Advertisement

Biomechanics and Modeling in Mechanobiology

, Volume 18, Issue 4, pp 1079–1093 | Cite as

On the compressibility and poroelasticity of human and murine skin

  • Adam WahlstenEmail author
  • Marco Pensalfini
  • Alberto Stracuzzi
  • Gaetana Restivo
  • Raoul Hopf
  • Edoardo MazzaEmail author
Original Paper

Abstract

A total of 37 human and 33 murine skin samples were subjected to uniaxial monotonic, cyclic, and relaxation experiments. Detailed analysis of the three-dimensional kinematic response showed that skin volume is significantly reduced as a consequence of a tensile elongation. This behavior is most pronounced in monotonic but persists in cyclic tests. The dehydration associated with volume loss depends on the osmolarity of the environment, so that tension relaxation changes as a consequence of modifying the ionic strength of the environmental bath. Similar to ex vivo observations, complementary in vivo stretching experiments on human volar forearms showed strong in-plane lateral contraction. A biphasic homogenized model is proposed which allows representing all relevant features of the observed mechanical response.

Keywords

Skin biomechanics Mechanical characterization Compressibility Porous media Osmotic pressure 

Notes

Acknowledgements

This work was conducted as part of the SKINTEGRITY flagship project of University Medicine Zurich and financially supported by the Swiss National Science Foundation (Grant No. 179012). We are grateful to the group of Prof. S. Werner (Institute of Molecular Health Sciences, ETH Zurich) for providing murine skins and to the group of Prof. E. Reichmann (Tissue Biology Research Unit, University Children’s Hospital Zurich) for use of their facilities in preparations for experiments on human skin.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

All experiments involving human participants and human tissue were approved by the local ethical committees; details are given in Sect. 2.

Informed consent

Signed informed consent was provided from all participants and tissue donors.

