Hydrothermal processing of 3D-printed calcium phosphate scaffolds enhances bone formation in vivo: a comparison with biomimetic treatment

C.L. Ventola, Medical applications for 3D printing: current and projected uses., P T. 39 (2014) 704–11. http://www.ncbi.nlm.nih.gov/pubmed/25336867. Hidalgo, 1989, Fibula free flap: a new method of mandible reconstruction, Plast. Reconstr. Surg., 84, 71, 10.1097/00006534-198907000-00014 Sen, 2007, Autologous iliac crest bone graft: Should it still be the gold standard for treating nonunions?, Injury, 38, S75, 10.1016/j.injury.2007.02.012 Felice, 2009, Vertical ridge augmentation of the atrophic posterior mandible with interpositional bloc grafts: bone from the iliac crest vs. bovine anorganic bone. Clinical and histological results up to one year after loading from a randomized-controlled clinical tria, Clin. Oral Implants Res., 20, 1386, 10.1111/j.1600-0501.2009.01765.x Parthasarathy, 2014, 3D modeling, custom implants and its future perspectives in craniofacial surgery, Ann. Maxillofac. Surg., 4, 9, 10.4103/2231-0746.133065 Mobbs, 2017, The utility of 3D printing for surgical planning and patient-specific implant design for complex spinal pathologies: case report, J. Neurosurg. Spine, 26, 513, 10.3171/2016.9.SPINE16371 Saijo, 2009, Maxillofacial reconstruction using custom-made artificial bones fabricated by inkjet printing technology, J. Artif. Organs., 12, 200, 10.1007/s10047-009-0462-7 Cesarano, 2005, Customization of load-bearing hydroxyapatite lattice scaffolds, Int. J. Appl. Ceram. Technol., 2, 212, 10.1111/j.1744-7402.2005.02026.x Tack, 2016, 3D-printing techniques in a medical setting: a systematic literature review, Biomed. Eng. Online, 15, 115, 10.1186/s12938-016-0236-4 Martelli, 2016, Advantages and disadvantages of 3-dimensional printing in surgery: a systematic review, Surgery, 159, 1485, 10.1016/j.surg.2015.12.017 J.C. Banwart, M.A. Asher, R.S. Hassanein, Iliac crest bone graft harvest donor site morbidity, Spine (Phila. Pa. 1976). 20 (1995) 1055–1060. doi:10.1097/00007632-199505000-00012. Anthony, 1995, Donor leg morbidity and function after fibula free flap mandible reconstruction, Plast. Reconstr. Surg., 96, 146, 10.1097/00006534-199507000-00022 Lewis, 2004, Direct writing in three dimensions, Mater. Today, 7, 32, 10.1016/S1369-7021(04)00344-X Miranda, 2006, Sintering and robocasting of β-tricalcium phosphate scaffolds for orthopaedic applications, Acta Biomater., 2, 457, 10.1016/j.actbio.2006.02.004 Franco, 2010, Direct write assembly of calcium phosphate scaffolds using a water-based hydrogel, Acta Biomater., 6, 218, 10.1016/j.actbio.2009.06.031 Marques, 2017, Biphasic calcium phosphate scaffolds fabricated by direct write assembly: mechanical, anti-microbial and osteoblastic properties, J. Eur. Ceram. Soc., 37, 359, 10.1016/j.jeurceramsoc.2016.08.018 Vallet-Regí, 2004, Calcium phosphates as substitution of bone tissues, Prog. Solid State Chem., 32, 1, 10.1016/j.progsolidstchem.2004.07.001 Lode, 2014, Fabrication of porous scaffolds by three-dimensional plotting of a pasty calcium phosphate bone cement under mild conditions, J. Tissue Eng. Regen. Med., 8, 682, 10.1002/term.1563 Maazouz, 2014, Robocasting of biomimetic hydroxyapatite scaffolds using self-setting inks, J. Mater. Chem. B, 2, 5378, 10.1039/C4TB00438H Sadowska, 2017, Biomimetic versus sintered calcium phosphates: the in vitro behavior of osteoblasts and mesenchymal stem cells, Tissue Eng. Part A, 23, 