journal article·2021-02-05Open access

Electrospun Poly(butylene-adipate-co-terephthalate)/Nano-hyDroxyapatite/Graphene Nanoribbon Scaffolds Improved the In Vivo Osteogenesis of the Neoformed Bone

Luana Marotta Reis Vasconcellos, Gabriela F. Santana-Melo, Edmundo Silva, Vanessa Fernandes Pereira, Juliani Caroline Ribeiro Araújo, André Diniz Rosa Silva, André S. A. Furtado, Conceição de Maria Vaz Elias, Bartolomeu Cruz Viana, Fernanda Roberta Marciano, Anderson Oliveira Lobo

Abstract

Electrospun ultrathin fibrous scaffold filed with synthetic nanohydroxyapatite (nHAp) and graphene nanoribbons (GNR) has bioactive and osteoconductive properties and is a plausible strategy to improve bone regeneration. Poly(butylene-adipate-co-terephthalate) (PBAT) has been studied as fibrous scaffolds due to its low crystallinity, faster biodegradability, and good mechanical properties; however, its potential for in vivo applications remains underexplored. We proposed the application of electrospun PBAT with high contents of incorporated nHAp and nHAp/GNR nanoparticles as bone grafts. Ultrathin PBAT, PBAT/nHAp, and PBAT/nHAp/GNR fibers were produced using an electrospinning apparatus. The produced fibers were characterized morphologically and structurally using scanning electron (SEM) and high-resolution transmission electron (TEM) microscopies, respectively. Mechanical properties were analyzed using a texturometer. All scaffolds were implanted into critical tibia defects in rats and analyzed after two weeks using radiography, microcomputed tomography, histological, histomorphometric, and biomechanical analyses. The results showed through SEM and high-resolution TEM characterized the average diameters of the fibers (ranged from 0.208 µm ± 0.035 to 0.388 µm ± 0.087) and nHAp (crystallite around 0.28, 0.34, and 0.69 nm) and nHAp/GNR (200–300 nm) nanoparticles distribution into PBAT matrices. Ultrathin fibers were obtained, and the incorporated nHAp and nHAp/GNR nanoparticles were well distributed into PBAT matrices. The addition of nHAp and nHAp/GNR nanoparticles improved the elastic modulus of the ultrathin fibers compared to neat PBAT. High loads of nHAp/GNR (PBATnH5G group) improved the in vivo lamellar bone formation promoting greater radiographic density, trabecular number and stiffness in the defect area 2 weeks after implantation than control and PBAT groups.
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Research context

OpenAlex topics: Bone Tissue Engineering Materials · Electrospun Nanofibers in Biomedical Applications · Graphene and Nanomaterials Applications

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

Affiliations

Department of Bioscience and Oral Diagnosis, Institute of Science and Technology, Sao Paulo State University, Sao Paulo 12450-000, Brazil

Air Force Academy, Brazilian Air Force, Pirassununga 13630-000, Brazil

LIMAV—Interdisciplinary Laboratory for Advanced Materials, UFPI-Federal University of Piaui, Teresina 64049-550, Brazil

Instituto Científico e Tecnológico, Universidade Brasil, Sao Paulo 12450-000, Brazil

Department of Physics, Federal University of Piaui, Teresina 64049-550, Brazil

Funding

Fundação de Amparo à Pesquisa do Estado de São Paulo · Conselho Nacional de Desenvolvimento Científico e Tecnológico

References (58)