References

  1. Achterberg VF, Buscemi L, Diekmann H, Smith-Clerc J, Schwengler H, Meister JJ, Wenck H, Gallinat S, Hinz B (2014) The nano-scale mechanical properties of the extracellular matrix regulate dermal fibroblast function. J Invest Dermatol 134(7):1862–1872Google Scholar
  2. Ateshian GA, Weiss JA (2010) Anisotropic hydraulic permeability under finite deformation. J Biomech Eng 132(11):111004Google Scholar
  3. Ateshian GA, Rajan V, Chahine NO, Canal CE, Hung CT (2009) Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J Biomech Eng 131(6):061003Google Scholar
  4. Azeloglu EU, Albro MB, Thimmappa VA, Ateshian GA, Costa KD (2008) Heterogeneous transmural proteoglycan distribution provides a mechanism for regulating residual stresses in the aorta. Am J Physiol Heart Circ Physiol 294(3):H1197–H1205Google Scholar
  5. Bader DL, Bowker P (1983) Mechanical characteristics of skin and underlying tissues in vivo. Biomaterials 4(4):305–308Google Scholar
  6. Bancelin S, Lynch B, Bonod-Bidaud C, Ducourthial G, Psilodimitrakopoulos S, Dokládal P, Allain JM, Schanne-Klein MC, Ruggiero F (2015) Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy. Sci Rep 5:1–14Google Scholar
  7. Baughman RH, Stafström S, Cui C, Dantas SO (1998) Materials with negative compressibilities in one or more dimensions. Science 279(5356):1522–1524Google Scholar
  8. Benítez JM, Montáns FJ (2017) The mechanical behavior of skin: structures and models for the finite element analysis. Comput Struct 190:75–107Google Scholar
  9. Bircher K, Ehret AE, Mazza E (2016) Mechanical characteristics of bovine Glisson’s capsule as a model tissue for soft collagenous membranes. J Biomech Eng 138(8):081005Google Scholar
  10. Brown AEX, Litvinov RI, Discher DE, Purohit PK, Weisel JW (2009) Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325(5941):741–744Google Scholar
  11. Brown IA (1973) A scanning electron microscope study of the effects of uniaxial tension on human skin. Br J Dermatol 89(4):383–393Google Scholar
  12. Buerzle W, Mazza E (2013) On the deformation behavior of human amnion. J Biomech 46(11):1777–1783Google Scholar
  13. Buganza Tepole A (2017) Computational systems mechanobiology of wound healing. Comput Methods Appl Mech Eng 314:46–70MathSciNetGoogle Scholar
  14. Buganza Tepole A, Gosain AK, Kuhl E (2014) Computational modeling of skin: using stress profiles as predictor for tissue necrosis in reconstructive surgery. Comput Struct 143:32–39Google Scholar
  15. Crichton ML, Donose BC, Chen X, Raphael AP, Huang H, Kendall MAF (2011) The viscoelastic, hyperelastic and scale dependent behaviour of freshly excised individual skin layers. Biomaterials 32(20):4670–4681Google Scholar
  16. Daly CH (1982) Biomechanical properties of dermis. J Invest Dermatol 79:48–51Google Scholar
  17. Donnan FG (1924) The theory of membrane equilibria. Chem Rev 1(1):73–90Google Scholar
  18. Ehlers W (2002) Foundations of multiphasic and porous materials. In: Ehlers W, Bluhm J (eds) Porous media. Springer, Berlin, pp 3–86Google Scholar
  19. Ehlers W, Karajan N, Markert B (2009) An extended biphasic model for charged hydrated tissues with application to the intervertebral disc. Biomech Model Mechanobiol 8(3):233–251Google Scholar
  20. Ehret AE, Hollenstein M, Mazza E, Itskov M (2011) Porcine dermis in uniaxial cyclic loading: sample preparation, experimental results and modeling. J Mech Mater Struct 6(7–8):1125–1135Google Scholar
  21. Ehret AE, Bircher K, Stracuzzi A, Marina V, Zündel M, Mazza E (2017) Inverse poroelasticity as a fundamental mechanism in biomechanics and mechanobiology. Nat Commun 8(1):1–9Google Scholar
  22. Eskandari M, Kuhl E (2015) Systems biology and mechanics of growth. Wiley Interdiscip Rev Syst Biol Med 7(6):401–412Google Scholar
  23. Federico S, Grillo A (2012) Elasticity and permeability of porous fibre-reinforced materials under large deformations. Mech Mater 44:58–71Google Scholar
  24. Frijns AJH, Huyghe JM, Janssen JD (1997) A validation of the quadriphasic mixture theory for intervertebral disc tissue. Int J Eng Sci 35(15):1419–1429zbMATHGoogle Scholar
  25. Gibson T, Kenedi RM, Craik JE (1965) The mobile micro-architecture of dermal collagen: a bio-engineering study. Br J Surg 52(10):764–770Google Scholar
  26. Gray ML, Pizzanelli AM, Grodzinsky AJ, Lee RC (1988) Mechanical and physicochemical determinants of the chondrocyte biosynthetic response. J Orthop Res 6(6):777–792Google Scholar
