journal article·2022-06-28Open access

3D printed hydroxyapatite-nacre-starch based bone grafts: Evaluation of biological and mechanical properties

Susmita Bose, Caitlin Koski, Arjak Bhattacharjee

Journal of Materials Research· Volume 37· Issue 12

Abstract

The possibilities of utilizing nacre as a reinforcing material to manufacture 3D printed bone grafts are yet to be explored. This work reports the feasibility of fabricating 3D printed nacre-hydroxyapatitestarch composite bone graft substitutes, emphasizing the effects of nacre addition on biological and mechanical properties. Pressure-less extrusion-based 3D printing of ceramic-polymer viscous slurry is challenging due to the composition and process-parameter variations. To overcome these challenges, a dual extrusion solid freeform fabricator (SFF) has been designed. An increase in nacre loading improves the compressive strength from 9.5 ± 0.1 MPa to 11.7 ± 0.2 MPa, without any post-processing or sintering. Nacre's in vitro osteogenic properties lead to a slight increase in hFOB cellular attachment on the graft surface by day 11. The fabricated structures show good mechanical integrity during the dissolution study in simulated body fluid (SBF). These bone graft substitutes may be utilized to repair low load bearing skeletal defects.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Bone Tissue Engineering Materials · 3D Printing in Biomedical Research · Calcium Carbonate Crystallization and Inhibition

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (42)