10.1089/ten.tea.2016.0406 Ginebra, 1997, Setting reaction and hardening of an apatitic calcium phosphate cement, J. Dent. Res., 76, 905, 10.1177/00220345970760041201 Ginebra, 2018, Bioceramics and bone healing, EFORT Open Rev., 3, 173, 10.1302/2058-5241.3.170056 Carrel, 2016, Large bone vertical augmentation using a three-dimensional printed TCP/HA bone graft: a pilot study in dog mandible, Clin. Implant Dent. Relat. Res., 18, 1183, 10.1111/cid.12394 Carrel, 2016, A 3D printed TCP/HA structure as a new osteoconductive scaffold for vertical bone augmentation, Clin. Oral Implants Res., 27, 55, 10.1111/clr.12503 Diloksumpan, 2020, Orthotopic bone regeneration within 3D printed bioceramic scaffolds with region-dependent porosity gradients in an equine model, Adv. Healthc. Mater., 1901807, 1 Vidal, 2020, Regeneration of segmental defects in metatarsus of sheep with vascularized and customized 3D-printed calcium phosphate scaffolds, Sci. Rep., 10, 7068, 10.1038/s41598-020-63742-w Barba, 2018, Osteogenesis by foamed and 3D-printed nanostructured calcium phosphate scaffolds: effect of pore architecture, Acta Biomater., 79, 135, 10.1016/j.actbio.2018.09.003 Ahlfeld, 2021, Toward biofabrication of resorbable implants consisting of a calcium phosphate cement and fibrin—a characterization in vitro and in vivo, Int. J. Mol. Sci., 22, 1218, 10.3390/ijms22031218 Akkineni, 2015, 3D plotting of growth factor loaded calcium phosphate cement scaffolds, Acta Biomater., 10.1016/j.actbio.2015.08.036 Ahlfeld, 2017, Design and Fabrication of complex scaffolds for bone defect healing: combined 3D plotting of a calcium phosphate cement and a growth factor-loaded hydrogel, Ann. Biomed. Eng., 45, 224, 10.1007/s10439-016-1685-4 Galea, 2015, Textured and hierarchically structured calcium phosphate ceramic blocks through hydrothermal treatment, Biomaterials, 67, 93, 10.1016/j.biomaterials.2015.07.026 Murakami, 2012, Hydrothermal synthesis of porous hydroxyapatite ceramics composed of rod-shaped particles and evaluation of their fracture behavior, Ceram. Int., 38, 1649, 10.1016/j.ceramint.2011.09.056 Raymond, 2018, Accelerated hardening of nanotextured 3D-plotted self-setting calcium phosphate inks, Acta Biomater., 75, 451, 10.1016/j.actbio.2018.05.042 Barba, 2017, Osteoinduction by foamed and 3D-Printed calcium phosphate scaffolds: effect of nanostructure and pore architecture, ACS Appl. Mater. Interfaces, 9, 41722, 10.1021/acsami.7b14175 Barba, 2019, Impact of biomimicry in the design of osteoinductive bone substitutes: nanoscale matters, ACS Appl. Mater. Interfaces, 11, 8818, 10.1021/acsami.8b20749 Davison, 2014, Submicron-scale surface architecture of tricalcium phosphate directs osteogenesis in vitro and in vivo, Eur. Cells Mater., 27, 281, 10.22203/eCM.v027a20 Duan, 2016, Submicron-surface structured tricalcium phosphate ceramic enhances the bone regeneration in canine spine environment, J. Orthop. Res., 34, 1865, 10.1002/jor.23201 Raymond, 2021, 3D printing non-cylindrical strands: morphological and structural implications, Addit. Manuf., 46 Westphal, 2009, Rietveld quantification of amorphous portions with an internal standard—Mathematical consequences of the experimental approach, Powder Diffr., 24, 239, 10.1154/1.3187828 PANalytical B.V., X'Pert HighScore Plus Help System Version 3.0. Operations Manual, 2009. Caglioti, 1958, Choice of collimators for a crystal spectrometer for neutron diffraction, Nucl. Instrum., 3, 223, 10.1016/0369-643X(58)90029-X Rueden, 