Akermanite reinforced PHBV scaffolds manufactured using selective laser sintering
Sven H. Diermann
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorMingyuan Lu
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorMatthew Dargusch
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorCorresponding Author
Lisbeth Grøndahl
School of Chemistry and Molecular Biosciences, The University of Queensland, Queensland, Australia
Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Queensland, Australia
Correspondence to: L. Grøndahl; e-mail: [email protected]; or H. Huang; e-mail: [email protected]Search for more papers by this authorCorresponding Author
Han Huang
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Correspondence to: L. Grøndahl; e-mail: [email protected]; or H. Huang; e-mail: [email protected]Search for more papers by this authorSven H. Diermann
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorMingyuan Lu
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorMatthew Dargusch
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Search for more papers by this authorCorresponding Author
Lisbeth Grøndahl
School of Chemistry and Molecular Biosciences, The University of Queensland, Queensland, Australia
Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Queensland, Australia
Correspondence to: L. Grøndahl; e-mail: [email protected]; or H. Huang; e-mail: [email protected]Search for more papers by this authorCorresponding Author
Han Huang
School of Mechanical and Mining Engineering, The University of Queensland, Queensland, Australia
Correspondence to: L. Grøndahl; e-mail: [email protected]; or H. Huang; e-mail: [email protected]Search for more papers by this authorAbstract
Scaffold assisted tissue engineering presents a promising approach to repair diseased and fractured bone. For successful bone repair, scaffolds need to be made of biomaterials that degrade with time and promote osteogenesis. Compared to the commonly used ß-tricalcium phosphate scaffolds, Akermanite (AKM) scaffolds were found to degrade faster and promote more osteogenesis. The objective of this study is to synthesize AKM micro and nanoparticle reinforced poly(3-hydroxybutyrate-co-3-hydroxyvalerate; PHBV) composite scaffolds using selective laser sintering (SLS). The synthesized composite scaffolds had an interconnected porous microstructure (61–64% relative porosity), large specific surface areas (31.1–64.2 mm−1) and pore sizes ranging from 303 to 366 and 279 to 357 μm in the normal and lateral direction, respectively, which are suitable for bone tissue repair. The observed hydrophilic nature of the scaffolds and the swift water uptake was due to the introduction of numerous carboxylic acid groups on the scaffold surface after SLS, circumventing the need for postprocessing. For the composite scaffolds, large amounts of AKM particles were exposed on the skeleton surface, which is a requirement for cell attachment. In addition, the particles embedded inside the skeleton helped to significantly reinforce the scaffold structure. The compressive strength and modulus of the composite scaffolds were up to 7.4 and 103 MPa, respectively, which are 149 and 197% of that of the pure PHBV scaffolds. © 2019 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater 107B:2596–2610, 2019.
REFERENCES
- 1Poh PSP, Hutmacher DW, Holzapfel BM, Solanki AK, Stevens MM, Woodruff MA. In vitro and in vivo bone formation potential of surface calcium phosphate-coated polycaprolactone and polycaprolactone/bioactive glass composite scaffolds. Acta Biomater 2016; 30: 319–333.
- 2Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006; 27(18): 3413–3431.
- 3O'Brien FJ. Biomaterials and scaffolds for tissue engineering. Mater Today 2011; 14(3): 88–95.
- 4Smith MH, Flanagan CL, Kemppainen JM, Sack JA, Chung H, Das S, Hollister SJ, Feinberg SE. Computed tomographybased tissue-engineered scaffolds in craniomaxillofacial surgery. Int J Med Robot 2007; 3(3): 207–216.
- 5Mazzoli A. Selective laser sintering in biomedical engineering. Med Biol Eng Comput 2013; 51(3): 245–256.
- 6Chia HN, Wu BM. Recent advances in 3D printing of biomaterials. J Biol Eng 2015; 9(1): 1–14.
- 7Chua CK, Yeong WY, An J. Special issue: 3D printing for biomedical engineering. Materials 2017; 10, 243.
