Abstract
We report an experimental and theoretical study of the rheological properties of magnetic biogels consisting of fibrin polymer networks with embedded magnetite nanoparticles, swollen by aqueous solutions. We studied two types of magnetic biogels, differenced by the presence or absence of an applied magnetic field during the initial steps of cross-linking. The experiments demonstrated very strong dependence of the elastic modulus of the magnetic biogels on the concentration of the magnetic particles. We finally developed some theoretical models that explain the observed strong concentration effects.
Similar content being viewed by others
References
Bose, H., Rabindranath, R., Ehrlich, J.: Soft magnetorheological elastomers as new actuators for valves. J. Intell. Mater. Syst. Struct. 23(9), 989–994 (2012)
Filipcsei, G., Csetneki, I., Szilagyi, A., Zrınyi, M.: Magnetic field-responsive smart polymer composites. In: Advances in Polymer Science, vol. 206. Springer, Berlin Heidelberg, pp. 137–189 (2007)
Boczkowska, A., Awietjan, S.: Tuning active magnetorheological elastomers for damping applications. Mater. Sci. Forum 636–637, 766–771 (2010)
Dyke, S., Spencer, B., Sain, M., Carlson, J.: Modeling and control of magnetorheological dampers for seismic response reduction. Smart Mater. Struct. 5(5), 565–575 (1996)
Occhiuzzi, A., Spizzuoco, M., Serino, G.: Experimental analysis of magnetorheological dampers for structural control. Smart Mater. Struct. 12, 703–711 (2003)
Carmona, F., Mouney, C.: Temperature-dependent resistivity and conduction mechanism in carbon particle-filled polymers. J. Mater. Sci. 27(5), 1322–1326 (1992)
Feller, J., Linossier, I., Grohens, Y.: Conductive polymer composites: comparative study of poly(ester)-short carbon fibres and poly(epoxy)-short carbon fibres mechanical and electrical properties. Mater. Lett. 57(1), 64–71 (2002)
Bañobre-López, M., Piñeiro-Redondo, Y., de Santis, R., Gloria, A., Ambrosio, L., Tampieri, A.: Poly(caprolactone) based magnetic scaffolds for bone tissue engineering. J. Appl. Phys. 109(7), 07B313 (2011)
Bock, N., Riminucci, A., Dionigi, C., Russo, A., Tampieri, A., Landi, E.: A novel route in bone tissue engineering: magnetic biomimetic scaffolds. Acta Biomater. 6(3), 786–796 (2010)
Lin, C., Metters, A.: Hydrogels in controlled release formulations: network design and mathematical modeling. Adv. Drug Deliv. Rev. 58(12–13), 1379–1408 (2006)
Langer, R.: New methods of drug delivery. Science 249(4976), 1527–1533 (1990)
Mitragotri, S., Lahann, J.: Physical approaches to biomaterial design. Nat. Mater. 8, 15–21 (2009)
Choi, N.W., Cabodi, M., Held, B., Gleghorn, J.P., Bonassar, L.J.: Microfluidic scaffolds for tissue engineering. Nat. Mater. 6, 908–915 (2007)
Kurlyandskaya, G.V., Fernández, E., Safronov, A.P., Svalov, A.V., Beketov, I., Beitia, A.B., García-Arribas, A., Blyakhman, F.A.: Giant magnetoimpedance biosensor for ferrogel detection: model system to evaluate properties of natural tissue. Appl. Phys. Lett. 106, 193702 (2015)
Thevenot, J., Oliveira, H., Sandre, O., Lecommandoux, S.: Magnetic responsive polymer composite materials. Chem. Soc. Rev. 42(17), 7099–7116 (2013)
Hunt, N.C., Grover, L.M.: Cell encapsulation using biopolymer gels for regenerative medicine. Biotechnol. Lett. 32(6), 733–742 (2010)
Das, B., Mandal, M., Upadhyay, A., Chattopadhyay, P., Karak, N.: Bio-based hyperbranched polyurethane/Fe\(_{3}\)O\(_{4}\) nanocomposites: smart antibacterial biomaterials for biomedical devices and implants. Biomed. Mater. 8(3), 035003 (2013)
de Santis, R., Gloria, A., Russo, T., d’Amora, U., Zeppetelli, S., Dionigi, C.: A basic approach toward the development of nanocomposite magnetic scaffolds for advanced bone tissue engineering. J. Appl. Polym. Sci. 122(6), 3599–3605 (2011)
