Abstract
Many structures and materials in nature and physiology have important “meso-scale” structures at the micron length-scale whose tensile responses have proven difficult to characterize mechanically. Although techniques such as atomic force microscopy and micro- and nano-identation are mature for compression and indentation testing at the nano-scale, and standard uniaxial and shear rheometry techniques exist for the macroscale, few techniques are applicable for tensile-testing at the micrometre-scale, leaving a gap in our understanding of hierarchical biomaterials. Here, we present a novel magnetic mechanical testing (MMT) system that enables viscoelastic tensile testing at this critical length scale. The MMT system applies non-contact loading, avoiding gripping and surface interaction effects. We demonstrate application of the MMT system to the first analyses of the pure tensile responses of several native and engineered tissue systems at the mesoscale, showing the broad potential of the system for exploring micro- and meso-scale analysis of structured and hierarchical biological systems.
Similar content being viewed by others
References
Meyers, M.A., McKittrick, J., Chen, P.Y.: Structural biological materials: critical mechanics-materials connections. Science 339, 773–779 (2013)
Chen, J., Wright, K.E., Birch, M.A.: Nanoscale viscoelastic properties and adhesion of polydimethylsiloxane for tissue engineering. Acta Mech. Sin. 30, 2–6 (2013)
Ji, B., Gao, H.: Mechanical properties of nanostructure of biological materials. Mech. Phys. Solids 52, 1963–1990 (2004)
Lin, S.Z., Li, B., Feng, X.Q.: A dynamic cellular vertex model of growing epithelial tissues. Acta Mech. Sin. 33, 250–259 (2017)
Hollister, S.J.: Porous scaffold design for tissue engineering. Nat. Mater. 4, 518–524 (2006)
Li, Y., Huang, G., Gao, B., et al.: Magnetically actuated cell-laden microscale hydrogels for probing strain-induced cell responses in three dimensions. NPG Asia Mater. 8, e238 (2016)
Reznikov, N., Shahar, R., Weiner, S.: Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815–3826 (2014)
Alexander, B., Daulton, T.L., Genin, G.M., et al.: The nanometre-scale physiology of bone: steric modelling and scanning transmission electron microscopy of collagen-mineral structure. J. R. Soc. Interface 9, 1774–1786 (2012)
Screen, H.R.C., Leem, D.A., Baderm, D.L., et al.: An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties. Proc. IME H J. Eng. Med. 218, 109–119 (2004)
Svensson, R.B., Hansen, P., Hassenkam, T., et al.: Mechanical properties of human patellar tendon at the hierarchical levels of tendon and fibril. J. Appl. Physiol. 112, 419–426 (2012)
Long, R., Hui, C.Y.: Crack buckling in soft gels under compression. Acta Mech. Sin. 28, 1098–1105 (2012)
Stammen, J.A., Williams, S., Ku, D.N., et al.: Mechanical properties of a novel PVA hydrogel in shear and unconfined compression. Biomaterials 22, 799–806 (2001)
Galford, J.E., McElhaney, J.H.: A viscoelastic study of scalp, brain, and dura. J. Biomech. 3, 211–221 (1970)
Zhang, T., Yuk, H., Lin, S., et al.: Tough and tunable adhesion of hydrogels: experiments and models. Acta Mech. Sin. 3, 1–12 (2017)
Chaudhuri, O., Gu, L., Klumpers, D., et al.: Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater. 15, 326 (2016)
Chaudhuri, O., Gu, L., Darnell, M., et al.: Substrate stress relaxation regulates cell spreading. Nat. Commun. 6, 6365 (2015)
Henderson, E., Haydon, P.G., Sakaguchi, D.S.: Actin filament dynamics in living glial cells imaged by atomic force microscopy. Science 257, 1944–1947 (1992)