- 8Chen L, Zhai D, Wu C, Chang J. Poly(d, l-lactic)-reinforced Akermanite bioceramic scaffolds: Preparation and characterization. Ceram Int 2014; 40(8, Part B): 12765–12775.
- 9Kim H-W, Knowles JC, Kim H-E. Hydroxyapatite/polycaprolactone composite coatings on hydroxyapatite porous bone scaffold for drug delivery. Biomaterials 2004; 25(7): 1279–1287.
- 10Shirazi SFS, Gharehkhani S, Mehrali M, Yarmand H, Metselaar HSC, Kadri NA, Osman NAA. A review on powder-based additive manufacturing for tissue engineering: Selective laser sintering and inkjet 3D printing. Sci Technol Adv Mater 2015; 16(3): 1–20.
- 11Partee B, Hollister SJ, Das S. Selective laser sintering process optimization for layered manufacturing of CAPA 6501 polycaprolactone bone tissue engineering scaffolds. J Manuf Sci Eng 2005; 128(2): 531–540. https://doi.org/10.1115/1.2162589.
- 12Eshraghi S, Das S. Mechanical and microstructural properties of polycaprolactone scaffolds with one-dimensional, twodimensional, and three-dimensional orthogonally oriented porous architectures produced by selective laser sintering. Acta Biomater 2010; 6(7): 2467–2476.
- 13Eshraghi S, Das S. Micromechanical finite-element modeling and experimental characterization of the compressive mechanical properties of polycaprolactone-hydroxyapatite composite scaffolds prepared by selective laser sintering for bone tissue engineering. Acta Biomater 2012; 8(8): 3138–3143.
- 14Wiria FE, Leong KF, Chua CK, Liu Y. Poly-epsilon-caprolactone/hydroxyapatite for tissue engineering scaffold fabrication via selective laser sintering. Acta Biomater 2007; 3(1): 1–12.
- 15Yeong WY, Sudarmadji N, Yu HY, Chua CK, Leong KF, Venkatraman SS, Boey YCF, Tan LP. Porous polycaprolactone scaffold for cardiac tissue engineering fabricated by selective laser sintering. Acta Biomater 2010; 6(6): 2028–2034.
- 16Chua CK, Leong KF, Sudarmadji N, Liu MJJ, Chou SM. Selective laser sintering of functionally graded tissue scaffolds. MRS Bull 2011; 36(12): 1006–1014.
- 17Sudarmadji N, Tan JY, Leong KF, Chua CK, Loh YT. Investigation of the mechanical properties and porosity relationships in selective laser-sintered polyhedral for functionally graded scaffolds. Acta Biomater 2011; 7(2): 530–537.
- 18S. Eosoly. Selective laser sintering of polycaprolactone/bioceramic composite bone scaffolds, Dublin, Republic of Ireland University: Dublin City University. PhD dissertation, 2009.
- 19Eosoly S, Brabazon D, Lohfeld S, Looney L. Selective laser sintering of hydroxyapatite/poly-epsilon-caprolactone scaffolds. Acta Biomater 2010; 6(7): 2511–2517.
- 20Eosoly S, Vrana NE, Lohfeld S, Hindie M, Looney L. Interaction of cell culture with composition effects on the mechanical properties of polycaprolactone-hydroxyapatite scaffolds fabricated via selective laser sintering (SLS). Mater Sci Eng C 2012; 32(8): 2250–2257.
- 21Lohfeld S, Tyndyk MA, Cahill S, Flaherty N, Barron V, McHugh PE. A method to fabricate small features on scaffolds for tissue engineering via selective laser sintering. J Biomed Sci Eng 2010; 3(2): 138–147.
10.4236/jbise.2010.32019 Google Scholar
- 22Lohfeld S, Cahill S, Barron V, McHugh P, Dürselen L, Kreja L, Bausewein C, Ignatius A. Fabrication, mechanical and in vivo performance of polycaprolactone/tricalcium phosphate composite scaffolds. Acta Biomater 2012; 8(9): 3446–3456.