Gloria, A., Russo, R., d’Amora, U., Zeppetelli, S., d’Alessandro, T., Sandri, M., et al.: Magnetic poly(\(\varepsilon \)-caprolactone)/iron-doped hydroxyapatite nanocomposite substrates for advanced bone tissue engineering. J. R. Soc Interface 10(80), 20120833 (2013)
Hu, S.H., Liu, T.Y., Tsai, C.H., Chen, S.Y.: Preparation and characterization of magnetic ferroscaffolds for tissue engineering. J. Magn. Magn. Mater. 310(2), 2871–2873 (2007)
Hu, H., Jiang, W., Lan, F., Zeng, X., Ma, S., Wu, Y.: Synergic effect of magnetic nanoparticles on the electrospun aligned superparamagnetic nanofibers as a potential tissue engineering scaffold. RSC Adv. 3, 879–886 (2013)
Lai, K., Jiang, W., Tang, J.Z., Wu, Y., He, B., Wang, G., et al.: Superparamagnetic nano-composite scaffolds for promoting bone cell proliferation and defect reparation without a magnetic field. RSC Adv. 2, 13007–13017 (2012)
Li, Y., Huang, G., Zhang, X., Li, B., Chen, Y., Lu, T.: Magnetic hydrogels and their potential biomedical applications. Adv. Funct. Mater. 23(6), 660–672 (2013)
Panseri, S., Cunha, C., Alessandro, T., Sandri, M., Giavaresi, G., Marcacci, M.: Intrinsically superparamagnetic Fe-hydroxyapatite nanoparticles positively influence osteoblast-like cell behaviour. J. Nanobiotechnol. 10, 32 (2012)
Skaat, H., Ziv-Polat, O., Shahar, A., Last, D., Mardor, Y., Margel, S.: Magnetic scaffolds enriched with bioactive nanoparticles for tissue engineering. Adv. Healthc Mater. 1(2), 168–171 (2012)
Tampieri, A., Landi, E., Valentini, F., Sandri, M., d’Alessandro, T., Dediu, V., et al.: A conceptually new type of bio-hybrid scaffold for bone regeneration. Nanotechnology 22(1), 015104 (2011)
Tampieri, A., d’Alessandro, T., Sandri, M., Sprio, S., Landi, E., Bertinetti, L.: Intrinsic magnetism and hyperthermia in bioactive Fe-doped hydroxyapatite. Acta Biomater. 8(2), 843–851 (2012)
Zeng, X.B., Hu, H., Xie, L.Q., Lan, F., Jiang, W., Wu, Y.: Magnetic responsive hydroxyapatite composite scaffolds construction for bone defect reparation. Int. J. Nanomed. 7, 3365–3378 (2012)
Zeng, X.B., Hu, H., Xie, L.Q., Lan, F., Wu, Y., Gu, Z.W.: Preparation and properties of supermagnetic calcium phosphate composite scaffold. J. Inorg. Mater. 28(1), 79–84 (2013)
Zhu, Y., Shang, F., Li, B., Dong, Y., Liu, Y., Lohe, M.R.: Magnetic mesoporous bioactive glass scaffolds: preparation, physicochemistry and biological properties. J. Mater. Chem. B 1(9), 1279–1288 (2013)
Ziv-Polat, O., Skaat, H., Shahar, A., Margel, S.: Novel magnetic fibrin hydrogel scaffolds containing thrombin and growth factors conjugated iron oxide nanoparticles for tissue engineering. Int. J. Nanomed. 7, 1259–1274 (2012)
Singh, R.K., Patel, K.D., Lee, J.H., Lee, E.J., Kim, J.H., Kim, T.H., et al.: Potential of magnetic nanofiber scaffolds with mechanical and biological properties applicable for bone regeneration. PLOS ONE 9, e91584 (2014)
Lopez-Lopez, M.T., Scionti, G., Oliveira, A.C., Duran, J.D.G., Campos, A., Alaminos, M., Rodriges, I.A.: Generation and characterization of novel magnetic field-responsive biomaterials. PLOS ONE 10(7), e0133878 (2015)
Nicodemus, G.D., Bryant, S.J.: Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng. Part B 14(2), 149–165 (2008)
Ladet, S., David, L., Domard, A.: Multi-membrane hydrogels. Nature 452, 76–79 (2008)
Caló, E., Khutoryanskiy, V.V.: Biomedical applications of hydrogels: a review of patents and commercial products. Eur. Polym. J. 65, 252–267 (2015)
Sharmin, F., et al.: Injectable hydrogels for regenerative engineering, pp. 1–32. Imperial College Press, London (2016)