Radmacher, M., Tillmann, R.W., Fritz, M., et al.: From molecules to cells: imaging soft samples with the atomic force microscope. Science 257, 1900–1906 (1992)
Yang, H.: Atomic Force Microscopy (AFM), Principles, Modes of Operation and Limitations. NOVA, New York (2014)
Hochmuth, R.M.: Micropipette aspiration of living cells. J. Biomech. 33, 15–22 (2000)
Hogan, B., Babataheri, A., Hwang, Y., et al.: Characterizing cell adhesion by using micropipette aspiration. Biophys. J. 109, 209–219 (2015)
Dowling, N.E.: Mechanical Behavior of Materials: Engineering Methods for Deformation, Fracture, and Fatigue. Prentice Hall, Englewood Cliffs (1993)
Drury, J.L., Dennis, R.G., Mooney, D.J.: The tensile properties of alginate hydrogels. Biomaterials 25, 3187–3199 (2004)
Chasiotis, I., Knauss, W.G.: A new microtensile tester for the study of MEMS materials with the aid of atomic force microscopy. Exp. Mech. 42, 51–57 (2002)
Thomson, N.H., Fritz, M., Radmacher, M., et al.: Protein tracking and detection of protein motion using atomic force microscopy. Biophys. J. 70, 2421–2431 (1996)
Schitter, G., Astrom, K.J., DeMartini, B.E., et al.: Design and modeling of a high-speed AFM-scanner. IEEE Trans. Control Syst. Technol. 15, 906–915 (2007)
Kim, J.H., Nizami, A., Hwangbo, Y., et al.: Tensile testing of ultra-thin films on water surface. Nat. Commun. 4, 2520 (2013)
Savin, T., Shyer, A.E., Mahadevan, L.: A method for tensile tests of biological tissues at the mesoscale. J. Appl. Phys. 111, 074704 (2012)
Souza, G.R., Molina, J.R., Raphael, R.M., et al.: Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol. 5, 291–296 (2010)
Sakar, M.S., Eyckmans, J., Pieters, R., et al.: Nat. Commun. 7, 11036 (2016)
Zhao, R., Boudou, T., Wang, W.G., et al.: Decoupling cell and matrix mechanics in engineered microtissues using magnetically actuated microcantilevers. Adv. Mater. 25, 1699–1705 (2013)
Li, Y., Huang, G., Zhang, X., et al.: Magnetic hydrogels and their potential biomedical applications. Adv. Funct. Mater. 23, 660–672 (2013)
Li, Y., Poon, C.T., Li, M., et al.: Chinese-noodle-inspired muscle myofiber fabrication. Adv. Funct. Mater. 25, 5999–6008 (2015)
Sun, J.Y., Zhao, X., Illeperuma, W.R.K., et al.: Highly stretchable and tough hydrogels. Nature 489, 133–136 (2012)
Zhao, X.: Multi-scale multi-mechanism design of tough hydrogels: building dissipation into stretchy networks. Soft Matter 10, 672–687 (2014)
Yue, K., Trujillo-de Santiago, G., Alvarez, M.M., et al.: Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 73, 254–271 (2015)
Lai, T.C., Yu, J., Tsai, W.B., et al.: Gelatin methacrylate/carboxybetaine methacrylate hydrogels with tunable crosslinking for controlled drug release. J. Mater. Chem. B 4, 2304–2313 (2016)
Marc, A.M., Po, Y.C., Albert, M.L., et al.: Biological materials: structure and mechanical properties. Prog. Mater. Sci. 53, 1–206 (2008)
Acknowledgements
This project was partially supported by the National Natural Science Foundation of China (Grants 11532009, 11372243, and 11522219) and the China Postdoctoral Science Foundation (Grant 2016M602810). This project was also supported by the Initiative Postdocs Supporting Program (Grant BX201600121).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Li, Y., Hong, Y., Xu, GK. et al. Non-contact tensile viscoelastic characterization of microscale biological materials. Acta Mech. Sin. 34, 589–599 (2018). https://doi.org/10.1007/s10409-017-0740-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10409-017-0740-1