2017, ImageJ2: ImageJ for the next generation of scientific image data, BMC Bioinf., 18, 529, 10.1186/s12859-017-1934-z Fedorov, 2012, 3D slicer as an image computing platform for the quantitative imaging network, Magn. Reson. Imag., 30, 1323, 10.1016/j.mri.2012.05.001 International Organization for Standardization, 14704:2016 Fine ceramics (advanced ceramics, advanced technical ceramics) — Test method for flexural strength of monolithic ceramics at room temperature, 2016. Gustavsson, 2011, Ion reactivity of calcium-deficient hydroxyapatite in standard cell culture media, Acta Biomater, 7, 4242, 10.1016/j.actbio.2011.07.016 Sadowska, 2018, In vitro response of mesenchymal stem cells to biomimetic hydroxyapatite substrates: a new strategy to assess the effect of ion exchange, Acta Biomater., 76, 319, 10.1016/j.actbio.2018.06.025 2011 Bishop, 2005 Gonzalez, 2018 Koutsopoulos, 2002, Synthesis and characterization of hydroxyapatite crystals: A review study on the analytical methods, J. Biomed. Mater. Res., 62, 600, 10.1002/jbm.10280 Markovic, 2004, Preparation and comprehensive characterization of a calcium hydroxyapatite reference material, J. Res. Natl. Inst. Stand. Technol., 109, 553, 10.6028/jres.109.042 Rodríguez-Lorenzo, 2000, Controlled crystallization of calcium phosphate apatites, Chem. Mater., 12, 2460, 10.1021/cm001033g Wei, 2007, Hydrolysis of α-tricalcium phosphate in simulated body fluid and dehydration behavior during the drying process, J. Am. Ceram. Soc., 90, 2315, 10.1111/j.1551-2916.2007.01682.x Rey, 2009, Bone mineral: update on chemical composition and structure, Osteoporos. Int., 20, 1013, 10.1007/s00198-009-0860-y Drouet, 2013, Apatite formation: why it may not work as planned, and how to conclusively identify apatite compounds, Biomed Res. Int., 2013, 1, 10.1155/2013/490946 Espanol, 2010, Investigation of the hydroxyapatite obtained as hydrolysis product of α-tricalcium phosphate by transmission electron microscopy, CrystEngComm, 12, 3318, 10.1039/c001754j Yoshimura, 1994, Hydrothermal synthesis of biocompatible whiskers, J. Mater. Sci., 29, 3399, 10.1007/BF00352039 Ioku, 1998, Hydrothermal Preparation of Porous Hydroxyapatite Ceramics, Rev. HIGH Press. Sci. Technol., 7, 1398, 10.4131/jshpreview.7.1398 Ioku, 2006, Hydrothermal preparation of tailored hydroxyapatite, J. Mater. Sci., 41, 1341, 10.1007/s10853-006-7338-5 Ginebra, 2004, Effect of the particle size on the micro and nanostructural features of a calcium phosphate cement: a kinetic analysis, Biomaterials, 25, 3453, 10.1016/j.biomaterials.2003.10.049 Pastorino, 2015, Multiple characterization study on porosity and pore structure of calcium phosphate cements, Acta Biomater., 28, 205, 10.1016/j.actbio.2015.09.017 Espanol, 2009, Intrinsic porosity of calcium phosphate cements and its significance for drug delivery and tissue engineering applications, Acta Biomater., 5, 2752, 10.1016/j.actbio.2009.03.011 Escobar-Chávez, 2006, Applications of thermo-reversible pluronic F-127 gels in pharmaceutical formulations, J. Pharm. Pharm. Sci., 9, 339 Abdeljawad, 2019, Sintering processes in direct ink write additive manufacturing: a mesoscopic modeling approach, Acta Mater., 169, 60, 10.1016/j.actamat.2019.01.011 Nommeots-nomm, 2018, Journal of the european ceramic society direct ink writing of highly bioactive glasses, J. Eur. Ceram. Soc., 38, 837, 10.1016/j.jeurceramsoc.2017.08.006 Fernández, 1995, Dimensional and thermal behaviour of calcium phosphate cements during setting