- 23Lohfeld S, Cahill S, Doyle H, McHugh PE. Improving the finite element model accuracy of tissue engineering scaffolds produced by selective laser sintering. J Mater Sci Mater Med 2015; 26(1): 1–12.
- 24Doyle H, Lohfeld S, McDonnell P, McHugh P. Evaluation of a multiscale modelling methodology to predict the mechanical properties of PCL/beta-TCP sintered scaffold materials. Ann Biomed Eng 2015; 43(8): 1989–1998.
- 25Doyle H, Lohfeld S, McHugh P. Evaluating the effect of increasing ceramic content on the mechanical properties, material microstructure and degradation of selective laser sintered polycaprolactone/beta-tricalcium phosphate materials. Med Eng Phys 2015; 37(8): 767–776.
- 26Du Y, Liu H, Shuang J, Wang J, Ma J, Zhang S. Microsphere-based selective laser sintering for building macroporous bone scaffolds with controlled microstructure and excellent biocompatibility. Colloids Surf B Biointerfaces 2015; 135: 81–89.
- 27Du Y, Liu H, Yang Q, Wang S, Wang J, Ma J, Noh I, Mikos AG, Zhang S. Selective laser sintering scaffold with hierarchical architecture and gradient composition for osteochondral repair in rabbits. Biomaterials 2017; 137: 37–48.
- 28Pereira TF, Silva MAC, Oliveira MF, Maia IA, Silva JVL, Costa MF, Thire RMSM. Effect of process parameters on the properties of selective laser sintered poly(3-hydroxybutyrate) scaffolds for bone tissue engineering. Virtual Phys Prototyp 2012; 7(4): 275–285.
10.1080/17452759.2012.738551 Google Scholar
- 29Saska S, Pires LC, Cominotte MA, Mendes LS, Fernandes de Oliveira M, Alves Maia I, Lopes da Silva JV, Lima Ribeiro SJ, Cirelli JA. Three-dimensional printing and in vitro evaluation of poly(3-hydroxybutyrate) scaffolds functionalized with osteogenic growth peptide for tissue engineering. Mater Sci Eng C 2018; 89: 265–273.
- 30Duan B, Wang M, Zhou WY, Cheung WL, Li ZY, Lu WW. Three-dimensional nanocomposite scaffolds fabricated via selective laser sintering for bone tissue engineering. Acta Biomater 2010; 6(12): 4495–4505.
- 31Freier T. Biopolyesters in Tissue Engineering Applications. Berlin, Heidelberg: Springer Berlin Heidelberg; 2006. pp. 1–61.
- 32Kumarasuriyar A, Jackson RA, Grøndahl L, Trau M, Nurcombe V, Cool SM. Poly (beta-hydroxybutyrate-co-beta-hydroxyvalerate) supports in vitro osteogenesis. Tissue Eng 2005; 11(7–8): 1281–1295.
- 33Sultana N, Wang M. Fabrication of HA/PHBV composite scaffolds through the emulsion freezing/freeze-drying process and characterisation of the scaffolds. J Mater Sci Mater Med 2007; 19(7): 2555–2561.
- 34Sultana N, Khan TH. In vitro degradation of PHBV scaffolds and nHA/PHBV composite scaffolds containing hydroxyapatite nanoparticles for bone tissue engineering. J Nanomater 2012; 2012: 1–12.
- 35Gogolewski S, Jovanovic M, Perren SM, Dillon JG, Hughes MK. Tissue response and in vivo degradation of selected polyhydroxyacids: Polylactides (PLA), poly (3-hydroxybutyrate)(PHB), and poly (3-hydroxybutyrate-co-3-hydroxyvalerate)(PHB/VA). J Biomed Mater Res Part A 1993; 27(9): 1135–1148.
- 36Diermann SH, Lu M, Edwards G, Dargusch M, Huang H. In vitro degradation of a unique porous PHBV scaffold manufactured using selective laser sintering. J Biomed Mater Res A 2019; 107(1): 154–162.
- 37Chen G-Q, Wu Q. The application of polyhydroxyalkanoates as tissue engineering materials. Biomaterials 2005; 26(33): 6565–6578.
