A Discussion Regarding the Application of the Hertz Contact Theory on Biological Samples in AFM Nanoindentation Experiments

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Abstract

Background: Atomic Force Microscopy (AFM) Nanoindentation procedure regarding biological samples poses significant challenges with respect to the accuracy of the provided results. These challenges are related to the inhomogeneity of biological samples, various uncertainties in experimental methods and certain approximations regarding the theoretical analysis. The most commonly used theoretical model for data processing at the linear elastic regime regarding biological samples is the Hertz model.

Objective: This paper focuses on the investigation of the resulting errors of the basic equation of the Hertz theory that depend on the ratio, indentation depth/indenter’s radius regarding the Young’s modulus calculation.

Methods: An extended new equation is derived which takes into account the influence of the indentation depth/indenter’s radius ratio on the calculation of the Young’s modulus and can be easily used for calculations. The derived equation is further combined with equations which take into account the shape of the sample.

Results: Several examples in the literature that do not take into account the value of the ratio indentation depth/indenter’s radius are reported and the related errors are calculated and discussed. Moreover, a rational explanation, regarding the extended differences of the Young’s modulus calculations using the same experimental results when these are processed using the Hertz model and the Oliver & Pharr analysis (which is the general model that applies for any axisymmetric indenter) is provided.

Conclusion: A complete and reliable theoretical tool was developed (that takes into account the indentation depth/indenter’s radius ratio and the shape of the sample) which can be generally applied in order to reduce the errors produced by the current methodology (Hertz model).

Keywords: Mechanical properties, hertz model, biological samples, Atomic Force Microscopy (AFM), nanoindentation, indentation values.