compared to PMMA bone cements, J. Mater. Sci. Lett., 14, 4, 10.1007/BF02565267 Raja, 2021, Low-temperature fabrication of calcium deficient hydroxyapatite bone scaffold by optimization of 3D printing conditions, Ceram. Int., 47, 7005, 10.1016/j.ceramint.2020.11.051 Montufar, 2020, Factors governing the dimensional accuracy and fracture modes under compression of regular and shifted orthogonal scaffolds, J. Eur. Ceram. Soc., 40, 4923, 10.1016/j.jeurceramsoc.2020.03.045 Cesarano, 1998, A review of robocasting technology, MRS Proc., 542, 133, 10.1557/PROC-542-133 Eqtesadi, 2018, Fabricating geometrically-complex B4C ceramic components by robocasting and pressureless spark plasma sintering (DOI MALAMENT REVISAR), Scr. Mater., 145, 14, 10.1016/j.scriptamat.2017.10.001 Houmard, 2013, On the structural, mechanical, and biodegradation properties of HA/β-TCP robocast scaffolds, J. Biomed. Mater. Res. Part B Appl. Biomater., 101, 1233, 10.1002/jbm.b.32935 Á.D.E. Pablos, M. Belmonte, M.I. Osendi, P. Miranzo, Cerámica y Vidrio microstructural designs of spark-plasma sintered silicon carbide ceramic scaffolds, 53 (2014) 93–100. doi:10.3989/cyv.132014. Feilden, 2017 Sadowska, 2018, Effect of nano-structural properties of biomimetic hydroxyapatite on osteoimmunomodulation, Biomaterials, 181, 318, 10.1016/j.biomaterials.2018.07.058 Habibovic, 2005, 3D microenvironment as essential element for osteoinduction by biomaterials, Biomaterials, 26, 3565, 10.1016/j.biomaterials.2004.09.056 Ciapetti, 2017, Osteoclast differentiation from human blood precursors on biomimetic calcium-phosphate substrates, Acta Biomater, 50, 102, 10.1016/j.actbio.2016.12.013 GUO, 2009, Biocompatibility and osteogenicity of degradable Ca-deficient hydroxyapatite scaffolds from calcium phosphate cement for bone tissue engineering, Acta Biomater, 5, 268, 10.1016/j.actbio.2008.07.018 Ambrosio, 2012, Injectable calcium-phosphate-based composites for skeletal bone treatments, Biomed. Mater., 7, 10.1088/1748-6041/7/2/024113 Diez-Escudero, 2017, In vitro degradation of calcium phosphates: Effect of multiscale porosity, textural properties and composition, Acta Biomater., 60, 81, 10.1016/j.actbio.2017.07.033 Gallinetti, 2014, Development and characterization of biphasic hydroxyapatite/β- <scp>TCP</scp>Cements, J. Am. Ceram. Soc., 97, 1065, 10.1111/jace.12861 Duan, 2019, Accelerated bone formation by biphasic calcium phosphate with a novel sub-micron surface topography, Eur. Cells Mater., 37, 60, 10.22203/eCM.v037a05 Davison, 2015, Influence of surface microstructure and chemistry on osteoinduction and osteoclastogenesis by biphasic calcium phosphate discs, Eur. Cells Mater., 29, 314, 10.22203/eCM.v029a24 Roohani-Esfahani, 2010, The influence hydroxyapatite nanoparticle shape and size on the properties of biphasic calcium phosphate scaffolds coated with hydroxyapatite–PCL composites, Biomaterials, 31, 5498, 10.1016/j.biomaterials.2010.03.058 Rustom, 2016, Micropore-induced capillarity enhances bone distribution in vivo in biphasic calcium phosphate scaffolds, Acta Biomater., 44, 144, 10.1016/j.actbio.2016.08.025 Lan Levengood, 2010, Multiscale osteointegration as a new paradigm for the design of calcium phosphate scaffolds for bone regeneration, Biomaterials, 31, 3552, 10.1016/j.biomaterials.2010.01.052 Benesch, 2008, Proteins and their peptide motifs in acellular apatite mineralization of scaffolds for tissue engineering, Tissue Eng. Part B Rev., 14, 433, 10.1089/ten.teb.2008.0121