- 38Wu CA, Pettit AR, Toulson S, Grøndahl L, Mackie EJ, Cassady AI. Responses in vivo to purified poly(3-hydroxybutyrate-co3-hydroxyvalerate) implanted in a murine tibial defect model. J Biomed Mater Res A 2009; 91A(3): 845–854.
- 39Grøndahl L, Jack KS, Goonasekera CS. Inorganic polymer composites for bone regeneration and repair. Bone Substitute Biomaterials. Cambridge, UK: Woodhead Publishing; 2014. pp. 261–293.
10.1533/9780857099037.3.261 Google Scholar
- 40Feng P, Wu P, Gao C, Yang Y, Guo W, Yang W, Shuai C. A multimaterial scaffold with tunable properties: Toward bone tissue repair. Adv Sci 2018; 5(6): 1700817.
10.1002/advs.201700817 Google Scholar
- 41Xu Y, Wu P, Feng P, Guo W, Yang W, Shuai C. Interfacial reinforcement in a poly-l-lactic acid/mesoporous bioactive glass scaffold via polydopamine. Colloids Surf B Biointerfaces 2018; 170: 45–53.
- 42Shuai C, Guo W, Wu P, Yang W, Hu S, Xia Y, Feng P. A graphene oxide-ag co-dispersing nanosystem: Dual synergistic effects on antibacterial activities and mechanical properties of polymer scaffolds. Chem Eng J 2018; 347: 322–333.
- 43Wu C, Chang J, Ni S, Wang J. In vitro bioactivity of Akermanite ceramics. J Biomed Mater Res A 2006; 76A(1): 73–80.
- 44Liu Q, Cen L, Yin S, Chen L, Liu G, Chang J, Cui L. A comparative study of proliferation and osteogenic differentiation of adipose-derived stem cells on Akermanite and beta-TCP ceramics. Biomaterials 2008; 29(36): 4792–4799.
- 45Razavi M, Fathi M, Savabi O, Razavi SM, Beni BH, Vashaee D, Tayebi L. Controlling the degradation rate of bioactive magnesium implants by electrophoretic deposition of Akermanite coating. Ceram Int 2014; 40(3): 3865–3872.
- 46Zanetti AS, McCandless GT, Chan JY, Gimble JM, Hayes DJ. In vitro human adipose-derived stromal/stem cells osteogenesis in Akermanite: Polycaprolactone scaffolds. J Biomater Appl 2014; 28(7): 998–1007.
- 47Xia L, Yin Z, Mao L, Wang X, Liu J, Jiang X, Zhang Z, Lin K, Chang J, Fang B. Akermanite bioceramics promote osteogenesis, angiogenesis and suppress osteoclastogenesis for osteoporotic bone regeneration. Sci Rep 2016; 6: 1–17.
- 48Sun H, Wu C, Dai K, Chang J, Tang T. Proliferation and osteoblastic differentiation of human bone marrow-derived stromal cells on Akermanite-bioactive ceramics. Biomaterials 2006; 27(33): 5651–5657.
- 49Huang Y, Jin X, Zhang X, Sun H, Tu J, Tang T, Chang J, Dai K. In vitro and in vivo evaluation of Akermanite bioceramics for bone regeneration. Biomaterials 2009; 30(28): 5041–5048.
- 50Liu A, Sun M, Yang X, Ma C, Liu Y, Yang X, Yan S, Gou Z. Three-dimensional printing Akermanite porous scaffolds for load-bearing bone defect repair: An investigation of osteogenic capability and mechanical evolution. J Biomater Appl 2016; 31(5): 650–660.
- 51Chen C, Watkins-Curry P, Smoak M, Hogan K, Deese S, McCandless GT, Chan JY, Hayes DJ. Targeting calcium magnesium silicates for polycaprolactone/ceramic composite scaffolds. ACS Biomater Sci Eng 2015; 1(2): 94–102.
- 52Zanetti AS, McCandless GT, Chan JY, Gimble JM, Hayes DJ. Characterization of novel Akermanite: Poly-e-caprolactone scaffolds for human adipose-derived stem cells bone tissue engineering. J Tissue Eng Regen Med 2011; 9(4): 389–404.
