Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-27T22:23:49.398Z Has data issue: false hasContentIssue false

Electrodeposition of bactericidal and bioactive nano-hydroxyapatite onto electrospun piezoelectric polyvinylidene fluoride scaffolds

Published online by Cambridge University Press:  16 November 2020

Pedro J. G. Rodrigues
Affiliation:
LIMAV — Interdisciplinary Laboratory for Advanced Materials, BioMatLab Group, Materials Science & Engineering Graduate Program, UFPI — Federal University of Piauí, 64049-550Teresina, Piauí, Brazil
Conceição de M. V. Elias
Affiliation:
Instituto Científico e Tecnológico, Universidade Brasil, 08230-030 São Paulo, Brazil
Bartolomeu C. Viana
Affiliation:
LIMAV — Interdisciplinary Laboratory for Advanced Materials, BioMatLab Group, Materials Science & Engineering Graduate Program, UFPI — Federal University of Piauí, 64049-550Teresina, Piauí, Brazil Department of Physics, UFPI — Federal University of Piauí, 64049-550Teresina, PI, Brazil
Luciana M. de Hollanda
Affiliation:
Universidade UniMetrocamp, 13035-500 Campinas, São Paulo, Brazil Faculty of Medical Sciences, State University of Campinas, 13083-970 Campinas, São Paulo, Brazil
Thiago D. Stocco
Affiliation:
Faculty of Medical Sciences, State University of Campinas, 13083-970 Campinas, São Paulo, Brazil University of Santo Amaro, 04829-300São Paulo, Brazil
Luana M. R. de Vasconcellos
Affiliation:
Department of Bioscience and Oral Diagnosis, Institute of Science and Technology, Sao Paulo State University, 12247-004 Sao Jose dos Campos, Sao Paulo, Brazil
Daphne de C. R. Mello
Affiliation:
Department of Bioscience and Oral Diagnosis, Institute of Science and Technology, Sao Paulo State University, 12247-004 Sao Jose dos Campos, Sao Paulo, Brazil
Francisco E. P. Santos
Affiliation:
LIMAV — Interdisciplinary Laboratory for Advanced Materials, BioMatLab Group, Materials Science & Engineering Graduate Program, UFPI — Federal University of Piauí, 64049-550Teresina, Piauí, Brazil Department of Physics, UFPI — Federal University of Piauí, 64049-550Teresina, PI, Brazil
Fernanda R. Marciano
Affiliation:
Department of Physics, UFPI — Federal University of Piauí, 64049-550Teresina, PI, Brazil
Anderson O. Lobo*
Affiliation:
LIMAV — Interdisciplinary Laboratory for Advanced Materials, BioMatLab Group, Materials Science & Engineering Graduate Program, UFPI — Federal University of Piauí, 64049-550Teresina, Piauí, Brazil
*
a)Address all correspondence to this author. e-mail: [email protected]
Get access

Abstract

The fibrous scaffolds for bone tissue engineering that mimic the extracellular matrix with bioactive and bactericidal properties could provide adequate conditions for regeneration of damaged bone. Electrospun ultrathin fiber covered with nano-hydroxyapatite is a favorable fibrous scaffold design. We developed a fast and reproducible strategy to produce polyvinylidene fluoride (PVDF)/nano-hydroxyapatite (nHAp) nanofibrous scaffolds with bactericidal and bioactive properties. Fibrous PVDF scaffolds were obtained first by the electrospinning method. Then, their surfaces were modified using oxygen plasma treatment followed by electrodeposition of nHAp. This process formed nanofibrous and superhydrophilic PVDF fibers (133.6 nm, fiber average diameter) covered with homogeneous nHAp (202.6 nm, average particle diameter) crystals. Energy-dispersive X-ray spectrometry demonstrated the presence of calcium phosphate, indicating a Ca/P molar ratio of approximately 1.64. X-ray diffraction, Fourier transform infrared spectroscopy, and Raman spectroscopy spectra identified β-phase of nHAp. Thermal analysis indicated a slight reduction in stability after nHAp electrodeposition. Bactericidal assays showed that nHAp exhibited 99.8% efficiency against Pseudomonas aeruginosa bacteria. The PVDF/Plasma and PVDF/nHAp groups had the highest cell viability, total protein, and alkaline phosphatase activity by 7 days after exposure of the scaffolds to MG63 cell culture. Therefore, the developed scaffolds are an exciting alternative for application in bone regeneration.