Show source-provided references
1. Berton, F., Porrelli, D., Di Lenarda, R., and Turco, G. (2019). A Critical Review on the Production of Electrospun Nanofibres for Guided Bone Regeneration in Oral Surgery. Nanomaterials, 10.10.3390/nano10010016 ↗
2. Development of biomimetic electrospun polymeric biomaterials for bone tissue engineering. A review10.1080/09205063.2019.1630699 ↗
3. Current progress in application of polymeric nanofibers to tissue engineering10.1186/s40580-019-0209-y ↗
4. Udomluck, N., Koh, W.G., Lim, D.J., and Park, H. (2020). Recent Developments in Nanofiber Fabrication and Modification for Bone Tissue Engineering. Int. J. Mol. Sci., 21.10.3390/ijms21010099 ↗
5. Poly(butylene adipate-co-terephthalate) scaffolds: Processing, structural characteristics and cellular responses10.1080/09205063.2016.1239945 ↗
6. Enhanced osteogenic activity with boron-doped nanohydroxyapatite-loaded poly (butylene adipate-co-terephthalate) fibrous 3D matrix10.1080/21691401.2018.1470522 ↗
7. Designing a novel nanocomposite for bone tissue engineering using electrospun conductive PBAT/polypyrrole as a scaffold to direct nanohydroxyapatite electrodeposition10.1039/C6RA00889E ↗
8. Elias, C.D.V., Maia, A.L.M., da Silva, L.R., do Amaral, F.P.D., Webster, T.J., Marciano, F.R., and Lobo, A.O. (2019). In Vivo Evaluation of the Genotoxic Effects of Poly(Butylene adipate-co-terephthalate)/Polypyrrole with Nanohydroxyapatite Scaffolds for Bone Regeneration. Materials, 12.10.3390/ma12081330 ↗
9. Neto, W., Santos, J., Averous, L., Schlatter, G., and Bretas, R. (2014, January 6–12). Composites Structures for Bone Tissue Reconstruction. Proceedings of the Preface: 30th International Conference of the Polymer, Cleveland, OH, USA.10.1063/1.4918448 ↗
10. Poly(butylene adipate-co-terephthalate)/hydroxyapatite composite structures for bone tissue recovery10.1016/j.polymdegradstab.2015.06.009 ↗
11. Influence of low contents of superhydrophilic MWCNT on the properties and cell viability of electrospun poly(butylene adipate-co-terephthalate) fibers10.1016/j.msec.2015.10.075 ↗
12. Electrospun ultrathin PBAT/nHAp fibers influenced the in vitro and in vivo osteogenesis and improved the mechanical properties of neoformed bone10.1016/j.colsurfb.2017.04.053 ↗
13. Silva, A.D., Rodrigues, B.V.M., Oliveira, F.C., Carvalho, J.O., de Vasconcellos, L.M.R., de Araujo, J.C.R., Marciano, F.R., and Lobo, A.O. (2019). Characterization and in vitro and in vivo assessment of poly(butylene adipate-co-terephthalate)/nano-hydroxyapatite composites as scaffolds for bone tissue engineering. J. Polym. Res., 26.10.1007/s10965-019-1706-8 ↗
14. An overview on properties and applications of poly (butylene adipate-co-terephthalate)–PBAT based composites10.1002/pen.24770 ↗
15. Nano-hydroxyapatite and its applications in preventive, restorative and regenerative dentistry: A review of literature
16. In vitro and in vivo studies of novel poly(D, L-lactic acid), superhydrophilic carbon nanotubes, and nanohydroxyapatite scaffolds for bone regeneration10.1021/acsami.5b01066 ↗
17. Assisted deposition of nano-hydroxyapatite onto exfoliated carbon nanotube oxide scaffolds10.1039/C4NR07317G ↗
18. Fast preparation of free-standing nanohydroxyapatite–vertically aligned carbon nanotube scaffolds10.1039/c3tb21525c ↗
19. Graphene oxide/multi-walled carbon nanotubes as nanofeatured scaffolds for the assisted deposition of nanohydroxyapatite: Characterization and biological evaluation
20. Three dimensional macroporous architectures and aerogels built of carbon nanotubes and/or graphene: Synthesis and applications10.1039/C2CS35353A ↗
21. A review on carbon nanotubes and graphene as fillers in reinforced polymer nanocomposites10.1016/j.jiec.2014.03.022 ↗
22. Large-scale molecular simulations on the mechanical response and failure behavior of a defective graphene: Cases of 5-8-5 defects
23. Strength and failure behavior of a graphene sheet containing bi-grain-boundaries10.1039/C4RA10126J ↗
24. In vitro and in vivo evaluation of rotary-jet-spun poly(-caprolactone) with high loading of nano-hydroxyapatite10.1007/s10856-019-6222-1 ↗
25. Graphene and carbon nanotube nanocomposite for gene transfection10.1016/j.msec.2014.03.002 ↗
26. Graphene oxide nanoribbons as nanomaterial for bone regeneration: Effects on cytotoxicity, gene expression and bactericidal effect10.1016/j.msec.2017.03.278 ↗
27. Nanohydroxyapatite/Graphene Nanoribbons Nanocomposites Induce in Vitro Osteogenesis and Promote in Vivo Bone Neoformation
28. In vitro osteogenesis process induced by hybrid nanohydroxyapatite/graphene nanoribbons composites10.1007/s10856-019-6271-5 ↗
