Skip to content
BY 4.0 license Open Access Published by De Gruyter Open Access December 31, 2020

Three-dimensionally printed polycaprolactone/multicomponent bioactive glass scaffolds for potential application in bone tissue engineering

  • Amirhosein Fathi , Farzad Kermani , Aliasghar Behnamghader , Sara Banijamali , Masoud Mozafari EMAIL logo , Francesco Baino and Saeid Kargozar EMAIL logo
From the journal Biomedical Glasses

Abstract

Over the last years, three-dimensional (3D) printing has been successfully applied to produce suitable substitutes for treating bone defects. In this work, 3D printed composite scaffolds of polycaprolactone (PCL) and strontium (Sr)- and cobalt (Co)-doped multi-component melt-derived bioactive glasses (BGs) were prepared for bone tissue engineering strategies. For this purpose, 30% of as-prepared BG particles (size <38 μm) were incorporated into PCL, and then the obtained composite mix was introduced into a 3D printing machine to fabricate layer-by-layer porous structures with the size of 12 × 12 × 2 mm3.

The scaffolds were fully characterized through a series of physico-chemical and biological assays. Adding the BGs to PCL led to an improvement in the compressive strength of the fabricated scaffolds and increased their hydrophilicity. Furthermore, the PCL/BG scaffolds showed apatite-forming ability (i.e., bioactivity behavior) after being immersed in simulated body fluid (SBF). The in vitro cellular examinations revealed the cytocompatibility of the scaffolds and confirmed them as suitable substrates for the adhesion and proliferation of MG-63 osteosarcoma cells. In conclusion, 3D printed composite scaffolds made of PCL and Sr- and Co-doped BGs might be potentially-beneficial bone replacements, and the achieved results motivate further research on these materials.


Amirhosein Fathi and Farzad Kermani contributed equally to this work


References

[1] Kargozar S., Mozafari M., Hamzehlou S., Brouki Milan P., Kim H.-W., Baino F.. Bone tissue engineering using human cells: a comprehensive review on recent trends, current prospects, and recommendations, Appl. Sci., 2019, 9 (1), 174.10.3390/app9010174Search in Google Scholar

[2] Qu H., Fu H., Han Z., Sun Y. 2019. Biomaterials for bone tissue engineering scaffolds: a review. RSC Adv 9 (45). 26252-26262.10.1039/C9RA05214CSearch in Google Scholar

[3] Neufurth M., Wang X., Wang S., Steffen R., Ackermann M., Haep N. D., et al. 2017. 3D printing of hybrid biomaterials for bone tissue engineering: Calcium-polyphosphate microparticles encapsulated by polycaprolactone. Acta Biomater. 64. 377-388.10.1016/j.actbio.2017.09.031Search in Google Scholar PubMed

[4] Dwivedi R., Kumar S., Pandey R., Mahajan A., Nandana D., Katti D. S., et al. 2020. Polycaprolactone as biomaterial for bone scaffolds: Review of literature. J Oral Biol Craniofac Res 10 (1). 381-388.10.1016/j.jobcr.2019.10.003Search in Google Scholar PubMed PubMed Central

[5] Calciolari E., Mardas N., Dereka X., Anagnostopoulos A., Tsangaris G., Donos N. 2018. Protein expression during early stages of bone regeneration under hydrophobic and hydrophilic titanium domes. A pilot study. J. Periodontal Res. 53 (2). 174-187.10.1111/jre.12498Search in Google Scholar PubMed

[6] Lotz E. M., Olivares-Navarrete R., Berner S., Boyan B. D., Schwartz Z. 2016. Osteogenic response of human MSCs and osteoblasts to hydrophilic and hydrophobic nanostructured titanium implant surfaces. J Biomed Mater Res A 104 (12). 3137-3148.10.1002/jbm.a.35852Search in Google Scholar PubMed

[7] Kermani F., Kargozar S., Tayarani-Najaran Z., Yousefi A., Beidokhti S. M., Moayed M. H. 2019. Synthesis of nano HA/βTCP mesoporous particles using a simple modification in granulation method. Mater. Sci. Eng., C 96. 859-871.Search in Google Scholar

[8] Mozafari M., Banijamali S., Baino F., Kargozar S., Hill R. G. 2019. Calcium carbonate: Adored and ignored in bioactivity assessment. Acta Biomater. 91. 35-47.10.1016/j.actbio.2019.04.039Search in Google Scholar PubMed