Type
Article
Copyright
Copyright © The Author(s), 2020, published on behalf of Materials Research Society by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Du, X., Wei, D., Huang, L., Zhu, M., Zhang, Y., and Zhu, Y.: 3D printing of mesoporous bioactive glass/silk fibroin composite scaffolds for bone tissue engineering. Mater. Sci. Eng. C 103, 109731 (2019).CrossRefGoogle ScholarPubMed
Siqueira, I.A.W.B., Corat, M.A.F., Cavalcanti, B.d.N., Neto, W.A.R., Martin, A.A., Bretas, R.E.S., Marciano, F.R., and Lobo, A.O.: In vitro and in vivo studies of novel poly(d,l-lactic acid), superhydrophilic carbon nanotubes, and nanohydroxyapatite scaffolds for bone regeneration. ACS Appl. Mater. Interfaces 7, 9385 (2015).CrossRefGoogle Scholar
Rodríguez-Hernández, J.: Antimicrobial/antifouling surfaces obtained by surface modification. In Polymers Against Microorganisms Race to Efficient Antimicrobial Mater, Rodríguez-Hernández, J., ed. (Springer International Publishing, Cham, 2017), pp. 95123.CrossRefGoogle Scholar
Machado-Paula, M.M., Corat, M.A.F., Lancellotti, M., Mi, G., Marciano, F.R., Vega, M.L., Hidalgo, A.A., Webster, T.J., and Lobo, A.O.: A comparison between electrospinning and rotary-jet spinning to produce PCL fibers with low bacteria colonization. Mater. Sci. Eng. C 111, 110706 (2020).CrossRefGoogle ScholarPubMed
Tandon, B., Kamble, P., Olsson, R.T., Blaker, J.J., and Cartmell, S.H.: Fabrication and characterisation of stimuli responsive piezoelectric PVDF and hydroxyapatite-filled PVDF fibrous membranes. Molecules 24, 1903 (2019).CrossRefGoogle ScholarPubMed
Dubey, A.K., Kinoshita, R., and Kakimoto, K.I.: Piezoelectric sodium potassium niobate mediated improved polarization and in vitro bioactivity of hydroxyapatite. RSC Adv. 5, 19638 (2015).CrossRefGoogle Scholar
Han, X., Zhou, X., Qiu, K., Feng, W., Mo, H., Wang, M., Wang, J., and He, C.: Strontium-incorporated mineralized PLLA nanofibrous membranes for promoting bone defect repair. Colloids Surf. B 179, 363 (2019).CrossRefGoogle ScholarPubMed
De Castro, J.G., Rodrigues, B.V.M., Ricci, R., Costa, M.M., Ribeiro, A.F.C., Marciano, F.R., and Lobo, A.O.: Designing a novel nanocomposite for bone tissue engineering using electrospun conductive PBAT/polypyrrole as a scaffold to direct nanohydroxyapatite electrodeposition. RSC Adv. 6, 32615 (2016).CrossRefGoogle Scholar
Bhattacharjee, P., Naskar, D., Maiti, T.K., Bhattacharya, D., and Kundu, S.C.: Non-mulberry silk fibroin grafted poly (Ie-caprolactone)/nano hydroxyapatite nanofibrous scaffold for dual growth factor delivery to promote bone regeneration. J. Colloid Interface Sci. 472, 16 (2016).CrossRefGoogle Scholar
Vaněk, P., Kolská, Z., Luxbacher, T., García, J.A.L., Lehocký, M., Vandrovcová, M., Bačáková, L., and Petzelt, J.: Electrical activity of ferroelectric biomaterials and its effects on the adhesion, growth and enzymatic activity of human osteoblast-like cells. J. Phys. D. Appl. Phys. 49, 175403 (2016).CrossRefGoogle Scholar
