Original Research Report
Doped tricalcium phosphate scaffolds by thermal decomposition of naphthalene: Mechanical properties and in vivo osteogenesis in a rabbit femur model
Dongxu Ke,
William Dernell,
Amit Bandyopadhyay,
Susmita Bose,
Dongxu Ke
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorWilliam Dernell
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorAmit Bandyopadhyay
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorCorresponding Author
Susmita Bose
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Correspondence to: S. Bose; e-mail: [email protected]Search for more papers by this authorDongxu Ke,
William Dernell,
Amit Bandyopadhyay,
Susmita Bose,
Dongxu Ke
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorWilliam Dernell
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorAmit Bandyopadhyay
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Search for more papers by this authorCorresponding Author
Susmita Bose
W. M. Keck Biomedical Materials Research Laboratory, School of Mechanical and Materials Engineering, Washington State University, Pullman, Washington, 99164-2920
Correspondence to: S. Bose; e-mail: [email protected]Search for more papers by this authorAbstract
Tricalcium phosphate (TCP) is a bioceramic that is widely used in orthopedic and dental applications. TCP structures show excellent biocompatibility as well as biodegradability. In this study, porous β-TCP scaffolds were prepared by thermal decomposition of naphthalene. Scaffolds with 57.64% ± 3.54% density and a maximum pore size around 100 μm were fabricated via removing 30% naphthalene at 1150°C. The compressive strength for these scaffolds was 32.85 ± 1.41 MPa. Furthermore, by mixing 1 wt % SrO and 0.5 wt % SiO2, pore interconnectivity improved, but the compressive strength decreased to 22.40 ± 2.70 MPa. However, after addition of polycaprolactone coating layers, the compressive strength of doped scaffolds increased to 29.57 ± 3.77 MPa. Porous scaffolds were implanted in rabbit femur defects to evaluate their biological property. The addition of dopants triggered osteoinduction by enhancing osteoid formation, osteocalcin expression, and bone regeneration, especially at the interface of the scaffold and host bone. This study showed processing flexibility to make interconnected porous scaffolds with different pore size and volume fraction porosity, while maintaining high compressive mechanical strength and excellent bioactivity. Results show that SrO/SiO2-doped porous TCP scaffolds have excellent potential to be used in bone tissue engineering applications. © 2014 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 103B: 1549–1559, 2015.
REFERENCES
- 1 Bose S, Tarafder S, Banerjee SS, Davies NM, Bandyopadhyay A. Understanding in vivo response and mechanical property variation in MgO, SrO and SiO2 doped beta-TCP. Bone 2011; 48: 1282–1290.
- 2 Yamada M, Shiota M, Yamashita Y, Kasugai S. Histological and histomorphometrical comparative study of the degradation and osteoconductive characteristics of α- and β-tricalcium phosphate in block grafts. J Biomed Mater Res Part B: Appl Biomater 2007; 82: 139–148.
- 3 Bai X, Sandukas S. Deposition and investigation of functionally graded calcium phosphate coatings on titanium. Acta Biomater 2009; 5: 3563–3572.
- 4 Ginebra MP, Espanol M. New processing approaches in calcium phosphate cements and their applications in regenerative medicine. Acta Biomater 2010; 6: 2863–2873.
- 5 Banerjee SS, Tarafder S, Davies NM, Bandyopadhyay A, Bose S. Understanding the influence of MgO and SrO binary doping on mechanical and biological properties of β-TCP ceramics. Acta Biomater 2010; 6: 4167–4174.
- 6 Götz HE, Müller M, Emmel A, Holzwarth U, Erben RG, Stangl R. Effect of surface finish on the osseointegration of laser-treated titanium alloy implants. Biomaterials 2004; 25: 4057–4064.
- 7 Kuboki Y, Jin Q, Takita H. Geometry of carriers controlling phenotypic expression in BMP-induced osteogenesis and chondrogenesis. J Bone Joint Surg Am 2001; 83(Suppl 1): S105–S115.