Graphical Abstract

[1]
Kontomaris, S.V.; Stylianou, A. Atomic force microscopy for university students: applications in biomaterials. Eur. J. Phys., 2017, 38(3)033003
[http://dx.doi.org/10.1088/1361-6404/aa5cd6]
[2]
Alessandrini, A.; Facci, R. AFM: a versatile tool in biophysics. Meas. Sci. Technol., 2005, 16, R65-R92.
[http://dx.doi.org/10.1088/0957-0233/16/6/R01]
[3]
Allison, D.P.; Mortensen, N.P.; Sullivan, C.J.; Doktycz, M.J. Atomic force microscopy of biological samples. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2010, 2(6), 618-634.
[http://dx.doi.org/10.1002/wnan.104]
[4]
Mateu, M.G. Mechanical properties of viruses analyzed by atomic force microscopy: a virological perspective. Virus Res., 2012, 168(1-2), 1-22.
[http://dx.doi.org/10.1016/j.virusres.2012.06.008]
[5]
Pharr, G.M.; Oliver, W.C.; Brotzen, F.R. On the generality of the relationship among contact stiffness, contact area, and elastic modulus during indentation. J. Mater. Res., 1992, 7(3), 613-617.
[http://dx.doi.org/10.1557/JMR.1992.0613]
[6]
Oliver, W.C.; Pharr, G.M. Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology. J. Mater. Res., 2004, 19(1), 3-20.
[http://dx.doi.org/10.1557/jmr.2004.19.1.3]
[7]
Darling, E.M. Force scanning: a rapid, high-resolution approach for spatial mechanical property mapping. Nanotechnology, 2011, 22(17)175707
[http://dx.doi.org/10.1088/0957-4484/22/17/175707]
[8]
Kurland, N.E.; Drira, Z.; Yadavalli, V.K. Measurement of nanomechanical properties of biomolecules using atomic force microscopy. Micron, 2012, 43(2-3), 116-128.
[http://dx.doi.org/10.1016/j.micron.2011.07.017]
[9]
Stylianou, A.; Kontomaris, S.V.; Yova, D. Assessing Collagen Nanoscale Thin Films Heterogeneity by AFM Multimode Imaging and Nanoindetation for NanoBioMedical Applications. Micro Nanosyst., 2014, 6(2), 95-102.
[http://dx.doi.org/10.2174/187640290602141127114448]
[10]
Stylianou, A.; Yova, D.; Alexandratou, E. Investigation of the influence of UV irradiation on collagen thin films by AFM imaging. Mater. Sci. Eng. C, 2014, 45, 455-468.
[http://dx.doi.org/10.1016/j.msec.2014.09.006]
[11]
Kontomaris, S.V.; Yova, D.; Stylianou, A.; Politopoulos, K. The significance of the percentage differences of Young’s modulus in the AFM nanoindentation procedure. Micro Nanosyst., 2015, 7(2), 86-97.
[http://dx.doi.org/10.2174/1876402908666151111234441]
[12]
Kontomaris, S.V.; Stylianou, A.; Malamou, A.; Stylianopoulos, T. A discussion regarding the approximation of cylindrical and spherical shaped samples as half spaces in AFM nanoindentation experiments. Mater. Res. Express, 2018, 5(8)085402
[http://dx.doi.org/10.1088/2053-1591/aad2c9]
[13]
Kontomaris, S.V.; Malamou, A. An extension of the general nanoindentation equation regarding cylindrical – shaped samples and a simplified model for the contact ellipse determination. Mater. Res. Express, 2018, 5(12)125403
[http://dx.doi.org/10.1088/2053-1591/aae0bc]
[14]
Kontomaris, S.V.; Yova, D.; Stylianou, A.; Balogiannis, G. The effects of UV irradiation on collagen D-band revealed by atomic force microscopy. Scanning, 2015, 37(2), 101-111.
[http://dx.doi.org/10.1002/sca.21185]
[15]
Kontomaris, S.V.; Stylianou, A.; Malamou, A.; Nikita, K.S. An alternative approach for the Young’s modulus determination of biological samples regarding AFM indentation experiments. Mater. Res. Express, 2018, 6(2)025407
[http://dx.doi.org/10.1088/2053-1591/aaef10]
[16]
Kontomaris, S.V. The hertz model in afm nanoindentation experiments: applications in biological samples and biomaterials. Micro Nanosyst., 2018, 10(1), 11-22.
[http://dx.doi.org/10.2174/1876402910666180426114700]
[17]
Johnson, K.L.; Greenwood, J.A. An adhesion map for the contact of elastic spheres. J. Colloid Interface Sci., 1997, 192(2), 326-333.
[http://dx.doi.org/10.1006/jcis.1997.4984]
[18]
Johnson, K.; Kendall, K.; Roberts, A. Surface energy and the contact of elasticsolids. Proc. R. Soc. Lond., 1971, 324, 301-313.
[http://dx.doi.org/10.1098/rspa.1971.0141]
[19]
Maugis, D. Adhesion of spheres: the JKR-DMT transition using a Dugdale model. J. Colloid Interface Sci., 1992, 150(1), 243-269.
[http://dx.doi.org/10.1016/0021-9797(92)90285-T]
[20]
Persch, G.; Born, C.; Utesch, B. Nano-hardness investigations of thin films by an atomic force microscope. Microelectron. Eng., 1994, 24(1-4), 113-121.
[http://dx.doi.org/10.1016/0167-9317(94)90061-2]
[21]
Radmacher, M. Studying the mechanics of cellular processes by atomic force microscopy. Methods Cell Biol., 2007, 83, 347-372.
[http://dx.doi.org/10.1016/S0091-679X(07)83015-9]
