Skip to main content
Log in

On the compressibility and poroelasticity of human and murine skin

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Notes

  1. A NaCl solution of salt concentration \(c_{{\mathrm {ext}}}\) has the osmolarity \(2c_{{\mathrm {ext}}}\).

  2. For the membrane response to be quasi-isotropic, N / 2 has to be an even integer.

References

  • 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):1862–1872

    Article  Google Scholar 

  • Ateshian GA, Weiss JA (2010) Anisotropic hydraulic permeability under finite deformation. J Biomech Eng 132(11):111004

    Article  Google Scholar 

  • 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):061003

    Article  Google Scholar 

  • 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–H1205

    Article  Google Scholar 

  • Bader DL, Bowker P (1983) Mechanical characteristics of skin and underlying tissues in vivo. Biomaterials 4(4):305–308

    Article  Google Scholar 

  • 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 5:1–14

    Article  Google Scholar 

  • Baughman RH, Stafström S, Cui C, Dantas SO (1998) Materials with negative compressibilities in one or more dimensions. Science 279(5356):1522–1524

    Article  Google Scholar 

  • Benítez JM, Montáns FJ (2017) The mechanical behavior of skin: structures and models for the finite element analysis. Comput Struct 190:75–107

    Article  Google Scholar 

  • 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):081005

    Article  Google Scholar 

  • 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):741–744

    Article  Google Scholar 

  • Brown IA (1973) A scanning electron microscope study of the effects of uniaxial tension on human skin. Br J Dermatol 89(4):383–393

    Article  Google Scholar 

  • Buerzle W, Mazza E (2013) On the deformation behavior of human amnion. J Biomech 46(11):1777–1783

    Article  Google Scholar 

  • Buganza Tepole A (2017) Computational systems mechanobiology of wound healing. Comput Methods Appl Mech Eng 314:46–70

    Article  MathSciNet  Google Scholar 

  • 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 143:32–39

    Article  Google Scholar 

  • 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):4670–4681

    Article  Google Scholar 

  • Daly CH (1982) Biomechanical properties of dermis. J Invest Dermatol 79:48–51

    Article  Google Scholar 

  • Donnan FG (1924) The theory of membrane equilibria. Chem Rev 1(1):73–90

    Article  Google Scholar 

  • Ehlers W (2002) Foundations of multiphasic and porous materials. In: Ehlers W, Bluhm J (eds) Porous media. Springer, Berlin, pp 3–86

    Chapter  MATH  Google Scholar 

  • 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):233–251

    Article  Google Scholar 

  • 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):1125–1135

    Article  Google Scholar 

  • 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):1–9

    Article  Google Scholar 

  • Eskandari M, Kuhl E (2015) Systems biology and mechanics of growth. Wiley Interdiscip Rev Syst Biol Med 7(6):401–412

    Article  Google Scholar 

  • Federico S, Grillo A (2012) Elasticity and permeability of porous fibre-reinforced materials under large deformations. Mech Mater 44:58–71

    Article  Google Scholar 

  • Frijns AJH, Huyghe JM, Janssen JD (1997) A validation of the quadriphasic mixture theory for intervertebral disc tissue. Int J Eng Sci 35(15):1419–1429

    Article  MATH  Google Scholar 

  • Gibson T, Kenedi RM, Craik JE (1965) The mobile micro-architecture of dermal collagen: a bio-engineering study. Br J Surg 52(10):764–770

    Article  Google Scholar 

  • Gray ML, Pizzanelli AM, Grodzinsky AJ, Lee RC (1988) Mechanical and physicochemical determinants of the chondrocyte biosynthetic response. J Orthop Res 6(6):777–792

    Article  Google Scholar 

  • Grodzinsky AJ (2011) Fields, forces and flows in biological systems. Garland Science, New York