Genchi, G.G., Sinibaldi, E., Ceseracciu, L., Labardi, M., Marino, A., Marras, S., De Simoni, G., Mattoli, V., and Ciofani, G.: Ultrasound-activated piezoelectric P(VDF-TrFE)/boron nitride nanotube composite films promote differentiation of human SaOS-2 osteoblast-like cells. Nanomed. Nanotechnol. Biol. Med. 14, 2421 (2018).CrossRefGoogle ScholarPubMed
Ardeshiri, F., Salehi, S., Peyravi, M., Jahanshahi, M., Amiri, A., and Rad, A.S.: PVDF membrane assisted by modified hydrophobic ZnO nanoparticle for membrane distillation. Asia-Pacific J. Chem. Eng. 13, 1 (2018).CrossRefGoogle Scholar
Villarreal-Gómez, L.J., Cornejo-Bravo, J.M., Vera-Graziano, R., and Grande, D.: Electrospinning as a powerful technique for biomedical applications: A critically selected survey. J. Biomater. Sci. Polym. Ed. 27, 157 (2016).CrossRefGoogle ScholarPubMed
Dayaghi, E., Bakhsheshi-Rad, H.R., Hamzah, E., Akhavan-Farid, A., Ismail, A.F., Aziz, M., and Abdolahi, E.: Magnesium-zinc scaffold loaded with tetracycline for tissue engineering application: In vitro cell biology and antibacterial activity assessment. Mater. Sci. Eng. C 102, 53 (2019).CrossRefGoogle ScholarPubMed
Martins, P., Lopes, A.C., and Lanceros-Mendez, S.: Electroactive phases of poly(vinylidene fluoride): Determination, processing and applications. Prog. Polym. Sci. 39, 683 (2014).CrossRefGoogle Scholar
Wang, A., Liu, Z., Hu, M., Wang, C., Zhang, X., Shi, B., Fan, Y., Cui, Y., Li, Z., and Ren, K.: Piezoelectric nanofibrous scaffolds as in vivo energy harvesters for modifying fibroblast alignment and proliferation in wound healing. Nano Energy 43, 63 (2018).CrossRefGoogle Scholar
Ribeiro, C., Pärssinen, J., Sencadas, V., Correia, V., Miettinen, S., Hytönen, V.P., and Lanceros-Méndez, S.: Dynamic piezoelectric stimulation enhances osteogenic differentiation of human adipose stem cells. J. Biomed. Mater. Res. A 103, 2172 (2015).CrossRefGoogle ScholarPubMed
Jeong, H.-G., Han, Y.-S., Jung, K.-H., and Kim, Y.-J.: Poly(vinylidene fluoride) composite nanofibers containing polyhedral oligomeric silsesquioxane–epigallocatechin gallate conjugate for bone tissue regeneration. Nanomaterials 9, 184 (2019).CrossRefGoogle ScholarPubMed
Ribeiro Neto, W.A., de Paula, A.C.C., Martins, T.M.M., Goes, A.M., Averous, L., Schlatter, G., and Suman Bretas, R.E.: Poly (butylene adipate-co-terephthalate)/hydroxyapatite composite structures for bone tissue recovery. Polym. Degrad. Stab. 120, 61 (2015).CrossRefGoogle Scholar
Xu, J., Hu, X., Jiang, S., Wang, Y., Parungao, R., Zheng, S., Nie, Y., Liu, T., and Song, K.: The application of multi-walled carbon nanotubes in bone tissue repair hybrid scaffolds and the effect on cell growth in vitro. Polymers 11, 230 (2019).CrossRefGoogle ScholarPubMed
Rahman, M.M., Shahruzzaman, Md., Islam, Md. S., Khan, M.N., and Haque, P.: Preparation and properties of biodegradable polymer/nano-hydroxyapatite bioceramic scaffold for spongybone regeneration. J. Polym. Eng. 29, 134 (2019).CrossRefGoogle Scholar
