Osteoconductive Performance of Carbon Nanotube Scaffolds Homogeneously Mineralized by Flow‐Through Electrodeposition

The treatment of bone lesions, including fractures, tumor resection and osteoporosis, is a common clinical practice where bone healing and repair are pursued. It is widely accepted that calcium phosphate-based materials improve integration of biomaterials with surrounding bone tissue and further serve as a template for proper function of bone-forming cells. Within this context, mineralization on preformed substrates appears as an interesting and successful alternative for mineral surface functionalization. However, mineralization of “true” 3D scaffolds –in which the magnitude of the third dimension is within the same scale as the other two– is by no means a trivial issue because of the diffi culty to obtain a homogeneous mineral layer deposited on the entire internal surface of the scaffold. Herein, a “fl ow-through” electrodeposition process is applied for mineralization of 3D scaffolds composed of multiwall carbon nanotubes and chitosan. It is demonstrated that, irrespective of the experimental conditions used for electrodeposition (e.g., time, temperature and voltages), the continuous feed of salts provided by the use of a fl ow-through confi guration is the main issue if one desires to coat the entire internal structure of 3D scaffolds with a homogeneous mineral layer. Finally, mineralized scaffolds not only showed a remarkable biocompatibility when tested with human osteoblast cells, but also enhanced osteoblast terminal differentiation (as early as 7 days in calcifying media).

[1]  Francisco del Monte,et al.  Multiwall carbon nanotube scaffolds for tissue engineering purposes. , 2008, Biomaterials.

[2]  Byung-Soo Kim,et al.  Poly(lactide-co-glycolide)/hydroxyapatite composite scaffolds for bone tissue engineering. , 2006, Biomaterials.

[3]  Stephen Mann,et al.  Fabrication of Graphene–Polymer Nanocomposites With Higher‐Order Three‐Dimensional Architectures , 2009 .

[4]  N. Kotov,et al.  Cell distribution profiles in three-dimensional scaffolds with inverted-colloidal-crystal geometry: modeling and experimental investigations. , 2005, Small.

[5]  Gautam Gupta,et al.  Fluorescent single-walled carbon nanotube aerogels in surfactant-free environments. , 2011, ACS nano.

[6]  P. Ma,et al.  Electrodeposition on Nanofibrous Polymer Scaffolds: Rapid Mineralization, Tunable Calcium Phosphate Composition and Topography , 2010, Advanced functional materials.

[7]  Jie Song,et al.  Mineralization of synthetic polymer scaffolds: a bottom-up approach for the development of artificial bone. , 2005, Journal of the American Chemical Society.

[8]  Eleftherios Tsiridis,et al.  Bone substitutes: an update. , 2005, Injury.

[9]  Andrew I. Cooper,et al.  Aligned two- and three-dimensional structures by directional freezing of polymers and nanoparticles , 2005, Nature materials.

[10]  Noam Eliaz,et al.  The effect of surface treatment on the surface texture and contact angle of electrochemically deposited hydroxyapatite coating and on its interaction with bone-forming cells. , 2009, Acta biomaterialia.

[11]  A. Naldoni,et al.  Electrochemically assisted deposition on TiO2 scaffold for Tissue Engineering: an apatite bio-inspired crystallization pathway , 2011 .

[12]  P. Fratzl,et al.  Size-controlled hydroxyapatite nanoparticles as self-organized organic-inorganic composite materials. , 2005, Biomaterials.

[13]  N. Sommerdijk,et al.  Biomimetic CaCO3 mineralization using designer molecules and interfaces. , 2008, Chemical reviews.

[14]  Jianfang Wang,et al.  Porous carbon and carbon/metal oxide microfibers with well-controlled pore structure and interface. , 2008, Journal of the American Chemical Society.

[15]  S. Mann Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry , 2002 .

[16]  A. Boccaccini,et al.  Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. , 2006, Biomaterials.

[17]  C. Mou,et al.  Solid-state NMR study of the transformation of octacalcium phosphate to hydroxyapatite: a mechanistic model for central dark line formation. , 2006, Journal of the American Chemical Society.

