AccScience Publishing / IJB / Online First / DOI: 10.36922/ijb.5964
Submit to IJB
Cite this article
75
Download
698
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
RESEARCH ARTICLE

3D printing of microstructured piezoelectric and bioactive PCL-composite scaffolds for bone regeneration

Phillip Barkow1 ,  Christian Polley1 ,  Lisa Schöbel2 ,  Janine Waletzko-Hellwig3 ,  Georg Schnell1 ,  Armin Springer4 ,  Rainer Bader3 ,  Aldo R. Boccaccini2 ,  Hermann Seitz1,5
Show Less
1 Chair of Microfluidics, University of Rostock, Rostock, Germany
2 Institute of Biomaterials, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany
3 Biomechanics and Implant Technology Research Laboratory, Department of Orthopedics, Rostock University Medical Center, Rostock, Germany
4 Electron Microscopy Centrum, Rostock University Medical Center, Rostock, Germany
5 Department of Life, Light & Matter, University of Rostock, Rostock, Germany
IJB, 5964 https://doi.org/10.36922/ijb.5964
Submitted: 14 November 2024 | Accepted: 23 December 2024 | Published: 23 December 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Despite the self-healing ability of bone tissue, the treatment of critical-size defects and the limited regenerative process in osteoporosis or avascular necrosis demand special medical attention. One of the goals of bone tissue engineering is to develop new patient-specific solutions for bone repair. In this study, we focus on the fabrication of degradable subchondral bone scaffolds made of highly loaded polycaprolactone (PCL) using direct ink writing. Barium titanate (BTO) and the bioactive glass 45S5 (BG) were used as filler materials to modify the material’s piezoelectric, mechanical, and bioresponsive properties. The mechanical properties of our composites are in the range of spongy bone, and a compressive modulus of around 181 MPa was achieved for PCL/BTO and 98.3 MPa for PCL/BTO/BG scaffolds. The use of 40 vol.% BTO in combination with PCL showed piezoelectric properties in the range of bone tissue with a d33 of 0.75 pC/N. While adding BG decreases the piezoelectric properties, it increases the bioactivity and the osteogenic response of primary human osteoblasts. In summary, these novel material compositions provide a promising approach for developing multiphasic scaffolds for bone tissue engineering.  

 