Chatzipetros, E., Christopoulos, P., Donta, C., Tosios, K.-I., Tsiambas, E., Tsiourvas, D., Kalogirou, E.-M., and Tsiklakis, K.: Application of nano-hydroxyapatite/chitosan scaffolds on rat calvarial critical-sized defects: A pilot study. Med. Oral Pathol. Oral Cir. Bucal. 23, e625 (2018).Google ScholarPubMed
Santana-Melo, G.F., Rodrigues, B.V.M., da Silva, E., Ricci, R., Marciano, F.R., Webster, T.J., Vasconcellos, L.M.R., and Lobo, A.O.: Electrospun ultrathin PBAT/nHAp fibers influenced the in vitro and in vivo osteogenesis and improved the mechanical properties of neoformed bone. Colloids Surf. B 155, 544 (2017).CrossRefGoogle ScholarPubMed
Siqueira, I.A.W.B., Oliveira, C.A.G.S., Zanin, H., Grinet, M.A.V.M., Granato, A.E.C., Porcionatto, M.A., Marciano, F.R., and Lobo, A.O.: Bioactivity behaviour of nano-hydroxyapatite/freestanding aligned carbon nanotube oxide composite. J. Mater. Sci. Mater. Med. 26, 1 (2015).CrossRefGoogle ScholarPubMed
Elias, C.d.M.V., Maia Filho, A.L.M., da Silva, L.R., do Amaral, F.P.d.M., Webster, T.J., Marciano, F.R., and Lobo, A.O.: In vivo evaluation of the genotoxic effects of poly (butylene adipate-co-terephthalate)/polypyrrole with nanohydroxyapatite scaffolds for bone regeneration. Materials 12, 1330 (2019).CrossRefGoogle ScholarPubMed
Zanin, H., Rosa, C.M.R., Eliaz, N., May, P.W., Marciano, F.R., and Lobo, A.O.: Assisted deposition of nano-hydroxyapatite onto exfoliated carbon nanotube oxide scaffolds. Nanoscale 7, 10218 (2015).CrossRefGoogle ScholarPubMed
Wang, S., Zhong, S., Lim, C.T., and Nie, H.: Effects of fiber alignment on stem cells-fibrous scaffold interactions. J. Mater. Chem. B 3, 3358 (2015).CrossRefGoogle ScholarPubMed
Correia, D.M., Ribeiro, C., Sencadas, V., Botelho, G., Carabineiro, S.A.C., Ribelles, J.L.G., and Lanceros-Méndez, S.: Influence of oxygen plasma treatment parameters on poly(vinylidene fluoride) electrospun fiber mats wettability. Prog. Org. Coatings 85, 151 (2015).CrossRefGoogle Scholar
Cassella, J.P., Garrington, N., Stamp, T.C.B., and Ali, S.H.: An electron probe X-ray microanalytical study of bone mineral in osteogenesis imperfecta. Calcif. Tissue Int. 56, 118 (1995).CrossRefGoogle ScholarPubMed
Yee, W.A., Kotaki, M., Liu, Y., and Lu, X.: Morphology, polymorphism behavior and molecular orientation of electrospun poly(vinylidene fluoride) fibers. Polymer 48, 512 (2007).CrossRefGoogle Scholar
Pereira, J.D.A.S., Camargo, R.C.T., Filho, J.C.S.C., Alves, N., Rodriguez-Perez, M.A., and Constantino, C.J.L.: Biomaterials from blends of fluoropolymers and corn starch—implant and structural aspects. Mater. Sci. Eng. C 36, 226 (2014).CrossRefGoogle ScholarPubMed
Martinelli, N.M., Ribeiro, M.J.G., Ricci, R., Marques, M.A., Lobo, A.O., and Marciano, F.R.: In vitro osteogenesis stimulation via nano-hydroxyapatite/carbon nanotube thin films on biomedical stainless steel. Materials 11, 1555 (2018).Google ScholarPubMed
Shepelin, N.A., Glushenkov, A.M., Lussini, V.C., Fox, P.J., Dicinoski, G.W., Shapter, J.G., and Ellis, A.V.: New developments in composites, copolymer technologies and processing techniques for flexible fluoropolymer piezoelectric generators for efficient energy harvesting. Energy Environ. Sci. 12, 1143 (2019).CrossRefGoogle Scholar