29. High loads of nano-hydroxyapatite/graphene nanoribbon composites guided bone regeneration using an osteoporotic animal model10.2147/IJN.S192456 ↗
30. (2021, February 04). NIH IMAGE, Available online: https://imagej.nih.gov/nih-image/.
31. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research10.1177/0271678X20943823 ↗
32. Titanium scaffold osteogenesis in healthy and osteoporotic rats is improved by the use of low-level laser therapy (GaAlAs)10.1007/s10103-016-1930-y ↗
33. Healing of normal and osteopenic bone with titanium implant and low-level laser therapy (GaAlAs): A histomorphometric study in rats10.1007/s10103-013-1326-1 ↗
34. Rotary-jet spun polycaprolactone/nano-hydroxyapatite scaffolds modified by simulated body fluid influenced the flexural mode of the neoformed bone10.1007/s10856-020-06403-8 ↗
35. Design of dental implants, influence on the osteogenesis and fixation10.1007/s10856-008-3421-6 ↗
36. A facile method to in situ formation of hydroxyapatite single crystal architecture for enhanced osteoblast adhesion10.1039/c2jm34367c ↗
37. Lee, H.-B., Hsu, H.-C., Wu, S.-C., Hsu, S.-K., Wang, P.-H., and Ho, W.-F. (2016). Microstructure and characteristics of calcium phosphate layers on bioactive oxide surfaces of air-sintered titanium foams after immersion in simulated body fluid. Materials, 9.10.3390/ma9120956 ↗
38. Beaded nanofibers formed during electrospinning10.1016/S0032-3861(99)00068-3 ↗
39. Mapping the Influence of Solubility and Dielectric Constant on Electrospinning Polycaprolactone Solutions10.1021/ma300656u ↗
40. Fabrication and characterization of three-dimensional nanofiber membrance of PCL–MWCNTs by electrospinning10.1016/j.msec.2010.05.003 ↗
41. The effect of multi-walled carbon nanotubes on morphology, crystallinity and mechanical properties of PBT/MWCNT composite nanofibers10.1007/s10965-012-0065-5 ↗
42. Biomechanical comparison of dynamic condylar screw and locking compression plate fixation in unstable distal femoral fractures: An in vitro study10.4103/0019-5413.121594 ↗
43. Estudo biomecânico da fixação da fratura sacroilíaca com barras de titânio e parafusos pediculares10.1590/1413-78522015230300970 ↗
44. Microstructure development in electrospun carbon nanotube reinforced polyvinylidene fluoride fibers and its influence on tensile strength and dielectric permittivity10.1016/j.compscitech.2013.08.021 ↗
45. Comparative Study of Bone Neoformation Using Autologous Grafing and Three Replancements: Bone Defects in Rats10.1590/S0102-36162009000400008 ↗
46. Fernández, R.F., Bucchi, C., Navarro, P., Beltrán, V., and Borie, E. (2015). Bone grafts utilized in dentistry: An analysis of patients’ preferences. BMC. Med. Ethics., 16.10.1186/s12910-015-0044-6 ↗
47. Li, B., and Webster, T. (2018). Biomaterials for Bone Tissue Engineering: Recent Advances and Challenges. Orthopedic Biomaterials: Progress in Biology, Manufacturing, and Industry Perspectives, Springer International Publishing.
48. Li, B., Moriarty, T.F., Webster, T., and Xing, M. (2020). Advances in Antimicrobial and Osteoinductive Biomaterials. Racing for the Surface: Antimicrobial and Interface Tissue Engineering, Springer International Publishing.10.1007/978-3-030-34471-9 ↗
49. Preparation and properties of elastomeric polyurethane/organically modified montmorillonite nanocomposites10.1007/s10965-009-9371-y ↗
50. Characterization of nanocomposites of poly(butylene adipate-co-terephthalate) blending with organoclay10.1007/s10965-011-9625-3 ↗
51. The optical properties of PVA/TiO2 composite nanofibers10.1002/app.39147 ↗
52. Baghdadite nanoparticle-coated poly l-lactic acid (PLLA) ceramics scaffold improved osteogenic differentiation of adipose tissue-derived mesenchymal stem cells10.1002/jbm.a.36638 ↗
53. PBAT based nanocomposites for medical and industrial applications10.1016/j.msec.2012.04.005 ↗
54. Versatility of chitosan-based biomaterials and their use as scaffolds for tissue regeneration10.1155/2017/8639898 ↗
55. Carbon based nanomaterials for tissue engineering of bone: Building new bone on small black scaffolds: A review10.1016/j.jare.2019.03.011 ↗
56. Li, Y., Liao, C., and Tjong, S.C. (2019). Synthetic biodegradable aliphatic polyester nanocomposites reinforced with nanohydroxyapatite and/or graphene oxide for bone tissue engineering applications. Nanomaterials, 9.10.3390/nano9040590 ↗
57. Effects of nanopores on the mechanical strength, osteoclastogenesis, and osteogenesis in honeycomb scaffolds10.1039/D0TB01498B ↗
58. 3D printed porous PLA/nHA composite scaffolds with enhanced osteogenesis and osteoconductivity in vivo for bone regeneration10.1088/1748-605X/ab388d ↗