- 53Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005; 26(27): 5474–5491.
- 54Cui W, Li X, Zhou S, Weng J. Degradation patterns and surface wettability of electrospun fibrous mats. Polym Degrad Stab 2008; 93(3): 731–738.
- 55Oliveira JM, Rodrigues MT, Silva SS, Malafaya PB, Gomes ME, Viegas CA, Dias IR, Azevedo JT, Mano JF, Reis RL. Novel hydroxyapatite/chitosan bilayered scaffold for osteochondral tissue-engineering applications: Scaffold design and its performance when seeded with goat bone marrow stromal cells. Biomaterials 2006; 27(36): 6123–6137.
- 56Woodruff MA, Hutmacher DW. The return of a forgotten polymer—Polycaprolactone in the 21st century. Prog Polym Sci 2010; 35(10): 1217–1256.
- 57Wang Y, Lu L, Zheng Y, Chen X. Improvement in hydrophilicity of PHBV films by plasma treatment. J Biomed Mater Res A 2006; 76A(3): 589–595.
- 58Li H, Du R, Chang J. Fabrication, characterization, and in vitro degradation of composite scaffolds based on PHBV and bioactive glass. J Biomater Appl 2005; 20(2): 137–155.
- 59Luk JZ, Rondeau E, Trau M, Cooper-White J, Grøndahl L. Characterisation of amine functionalised poly(3-hydroxybuturate-co-3-hydroxyvalerate) surfaces. Polymer 2011; 52(15): 3251–3258.
- 60Luk JZ, Cooper-White J, Rintoul L, Taran E, Grøndahl L. Functionalised polycaprolactone films and 3D scaffolds via gamma irradiation-induced grafting. J Mater Chem B 2013; 1(33): 4171–4181.
- 61Duan B, Wang M. Customized Ca-P/PHBV nanocomposite scaffolds for bone tissue engineering: Design, fabrication, surface modification and sustained release of growth factor. J R Soc Interface 2010; 7(Suppl 5): S615–S629.
- 62Diermann SH, Lu M, Zhao Y, Vandi L-J, Dargusch M, Huang H. Synthesis, microstructure, and mechanical behaviour of a unique porous PHBV scaffold manufactured using selective laser sintering. J Mech Behav Biomed Mater 2018; 84: 151–160.
- 63Shahzad K, Deckers J, Kruth J-P, Vleugels J. Additive manufacturing of alumina parts by indirect selective laser sintering and post processing. J Mater Process Technol 2013; 213(9): 1484–1494.
- 64Grøndahl L, Chandler-Temple A, Trau M. Polymeric grafting of acrylic acid onto poly(3-hydroxybutyrate-co-3hydroxyvalerate): Surface functionalization for tissue engineering applications. Biomacromolecules 2005; 6(4): 2197–2203.
- 65Hinrichs WLJ, ten Hoopen HWM, Wissink MJB, Engbers GHM, Feijen J. Design of a new type of coating for the controlled release of heparin. J Control Release 1997; 45(2): 163–176.
- 66Artsis MI, Bonartsev AP, Iordanskii AL, Bonartseva GA, Zaikov GE. Biodegradation and medical application of microbial poly(3-hydroxybutyrate). Mol Cryst Liq Cryst 2010; 523(1): 21/[593]–49/[621].
- 67Gunaratne LMWK, Shanks RA, Amarasinghe G. Thermal history effects on crystallisation and melting of poly(3-hydroxybutyrate). Thermochim Acta 2004; 423(1–2): 127–135.
- 68Bruker. Manual for Bruker-microCT CT-Analyser v. 1.13, 2013. http://bruker-microct.com/next/CTan_UserManual.pdf.
- 69Zein I, Hutmacher DW, Tan KC, Teoh SH. Fused deposition modeling of novel scaffold architectures for tissue engineering applications. Biomaterials 2002; 23(4): 1169–1185.