[18]  P. Walsh,et al.  Designs from the deep: marine organisms for bone tissue engineering. , 2011, Biotechnology advances.

[19]  T. Albrektsson,et al.  Osteoinduction, osteoconduction and osseointegration , 2001, European Spine Journal.

[20]  Miqin Zhang,et al.  Preparation of porous hydroxyapatite scaffolds by combination of the gel-casting and polymer sponge methods. , 2003, Biomaterials.

[21]  M. Horton,et al.  Adhesive properties of isolated chick osteocytes in vitro. , 1996, Bone.

[22]  W. Murphy,et al.  Mineral Coatings for Temporally Controlled Delivery of Multiple Proteins , 2011, Advanced materials.

[23]  L. Bonewald Osteocytes as Dynamic Multifunctional Cells , 2007, Annals of the New York Academy of Sciences.

[24]  Yong Xu,et al.  Pre-osteoblast infiltration and differentiation in highly porous apatite-coated PLLA electrospun scaffolds. , 2011, Biomaterials.

[25]  S. Mann,et al.  Morphosynthesis of Octacalcium Phosphate Hollow Microspheres by Polyelectrolyte-Mediated Crystallization , 2002 .

[26]  H. Tamon,et al.  Formation of monolithic silica gel microhoneycombs (SMHs) using pseudosteady state growth of microstructural ice crystals. , 2004, Chemical communications.

[27]  Jian Wang,et al.  Fluoridated hydroxyapatite coatings on titanium obtained by electrochemical deposition. , 2009, Acta biomaterialia.

[28]  Stephen Mann,et al.  Biomimetic Materials Chemistry , 1995 .

[29]  Amit Kumar,et al.  Ultralight multiwalled carbon nanotube aerogel. , 2010, ACS nano.

[30]  Changsong Dai,et al.  Fabrication of calcium phosphate/chitosan coatings on AZ91D magnesium alloy with a novel method , 2010 .

[31]  M. Gutiérrez,et al.  Three-dimensional microchanelled electrodes in flow-through configuration for bioanode formation and current generation , 2011 .

[32]  P. Ajayan,et al.  Three-dimensional carbon nanotube scaffolds as particulate filters and catalyst support membranes. , 2010, ACS nano.

[33]  S. Ejiri,et al.  Matrix Mineralization as a Trigger for Osteocyte Maturation , 2008, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[34]  N. Lane,et al.  Epidemiology, etiology, and diagnosis of osteoporosis. , 2006, American journal of obstetrics and gynecology.

[35]  M. Shirkhanzadeh Direct formation of nanophase hydroxyapatite on cathodically polarized electrodes , 1998, Journal of materials science. Materials in medicine.

[36]  Y. Leng,et al.  Electrochemical deposition of octacalcium phosphate micro-fiber/chitosan composite coatings on titanium substrates , 2008 .

[37]  F. Meldrum,et al.  Controlling mineral morphologies and structures in biological and synthetic systems. , 2008, Chemical reviews.

[38]  M. Antonietti,et al.  Polymer-Controlled Morphosynthesis and Mineralization of Metal Carbonate Superstructures (†). , 2003, The journal of physical chemistry. B.

[39]  Eduardo Saiz,et al.  Ice-templated porous alumina structures , 2007, 1710.04651.

[40]  Xiong Lu,et al.  The simulation of the electrochemical cathodic Ca–P deposition process , 2009 .

[41]  C. Hawker,et al.  Ice‐Templating of Core/Shell Microgel Fibers through ‘Bricks‐and‐Mortar’ Assembly** , 2007, Advanced Materials.

[42]  H. Benhayoune,et al.  Behavior of human osteoblast-like cells in contact with electrodeposited calcium phosphate coatings. , 2006, Journal of biomedical materials research. Part B, Applied biomaterials.