  27. Grodzinsky AJ (2011) Fields, forces and flows in biological systems. Garland Science, New YorkGoogle Scholar
  28. Groves RB, Coulman SA, Birchall JC, Evans SL (2013) An anisotropic, hyperelastic model for skin: experimental measurements, finite element modelling and identification of parameters for human and murine skin. J Mech Behav Biomed Mater 18:167–180Google Scholar
  29. Gu WY, Yao H, Vega AL, Flagler D (2004) Diffusivity of ions in agarose gels and intervertebral disc: effect of porosity. Ann Biomed Eng 32(6):1710–1717Google Scholar
  30. Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS (2009) Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5(1):17–26Google Scholar
  31. Har-Shai Y, Bodner SR, Egozy-Golan D, Lindenbaum E, Ben-Izhak O, Mitz V, Hirshowitz B (1996) Mechanical properties and microstructure of the superficial musculoaponeurotic system. Plast Reconstr Surg 98:59–70Google Scholar
  32. Hendriks FM, Brokken D, Oomens CWJ, Bader DL, Baaijens FPT (2006) The relative contributions of different skin layers to the mechanical behavior of human skin in vivo using suction experiments. Med Eng Phys 28(3):259–266Google Scholar
  33. Hollenstein M, Ehret AE, Itskov M, Mazza E (2011) A novel experimental procedure based on pure shear testing of dermatome-cut samples applied to porcine skin. Biomech Model Mechanobiol 10(5):651–661Google Scholar
  34. Hong W, Liu Z, Suo Z (2009) Inhomogeneous swelling of a gel in equilibrium with a solvent and mechanical load. Int J Solids Struct 46(17):3282–3289zbMATHGoogle Scholar
  35. Hopf R, Bernardi L, Menze J, Zündel M, Mazza E, Ehret AE (2016) Experimental and theoretical analyses of the age-dependent large-strain behavior of Sylgard 184 (10:1) silicone elastomer. J Mech Behav Biomed Mater 60:425–437Google Scholar
  36. Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15(12):802–812Google Scholar
  37. Huyghe JM, Janssen JD (1997) Quadriphasic mechanics of swelling incompressible porous media. Int J Eng Sci 35(8):793–802zbMATHGoogle Scholar
  38. Imai SI (2009) The NAD world: a new systemic regulatory network for metabolism and aging-Sirt1, systemic NAD biosynthesis, and their importance. Cell Biochem Biophys 53(2):65–74Google Scholar
  39. Jayyosi C, Affagard JS, Ducourthial G, Bonod-Bidaud C, Lynch B, Bancelin S, Ruggiero F, Schanne-Klein MC, Allain JM, Bruyère-Garnier K, Coret M (2017) Affine kinematics in planar fibrous connective tissues: an experimental investigation. Biomech Model Mechanobiol 16(4):1459–1473Google Scholar
  40. Johnson ZI, Shapiro IM, Risbud MV (2014) Extracellular osmolarity regulates matrix homeostasis in the intervertebral disc and articular cartilage: evolving role of TonEBP. Matrix Biol 40:10–16Google Scholar
  41. Kitano H (2002) Computational systems biology. Nature 420(6912):206–210Google Scholar
  42. Kolarsick PAJ, Kolarsick MA, Goodwin C (2011) Anatomy and physiology of the skin. J Dermatol Nurses Assoc 3(4):203–213Google Scholar
  43. Lai WM, Hou JS, Mow VC (1991) A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113(3):245–258Google Scholar
  44. Lake SP, Barocas VH (2011) Mechanical and structural contribution of non-fibrillar matrix in uniaxial tension: a collagen-agarose co-gel model. Ann Biomed Eng 39(7):1891–1903Google Scholar
  45. Lanir Y (1987) Biorheology and fluid flux in swelling tissues. I. Bicomponent theory for small deformations, including concentration effects. Biorheology 24(2):173–187Google Scholar
  46. Lanir Y (2017) Multi-scale structural modeling of soft tissues mechanics and mechanobiology. J Elast 129(1–2):7–48MathSciNetzbMATHGoogle Scholar
  47. Lanir Y, Fung YC (1974) Two-dimensional mechanical properties of rabbit skin-II. Experimental results. J Biomech 7(2):171–182Google Scholar
  48. Latorre M, Romero X, Montáns FJ (2016) The relevance of transverse deformation effects in modeling soft biological tissues. Int J Solids Struct 99:57–70Google Scholar
  49. Leyva-Mendivil MF, Page A, Bressloff NW, Limbert G (2015) A mechanistic insight into the mechanical role of the stratum corneum during stretching and compression of the skin. J Mech Behav Biomed Mater 49:197–219Google Scholar
  50. Limbert G (2011) A mesostructurally-based anisotropic continuum model for biological soft tissues-decoupled invariant formulation. J Mech Behav Biomed Mater 4(8):1637–1657Google Scholar