Graphical abstract
Keywords
Direct-ink-writing
Bone tissue engineering
Polycaprolactone
Barium titanate
Bioactive glass
Composite scaffolds
Funding
This research was funded by Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – SFB 1270/1,2 – 299150580 to Hermann Seitz, Aldo R. Boccaccini and Rainer Bader.
Conflict of interest
Aldo R. Boccaccini serves as the Editorial Board Member of the journal, but did not in any way involve in the editorial and peer-review process conducted for this paper, directly or indirectly. Other authors declare they have no competing interests.
References
  1. Donate R, Paz R, Moriche R, Sayagués MJ, Alemán- Domínguez ME, Monzón M. An overview of polymeric composite scaffolds with piezoelectric properties for improved bone regeneration. Mater Des. 2023;231:112085. doi: 10.1016/j.matdes.2023.112085
  2. Koons GL, Diba M, Mikos AG. Materials design for bone-tissue engineering. Nat Rev Mater. 2020;5:584-603. doi: 10.1038/s41578-020-0204-2
  3. Ahn AC, Grodzinsky AJ. Relevance of collagen piezoelectricity to “Wolff ’s Law”: a critical review. Med Eng Phys. 2009:;31:733-741. doi: 10.1016/j.medengphy.2009.02.006
  4. Khare D, Basu B, Dubey AK. Electrical stimulation and piezoelectric biomaterials for bone tissue engineering applications. Biomaterials. 2020;258:120280. doi: 10.1016/j.biomaterials.2020.120280
  5. Rajabi AH, Jaffe M, Arinzeh TL. Piezoelectric materials for tissue regeneration: a review. Acta Biomater. 2015;24:12-23. doi: 10.1016/j.actbio.2015.07.010
  6. Li S, Shan Y, Chen J, et al. 3D printing and biomedical applications of piezoelectric composites: a critical review. Adv Mater Technol. 2024. doi: 10.1002/admt.202401160
  7. Sundelacruz S, Li C, Choi YJ, Levin M, Kaplan DL. Bioelectric modulation of wound healing in a 3D in vitro model of tissue-engineered bone. Biomaterials. 2013;34:6695-6705. doi: 10.1016/j.biomaterials.2013.05.040
  8. Tandon B, Blaker JJ, Cartmell SH. Piezoelectric materials as stimulatory biomedical materials and scaf‍folds for bone repair. Acta Biomater. 2018;73:1-20. doi: 10.1016/j.actbio.2018.04.026
  9. Kapat K, Shubhra QTH, Zhou M, Leeuwenburgh S. Piezoelectric nano‐biomaterials for biomedicine and tissue regeneration. Adv Funct Mater. 2020;30. doi: 10.1002/adfm.201909045
  10. Acosta M, Novak N, Rojas V, et al. BaTiO3-based piezoelectrics: fundamentals, current status, and perspectives. Appl Phys Rev. 2017;4. doi: 10.1063/1.4990046
  11. Mancuso E, Shah L, Jindal S, et al. Additively manufactured BaTiO3 composite scaffolds: a novel strategy for load bearing bone tissue engineering applications. Mater Sci Eng C Mater Biol Appl. 2021;126:112192. doi: 10.1016/j.msec.2021.112192
  12. Liu W, Yang D, Wei X, et al. Fabrication of piezoelectric porous BaTiO3 scaffold to repair large segmental bone defect in sheep. J Biomater Appl. 2020;35:544-552. doi: 10.1177/0885328220942906
  13. Polley C, Distler T, Detsch R, et al. 3D printing of piezoelectric barium titanate-hydroxyapatite scaffolds with interconnected porosity for bone tissue engineering. Materials (Basel, Switzerland). 2020;13:1773. doi: 10.3390/ma13071773
  14. Polley C, Distler T, Scheufler C, et al. 3D printing of piezoelectric and bioactive barium titanate-bioactive glass scaffolds for bone tissue engineering. Mater Today Bio. 2023;21:100719. doi: 10.1016/j.mtbio.2023.100719
  15. Hench LL. Chronology of bioactive glass development and clinical applications. NJGC. 2013;03:67-73. doi: 10.4236/njgc.2013.32011
  16. Filho OP, La Torre GP, Hench LL. Effect of crystallization on apatite-layer formation of bioactive glass 45S5. J Biomed Mater Res. 1996;30:509-514. doi: 10.1002/(SICI)1097-4636(199604)30:4<509::AID-JBM9>3.0.CO;2-T
  17. Hench LL, Splinter RJ, Allen WC, Greenlee TK. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res. 1971;5:117-141. doi: 10.1002/jbm.820050611
  18. Soni R, Kumar NV, Chameettachal S, Pati F, Narayan Rath S. Synthesis and optimization of PCL-bioactive glass composite scaffold for bone tissue engineering. Mater Today Proc. 2019;15:294-299. doi: 10.1016/j.matpr.2019.05.008
  19. Petretta M, Gambardella A, Boi M, et al. Composite scaffolds for bone tissue regeneration based on PCL and Mg-containing bioactive glasses. Biology. 2021;10:398. doi: 10.3390/biology10050398
  20. Bi L, Li D, Liu J, et al. Fabrication and characterization of a biphasic scaffold for osteochondral tissue engineering. Mater Lett. 2011;65:2079-2082. doi: 10.1016/j.matlet.2011.04.013
  21. Mukundan LM, Nirmal RS, Nair PD. Growth and regeneration of osteochondral cells in bioactive niche: a promising approach for osteochondral tissue repair. ACS Appl Bio Mater. 2022;5:2676-2688. doi: 10.1021/acsabm.2c00125