[9] da Fonseca G. F., Avelino S. d. O. M., Mello D. d. C. R., do Prado R. F., Campos T. M. B., de Vasconcellos L. M. R., et al. 2020. Scaffolds of PCL combined to bioglass: synthesis, characterization and biological performance. J. Mater. Sci. Mater. Med. 31. 41.Search in Google Scholar

[10] Kolan K., Li J., Roberts S., Semon J. A., Park J., Day D. E., et al. 2019. Near-field electrospinning of a polymer/bioactive glass composite to fabricate 3D biomimetic structures. International Journal of Bioprinting 5 (1).10.18063/ijb.v5i1.163Search in Google Scholar PubMed PubMed Central

[11] Tamjid E., Bagheri R., Vossoughi M., Simchi A. 2011. Effect of particle size on the in vitro bioactivity, hydrophilicity and mechanical properties of bioactive glass-reinforced polycaprolactone composites. Mater. Sci. Eng., C 31 (7). 1526-1533.Search in Google Scholar

[12] Hoppe A., Mouriño V., Boccaccini A. R. 2013. Therapeutic inorganic ions in bioactive glasses to enhance bone formation and beyond. Biomater. Sci 1 (3). 254-256.10.1039/C2BM00116KSearch in Google Scholar PubMed

[13] Kermani F., Mollazadeh Beidokhti S., Baino F., Gholamzadeh-Virany Z., Mozafari M., Kargozar S. 2020. Strontium-and Cobalt-Doped Multicomponent Mesoporous Bioactive Glasses (MBGs) for Potential Use in Bone Tissue Engineering Applications. Materials 13 (6). 1348.10.3390/ma13061348Search in Google Scholar PubMed PubMed Central

[14] Kargozar S., Montazerian M., Fiume E., Baino F. 2019. Multiple and promising applications of Sr-containing bioactive glasses in bone tissue engineering. Front. Bioeng. Biotechnol. 7. 161.10.3389/fbioe.2019.00161Search in Google Scholar

[15] Kargozar S., Lotfibakhshaiesh N., Ai J., Mozafari M., Brouki Milan P., Hamzehlou S., et al. 2017. Strontium- and cobalt-substituted bioactive glasses seeded with human umbilical cord perivascular cells to promote bone regeneration via enhanced osteogenic and angiogenic activities. Acta Biomater. 58. 502-514.10.1016/j.actbio.2017.06.021Search in Google Scholar

[16] Ma H., Feng C., Chang J., Wu C. 2018. 3D-printed bioceramic scaffolds: From bone tissue engineering to tumor therapy. Acta Biomater. 79. 37-59.10.1016/j.actbio.2018.08.026Search in Google Scholar

[17] Haleem A., Javaid M., Khan R. H., Suman R. 2020. 3D printing applications in bone tissue engineering. J Clin Orthop Trauma 11. S118-S124.10.1016/j.jcot.2019.12.002Search in Google Scholar

[18] Hutmacher D. W. 2000. Scaffolds in tissue engineering bone and cartilage. Biomaterials 21 (24). 2529-2543.10.1016/S0142-9612(00)00121-6Search in Google Scholar

[19] Barbeck M., Serra T., Booms P., Stojanovic S., Najman S., Engel E., et al. 2017. Analysis of the in vitro degradation and the in vivo tissue response to bi-layered 3d-printed scaffolds combining pla and biphasic pla/bioglass components–guidance of the inflammatory response as basis for osteochondral regeneration. Bioact. Mater. 2 (4). 208-223.10.1016/j.bioactmat.2017.06.001Search in Google Scholar

[20] Serra T., Planell J. A., Navarro M. 2013. High-resolution PLA-based composite scaffolds via 3-D printing technology. Acta Biomater. 9 (3). 5521-5530.10.1016/j.actbio.2012.10.041Search in Google Scholar

[21] Kolan K. C., Semon J. A., Bindbeutel A. T., Day D. E., Leu M. C. 2020. Bioprinting with bioactive glass loaded polylactic acid composite and human adipose stem cells. Bioprinting 18. e00075.10.1016/j.bprint.2020.e00075Search in Google Scholar

[22] Kargozar S., Lotfibakhshaiesh N., Ai J., Samadikuchaksaraie A., Hill R. G., Shah P. A., et al. 2016. Synthesis, physico-chemical and biological characterization of strontium and cobalt substituted bioactive glasses for bone tissue engineering. J. Non-Cryst. Solids 449. 133-140.Search in Google Scholar

[23] Yun H.-s., Kim S.-e., Park E. K. 2011. Bioactive glass–poly (ɛ-caprolactone) composite scaffolds with 3 dimensionally hierarchical pore networks. Mater. Sci. Eng., C 31 (2). 198-205.Search in Google Scholar