- 8 Xue W, Krishna BV, Bandyopadhyay A, Bose S. Processing and biocompatibility evaluation of laser processed porous titanium. Acta Biomater 2007; 3: 1007–1018.
- 9 Holy CE, Shoichet MS, Davies JE. Engineering three-dimensional bone tissue in vitro using biodegradable scaffolds: Investigating initial cell-seeding density and culture period. J Biomed Mater Res 2000; 51: 376–382.
- 10 Hulbert SF, Young FA, Mathews RS, Klawitter JJ, Talbert CD, Stelling FH. Potential of ceramic materials as permanently implantable skeletal prostheses. J Biomed Mater Res 1970; 4: 433–456.
- 11 Tarafder S, Balla VK, Davies NM, Bandyopadhyay A, Bose S. Microwave-sintered 3D printed tricalcium phosphate scaffolds for bone tissue engineering. J Tissue Eng Regen Med 2012; 7: 631–641.
- 12 Kalita SJ, Bose S, Hosick HL, Bandyopadhyay A. Development of controlled porosity polymer-ceramic composite scaffolds via fused deposition modeling. Mater Sci Eng C 2003; 23: 611–620.
- 13 Bose S, Darsell J, Kintner M, Hosick H, Bandyopadhyay A. Pore size and pore volume effects on alumina and TCP ceramic scaffolds. Mater Sci Eng C 2003; 23: 479–486.
- 14 Kim M, Park IH, Song HY, Min YK, Lee BT. Fabrication and characterization of strengthened BCP scaffold through infiltration of PCL in the frame. Bioceram Dev Appl 2011; 1: 1–4.
- 15 Xue W, Bandyopadhyay A, Bose S. Polycaprolactone coated porous tricalcium phosphate scaffolds for controlled release of protein for tissue engineering. J Biomed Mater Res Part B: Appl Biomater 2009; 91: 831–838.
- 16 Chang H, Lau YC, Yan C, Coombes AGA. Controlled release of an antibiotic, gentamicin sulphate, from gravity spun polycaprolactone fibers. J Biomed Mater Res Part A 2008; 84: 230–237.
- 17 Izquierdo R, Garcia-Giralt N, Rodriguez MT, Caceres E, Garcia SJ, Gomez RJL, Monleon M, Monllau JC, Suay J. Biodegradable PCL scaffolds with an interconnected spherical pore network for tissue engineering. J Biomed Mater Res Part A 2008; 85: 25–35.
- 18 Li WJ, Danielson KG, Alexander PG, Tuan RS. Biological response of chondrocytes cultured in three-dimensional nanofibrous poly(epsilon-caprolactone) scaffolds. J Biomed Mater Res Part A 2003; 67: 1105–1114.
- 19 Rai B, Oest ME, Dupont KM, Ho KH, Teoh SH, Guldberg RE. Combination of platelet-rich plasma with polycaprolactone-tricalcium phosphate scaffolds for segmental bone defect repair. J Biomed Mater Res Part A 2007; 81: 888–899.
- 20 Swieszkowski W, Tuan BHS, Kurzydlowski KJ, Hutmacher DW. Repair and regeneration of osteochondral defects in the articular joints. Biomol Eng 2007; 24: 489–495.
- 21 Rai B, Teoh SH, Hutmacher DW, Cao T, Ho KH. Novel PCL-based honeycomb scaffolds as drug delivery systems for rhBMP-2. Biomaterials 2005; 26: 3739–3748.
- 22 Bezwada RS, Jamiolkowski DD, Lee IY, Agarwal V, Trenka-Benthin S, Erneta M, Suryadevara J, Yang A, Liu S. Monocryl suture, a new ultra-pliable absorbable monofilament suture. Biomaterials 1995; 16: 1141–1148.
- 23 Darney PD, Monroe SE, Klaisle CM, Alvarado A. Clinical evaluation of the Capronor contraceptive implant: Preliminary report. Am J Obstet Gynecol 1989; 160: 1292–1295.
