Abstract
Skin is a highly non-linear, anisotropic, rate dependent inelastic, and nearly incompressible material which exhibits substantial hysteresis even under very slow (quasistatic) loading conditions. In this paper, a series of uniaxial cyclic loading tests of porcine and rat skin at different strain rates and with samples oriented in different directions (with respect to the spine) were conducted to study the effect of strain rate and samples orientations with respect to spine on Mullins-type softening and skin inelastic response. A noteworthy feature of skin is that, similar to certain filled rubbers, its mechanical response shifts after the first extension and exhibits softening and hysteresis when loaded under cyclic tension and Mullins-type softening is observed. The results of these strain-controlled cyclic loading tests also indicated that the extent of softening is different for different strain rates and orientations. Also, a substantial hysteresis persists even at very low strain rates indicating inelastic behavior beyond the rate sensitive viscoelastic response. Through this series of experiments, by investigating the effect of strain rate on pig skin and rat skin, we conclude that the skin response is rate dependent but inelastic and shows irreversible changes in fiber orientation which are observed in histology results. Also, skin shows persistent deformation that is only partially recovered even after a long period of unloading.
Similar content being viewed by others
References
McGrath JA, Uitto J (2010) Anatomy and organization of human skin, chap. 3. Wiley-Blackwell, pp 1–53. https://doi.org/10.1002/9781444317633.ch3. https://onlinelibrary.wiley.com/doi/abs/10.1002/9781444317633.ch3
Benias PC, Wells RG, Sackey-Aboagye B, Klavan H, Reidy J, Buonocore D, Miranda M, Kornacki S, Wayne M, Carr-Locke DL et al (2018) Structure and distribution of an unrecognized interstitium in human tissues. Sci Rep 8(1):4947
Ricard-Blum S (2011) The collagen family. Cold Spring Harbor Perspectives in Biology 3(1):a004978
Oxlund H, Manschot J, Viidik A (1988) The role of elastin in the mechanical properties of skin. J Biomech 21(3):213–218. https://doi.org/10.1016/0021-9290(88)90172-8. http://www.sciencedirect.com/science/article/pii/0021929088901728
Naylor EC, Watson RE, Sherratt MJ (2011) Molecular aspects of skin ageing. Maturitas 69(3):249–256. https://doi.org/10.1016/j.maturitas.2011.04.011. http://www.sciencedirect.com/science/article/pii/S0378512211001496
Liao H, Belkoff SM (1999) A failure model for ligaments. J Biomech 32(2):183–188. https://doi.org/10.1016/S0021-9290(98)00169-9. http://www.sciencedirect.com/science/article/pii/S0021929098001699
Hill MR, Duan X, Gibson GA, Watkins S, Robertson AM (2012) A theoretical and non-destructive experimental approach for direct inclusion of measured collagen orientation and recruitment into mechanical models of the artery wall. J Biomech 45(5):762–771. https://doi.org/10.1016/j.jbiomech.2011.11.016. http://www.sciencedirect.com/science/article/pii/S00219290110 06981. Special Issue on Cardiovascular Solid Mechanics
Brown IA (1973) A scanning electron microscope study of the effects of uniaxial tension on human skin. British J Dermatol 89(4):383–393
Xu F, Lu T (2011) Skin mechanical behaviour, chap. 5. Springer, Berlin, pp 87–104
Haut R (1989) The effects of orientation and location on the strength of dorsal rat skin in high and low speed tensile failure experiments. J Biomech Eng 111(2):136–140
Swaim SF, Henderson RA, Pidgeon RS, et al. (1990) Small animal wound management. Lea & Febiger
Dombi GW, Haut RC, Sullivan WG (1993) Correlation of high-speed tensile strength with collagen content in control and lathyritic rat skin. J Surg Res 54(1):21–28. https://doi.org/10.1006/jsre.1993.1004. http://www.sciencedirect.com/science/article/pii/S0022480483710048
Annaidh AN, Bruyère K, Destrade M, Gilchrist MD, Otténio M (2012) Characterization of the anisotropic mechanical properties of excised human skin. J Mech Behav Biomed Mater 5(1):139–148. https://doi.org/10.1016/j.jmbbm.2011.08.016. http://www.sciencedirect.com/science/article/pii/S17516161110 02219