    Google Scholar 

  • 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 18:167–180

    Article  Google Scholar 

  • 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):1710–1717

    Article  Google Scholar 

  • 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):17–26

    Article  Google Scholar 

  • 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 98:59–70

    Article  Google Scholar 

  • 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):259–266

    Article  Google Scholar 

  • 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):651–661

    Article  Google Scholar 

  • 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):3282–3289

    Article  MATH  Google Scholar 

  • 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 60:425–437

    Article  Google Scholar 

  • Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15(12):802–812

    Article  Google Scholar 

  • Huyghe JM, Janssen JD (1997) Quadriphasic mechanics of swelling incompressible porous media. Int J Eng Sci 35(8):793–802

    Article  MATH  Google Scholar 

  • 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):65–74

    Article  Google Scholar 

  • 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):1459–1473

    Article  Google Scholar 

  • 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 40:10–16

    Article  Google Scholar 

  • Kitano H (2002) Computational systems biology. Nature 420(6912):206–210

    Article  Google Scholar 

  • Kolarsick PAJ, Kolarsick MA, Goodwin C (2011) Anatomy and physiology of the skin. J Dermatol Nurses Assoc 3(4):203–213

    Article  Google Scholar 

  • Lai WM, Hou JS, Mow VC (1991) A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113(3):245–258

    Article  Google Scholar 

  • 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):1891–1903

    Article  Google Scholar 

  • Lanir Y (1987) Biorheology and fluid flux in swelling tissues. I. Bicomponent theory for small deformations, including concentration effects. Biorheology 24(2):173–187

    Article  Google Scholar 

  • Lanir Y (2017) Multi-scale structural modeling of soft tissues mechanics and mechanobiology. J Elast 129(1–2):7–48

    Article  MathSciNet  MATH  Google Scholar 

  • Lanir Y, Fung YC (1974) Two-dimensional mechanical properties of rabbit skin-II. Experimental results. J Biomech 7(2):171–182

    Article  Google Scholar 

  • Latorre M, Romero X, Montáns FJ (2016) The relevance of transverse deformation effects in modeling soft biological tissues. Int J Solids Struct 99:57–70

    Article  Google Scholar 

  • 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 49:197–219

    Article  Google Scholar 

  • Limbert G (2011) A mesostructurally-based anisotropic continuum model for biological soft tissues-decoupled invariant formulation. J Mech Behav Biomed Mater 4(8):1637–1657

    Article  Google Scholar 

  • Limbert G (2017) Mathematical and computational modelling of skin biophysics: a review. Proc R Soc A 473:20170257

    Article  MathSciNet  MATH  Google Scholar 

  • 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):2201–2214

    Article  MATH  Google Scholar 

  • Lucantonio A, Nardinocchi P, Teresi L (2013) Transient analysis of swelling-induced large deformations in polymer gels. J Mech Phys Solids 61(1):205–218

    Article  MathSciNet  Google Scholar 

  • Lukashev ME, Werb Z (1998) ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol 8(11):437–441

    Article  Google Scholar 

  • 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):421–429

    Article  Google Scholar 

  • Markert B (2007) A constitutive approach to 3-d nonlinear fluid flow through finite deformable porous continua. Transp Porous Media 70(3):427–450

    Article  MathSciNet  Google Scholar 

  • Maroudas A (1968) Physicochemical properties of cartilage in the light of ion exchange theory. Biophys J 8(5):575–595

    Article  Google Scholar 

  • Maroudas A (1976) Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 260:808–809

    Article  Google Scholar 

  • 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):1606–1613

    Article  Google Scholar 

  • 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):314–323

    Article  Google Scholar 

  • 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):1005–1017

    Article  Google Scholar 

  • 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):413–417

    Article  Google Scholar 

  • Mouw JK, Ou G, Weaver VM (2014) Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 15(12):771–785

    Article  Google Scholar 

  • 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):93–99

    Article  Google Scholar 

  • 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):137–141

    Article  Google Scholar 

  • Ng CP, Hinz B, Swartz MA (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(20):4731–4739