- 24 Bose S, Darsell J, Hosick HL, Yang L, Sarkar DK, Bandyopadhyay A. Processing and characterization of porous alumina scaffolds. J Mater Sci Mater Med 2002; 13: 23–28.
- 25 Bose S, Suguira S, Bandyopadhyay A. Processing of controlled porosity ceramic structures via fused deposition. Scripta Materialia 1999; 41: 1009–1014.
- 26 Fielding GA, Bandyopadhyay A, Bose S. Effects of silica and zinc oxide doping on mechanical and biological properties of 3D printed tricalcium phosphate tissue engineering scaffolds. Dent Mater 2012; 28, 113–122.
- 27 McCullen SD, Zhu Y, Bernacki SH, Narayan RJ, Pourdeyhimi B, Gorga RE, Loboa EG. Electrospun composite poly(l-lactic acid)/tricalcium phosphate scaffolds induce proliferation and osteogenic differentiation of human adipose-derived stem cells. Biomed Mater 2009; 4: 035002.
- 28 Macchetta A, Turner IG, Bowen CR. Fabrication of HA/TCP scaffolds with a graded and porous structure using a camphene-based freeze-casting method. Acta Biomater 2009; 5: 1319–1327.
- 29 Bohner M, Van Lenthe GH, Grünenfelder S, Hirsiger W, Evison R, Müller R. Synthesis and characterization of porous beta-tricalcium phosphate blocks. Biomaterials 2005; 26: 6099–6105.
- 30 Lin K, Chang J, Zeng Y, Qian W. Preparation of macroporous calcium silicate ceramics. Mater Lett 2004; 58: 2109–2113.
- 31 Wang C, Kasuga T, Nogami M. Macroporous calcium phosphate glass-ceramic prepared by two-step pressing technique and using sucrose as a pore former. J Mater Sci Mater Med 2005; 16: 739–744.
- 32 Pecqueux F, Tancret F, Payraudeau N, Bouler JM. Influence of microporosity and macroporosity on the mechanical properties of biphasic calcium phosphate bioceramics: Modelling and experiment. J Eur Ceram Soc 2010; 30: 819–829.
- 33 Tancret F, Bouler JM, Chamousset J, Minois LM. Modelling the mechanical properties of microporous and macroporous biphasic calcium phosphate bioceramics. J Eur Ceram Soc 2006; 26: 3647–3656.
- 34 Banerjee SS, Tarafder S, Davies NM, Bandyopadhyay A, Bose S. Understanding the influence of MgO and SrO binary doping on the mechanical and biological properties of beta-TCP ceramics. Acta Biomater 2010; 6: 4167–4174.
- 35 Canalis E, Hott M, Deloffre P, Tsouderos Y, Marie PJ. The divalent strontium salt S12911 enhances bone cell replication and bone formation in vitro. Bone 1996; 18: 517–523.
- 36 Hashizume M, Yamaguchi M. Stimulatory effect of beta-alanyl-l-histidinato zinc on cell proliferation is dependent on protein synthesis in osteoblastic MC3T3-E1 cells. Mol Cell Biochem 1993; 122: 59–64.
- 37 Xue W, Dahlquist K, Banerjee A, Bandyopadhyay A, Bose S. Synthesis and characterization of tricalcium phosphate with Zn and Mg based dopants. J Mater Sci Mater Med 2008; 19: 2669–2677.
- 38 Bandyopadhyay A, Bernard S, Xue W, Bose S. Calcium phosphate-based resorbable ceramics: Influence of MgO, ZnO, and SiO2 dopants. J Am Ceram Soc 2006; 89: 2675–2688.
- 39 Gomes PS, Botelho C, Lopes MA, Santos JD, Fernandes MH. Effect of silicon-containing hydroxyapatite coatings on the human in vitro osteoblastic response. Bone 2009; 44: S267.
- 40 Jones JR, Tsigkou O, Coates EE, Stevens MM, Polak JM, Hench LL. Extracellular matrix formation and mineralization on a phosphate-free porous bioactive glass scaffold using primary human osteoblast (HOB) cells. Biomaterials 2007; 28: 1653–1663.