North JF, Gibson F (1978) Volume compressibility of human abdominal skin. J Biomech 11(4):203207–205
Fung YC (2013) Biomechanics: mechanical properties of living tissues. Springer Science & Business Media
Kang G, Wu X (2011) Ratchetting of porcine skin under uniaxial cyclic loading. J Mech Behav Biomed Mater 4(3):498–506. https://doi.org/10.1016/j.jmbbm.2010.12.015. http://www.sciencedirect.com/science/article/pii/S1751616110001906
Holzapfel GA (2005) Similarities between soft biological tissues and rubberlike materials. In: Constitutive models for rubber-proceedings-, vol 4. Balkema, p 607
Mullins L (1949) Permanent set in vulcanized rubber. Rubber Chem Technol 22 (4):1036–1044. https://doi.org/10.5254/1.3543010
Diani J, Fayolle B, Gilormini P (2009) A review on the mullins effect. Eur Polym J 45(3):601–612
Blanchard AF, Parkinson D (1952) Breakage of carbon-rubber networks by applied stress. Indus Eng Chem 44(4):799–812. https://doi.org/10.1021/ie50508a034
Houwink R (1955) Slipping of molecules during the deformation of reinforced rubber. Rubber Chem Technol 29(3):888–893. https://doi.org/10.5254/1.3542602
Kraus G, Childers CW, Rollmann KW (1966) Stress softening in carbon black-reinforced vulcanizates. Strain rate and temperature effects. J Appl Polymer Sci 10(2):229–244. https://doi.org/10.1002/app.1966.070100205
Hanson DE, Hawley M, Houlton R, Chitanvis K, Rae P, Orler EB, Wrobleski DA (2005) Stress softening experiments in silica-filled polydimethylsiloxane provide insight into a mechanism for the mullins effect. Polymer 46(24):10989–10995. https://doi.org/10.1016/j.polymer.2005.09.039
Fukahori Y (2005) New progress in the theory and model of carbon black reinforcement of elastomers. J Appl Polymer Sci 95(1):60–67. https://doi.org/10.1002/app.20802
Lanir Y, Fung Y (1974) Two-dimensional mechanical properties of rabbit skin—ii. experimental results. J Biomech 7(2):171IN9175–174182
Daly CH, Odland GF (1979) Age-related changes in the mechanical properties of human skin. J Investig Dermatol 73(1):84–87
Lokshin O, Lanir Y (2009) Viscoelasticity and preconditioning of rat skin under uniaxial stretch: microstructural constitutive characterization. J Biomech Eng 131(3):031009
Nava A, Mazza E, Haefner O, Bajka M (2004) Experimental observation and modelling of preconditioning in soft biological tissues. In: Cotin S, Metaxas D (eds) Medical simulation. Springer, Berlin, pp 1–8
Avis NJ (2000) Virtual environment technologies. Minimally Invasive Therapy & Allied Technologies 9(5):333–339. https://doi.org/10.3109/13645700009061455
Satava RM, et al. (1999) Virtual reality in medicine. Bmj 319(7220):1305
Muñoz M, Bea J, Rodríguez J, Ochoa I, Grasa J, del Palomar AP, Zaragoza P, Osta R, Doblaré M (2008) An experimental study of the mouse skin behaviour: damage and inelastic aspects. J Biomech 41(1):93–99. https://doi.org/10.1016/j.jbiomech.2007.07.013. http://www.sciencedirect.com/science/article/pii/S002192900700320X
Zhu Y, Kang G, Kan Q, Yu C (2014) A finite viscoelastic–plastic model for describing the uniaxial ratchetting of soft biological tissues. J Biomech 47(5):996–1003. https://doi.org/10.1016/j.jbiomech.2014.01.004. http://www.sciencedirect.com/science/article/pii/S0021929014000177
Carew E, Barber J, Vesely I (2000) Role of preconditioning and recovery time in repeated testing of aortic valve tissues: validation through quasilinear viscoelastic theory. Ann Biomed Eng 28(9):1093–1100
Karimi A, Navidbakhsh M, Shojaei A (2015) A combination of histological analyses and uniaxial tensile tests to determine the material coefficients of the healthy and atherosclerotic human coronary arteries. Tissue Cell 47(2):152–158
Chen Q, Wang Y, Li ZY (2016) Re-examination of the mechanical anisotropy of porcine thoracic aorta by uniaxial tensile tests. Biomed Eng Online 15(2):167
Berardesca E, Elsner P, Wilhelm KP, Maibach HI (1995) Bioengineering of the skin: methods and instrumentation, vol 3. CRC Press