    Article  Google Scholar 

  • 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):8366–8389

    Article  MATH  Google Scholar 

  • 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):1666–1678

    Article  Google Scholar 

  • 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):139–148

    Article  Google Scholar 

  • North JF, Gibson F (1978) Volume compressibility of human abdominal skin. J Biomech 11(4):203–207

    Article  Google Scholar 

  • 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 70:249–259

    Article  Google Scholar 

  • Oomens CWJ, van Campen DH, Grootenboer HJ (1987) A mixture approach to the mechanics of skin. J Biomech 20(9):877–885

    Article  Google Scholar 

  • Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233

    Article  Google Scholar 

  • Pensalfini M, Haertel E, Hopf R, Wietecha M, Werner S, Mazza E (2018) The mechanical fingerprint of murine excisional wounds. Acta Biomater 65:226–236

    Article  Google Scholar 

  • 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):021002

    Article  Google Scholar 

  • 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 111:573–583

    Google Scholar 

  • Rosso F, Giordano A, Barbarisi M, Barbarisi A (2004) From cell-ECM interactions to tissue engineering. J Cell Physiol 199(2):174–180

    Article  Google Scholar 

  • Rubin MB, Bodner SR (2002) A three-dimensional nonlinear model for dissipative response of soft tissue. Int J Solids Struct 39(19):5081–5099

    Article  MATH  Google Scholar 

  • Rutkowski JM, Swartz MA (2007) A driving force for change: interstitial flow as a morphoregulator. Trends Cell Biol 17(1):44–50

    Article  Google Scholar 

  • 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):393–408

    Article  Google Scholar 

  • Smith CW, Wootton RJ, Evans KE (1999) Interpretation of experimental data for Poisson’s ratio of highly nonlinear materials. Exp Mech 39(4):356–362

    Article  Google Scholar 

  • 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):179–183

    Article  Google Scholar 

  • 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):2135–2154

    Article  MathSciNet  Google Scholar 

  • 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):1027–1059

    Article  MathSciNet  MATH  Google Scholar 

  • 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):5913–5925

    Article  Google Scholar 

  • 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):5926–5942

    Article  Google Scholar 

  • Tracy LE, Minasian RA, Caterson EJ (2016) Extracellular matrix and dermal fibroblast function in the healing wound. Adv Wound Care 5(3):119–136

    Article  Google Scholar 

  • 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):262–270

    Article  Google Scholar 

  • Veronda DR, Westmann RA (1970) Mechanical characterization of skin—finite deformations. J Biomech 3(1):111–124

    Article  Google Scholar 

  • Vossoughi J, Vaishnav RN (1979) Comments on the paper “Volume compressibility of human abdominal skin”. J Biomech 12:481

    Article  Google Scholar 

  • 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):2091–2106

    Article  Google Scholar 

  • Weickenmeier J, Jabareen M, Mazza E (2015) Suction based mechanical characterization of superficial facial soft tissues. J Biomech 48(16):4279–4286

    Article  Google Scholar 

  • 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 47:111–121

    Article  Google Scholar 

  • 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):158–165

    Article  Google Scholar 

  • Wilson W, van Donkelaar CC, van Rietbergen B, Huiskes R (2005b) A fibril-reinforced poroviscoelastic swelling model for articular cartilage. J Biomech 38(6):1195–1204

    Article  Google Scholar 

  • 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):433–446

    Article  Google Scholar 

  • 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):437–446

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Adam Wahlsten or Edoardo Mazza.

Ethics declarations

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.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Adam Wahlsten and Marco Pensalfini share first authorship of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wahlsten, A., Pensalfini, M., Stracuzzi, A. et al. On the compressibility and poroelasticity of human and murine skin. Biomech Model Mechanobiol 18, 1079–1093 (2019). https://doi.org/10.1007/s10237-019-01129-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-019-01129-1

Keywords

Navigation