodic scaffolds. , 2005, Biomaterials.

[59]  A. Husmann,et al.  A design protocol for tailoring ice-templated scaffold structure , 2014, Journal of The Royal Society Interface.

[60]  J. Chevalier,et al.  Effect of micro- and macroporosity of bone substitutes on their mechanical properties and cellular response , 2003, Journal of materials science. Materials in medicine.

[61]  D. Long,et al.  The crossover from 2D to 3D percolation: Theory and numerical simulations , 2003, The European physical journal. E, Soft matter.

[62]  J. Dunlop,et al.  A theoretical model for tissue growth in confined geometries , 2010 .

[63]  Lisa E. Freed,et al.  Accordion-Like Honeycombs for Tissue Engineering of Cardiac Anisotropy , 2008, Nature materials.

[64]  Jin Man Kim,et al.  In vitro and in vivo characteristics of PCL scaffolds with pore size gradient fabricated by a centrifugation method. , 2007, Biomaterials.

[65]  Robert M. Hoffman,et al.  Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force , 2013, The Journal of cell biology.

[66]  Hsin-I Chang,et al.  Cell Responses to Surface and Architecture of Tissue Engineering Scaffolds , 2011 .

[67]  D. Ambrosi,et al.  Growth and dissipation in biological tissues , 2007 .

[68]  M. Bohner,et al.  Microporous calcium phosphate ceramics as tissue engineering scaffolds for the repair of osteochondral defects: Histological results. , 2013, Acta biomaterialia.

[69]  Peter Fratzl,et al.  The effect of geometry on three-dimensional tissue growth , 2008, Journal of The Royal Society Interface.

[70]  D. Salter,et al.  Signalling cascades in mechanotransduction: cell–matrix interactions and mechanical loading , 2009, Scandinavian journal of medicine & science in sports.

[71]  S. Hollister,et al.  Optimal design and fabrication of scaffolds to mimic tissue properties and satisfy biological constraints. , 2002, Biomaterials.

[72]  H. Takita,et al.  Geometry of Carriers Controlling Phenotypic Expression in BMP-Induced Osteogenesis and Chondrogenesis , 2001, The Journal of bone and joint surgery. American volume.

[73]  Anselm Wiskott,et al.  A 3D printed TCP/HA structure as a new osteoconductive scaffold for vertical bone augmentation. , 2016, Clinical oral implants research.

[74]  D. Kaplan,et al.  Porosity of 3D biomaterial scaffolds and osteogenesis. , 2005, Biomaterials.

[75]  A. Lode,et al.  Synthesis and physicochemical, in vitro and in vivo evaluation of an anisotropic, nanocrystalline hydroxyapatite bisque scaffold with parallel‐aligned pores mimicking the microstructure of cortical bone , 2015, Journal of tissue engineering and regenerative medicine.

[76]  D B Burr,et al.  Errors in bone remodeling: toward a unified theory of metabolic bone disease. , 1989, The American journal of anatomy.

[77]  Cato T Laurencin,et al.  Tissue engineered bone: measurement of nutrient transport in three-dimensional matrices. , 2003, Journal of biomedical materials research. Part A.

[78]  Maxence Bigerelle,et al.  Effect of grooved titanium substratum on human osteoblastic cell growth. , 2002, Journal of biomedical materials research.

[79]  D. Deligianni,et al.  Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. , 2001, Biomaterials.

[80]  J. Fredberg,et al.  Collective cell guidance by cooperative intercellular forces , 2010, Nature materials.

[81]  M J Yaszemski,et al.  Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds. , 1997, Journal of biomedical materials research.

[82]  A. Boccaccini,et al.  Taking a deep look: modern microscopy technologies to optimize the design and functionality of biocompatible scaffolds for tissue engineering in regenerative medicine , 2013, Journal of The Royal Society Interface.

[83]  Cécile M. Bidan,et al.  Modelling the role of surface stress on the kinetics of tissue growth in confined geometries. , 2013, Acta biomaterialia.

[84]  Ted A. Bateman,et al.  Porous Materials for Bone Engineering , 1997 .

[85]  K. Anselme,et al.  Influence of hydroxyapatite microstructure on human bone cell response. , 2006, Journal of biomedical materials research. Part A.

[86]  G. Genin,et al.  A mechanism for effective cell-seeding in rigid, microporous substrates. , 2013, Acta biomaterialia.

[87]  P. Fiala,et al.  Spatial organization of the haversian bone in man. , 1996, Journal of biomechanics.

[88]  C. Please,et al.  Pore Geometry Regulates Early Stage Human Bone Marrow Cell Tissue Formation and Organisation , 2013, Annals of Biomedical Engineering.

[89]  S. Majumdar,et al.  High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. , 1998, Bone.

[90]  Cécile M. Bidan,et al.  A three-dimensional model for tissue deposition on complex surfaces , 2013, Computer methods in biomechanics and biomedical engineering.

[91]  D B Burr,et al.  Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[92]  Philip Kollmannsberger,et al.  Geometry as a Factor for Tissue Growth: Towards Shape Optimization of Tissue Engineering Scaffolds , 2013, Advanced healthcare materials.

[93]  P. A. Revell,et al.  Microporosity enhances bioactivity of synthetic bone graft substitutes , 2005, Journal of materials science. Materials in medicine.

[94]  J. Planell,et al.  Hydroxyapatite ceramic bodies with tailored mechanical properties for different applications. , 2002, Journal of biomedical materials research.

[95]  Dominique Bernard,et al.  Non-destructive quantitative 3D analysis for the optimisation of tissue scaffolds. , 2007, Biomaterials.

[96]  B. Bal,et al.  In vitro cellular response to hydroxyapatite scaffolds with oriented pore architectures , 2009 .

[97]  R. Cameron,et al.  Cell Invasion in Collagen Scaffold Architectures Characterized by Percolation Theory , 2015, Advanced healthcare materials.

[98]  Ugo Ripamonti,et al.  Osteoinductive hydroxyapatite-coated titanium implants. , 2012, Biomaterials.

[99]  K. Leong,et al.  Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. , 2003, Biomaterials.

[100]  M Bohner,et al.  Commentary: Deciphering the link between architecture and biological response of a bone graft substitute. , 2011, Acta biomaterialia.

[101]  R. Cameron,et al.  Quantitative architectural description of tissue engineering scaffolds , 2014 .

[102]  Alexander A Spector,et al.  Emergent patterns of growth controlled by multicellular form and mechanics. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[103]  Larry L. Hench,et al.  Analysis of pore interconnectivity in bioactive glass foams using X-ray microtomography , 2004 .

[104]  Pieter Buma,et al.  Anisotropic Porous Biodegradable Scaffolds for Musculoskeletal Tissue Engineering , 2009, Materials.

[105]  Benjamin M Wu,et al.  Recent advances in 3D printing of biomaterials , 2015, Journal of Biological Engineering.