  51. Limbert G (2017) Mathematical and computational modelling of skin biophysics: a review. Proc R Soc A 473:20170257MathSciNetzbMATHGoogle Scholar
  52. Loret B, Simões FMF (2010) Effects of the pH on the mechanical behavior of articular cartilage and corneal stroma. Int J Solids Struct 47(17):2201–2214zbMATHGoogle Scholar
  53. Lucantonio A, Nardinocchi P, Teresi L (2013) Transient analysis of swelling-induced large deformations in polymer gels. J Mech Phys Solids 61(1):205–218MathSciNetGoogle Scholar
  54. Lukashev ME, Werb Z (1998) ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol 8(11):437–441Google Scholar
  55. Mak AFT, Huang L, Wang Q (1994) A biphasic poroelastic analysis of the flow dependent subcutaneous tissue pressure and compaction due to epidermal loadings: issues in pressure sore. J Biomech Eng 116(4):421–429Google Scholar
  56. Markert B (2007) A constitutive approach to 3-d nonlinear fluid flow through finite deformable porous continua. Transp Porous Media 70(3):427–450MathSciNetGoogle Scholar
  57. Maroudas A (1968) Physicochemical properties of cartilage in the light of ion exchange theory. Biophys J 8(5):575–595Google Scholar
  58. Maroudas A (1976) Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 260:808–809Google Scholar
  59. Mauri A, Ehret AE, Perrini M, Maake C, Ochsenbein-Kölble N, Ehrbar M, Oyen ML, Mazza E (2015a) Deformation mechanisms of human amnion: quantitative studies based on second harmonic generation microscopy. J Biomech 48(9):1606–1613Google Scholar
  60. Mauri A, Perrini M, Ehret AE, De Focatiis DSA, Mazza E (2015b) Time-dependent mechanical behavior of human amnion: macroscopic and microscopic characterization. Acta Biomater 11(1):314–323Google Scholar
  61. Mauri A, Ehret AE, De Focatiis DSA, Mazza E (2016) A model for the compressible, viscoelastic behavior of human amnion addressing tissue variability through a single parameter. Biomech Model Mechanobiol 15(4):1005–1017Google Scholar
  62. Metcalfe AD, Ferguson MWJ (2007) Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration. J R Soc Interface 4(14):413–417Google Scholar
  63. Mouw JK, Ou G, Weaver VM (2014) Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 15(12):771–785Google Scholar
  64. Muñoz MJ, Bea JA, Rodríguez JF, Ochoa I, Grasa J, Pérez del Palomar A, Zaragoza P, Osta R, Doblaré M (2008) An experimental study of the mouse skin behaviour: damage and inelastic aspects. J Biomech 41(1):93–99Google Scholar
  65. Nakagawa N, Matsumoto M, Sakai S (2010) In vivo measurement of the water content in the dermis by confocal raman spectroscopy. Skin Res Technol 16(2):137–141Google Scholar
  66. Ng CP, Hinz B, Swartz MA (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(20):4731–4739Google Scholar
  67. Nguyen TD, Jones RE, Boyce BL (2007) Modeling the anisotropic finite-deformation viscoelastic behavior of soft fiber-reinforced composites. Int J Solids Struct 44(25–26):8366–8389zbMATHGoogle Scholar
  68. Ní Annaidh A, Bruyère K, Destrade M, Gilchrist MD, Maurini C, Otténio M, Saccomandi G (2012a) Automated estimation of collagen fibre dispersion in the dermis and its contribution to the anisotropic behaviour of skin. Ann Biomed Eng 40(8):1666–1678Google Scholar
  69. Ní Annaidh A, Bruyère K, Destrade M, Gilchrist MD, Otténio M (2012b) Characterization of the anisotropic mechanical properties of excised human skin. J Mech Behav Biomed Mater 5(1):139–148Google Scholar
  70. North JF, Gibson F (1978) Volume compressibility of human abdominal skin. J Biomech 11(4):203–207Google Scholar
  71. Oftadeh R, Connizzo BK, Nia HT, Ortiz C, Grodzinsky AJ (2018) Biological connective tissues exhibit viscoelastic and poroelastic behavior at different frequency regimes: application to tendon and skin biophysics. Acta Biomater 70:249–259Google Scholar
  72. Oomens CWJ, van Campen DH, Grootenboer HJ (1987) A mixture approach to the mechanics of skin. J Biomech 20(9):877–885Google Scholar
  73. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233Google Scholar
  74. Pensalfini M, Haertel E, Hopf R, Wietecha M, Werner S, Mazza E (2018) The mechanical fingerprint of murine excisional wounds. Acta Biomater 65:226–236Google Scholar
  75. Picu RC, Deogekar S, Islam MR (2018) Poisson’s contraction and fiber kinematics in tissue: insight from collagen network simulations. J Biomech Eng 140(2):021002Google Scholar