Banobre-Lopez, M., Pineiro-Redondo, Y., de Santis, R., Gloria, A., Ambrosio, L., Tampieri, A., Dediu, V., Rivas, J.: Poly(caprolactone) based magnetic scaffolds for bone tissue engineering. J. Appl. Phys. 109, 07B313 (2011)
Yun, H.M., Ahn, S.J., Park, K.R., Kim, M.J., Kim, J.J., Jinc, G.Z., Kim, H.W., Kim, E.C.: Magnetic nanocomposite scaffolds combined with static magnetic field in the stimulation of osteoblastic differentiation and bone formation. Biomaterials 85, 88–98 (2016)
Rodriguez-Arco, L., Rodriguez, I.A., Carriel, V., Bonhome-Espinosa, A.B., Campos, F., Kuzhir, P., Duran, J.D.G., Lopez-Lopez, M.T.: Biocompatible magnetic core-shell nanocomposites for engineered magnetic tissues. Nanoscale 8(15), 8138–8150 (2016)
Lopez-Lopez, M.T., Rodriguez, I.A., Rodriguez-Arco, L., Carriel, V., Bonhome-Espinosa, A.B., Campos, F., Zubarev, A., Duran, J.D.G.: Synthesis, characterization and in vivo evaluation of biocompatible ferrogels. J. Magn. Magn. Mater. 431, 110–114 (2017)
Bonhome-Espinosa, A.B., Campos, F., Rodriguez, I.A., Carriel, V., Marins, J.A., Zubarev, A., Duran, J.D.G., Lopez-Lopez, M.T.: Effect of particle concentration on the microstructural and macromechanical properties of biocompatible magnetic hydrogels. Soft Matter 13, 2928–2941 (2017)
Scionti, G., Moral, M., Toledano, M., Osorio, R., Durán, J.D.G., Alaminos, M., Campos, A., López-López, M.T.: Effect of the hydration on the biomechanical properties in a fibrin–agarose tissue-like model. J. Biomed. Mater. Res. Part A 102A, 2573–2582 (2014)
Alaminos, M., Sanchez-Quevedo, M.C., Munoz-Avila, J.I., Serrano, D., Medialdea, S., Carreras, I.: Construction of a complete rabbit cornea substitute using a fibrin–agarose scaffold. Invest. Ophthalmol. Vis. Sci. 47, 3311–3317 (2006)
Bychkova, A.V., Sorokina, O.N., Kovarski, A.L., Shapiro, A.B., Leonova, V.B., Rozenfeld, M.A.: Interaction of fibrinogen with magnetite nanoparticles. Biophysics 55(4), 544–549 (2010)
Cote, H.C.F., Lord, S.T., Pratt, K.P.: \(\gamma \)-Chain dysfibrinogenemias: molecular structure-function relationships of naturally occurring mutations in the \(\gamma \)-chain of human fibrinogen. Blood 92(7), 2195–2212 (1998)
Zeliszewska, P., Bratek-Skicki, A., Adamczyk, Z., Ciesla, M.: Human fibrinogen adsorption on positively charged latex particles. Langmuir 30(37), 11165–11174 (2014)
Pitaevskii, L.P., Lifshits, E.M.: Physical Kinetics. Butterworth-Heinemann, Oxford (1999)
Rubistein, M., Colby, R.H.: Polymer Physics. Oxford University, New York (2003)
Grosberg, A., Khokhlov, A.: Statistical Physics of Macromolecules. Springer, Berlin (1994)
Christensen, R.M.: Mechanics of Composite Materials. Krieger Publishing Company, Malabar (1991)
Acknowledgements
This study was supported by projects FIS2013-41821-R (Plan Nacional de Investigación Científica, Desarrollo e Innovación Tecnológica, MINECO, Spain, co-funded by ERDF, European Union) and FIS2017-85954-R (Ministerio de Economía, Industria y Competitividad, MINECO, and Agencia Estatal de Investigación, AEI, Spain, co-funded by Fondo Europeo de Desarrollo Regional, FEDER, European Union). A.Z. is grateful to the program of the Ministry of Education and Science of the Russian Federation, projects 02.A03.21.0006, 3.1438.2017/4.6, and 3.5214.2017/6.7, as well as to the Russian Fund of Basic Researches, project 18-08-00178.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical statement
This study was approved by the Ethics Committee of the University of Granada, Granada, Spain.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zubarev, A., Bonhome-Espinosa, A.B., Alaminos, M. et al. Rheological properties of magnetic biogels. Arch Appl Mech 89, 91–103 (2019). https://doi.org/10.1007/s00419-018-1450-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00419-018-1450-2