  22. Fathi A, Kermani F, Behnamghader A, et al. Three-dimensionally printed polycaprolactone/multicomponent bioactive glass scaffolds for potential application in bone tissue engineering. Biomed Glass. 2020;6:57-69. doi: 10.1515/bglass-2020-0006
  23. Rotan M, Zhuk M, Glaum J. Activation of ferroelectric implant ceramics by corona discharge poling. J European Ceram Soc. 2020;40:5402-5409. doi: 10.1016/j.jeurceramsoc.2020.06.058
  24. Riaz A, Polley C, Lund H, Springer A, Seitz H. A novel approach to fabricate load-bearing Ti6Al4V-Barium titanate piezoelectric bone scaffolds by coupling electron beam melting and field-assisted sintering. Mater Des. 2023;225:111428. doi: 10.1016/j.matdes.2022.111428
  25. Polley C, Riaz A, Lund H, Boccaccini AR, Seitz H. Field-assisted sintering of barium titanate and 45S5 bioactive glass for biomedical applications. Ceramics Int. 2024;50(19): 37314-37321. doi: 10.1016/j.ceramint.2024.07.107
  26. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity?. Biomaterials. 2006;27:2907-2915. doi: 10.1016/j.biomaterials.2006.01.017
  27. Jonitz-Heincke A, Sellin ML, Seyfarth A, et al. Analysis of cellular activity short-term exposure to cobalt and chromium ions in mature human osteoblasts. Materials (Basel, Switzerland). 2019;12:2771. doi: 10.3390/ma12172771
  28. Peng Y, Zhuang Y, Liu Y, et al. Bioinspired gradient scaffolds for osteochondral tissue engineering. Exploration (Beijing, China). 2023;3:20210043. doi: 10.1002/EXP.20210043
  29. Ronca D, Langella F, Chierchia M, et al. Bone tissue engineering: 3D PCL-based nanocomposite scaffolds with tailored properties. Procedia CIRP. 2016;49:51-54. doi: 10.1016/j.procir.2015.07.028
  30. Rouwkema J, Rivron NC, van Blitterswijk CA. Vascularization in tissue engineering. Trends Biotechnol. 2008;26:434-441. doi: 10.1016/j.tibtech.2008.04.009
  31. Abbasi N, Hamlet S, Love RM, Nguyen NT. Porous scaffolds for bone regeneration. J Sci Adv Mater Dev. 2020;5:1-9. doi: 10.1016/j.jsamd.2020.01.007
  32. Sandino C, Lacroix D. A dynamical study of the mechanical stimuli and tissue differentiation within a CaP scaffold based on micro-CT finite element models. Biomech Model Mechanobiol. 2011;10:565-576. doi: 10.1007/s10237-010-0256-0
  33. Baier RV, Contreras Raggio JI, Giovanetti CM, et al. Shape fidelity, mechanical and biological performance of 3D printed polycaprolactone-bioactive glass composite scaffolds. Biomater Adv. 2022;134:112540. doi: 10.1016/j.msec.2021.112540
  34. Tian L, Zhang Z, Tian B, Zhang X, Wang N. Study on antibacterial properties and cytocompatibility of EPL coated 3D printed PCL/HA composite scaffolds. RSC Adv. 2020;10:4805-4816. doi: 10.1039/C9RA10275B
  35. Olate-Moya F, Arens L, Wilhelm M, Mateos-Timoneda MA, Engel E, Palza H. Chondroinductive alginate-based hydrogels having graphene oxide for 3D printed scaffold fabrication. ACS Appl Mater Interfaces. 2020;12:4343-4357. doi: 10.1021/acsami.9b22062
  36. Fabbri P, Cannillo V, Sola A, Dorigato A, Chiellini F. Highly porous polycaprolactone-45S5 Bioglass® scaffolds for bone tissue engineering. Comp Sci Technol. 2010;70:1869-1878. doi: 10.1016/j.compscitech.2010.05.029
  37. Pierantozzi D, Scalzone A, Jindal S, et al. 3D printed Sr-containing composite scaffolds: effect of structural design and material formulation towards new strategies for bone tissue engineering. Comp Sci Technol. 2020;191:108069. doi: 10.1016/j.compscitech.2020.108069
  38. Gómez-Lizárraga KK, Flores-Morales C, Del Prado-Audelo ML, Álvarez-Pérez MA, Piña-Barba MC, Escobedo C. Polycaprolactone- and polycaprolactone/ceramic-based 3D-bioplotted porous scaffolds for bone regeneration: a comparative study. Mater Sci Eng C Mater Biol Appl. 2017;79:326-335. doi: 10.1016/j.msec.2017.05.003
  39. Ródenas-Rochina J, Ribelles JLG, Lebourg M. Comparative study of PCL-HAp and PCL-bioglass composite scaffolds for bone tissue engineering. J Mater Sci Mater Med. 2013;24:1293-1308. doi: 10.1007/s10856-013-4878-5
  40. Seo C, Zhang C, Liu H. A review on the 3D printing of composite scaffolds for bone tissue engineering. In: Musculoskeletal Tissue Engineering. Elsevier. 2022:201-241. doi: 10.1016/B978-0-12-823893-6.00001-2
  41. Heng BC, Bai Y, Li X, et al. The bioelectrical properties of bone tissue. Animal Model Exp Med. 2023;6:120-130. doi: 10.1002/ame2.12300
  42. Liu J, Gu H, Liu Q, Ren L, Li G. An intelligent material for tissue reconstruction: the piezoelectric property of polycaprolactone/barium titanate composites. Mater Lett. 2019;236:686-689. doi: 10.1016/j.matlet.2018.11.036