Salimi, A. and Yousefi, A.A.: FTIR studies of β-phase crystal formation in stretched PVDF films. Polym. Test 22, 699 (2003).CrossRefGoogle Scholar
Sajkiewicz, P., Wasiak, A., and Goclowski, Z.: Phase transitions during stretching of poly(vinylidene fluoride). Eur. Polym. J. 35, 423 (1999).CrossRefGoogle Scholar
Hélary, G., Noirclère, F., Mayingi, J., and Migonney, V.: A new approach to graft bioactive polymer on titanium implants: Improvement of MG 63 cell differentiation onto this coating. Acta Biomater. 5, 124 (2009).CrossRefGoogle ScholarPubMed
Janakiraman, S., Surendran, A., Ghosh, S., Anandhan, S., and Venimadhav, A.: Electroactive poly(vinylidene fluoride) fluoride separator for sodium ion battery with high coulombic efficiency. Solid State Ionics 292, 130 (2016).CrossRefGoogle Scholar
Awanis Hashim, N., Liu, Y., and Li, K.: Stability of PVDF hollow fibre membranes in sodium hydroxide aqueous solution. Chem. Eng. Sci. 66, 1565 (2011).CrossRefGoogle Scholar
Correia, D.M., Nunes-Pereira, J., Alikin, D., Kholkin, A.L., Carabineiro, S.A.C., Rebouta, L., Rodrigues, M.S., Vaz, F., Costa, C.M., and Lanceros-Méndez, S.: Surface wettability modification of poly(vinylidene fluoride) and copolymer films and membranes by plasma treatment. Polymer 169, 138 (2019).CrossRefGoogle Scholar
Bormashenko, Y., Pogreb, R., Stanevsky, O., and Bormashenko, E.: Vibrational spectrum of PVDF and its interpretation. Polym. Test 23, 791 (2004).CrossRefGoogle Scholar
Rahimpour, A., Madaeni, S.S., Zereshki, S., and Mansourpanah, Y.: Preparation and characterization of modified nano-porous PVDF membrane with high antifouling property using UV photo-grafting. Appl. Surf. Sci. 255, 7455 (2009).CrossRefGoogle Scholar
Persano, L., Dagdeviren, C., Su, Y., Zhang, Y., Girardo, S., Pisignano, D., Huang, Y., and Rogers, J.A.: High performance piezoelectric devices based on aligned arrays of nanofibers of poly(vinylidenefluoride-co-trifluoroethylene). Nat. Commun. 4, 1610 (2013).CrossRefGoogle Scholar
Krajewski, A., Mazzocchi, M., Buldini, P.L., Ravaglioli, A., Tinti, A., Taddei, P., and Fagnano, C.: Synthesis of carbonated hydroxyapatites: Efficiency of the substitution and critical evaluation of analytical methods. J. Mol. Struct. 744–747, 221 (2005).CrossRefGoogle Scholar
De Paula, M.M.M., Bassous, N.J., Afewerki, S., Harb, S.V., Ghannadian, P., Marciano, F.R., Viana, B.C., Tim, C.R., Webster, T.J., and Lobo, A.O.: Understanding the impact of crosslinked PCL/ PEG/GelMA electrospun nanofibers on bactericidal activity. PLoS One 13, 1 (2018).CrossRefGoogle ScholarPubMed
Jacobs, M.A., Alwood, A., Thaipisuttikul, I., Spencer, D., Haugen, E., Ernst, S., Will, O., Kaul, R., Raymond, C., Levy, R., Chun-Rong, L., Guenthner, D., Bovee, D., Olson, M.V., and Manoil, C.: A genome-scale analysis for identification of genes required for growth or survival of haemophilus influenzae. Proc. Natl Acad. Sci. USA 99, 966 (2003).Google Scholar