[22]
Johnson, K.L. Contact mechanics; Cambridge University Press: Cambridge, 1985.
[http://dx.doi.org/10.1017/CBO9781139171731]
[23]
Wenger, M.P.E.; Bozec, L.; Horton, M.A.; Mesquida, P. Mechanical properties of collagen fibrils. Biophys. J., 2007, 93(4), 1255-1263.
[http://dx.doi.org/10.1529/biophysj.106.103192]
[24]
Kontomaris, S.V.; Stylianou, A.; Nikita, K.S.; Malamou, A.; Stylianopoulos, T. A simplified approach for the determination of fitting constants in Oliver-Pharr method regarding biological samples. Phys. Biol., 2019, 16(5)056003
[http://dx.doi.org/10.1088/1478-3975/ab252e]
[25]
Guo, X.; Bonin, K.; Scarpinato, K.; Guthold, M. The effect of neighboring cells on the stiffness of cancerous and non-cancerous human mammary epithelial cells. New J. Phys., 2014, 16(10)105002
[http://dx.doi.org/10.1088/1367-2630/16/10/105002]
[26]
Shimizu, Y.; Kihara, T.; Haghparast, S.M.; Yuba, S.; Miyake, J.; Miyake, J. Simple display system of mechanical properties of cells and their dispersion. PLoS One, 2012, 7(3)e34305
[http://dx.doi.org/10.1371/journal.pone.0034305]
[27]
Grant, C.A.; Brockwell, D.J.; Radford, S.E.; Thomson, N.H. Tuning the elastic modulus of hydrated collagen fibrils. Biophys. J., 2009, 97(11), 2985-2992.
[http://dx.doi.org/10.1016/j.bpj.2009.09.010]
[28]
Sajeesh, P.; Raj, A.; Dobleb, M.; Sen, A.K. Characterization and sorting of cells based on stiffness contrast in a microfluidic channel. RSC Advances, 2016, 6, 74704-74714.
[http://dx.doi.org/10.1039/C6RA09099K]
[29]
Andriotis, O.G.; Manuyakorn, W.; Zekonyte, J.; Katsamenis, O.L.; Fabri, S.; Howarth, P.H.; Davies, D.E.; Thurner, P.J. Nanomechanical assessment of human and murine collagen fibrils via atomic force microscopy cantilever-based nanoindentation. J. Mech. Behav. Biomed. Mater., 2014, 39, 9-26.
[http://dx.doi.org/10.1016/j.jmbbm.2014.06.015]
[30]
Heim, A.J.; Matthews, W.G.; Koob, T.J. Determination of the elastic modulus of native collagen fibrils via radial indentation. Appl. Phys. Lett., 2006, 89(18)181902
[http://dx.doi.org/10.1063/1.2367660]
[31]
Kontomaris, S.V.; Stylianou, A.; Nikita, K.S.; Malamou, A. Determination of the linear elastic regime in AFM nanoindentation experiments on cells. Mater. Res. Express, 2019, 6(11)115410
[http://dx.doi.org/10.1088/2053-1591/ab4f42]
[32]
Gai, M.; Frueh, J.; Kudryavtseva, V.L.; Mao, R.; Kiryukhin, M.V.; Sukhorukov, G.B. Patterned microstructure fabrication: polyelectrolyte complexes vs polyelectrolyte multilayers. Sci. Rep., 2016, 6, 37000.
[http://dx.doi.org/10.1038/srep37000]
[33]
Gai, M.; Frueh, J.; Kudryavtseva, V.L.; Yashchenok, A.M.; Sukhorukov, G.B. Polylactic acid sealed polyelectrolyte multilayer microchambers for entrapment of salts and small hydrophilic molecules precipitates. ACS Appl. Mater. Interfaces, 2017, 9(19), 16536-16545.
[http://dx.doi.org/10.1021/acsami.7b03451]
[34]
Seppä, J.; Reischl, B.; Sairanen, H.; Korpelainen, V.; Husu, H.; Heinonen, M.; Raiteri, P.; Rohl, A.L.; Nordlund, K.; Lassila, A. Atomic force microscope adhesion measurements and atomistic molecular dynamics simulations at different humidities. Meas. Sci. Technol., 2017, 28(3)034004
[http://dx.doi.org/10.1088/1361-6501/28/3/034004]
[35]
Liu, P.; He, J.H. Geometric potential: An explanation of nanofiber’s wettability. Therm. Sci., 2017, 22(1), 146-146.
[36]
Li, X.X.; He, J.H. Nanoscale adhesion and attachment oscillation under the geometric potential. Part 1: The formation mechanism of nanofiber membrane in the electrospinning. Results Phys., 2019, 12, 1405-1410.
[http://dx.doi.org/10.1016,/j.rinp.2019.01.043]
[37]
He, J.H. A Note on Elementary Cobordism and Negative Space. Int. J. Nonlin. Sci. Num., 2010, 11(12), 1093-1095.
[http://dx.doi.org/10.1515/IJNSNS.2010.11.12.1093]
[38]
He, J.H. Frontier of Modern Textile Engineering and Short Remarks on Some Topics in Physics. Int. J. Nonlin. Sci. Num., 2010, 11(7), 555-563.
[http://dx.doi.org/10.1515/IJNSNS.2010.11.7.555]
[39]
He, J.H. Inverse Problems of Newton’s Laws. Int. J. Nonlin. Sci. Num., 2009, 10(9), 1087-1091.
[http://dx.doi.org/10.1515/IJNSNS.2009.10.9.1087]
[40]
He, W.; Frueh, J.; Wu, Z.; He, Q. How Leucocyte Cell Membrane Modified Janus Microcapsules are Phagocytosed by Cancer Cells. ACS Appl. Mater. Interfaces, 2016, 8(7), 4407-4415.
[http://dx.doi.org/10.1021/acsami.5b10885 PMID: 26824329]
[41]
Hermanowicz, P.; Sarna, M.; Burda, K.; Gabryś, H. AtomicJ: an open source software for analysis of force curves. Rev. Sci. Instrum., 2014, 85(6)063703
[http://dx.doi.org/10.1063/1.4881683]