Zhou B, Xu F, Chen CQ, Lu TJ (2010) Strain rate sensitivity of skin tissue under thermomechanical loading. Philos Trans R Soc London A: Math Phys Eng Sci 368(1912):679–690. https://doi.org/10.1098/rsta.2009.0238. http://rsta.royalsocietypublishing.org/content/368/1912/679
Minns R, Soden P, Jackson D (1973) The role of the fibrous components and ground substance in the mechanical properties of biological tissues: a preliminary investigation. J Biomech 6(2):153–165. https://doi.org/10.1016/0021-9290(73)90084-5. http://www.sciencedirect.com/science/article/pii/0021929073900845
Eshel H, Lanir Y (2001) Effects of strain level and proteoglycan depletion on preconditioning and viscoelastic responses of rat dorsal skin. Ann Biomed Eng 29(2):164–172
Ottenio M, Tran D, Annaidh AN, Gilchrist MD, Bruyère K (2015) Strain rate and anisotropy effects on the tensile failure characteristics of human skin. J Mech Behav Biomed Mater 41:241–250. https://doi.org/10.1016/j.jmbbm.2014.10.006. http://www.sciencedirect.com/science/article/pii/S1751616114003282
Mullins L (1948) Effect of stretching on the properties of rubber. Rubber Chem Technol 21(2):281–300. https://doi.org/10.5254/1.3546914
Lanir Y (1979) The rheological behavior of the skin: experimental results and a structural model. Biorheology 16(3):191
Xu F, Lu T, Seffen K (2008) Biothermomechanics of skin tissues. J Mech Phys Solids 56 (5):1852–1884. https://doi.org/10.1016/j.jmps.2007.11.011. http://www.sciencedirect.com/science/article/pii/S002250960700227X
Sellaro TL, Hildebrand D, Lu Q, Vyavahare N, Scott M, Sacks MS (2007) Effects of collagen fiber orientation on the response of biologically derived soft tissue biomaterials to cyclic loading. J Biomed Mater Resarch Part A 80(1):194–205
Kazerooni NA, Srinivasa A, Criscione J Inelastic response of skin under uniaxial cyclic mechanical loading-multinetwork model comparison with experiments. International Journal of Engineering Science (Under Review)
Srinivasa AR, Srinivasan SM (2009) Inelasticity of materials: an engineering approach and a practical guide, vol 80. World Scientific Publishing Company
Rajagopal KR, Srinivasa AR (2016) An implicit three-dimensional model for describing the inelastic response of solids undergoing finite deformation. Zeitschrift für angewandte Mathematik und Physik 67(4):86. https://doi.org/10.1007/s00033-016-0671-x
Acknowledgements
The authors gratefully thank Dr. Terry Creasy from Texas A&M University for allowing us to use his facilities.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix
Appendix
In order to compare the Instron cross-head strain and the strain measured by DIC, the strain from grip displacement and the strain from image correlation along the sample from different positions of the sample were calculated, it was seen that the difference between both measurement was less than 5 percent.
Samples with a width of 10.4 mm, thickness of 1.65 mm and initial length of 54 mm were tested under a simple tension test. The measured engineering strain from crosshead displacement was 1.85 (εc). Also, engineering strain was measured by DIC; 5 different lines were chosen from different positions of the sample Fig. 14. The engineering strain (εd) was calculated as the differences between displacements of the top and bottom point of the line (y1 and y2) and divided by the difference between positions of these points on the line (u1 and u2). Table 1 shows strains measured by both DIC and Instron cross-head. The differences between εd and εc are less than 5 percent on each line and by getting the average of strain on all 5 lines, the difference is 2.7 percent which conforms to the strain measurement by the Instron cross-head.
Rights and permissions
About this article
Cite this article
Afsar-Kazerooni, N., Srinivasa, A. & Criscione, J. Experimental Investigation of the Inelastic Response of Pig and Rat Skin Under Uniaxial Cyclic Mechanical Loading. Exp Mech 60, 535–551 (2020). https://doi.org/10.1007/s11340-019-00556-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11340-019-00556-6