[24] Landi E., Tampieri A., Celotti G., Sprio S. 2000. Densification behaviour and mechanisms of synthetic hydroxyapatites. J. Eur. Ceram. Soc. 20 (14-15). 2377-2387.10.1016/S0955-2219(00)00154-0Search in Google Scholar

[25] Kokubo T., Takadama H. 2006. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27 (15). 2907-2915.10.1016/j.biomaterials.2006.01.017Search in Google Scholar PubMed

[26] Nommeots-Nomm A., Labbaf S., Devlin A., Todd N., Geng H., Solanki A. K., et al. 2017. Highly degradable porous melt-derived bioactive glass foam scaffolds for bone regeneration. Acta Bio-mater. 57. 449-461.10.1016/j.actbio.2017.04.030Search in Google Scholar

[27] Ghasemi-Mobarakeh L., Prabhakaran M. P., Morshed M., Nasr-Esfahani M.-H., Ramakrishna S. 2008. Electrospun poly (ε-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29 (34). 4532-4539.10.1016/j.biomaterials.2008.08.007Search in Google Scholar

[28] Li X., Shi J., Dong X., Zhang L., Zeng H. 2008. A mesoporous bioactive glass/polycaprolactone composite scaffold and its bioactivity behavior. J Biomed Mater Res A 84 (1). 84-91.10.1002/jbm.a.31371Search in Google Scholar

[29] Ma T., MacKenzie J. D. 2019. Fully printed, high energy density flexible zinc-air batteries based on solid polymer electrolytes and a hierarchical catalyst current collector. Flex. Print. Electron. 4 (1). 015010.Search in Google Scholar

[30] Thornton A., Saad J., Clayton J. 2019. Measuring the critical attributes of AM powders. Met. Powder Rep. 74 (6). 314-319.10.1016/j.mprp.2019.01.006Search in Google Scholar

[31] Rad R. M., Alshemary A. Z., Evis Z., Keskin D., Tezcaner A. 2020. Cellulose acetate-gelatin coated boron-bioactive glass biocomposite scaffolds for bone tissue engineering. Biomed Mater.Search in Google Scholar

[32] Narayanan V., Sumathi S., Narayanasamy A. N. R. 2020. Tri-component composite containing copper-hydroxyapatite/chitosan/polyvinyl pyrrolidone for bone tissue engineering. J Biomed Mater Res A 108 (9). 1867-1880.10.1002/jbm.a.36950Search in Google Scholar

[33] Baino F., Fiume E., Barberi J., Kargozar S., Marchi J., Massera J., et al. 2019. Processing methods for making porous bioactive glass-based scaffolds—A state-of-the-art review. Int. J. Appl. Ceram. Technol. 16 (5). 1762-1796.10.1111/ijac.13195Search in Google Scholar

[34] Kweon H., Yoo M. K., Park I. K., Kim T. H., Lee H. C., Lee H.-S., et al. 2003. A novel degradable polycaprolactone networks for tissue engineering. Biomaterials 24 (5). 801-808.10.1016/S0142-9612(02)00370-8Search in Google Scholar

[35] Chen E.-C., Wu T.-M. 2007. Isothermal crystallization kinetics and thermal behavior of poly (ɛ-caprolactone)/multi-walled carbon nanotube composites. Polym. Degradation Stab. 92 (6). 1009-1015.10.1016/j.polymdegradstab.2007.02.019Search in Google Scholar

[36] Visan A. I., Popescu-Pelin G., Gherasim O., Mihailescu A., Socol M., Zgura I., et al. 2020. Long-term evaluation of dip-coated pcl-blend-peg coatings in simulated conditions. Polymers 12 (3). 717.10.3390/polym12030717Search in Google Scholar PubMed PubMed Central

[37] An J., Teoh J. E. M., Suntornnond R., Chua C. K. 2015. Design and 3D printing of scaffolds and tissues. Engineering 1 (2). 261-268.10.15302/J-ENG-2015061Search in Google Scholar

[38] Ishutov S., Hasiuk F. J., Harding C., Gray J. N. 2015. 3D printing sandstone porosity models. Interpretation 3 (3). SX49-SX61.10.1190/INT-2014-0266.1Search in Google Scholar

[39] Correa E., Moncada M., Zapata V. 2017. Electrical characterization of an ionic conductivity polymer electrolyte based on polycaprolactone and silver nitrate for medical applications. Mater. Lett. 205. 155-157.10.1016/j.matlet.2017.06.046Search in Google Scholar