Eliaz, N., Kopelovitch, W., Burstein, L., Kobayashi, E., and Hanawa, T.: Electrochemical processes of nucleation and growth of calcium phosphate on titanium supported by real-time quartz crystal microbalance measurements and X-ray photoelectron spectroscopy analysis. J. Biomed. Mater. Res. A 89, 270 (2009).CrossRefGoogle ScholarPubMed
Chan, C.M., Ko, T.M., and Hiraoka, H.: Polymer surface modification by plasmas and photons. Surf. Sci. Rep. 24, 1 (1996).CrossRefGoogle Scholar
Yildirim, E.D., Ayan, H., Vasilets, V.N., Fridman, A., Guceri, S., and Sun, W.: Effect of dielectric barrier discharge plasma on the attachment and proliferation of osteoblasts cultured over poly(ε-caprolactone) scaffolds. Plasma Process. Polym. 5, 58 (2008).CrossRefGoogle Scholar
Hao, L. and Lawrence, J.: On the role of CO2 laser treatment in the human serum albumin and human plasma fibronectin adsorption on zirconia (MGO-PSZ) bioceramic surface. J. Biomed. Mater. Res. A 69, 748 (2004).CrossRefGoogle ScholarPubMed
Kitsara, M., Blanquer, A., Murillo, G., Humblot, V., De Bragança Vieira, S., Nogués, C., Ibáñez, E., Esteve, J., and Barrios, L.: Permanently hydrophilic, piezoelectric PVDF nanofibrous scaffolds promoting unaided electromechanical stimulation on osteoblasts. Nanoscale 11, 8906 (2019).CrossRefGoogle ScholarPubMed
Silva, M.P., Costa, C.M., Sencadas, V., Paleo, A.J., and Lanceros-Méndez, S.: Degradation of the dielectric and piezoelectric response of β-poly(vinylidene fluoride) after temperature annealing. J. Polym. Res. 18, 1451 (2011).CrossRefGoogle Scholar
Mangindaan, D., Yared, I., Kurniawan, H., Sheu, J.-R., and Wang, M.-J.: Modulation of biocompatibility on poly(vinylidene fluoride) and polysulfone by oxygen plasma treatment and dopamine coating. J. Biomed. Mater. Res. A 100A, 3177 (2012).CrossRefGoogle Scholar
Chavan, P.N., Bahir, M.M., Mene, R.U., Mahabole, M.P., and Khairnar, R.S.: Study of nanobiomaterial hydroxyapatite in simulated body fluid: Formation and growth of apatite. Mater. Sci. Eng. B Solid-State Mater. Adv. Technol. 168, 224 (2010).CrossRefGoogle Scholar
Öner, M. and Ilhan, B.: Fabrication of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) biocomposites with reinforcement by hydroxyapatite using extrusion processing. Mater. Sci. Eng. C 65, 19 (2016).CrossRefGoogle ScholarPubMed
Oliveira, F.C., Carvalho, J.O., Gusmão, S.B.S., Gonçalves, L.d.S., Soares Mendes, L.M., Freitas, S.A.P., Gusmão, G.O.d.M., Viana, B.C., Marciano, F.R., and Lobo, A.O.: High loads of nano-hydroxyapatite/graphene nanoribbon composites guided bone regeneration using an osteoporotic animal model. Int. J. Nanomed. 14, 865 (2019).CrossRefGoogle ScholarPubMed
LeGeros, R.Z.: Monographs in oral science. In Calcium Phosphates in Oral Biology and Medicine, LeGeros, R.Z., ed. (Karger, New York, NY, 1991).Google ScholarPubMed
Zhang, M., juan Wang, A., ming Li, J., and Song, N.: Effect of stearic acid modified HAp nanoparticles in different solvents on the properties of Pickering emulsions and HAp/PLLA composites. Mater. Sci. Eng. C 79, 255 (2017).CrossRefGoogle ScholarPubMed