[43]  M. Gutiérrez,et al.  Ice-Templated Materials: Sophisticated Structures Exhibiting Enhanced Functionalities Obtained after Unidirectional Freezing and Ice-Segregation-Induced Self-Assembly† , 2008 .

[44]  Eduardo Saiz,et al.  Freezing as a Path to Build Complex Composites , 2006, Science.

[45]  M. Gutiérrez,et al.  Enzymatic Synthesis of Amorphous Calcium Phosphate−Chitosan Nanocomposites and Their Processing into Hierarchical Structures , 2008 .

[46]  María C. Gutiérrez,et al.  Macroporous 3D Architectures of Self-Assembled MWCNT Surface Decorated with Pt Nanoparticles as Anodes for a Direct Methanol Fuel Cell , 2007 .

[47]  Y. Mutoh,et al.  Electrochemical depositions of calcium phosphate film on commercial pure titanium and Ti–6Al–4V in two types of electrolyte at room temperature , 2009 .

[48]  P. Dove,et al.  Peptide Controls on Calcite Mineralization: Polyaspartate Chain Length Affects Growth Kinetics and Acts as a Stereochemical Switch on Morphology , 2006 .

[49]  J. L. López-Lacomba,et al.  Urea assisted hydroxyapatite mineralization on MWCNT/CHI scaffolds , 2008 .

[50]  X. Tao,et al.  Construction of a fluorescent nanostructured chitosan-hydroxyapatite scaffold by nanocrystallon induced biomimetic mineralization and its cell biocompatibility. , 2011, ACS applied materials & interfaces.

[51]  Thierry Balaguer,et al.  Human Primary Osteocyte Differentiation in a 3D Culture System , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[52]  M. Antonietti,et al.  Inorganic/Organic Mesostructures with Complex Architectures: Precipitation of Calcium Phosphate in the Presence of Double‐Hydrophilic Block Copolymers , 1998 .

[53]  M. Gutiérrez,et al.  Hydrogel Scaffolds with Immobilized Bacteria for 3D Cultures , 2007 .

[54]  M. Bohner,et al.  Technological issues for the development of more efficient calcium phosphate bone cements: a critical assessment. , 2005, Biomaterials.

[55]  L. Bonewald,et al.  Time Lapse Imaging Techniques for Comparison of Mineralization Dynamics in Primary Murine Osteoblasts and the Late Osteoblast/Early Osteocyte-Like Cell Line MLO-A5 , 2008, Cells Tissues Organs.

[56]  J. Klein-Nulend,et al.  Responses of Bone Cells to Biomechanical Forces in Vitro , 1999, Advances in dental research.

[57]  David F. Williams On the mechanisms of biocompatibility. , 2008, Biomaterials.

[58]  P. Atanassov,et al.  Conductive macroporous composite chitosan-carbon nanotube scaffolds. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[59]  S. Mallapragada,et al.  Synthesis and characterization of self-assembled block copolymer templated calcium phosphate nanocomposite gels , 2007 .

[60]  Heejoo Kim,et al.  Nanofiber Generation of Gelatin–Hydroxyapatite Biomimetics for Guided Tissue Regeneration , 2005 .

[61]  G. Pastorin,et al.  Thin films of functionalized multiwalled carbon nanotubes as suitable scaffold materials for stem cells proliferation and bone formation. , 2010, ACS Nano.

[62]  G. Pastorin,et al.  Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. , 2011, ACS nano.

[63]  Xiaoliang Cheng,et al.  Electrochemically assisted co-precipitation of protein with calcium phosphate coatings on titanium alloy. , 2004, Biomaterials.

[64]  J. Millán,et al.  The Appearance and Modulation of Osteocyte Marker Expression during Calcification of Vascular Smooth Muscle Cells , 2011, PloS one.

[65]  María J. Hortigüela,et al.  Biocompatible MWCNT scaffolds for immobilization and proliferation of E. coli , 2007 .

[66]  Eduardo Saiz,et al.  Bioactive glass scaffolds for bone tissue engineering: state of the art and future perspectives. , 2011, Materials science & engineering. C, Materials for biological applications.