Show source-provided references
1. A. Litwic, M.H. Edwards, E.M. Dennison, C. Cooper, Epidemiology and burden of osteoarthritis. Br. Med. Bull. 105(1), 185 (2013)10.1093/bmb/lds038 ↗
2. T. Kokubo, H.-M. Kim, M. Kawashita, Novel bioactive materials with different mechanical properties. Biomaterials 24(13), 2161 (2003)10.1016/S0142-9612(03)00044-9 ↗
3. S. Bose, S. Vahabzadeh, A. Bandyopadhyay, Bone tissue engineering using 3D printing. Mater. Today 16(12), 496 (2013)10.1016/j.mattod.2013.11.017 ↗
4. M. Dziadek, E. Stodolak-Zych, K. Cholewa-Kowalska, Biodegradable ceramic-polymer composites for biomedical applications: a review. Mater. Sci. Eng. C 71, 1175 (2017)10.1016/j.msec.2016.10.014 ↗
5. N. Top, İ Şahin, H. Gökçe, H. Gökçe, Computer-aided design and additive manufacturing of bone scaffolds for tissue engineering: state of the art. J. Mater. Res. 36, 3725–3745 (2021)10.1557/s43578-021-00156-y ↗
6. G.E. Daoud, D.L. Pezzutti, C.J. Dolatowski, R.L. Carrau, M. Pancake, E. Herderick, K.K. VanKoevering, Establishing a point-of-care additive manufacturing workflow for clinical use. J. Mater. Res. 36, 3761–3780 (2021)10.1557/s43578-021-00270-x ↗
7. A. Mostafaei, A.M. Elliott, J.E. Barnes, F. Li, W. Tan, C.L. Cramer, P. Nandwana, M. Chmielus, Binder jet 3D printing—process parameters, materials, properties, and challenges. Prog. Mater. Sci. 119, 100707 (2020)10.1016/j.pmatsci.2020.100707 ↗
8. W. Chengwei, P. Weiwei, B. Qiang, C. Huachen, H. Ryan, W. Ruiliu, B.A.H., X. Zhenpeng, D. Jiaqi, P. Yong, Z. Chaolun, P. Glenn, G. Jinlong, W. Xizheng, W. Howard, Z. Ji-Cheng, Y. Bao, Z. X. (Rayne), L. Jian, M. Yifei, D. Bruce, and H. Liangbing: A general method to synthesize and sinter bulk ceramics in seconds. Science (80–) 368(6490), 521 (2020)10.1126/science.aaz7681 ↗
9. R. Masaeli, K. Zandsalimi, M. Rasoulianboroujeni, L. Tayebi, Challenges in three-dimensional printing of bone substitutes. Tissue Eng. Part B Rev. 25(5), 387 (2019)10.1089/ten.teb.2018.0381 ↗
10. U. Gbureck, T. Hölzel, U. Klammert, K. Würzler, F.A. Müller, J.E. Barralet, Resorbable dicalcium phosphate bone substitutes prepared by 3D powder printing. Adv. Funct. Mater. 17(18), 3940 (2007)10.1002/adfm.200700019 ↗
11. J.-H. Shim, J.Y. Kim, M. Park, J. Park, D.-W. Cho, Development of a hybrid scaffold with synthetic biomaterials and hydrogel using solid freeform fabrication technology. Biofabrication 3(3), 34102 (2011)10.1088/1758-5082/3/3/034102 ↗
12. S.L. Morissette, J.A. Lewis, J. Cesarano, D.B. Dimos, T. Baer, Solid freeform fabrication of aqueous alumina–poly(vinyl alcohol) gelcasting suspensions. J. Am. Ceram. Soc. 83(10), 2409 (2000)10.1111/j.1151-2916.2000.tb01569.x ↗
13. A. Hadian, L. Koch, P. Koberg, F. Sarraf, A. Liersch, T. Sebastian, F. Clemens, Material extrusion based additive manufacturing of large zirconia structures using filaments with ethylene vinyl acetate based binder composition. Addit. Manuf. 47, 102227 (2021)
14. C. Koski, B. Onuike, A. Bandyopadhyay, S. Bose, Starch-hydroxyapatite composite bone scaffold fabrication utilizing a slurry extrusion-based solid freeform fabricator. Addit. Manuf. 24, 47 (2018)
15. P. Westbroek, F. Marin, A marriage of bone and nacre. Nature 392(6679), 861 (1998)10.1038/31798 ↗
16. Y. Yang, X. Li, M. Chu, H. Sun, J. Jin, K. Yu, Q. Wang, Q. Zhou, Y. Chen, Electrically assisted 3D printing of nacre-inspired structures with self-sensing capability. Sci. Adv. 5(4), eaau9490 (2019)10.1126/sciadv.aau9490 ↗
17. M. Ni, B.D. Ratner, Nacre surface transformation to hydroxyapatite in a phosphate buffer solution. Biomaterials 24(23), 4323 (2003)10.1016/S0142-9612(03)00236-9 ↗
18. M. Lamghari, M.J. Almeida, S. Berland, H. Huet, A. Laurent, C. Milet, E. Lopez, Stimulation of bone marrow cells and bone formation by nacre: in vivo and in vitro studies. Bone 25(2 Suppl), 91S (1999)10.1016/S8756-3282(99)00141-6 ↗
19. M. Lamghari, S. Berland, A. Laurent, H. Huet, E. Lopez, Bone reactions to nacre injected percutaneously into the vertebrae of sheep. Biomaterials 22(6), 555 (2001)10.1016/S0142-9612(00)00213-1 ↗
20. K. Ko, S. Jin, S.E. Lee, J.-W. Hong, Impact resistance of nacre-like composites diversely patterned by 3D printing. Compos. Struct. 238, 111951 (2020)10.1016/j.compstruct.2020.111951 ↗
21. D. Verma, K. Katti, D. Katti, Photoacoustic FTIR spectroscopic study of undisturbed nacre from red abalone. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 64(4), 1051 (2006)10.1016/j.saa.2005.09.014 ↗