Nie, S., Zeng, J., Qin, H., Xu, X., Zeng, J., Yang, C., and Luo, J.: Improvement in the blood compatibility of polyvinylidene fluoride membranes via in situ cross-linking polymerization. Polym. Adv. Technol. 30, 923 (2019).CrossRefGoogle Scholar
Kumar, P.T.S., Srinivasan, S., Lakshmanan, V.K., Tamura, H., Nair, S.V., and Jayakumar, R.: Synthesis, characterization and cytocompatibility studies of α-chitin hydrogel/nano hydroxyapatite composite scaffolds. Int. J. Biol. Macromol. 49, 20 (2011).CrossRefGoogle ScholarPubMed
Tsonos, C., Zois, H., Kanapitsas, A., Soin, N., Siores, E., Peppas, G.D., Pyrgioti, E.C., Sanida, A., Stavropoulos, S.G., and Psarras, G.C.: Polyvinylidene fluoride/magnetite nanocomposites: Dielectric and thermal response. J. Phys. Chem. Solids 129, 378 (2019).CrossRefGoogle Scholar
Enayati, M.S., Esmaeely Neisiany, R., Sajkiewicz, P., Behzad, T., Denis, P., and Pierini, F.: Effect of nanofiller incorporation on thermomechanical and toughness of poly (vinyl alcohol)-based electrospun nanofibrous bionanocomposites. Theor. Appl. Fract. Mech. 99, 44 (2019).CrossRefGoogle Scholar
Dhom, J., Bloes, D.A., Peschel, A., and Hofmann, U.K.: Bacterial adhesion to suture material in a contaminated wound model: Comparison of monofilament, braided, and barbed sutures. J. Orthop. Res. 35, 925 (2017).CrossRefGoogle Scholar
Saravanan, S., Nethala, S., Pattnaik, S., Tripathi, A., Moorthi, A., and Selvamurugan, N.: Preparation, characterization and antimicrobial activity of a bio-composite scaffold containing chitosan/nano-hydroxyapatite/nano-silver for bone tissue engineering. Int. J. Biol. Macromol. 49, 188 (2011).CrossRefGoogle ScholarPubMed
Lincks, J., Boyan, B.D., Blanchard, C.R., Lohmann, C.H., Liu, Y., Cochran, D.L., Dean, D.D., and Schwartz, Z.: Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomater. Silver Jubil. Compend. 19, 147 (1998).CrossRefGoogle ScholarPubMed
Tang, Y., Wu, C., Wu, Z., Hu, L., Zhang, W., and Zhao, K.: Fabrication and in vitro biological properties of piezoelectric bioceramics for bone regeneration. Sci. Rep. 7, 1 (2017).Google ScholarPubMed
Abazari, M.F., Hosseini, Z., Zare Karizi, S., Norouzi, S., Amini Faskhoudi, M., Saburi, E., Enderami, S.E., Ardeshirylajimi, A., and Mohajerani, H.: Different osteogenic differentiation potential of mesenchymal stem cells on three different polymeric substrates. Gene 740, 144534 (2020).CrossRefGoogle ScholarPubMed
De Andrade, D.P., De Vasconcellos, L.M.R., Silva Carvalho, I.C., Forte, L.F.D.B.P., De Souza Santos, E.L., Do Prado, R.F., Dos Santos, D.R., Alves Cairo, C.A., and Carvalho, Y.R.: Titanium-35niobium alloy as a potential material for biomedical implants: In vitro study. Mater. Sci. Eng. C 56, 538 (2015).CrossRefGoogle ScholarPubMed

Rodrigues et al. supplementary material

Rodrigues et al. supplementary material

Download Rodrigues et al. supplementary material(Video)
Video 10.2 MB