  76. Quinn TM, Grodzinsky AJ, Buschmann MD, Kim YJ, Hunziker EB (1998) Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J Cell Sci 111:573–583Google Scholar
  77. Rosso F, Giordano A, Barbarisi M, Barbarisi A (2004) From cell-ECM interactions to tissue engineering. J Cell Physiol 199(2):174–180Google Scholar
  78. Rubin MB, Bodner SR (2002) A three-dimensional nonlinear model for dissipative response of soft tissue. Int J Solids Struct 39(19):5081–5099zbMATHGoogle Scholar
  79. Rutkowski JM, Swartz MA (2007) A driving force for change: interstitial flow as a morphoregulator. Trends Cell Biol 17(1):44–50Google Scholar
  80. Schneiderman R, Keret D, Maroudas A (1986) Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J Orthop Res 4(4):393–408Google Scholar
  81. Smith CW, Wootton RJ, Evans KE (1999) Interpretation of experimental data for Poisson’s ratio of highly nonlinear materials. Exp Mech 39(4):356–362Google Scholar
  82. Stark HL, Al-Haboubi A (1980) The relationship of width, thickness, volume and load to extension for human skin in vitro. Eng Med 9(4):179–183Google Scholar
  83. Stracuzzi A, Mazza E, Ehret AE (2018) Chemomechanical models for soft tissues based on the reconciliation of porous media and swelling polymer theories. Z Angew Math Mech 98(12):2135–2154MathSciNetGoogle Scholar
  84. Tomic A, Grillo A, Federico S (2014) Poroelastic materials reinforced by statistically oriented fibres—numerical implementation and application to articular cartilage. IMA J Appl Math 79(5):1027–1059MathSciNetzbMATHGoogle Scholar
  85. Tonge TK, Atlan LS, Voo LM, Nguyen TD (2013a) Full-field bulge test for planar anisotropic tissues: part I—experimental methods applied to human skin tissue. Acta Biomater 9(4):5913–5925Google Scholar
  86. Tonge TK, Voo LM, Nguyen TD (2013b) Full-field bulge test for planar anisotropic tissues: part II—a thin shell method for determining material parameters and comparison of two distributed fiber modeling approaches. Acta Biomater 9(4):5926–5942Google Scholar
  87. Tracy LE, Minasian RA, Caterson EJ (2016) Extracellular matrix and dermal fibroblast function in the healing wound. Adv Wound Care 5(3):119–136Google Scholar
  88. Urban JP, Hall AC, Gehl KA (1993) Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 154(2):262–270Google Scholar
  89. Veronda DR, Westmann RA (1970) Mechanical characterization of skin—finite deformations. J Biomech 3(1):111–124Google Scholar
  90. Vossoughi J, Vaishnav RN (1979) Comments on the paper “Volume compressibility of human abdominal skin”. J Biomech 12:481Google Scholar
  91. Wang J, Zhang Y, Zhang N, Wang C, Herrler T, Li Q (2015) An updated review of mechanotransduction in skin disorders: transcriptional regulators, ion channels, and microRNAs. Cell Mol Life Sci 72(11):2091–2106Google Scholar
  92. Weickenmeier J, Jabareen M, Mazza E (2015) Suction based mechanical characterization of superficial facial soft tissues. J Biomech 48(16):4279–4286Google Scholar
  93. Wiig H, Rubin K, Reed RK (2003) New and active role of the interstitium in control of interstitial fluid pressure: potential therapeutic consequences. Acta Anaesthesiol Scand 47:111–121Google Scholar
  94. Wilson W, van Donkelaar CC, Huyghe JM (2005a) A comparison between mechano-electrochemical and biphasic swelling theories for soft hydrated tissues. J Biomech Eng 127(1):158–165Google Scholar
  95. Wilson W, van Donkelaar CC, van Rietbergen B, Huiskes R (2005b) A fibril-reinforced poroviscoelastic swelling model for articular cartilage. J Biomech 38(6):1195–1204Google Scholar
  96. Wong WLE, Joyce TJ, Goh KL (2016) Resolving the viscoelasticity and anisotropy dependence of the mechanical properties of skin from a porcine model. Biomech Model Mechanobiol 15(2):433–446Google Scholar
  97. Woo SL, Lubock P, Gomez MA, Jemmott GF, Kuei SC, Akeson WH (1979) Large deformation nonhomogeneous and directional properties of articular cartilage in uniaxial tension. J Biomech 12(6):437–446Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Mechanical and Process Engineering, Institute for Mechanical SystemsETH ZurichZurichSwitzerland
  2. 2.Department of DermatologyUniversity Hospital ZurichZurichSwitzerland
  3. 3.Empa, Swiss Federal Laboratories for Materials Science and TechnologyDübendorfSwitzerland

Personalised recommendations