22. Y. Ma, Y. Gao, Q. Feng, Characterization of organic matrix extracted from fresh water pearls. Mater. Sci. Eng. C 31(7), 1338 (2011)10.1016/j.msec.2011.04.016 ↗
23. H. Chim, D.W. Hutmacher, A.M. Chou, A.L. Oliveira, R.L. Reis, T.C. Lim, J.-T. Schantz, A comparative analysis of scaffold material modifications for load-bearing applications in bone tissue engineering. Int. J. Oral Maxillofac. Surg. 35(10), 928 (2006)10.1016/j.ijom.2006.03.024 ↗
24. Y. Song, Y. Lu, H. Ding, H. Lv, G. Gao, C. Sun, Structural characteristics at the adductor muscle and shell interface in mussel. Appl. Biochem. Biotechnol. 171(5), 1203 (2013)10.1007/s12010-013-0194-2 ↗
25. G.L. Koons, M. Diba, A.G. Mikos, Materials design for bone-tissue engineering. Nat. Rev. Mater. 5(8), 584 (2020)10.1038/s41578-020-0204-2 ↗
26. Y. Yang, X. Song, X. Li, Z. Chen, C. Zhou, Q. Zhou, Y. Chen, Recent Progress in biomimetic additive manufacturing technology: from materials to functional structures. Adv. Mater. 30(36), 1706539 (2018)10.1002/adma.201706539 ↗
27. C. Koski, S. Bose, Effects of amylose content on the mechanical properties of starch-hydroxyapatite 3D printed bone scaffolds. Addit. Manuf. 30, 100817 (2019)
28. S.F. Robertson, S. Bose, Enhanced osteogenesis of 3D printed β-TCP scaffolds with Cissus quadrangularis extract-loaded polydopamine coatings. J. Mech. Behav. Biomed. Mater. 111, 103945 (2020)10.1016/j.jmbbm.2020.103945 ↗
29. P.-Y. Chen, A.Y.M. Lin, Y.-S. Lin, Y. Seki, A.G. Stokes, J. Peyras, E.A. Olevsky, M.A. Meyers, J. McKittrick, Structure and mechanical properties of selected biological materials. J. Mech. Behav. Biomed. Mater. 1(3), 208 (2008)10.1016/j.jmbbm.2008.02.003 ↗
30. I.M. Weiss, W. Göhring, M. Fritz, K. Mann, Perlustrin, a Haliotis laevigata (Abalone) nacre protein, is homologous to the insulin-like growth factor binding protein N-terminal module of vertebrates. Biochem. Biophys. Res. Commun. 285(2), 244 (2001)10.1006/bbrc.2001.5170 ↗
31. C. Bergmann, M. Lindner, W. Zhang, K. Koczur, A. Kirsten, R. Telle, H. Fischer, 3D printing of bone substitute implants using calcium phosphate and bioactive glasses. J. Eur. Ceram. Soc. 30(12), 2563 (2010)10.1016/j.jeurceramsoc.2010.04.037 ↗
32. Y.-W. Kim, J.-J. Kim, Y.H. Kim, J.-Y. Rho, Effects of organic matrix proteins on the interfacial structure at the bone–biocompatible nacre interface in vitro. Biomaterials 23(9), 2089 (2002)10.1016/S0142-9612(01)00340-4 ↗
33. S.S. Banerjee, A. Bandyopadhyay, S. Bose, Biphasic resorbable calcium phosphate ceramic for bone implants and local alendronate delivery. Adv. Eng. Mater. 12(5), B148 (2010)10.1002/adem.200980072 ↗
34. W. Xue, B.V. Krishna, A. Bandyopadhyay, S. Bose, Processing and biocompatibility evaluation of laser processed porous titanium. Acta Biomater. 3(6), 1007 (2007)10.1016/j.actbio.2007.05.009 ↗
35. D.W. Green, H.-J. Kwon, H.-S. Jung, Osteogenic potency of nacre on human mesenchymal stem cells. Mol. Cells 38(3), 267 (2015)10.14348/molcells.2015.2315 ↗
36. E.V. Alakpa, K.E.V. Burgess, P. Chung, M.O. Riehle, N. Gadegaard, M.J. Dalby, M. Cusack, Nacre topography produces higher crystallinity in bone than chemically induced osteogenesis. ACS Nano 11(7), 6717 (2017)10.1021/acsnano.7b01044 ↗
37. C. Silve, E. Lopez, B. Vidal, D.C. Smith, S. Camprasse, G. Camprasse, G. Couly, Nacre initiates biomineralization by human osteoblasts maintained in vitro. Calcif. Tissue Int. 51(5), 363 (1992)10.1007/BF00316881 ↗
38. Y. Cheng, W. Zhang, H. Fan, P. Xu, Water-soluble nano-pearl powder promotes MC3T3-E1 cell differentiation by enhancing autophagy via the MEK/ERK signaling pathway. Mol. Med. Rep. 18(1), 993 (2018)
39. A. Wang, H. Zhang, Z. Liang, K. Xu, W. Qiu, Y. Tian, H. Guo, J. Jia, E. Xing, R. Chen, Z. Xiang, J. Liu, U0126 attenuates ischemia/reperfusion-induced apoptosis and autophagy in myocardium through MEK/ERK/EGR-1 pathway. Eur. J. Pharmacol. 788, 280 (2016)10.1016/j.ejphar.2016.06.038 ↗
40. S. Bose, A. Bhattacharjee, D. Banerjee, A.R. Boccaccini, A. Bandyopadhyay, Influence of random and designed porosities on 3D printed tricalcium phosphate-bioactive glass scaffolds. Addit. Manuf. 40, 101895 (2021)
41. M. Roy, G.A. Fielding, A. Bandyopadhyay, S. Bose, Effects of zinc and strontium substitution in tricalcium phosphate on osteoclast differentiation and resorption. Biomater. Sci. 1(1), 74 (2013)10.1039/C2BM00012A ↗
42. S. Tarafder, S. Banerjee, A. Bandyopadhyay, S. Bose, Electrically polarized biphasic calcium phosphates: adsorption and release of bovine serum albumin. Langmuir 26(22), 16625 (2010)10.1021/la101851f ↗