[40] Poh P. S., Hutmacher D. W., Stevens M. M., Woodruff M. A. 2013. Fabrication and in vitro characterization of bioactive glass composite scaffolds for bone regeneration. Biofabrication 5 (4). 045005.10.1088/1758-5082/5/4/045005Search in Google Scholar PubMed

[41] Tainio J., Paakinaho K., Ahola N., Hannula M., Hyttinen J., Kellomäki M., et al. 2017. In vitro degradation of borosilicate bioactive glass and poly (l-lactide-co-ɛ-caprolactone) composite scaffolds. Materials 10 (11). 1274.10.3390/ma10111274Search in Google Scholar PubMed PubMed Central

[42] Hench L. L. 1991. Bioceramics: from concept to clinic. J. Am. Ceram. Soc. 74 (7). 1487-1510.10.1111/j.1151-2916.1991.tb07132.xSearch in Google Scholar

[43] Kermani F., Mollazadeh S., Khaki J. V. 2019. A simple thermodynamics model for estimation and comparison the concentration of oxygen vacancies generated in oxide powders synthesized via the solution combustion method. Ceram. Int. 45 (10). 13496-13501.10.1016/j.ceramint.2019.04.053Search in Google Scholar

[44] Kermani F., Gharavian A., Mollazadeh S., Kargozar S., Youssefi A., Vahdati Khaki J. 2020. Silicon-doped calcium phosphates; the critical effect of synthesis routes on the biological performance. Mater. Sci. Eng., C 111. 110828.Search in Google Scholar

[45] Nazeer M. A., Yilgor E., Yilgor I. 2019. Electrospun polycaprolactone/silk fibroin nanofibrous bioactive scaffolds for tissue engineering applications. Polymer 168. 86-94.10.1016/j.polymer.2019.02.023Search in Google Scholar

[46] Heid S., Boccaccini A. R. 2020. Advancing bioinks for 3D bioprinting using reactive fillers: A review. Acta Biomater. 113. 1-22.10.1016/j.actbio.2020.06.040Search in Google Scholar PubMed

[47] Distler T., Fournier N., Grünewald A., Polley C., Seitz H., Detsch R., et al. 2020. Polymer-Bioactive Glass Composite Filaments for 3D Scaffold Manufacturing by Fused Deposition Modeling: Fabrication and Characterization. Front. Bioeng. Biotechnol. 8. 552.10.3389/fbioe.2020.00552Search in Google Scholar PubMed PubMed Central

[48] Bejarano J., Boccaccini A. R., Covarrubias C., Palza H. 2020. Effect of Cu-and Zn-Doped Bioactive Glasses on the In Vitro Bioactivity, Mechanical and Degradation Behavior of Biodegradable PDLLA Scaffolds. Materials 13 (13). 2908.Search in Google Scholar

[49] Shorvazi S., Kermani F., Mollazadeh S., Kiani-Rashid A., Kargozar S., Youssefi A. 2020. Coating Ti6Al4V substrate with the triple-layer glass-ceramic compositions using sol–gel method; the critical effect of the composition of the layers on the mechanical and in vitro biological performance. J. Sol-Gel Sci. Technol. 1-11.10.1007/s10971-020-05233-ySearch in Google Scholar

[50] Houaoui A., Lyyra I., Agniel R., Pauthe E., Massera J., Boissière M. 2020. Dissolution, bioactivity and osteogenic properties of composites based on polymer and silicate or borosilicate bioactive glass. Mater. Sci. Eng., C 107. 110340.Search in Google Scholar

[51] López-Noriega A., Arcos D., Izquierdo-Barba I., Sakamoto Y., Terasaki O., Vallet-Regí M. 2006. Ordered mesoporous bioactive glasses for bone tissue regeneration. Chem. Mater. 18 (13). 3137-3144.10.1021/cm060488oSearch in Google Scholar

[52] Mondal D., Griffith M., Venkatraman S. S. 2016. Polycaprolactone-based biomaterials for tissue engineering and drug delivery: Current scenario and challenges. Int J Polym Mater 65 (5). 255-265.10.1080/00914037.2015.1103241Search in Google Scholar

Received: 2020-08-10
Revised: 2020-12-02
Accepted: 2020-12-02
Published Online: 2020-12-31

© 2020 Amirhosein Fathi et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Downloaded on 1.3.2024 from https://www.degruyter.com/document/doi/10.1515/bglass-2020-0006/html
Scroll to top button