- 70Jansen RJJ, van Bekkum H. XPS of nitrogen-containing functional groups on activated carbon. Carbon 1995; 33(8): 1021–1027.
- 71O'Brien FJ, Harley BA, Yannas IV, Gibson LJ. The effect of pore size on cell adhesion in collagen-gag scaffolds. Biomaterials 2005; 26(4): 433–441.
- 72Cahill S, Lohfeld S, McHugh PE. Finite element predictions compared to experimental results for the effective modulus of bone tissue engineering scaffolds fabricated by selective laser sintering. J Mater Sci Mater Med 2009; 20(6): 1255–1262.
- 73Murphy CM, Haugh MG, O'Brien FJ. 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.
- 74Ho ST, Hutmacher DW. A comparison of micro CT with other techniques used in the characterization of scaffolds. Biomaterials 2006; 27(8): 1362–1376.
- 75Jones AC, Arns CH, Sheppard AP, Hutmacher DW, Milthorpe BK, Knackstedt MA. Assessment of bone ingrowth into porous biomaterials using micro-ct. Biomaterials 2007; 28(15): 2491–2504.
- 76Mygind T, Stiehler M, Baatrup A, Li H, Zou X, Flyvbjerg A, Kassem M, Buenger C. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 2007; 28(6): 1036–1047.
- 77Ochoa I, Sanz-Herrera JA, Garcia-Aznar JM, Doblare M, Yunos DM, Boccaccini AR. Permeability evaluation of 45S5 bioglass-based scaffolds for bone tissue engineering. J Biomech 2009; 42(3): 257–260.
- 78Grassie N, Murray EJ, Holmes PA. The thermal degradation of poly(-(d)-beta-hydroxybutyric acid): Part 3-the reaction mechanism. Polym Degrad Stab 1984; 6(3): 127–134.
- 79Liu Q-S, Zhu M-F, Wu W-H, Qin Z-Y. Reducing the formation of six-membered ring ester during thermal degradation of biodegradable PHBV to enhance its thermal stability. Polym Degrad Stab 2009; 94(1): 18–24.
- 80Duan B, Wang M, Zhou WY, Cheung WL. Synthesis of Ca-P nanoparticles and fabrication of Ca-P/PHBV nanocomposite microspheres for bone tissue engineering applications. Appl Surf Sci 2008; 255(2): 529–533.
- 81Duan B, Wang M. Encapsulation and release of biomolecules from Ca-P/PHBV nanocomposite microspheres and three-dimensional scaffolds fabricated by selective laser sintering. Polym Degrad Stab 2010; 95(9): 1655–1664.
- 82Duan B, Cheung WL, Wang M. Optimized fabrication of Ca-P/PHBV nanocomposite scaffolds via selective laser sintering for bone tissue engineering. Biofabrication 2011; 3(1): 1–13.
- 83Ahmed S, Jones FR. A review of particulate reinforcement theories for polymer composites. J Mater Sci 1990; 25(12): 4933–4942.
- 84Simpson RL, Wiria FE, Amis AA, Chua CK, Leong KF, Hansen UN, Chandrasekaran M, Lee MW. Development of a 95/5 poly(l-lactide-co-glycolide)/hydroxylapatite and beta-tricalcium phosphate scaffold as bone replacement material via selective laser sintering. J Biomed Mater Res B Appl Biomater 2008; 84B(1): 17–25.
- 85Williams JM, Adewunmi A, Schek RM, Flanagan CL, Krebsbach PH, Feinberg SE, Hollister SJ, Das S. Bone tissue engineering using polycaprolactone scaffolds fabricated via selective laser sintering. Biomaterials 2005; 26(23): 4817–4827.
- 86Ramay HRR, Zhang M. Biphasic calcium phosphate nanocomposite porous scaffolds for load-bearing bone tissue engineering. Biomaterials 2004; 25(21): 5171–5180.
- 87Karim L, Hussein AI, Morgan EF, Bouxsein ML. The mechanical behavior of bone. The Mechanical Behavior of Bone, 4th ed. San Diego: Academic Press; 2013. pp. 431–452.