- 41 Reffitt DM, Ogston N, Jugdaohsingh R, Cheung HFJ, Evans BAJ, Thompson RPH, Powell JJ, Hampson GN. Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 2003; 32: 127–135.
- 42 Yin X, Calderin L, Stott MJ, Sayer M. Density functional study of structural, electronic and vibrational properties of Mg- and Zn-doped tricalcium phosphate biomaterials. Biomaterials 2002; 23: 4155–4163.
- 43 Bandyopadhyay A, Petersen J, Fielding G, Banerjee S, Bose S. ZnO, SiO2 and SrO doping in resorbable tricalcium phosphates: Influence on strength degradation, mechanical properties, and in vitro bone-cell material interactions. J Biomed Mater Res Part B: Appl Biomater 2012; 100: 2203–2212.
- 44 Pattanayak DK, Dash R, Prasad RC, Rao BT, Rama Mohan TR. Synthesis and sintered properties evaluation of calcium phosphate ceramics. Mater Sci Eng C 2007; 27: 684–690.
- 45 Le Huec JC, Schaeverbeke T, Clement D, Faber J, Le Rebeller A. Influence of porosity on the mechanical resistance of hydroxyapatite ceramics under compressive stress. Biomaterials 1995; 16: 113–118.
- 46 Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005; 26: 5474–5491.
- 47 Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000; 21: 2529–2543.
- 48 Perera FH, Martínez-Vázquez FJ, Miranda P, Ortiz AL, Pajares A. Clarifying the effect of sintering conditions on the microstructure and mechanical properties of β-tricalcium phosphate. Ceram Int 2010; 36: 1929–1935.
- 49 Ryu HS, Youn HJ, Sun Hong K, Chang BS, Lee CK, Chung SS. An improvement in sintering property of β-tricalcium phosphate by addition of calcium pyrophosphate. Biomaterials 2002; 23: 909–914.
- 50 Ng CS, Teoh SH, Chung TS, Hutmacher DW. Simultaneous biaxial drawing of poly (εϵ-caprolactone) films. Polymer 2000; 41: 5855–5864.
- 51 Sims NA, Gooi JH. Bone remodeling: Multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 2008; 19: 444–451.
- 52 Tarafder S, Davies NM, Bandyopadhyay A, Bose S. 3D printed tricalcium phosphate bone tissue engineering scaffolds: Effect of SrO and MgO doping on in vivo osteogenesis in a rat distal femoral defect model. Biomater Sci 2013; 1: 1250–1259.
- 53 Glover SJ, Eastell R, McCloskey EV, Rogers A, Garnero P, Lowery J, Belleli R, Wright TM, John MR. Rapid and robust response of biochemical markers of bone formation to teriparatide therapy. Bone 2009; 45: 1053–1058.
- 54 Swaminathan R. Biochemical markers of bone turnover. Clin Chim Acta 2001; 313: 95–105.
- 55 Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L. Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling. Stem Cells 2011; 29: 981–991.
- 56 Bjerre L, Bunger CE, Kassem M, Mygind T. Flow perfusion culture of human mesenchymal stem cells on silicate-substituted tricalcium phosphate scaffolds. Biomaterials 2008; 29; 2616–2627.
- 57 Gupta G, Kirakodu S, El-Ghannam A. Effects of exogenous phosphorus and silicon on osteoblast differentiation at the interface with bioactive ceramics. J Biomed Mater Res Part A 2010; 95: 882–890.
- 58 Obata A, Tokuda S, Kasuga T. Enhanced in vitro cell activity on silicon-doped vaterite/poly(lactic acid) composites. Acta Biomater 2009; 5: 57–62.
- 59 Matsko NB, Znidarsic N, Letofsky-Papst I, Dittrich M, Grogger W, Strus J, Hofer F. Silicon: The key element in early stages of biocalcification. J Struct Biol 2011; 174: 180–186.