  43. Köllner D, Simon S, Niedermeyer S, et al. Relation between structure, mechanical and piezoelectric properties in cellular ceramic auxetic and honeycomb structures. Adv Eng Mater. 2023;25. doi: 10.1002/adem.202201387
  44. Liu J, He X, Wang F, Zhou X, Li G. Dielectric and mechanical properties of polycaprolactone/nano-barium titanate piezoelectric composites. Plast Rubber Compos. 2021;50:299-306. doi: 10.1080/14658011.2021.1893517
  45. Sikder P, Nagaraju P, Naganaboyina HPS. 3D-printed piezoelectric porous bioactive scaffolds and clinical ultrasonic stimulation can help in enhanced bone regeneration. Bioengineering (Basel, Switzerland). 2022;9:679. doi: 10.3390/bioengineering9110679
  46. Ranella A, Barberoglou M, Bakogianni S, Fotakis C, Stratakis E. Tuning cell adhesion by controlling the roughness and wettability of 3D micro/nano silicon structures. Acta Biomater. 2010;6:2711-2720. doi: 10.1016/j.actbio.2010.01.016
  47. Fu SZ, Wang XH, Guo G, et al. Preparation and properties of nano-hydroxyapatite/PCL-PEG-PCL composite membranes for tissue engineering applications. J Biomed Mater Res B Appl Biomater. 2011;97:74-83. doi: 10.1002/jbm.b.31788
  48. Ji L, Wang W, Jin D, Zhou S, Song X. In vitro bioactivity and mechanical properties of bioactive glass nanoparticles/ polycaprolactone composites. Mater Sci Eng C Mater Biol Appl. 2015;46:1-9. doi: 10.1016/j.msec.2014.09.041
  49. Kim Y, Lim JY, Yang GH, Seo JH, Ryu HS, Kim G. 3D-printed PCL/bioglass (BGS-7) composite scaffolds with high toughness and cell-responses for bone tissue regeneration. J Indus Eng Chem. 2019;79:163-171. doi: 10.1016/j.jiec.2019.06.027
  50. Li X, Shi J, Dong X, Zhang L, Zeng H. A mesoporous bioactive glass/polycaprolactone composite scaffold and its bioactivity behavior. J Biomed Mater Res A. 2008;84:84-91. doi: 10.1002/jbm.a.31371
  51. Paxton NC, Ho SWK, Tuten BT, Lipton-Duffin J, Woodruff MA. Degradation of melt electrowritten PCL scaffolds following melt processing and plasma surface treatment. Macromol Rapid Commun. 2021;42:e2100433. doi: 10.1002/marc.202100433
  52. Yeo A, Wong WJ, Teoh SH. Surface modification of PCL-TCP scaffolds in rabbit calvaria defects: evaluation of scaffold degradation profile, biomechanical properties and bone healing patterns. J Biomed Mater Res A. 2010;93:1358-1367. doi: 10.1002/jbm.a.32633
  53. Poh PSP, Hutmacher DW, Stevens MM, Woodruff MA. Fabrication and in vitro characterization of bioactive glass composite scaffolds for bone regeneration. Biofabrication. 2013;5:45005. doi: 10.1088/1758-5082/5/4/045005
  54. Zheng T, Yu Y, Pang Y, et al. Improving bone regeneration with composites consisting of piezoelectric poly(l-lactide) and piezoelectric calcium/manganese co-doped barium titanate nanofibers. Comp B Eng. 2022;234:109734. doi: 10.1016/j.compositesb.2022.109734
  55. Sims NA. Influences of the IL-6 cytokine family on bone structure and function. Cytokine. 2021;146:155655. doi: 10.1016/j.cyto.2021.155655
  56. Nalesso PRL, Vedovatto M, Gregório JES, et al. Early in vivo osteogenic and inflammatory response of 3D printed polycaprolactone/carbon nanotube/hydroxyapatite/ tricalcium phosphate composite scaffolds. Polymers. 2023;15:2952. doi: 10.3390/polym15132952
  57. Hayami T, Kapila YL, Kapila S. MMP-1 (collagenase-1) and MMP-13 (collagenase-3) differentially regulate markers of osteoblastic differentiation in osteogenic cells. Matrix Biol. 2008;27:682-692. doi: 10.1016/j.matbio.2008.07.005
  58. Rozila I, Azari P, Munirah S, Safwani WKZW, Pingguan- Murphy B, Chua KH. Polycaprolactone-based scaffolds facilitates osteogenic differentiation of human adipose-derived stem cells in a co-culture system. Polymers. 2021;13:597. doi: 10.3390/polym13040597
  59. Antunovic F, Tolosa F, Klein C, Ocaranza R. Polycaprolactone-based scaffolds for guided tissue regeneration in periodontal therapy: a systematic review. J Appl Biomater Funct Mater. 2023;21:22808000231211416. doi: 10.1177/22808000231211416
  60. Xu X, Xiao L, Xu Y, et al. Vascularized bone regeneration accelerated by 3D-printed nanosilicate-functionalized polycaprolactone scaffold. Regen Biomater. 2021;8:rbab061. doi: 10.1093/rb/rbab061
  61. Haxaire C, Haÿ E, Geoffroy V. Runx2 controls bone resorption through the down-regulation of the Wnt pathway in osteoblasts. Am J Pathol. 2016;186:1598-1609. doi: 10.1016/j.ajpath.2016.01.016
  62. Amarasekara DS, Kim S, Rho J. Regulation of osteoblast differentiation by cytokine networks. Int J Mol Sci. 2021;22:2851. doi: 10.3390/ijms22062851

 

 

 

 

Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept