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Modelling methods for In Vitro biomechanical properties of the skin: A review

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Abstract

Propose

In vitro biomechanical properties of the skin are of important to cosmetic product development, plastic surgery, surgical practice, skin disease pathology, mechanical trauma and artificial skin design. However, complex biomechanical properties of the skin have not been fully understood so far. The literature of histology, in vitro biomechanical properties and modelling methods of the skin is reviewed to identify important problems that need to be tackled.

Methods

A PubMed literature search was conducted using the terms ‘skin,’ ‘biomechanical property,’ ‘damage,’ ‘collagen fibre,’ ‘viscoelastic’ and ‘dermis.’ Relevant papers were read and analysed.

Results

The histology of the skin has been studied considerably by means of optical and electron microscopies. The collagen fibre structure in the dermis has been observed with image analysis approach, and a few formulas for fibre orientation dispersion are proposed. The uniaxial, biaxial and bulge test methods were commonly applied to determine in vitro biomechanical properties of the skin.In vitro biomechanical properties exhibit nonlinear anisotropic behaviour, and at a higher strain rate, there is damage effect. Simple elongation model, isotropic model, collagen fibre recruitment model and micro-structure based model are applicable for the skin. The biomechanical property constants can be determined from the stress-stretch curves obtained in uniaxial or biaxial or multi-axial or bulge tests.

Conclusions

The collagen fibre network 3D structure remain unclear and the fibre orientation dispersion characteristics are not totally understood. The damage effect in the skin has not been tackled by using constitutive laws so far. The tensile damage and fracture process, multi-layer biomechanical models developing, viscoelastic property testing and modelling in the skin should be paid significant attention in future.

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References

  1. Goldsmith LA. My organ is bigger than your organ. Arch Dermatol. 1990; 126:301–2.

    Article  Google Scholar 

  2. Edwards C, Marks R. Evaluation of biomechanical properties of human skin. Clin Dermatol. 1995; 13:375–80.

    Article  Google Scholar 

  3. Silver FH, Siperko LM, Seehra GP. Mechanobiology of force transduction in dermal tissue. Skin Res Technol. 2003; 9:3–23.

    Article  Google Scholar 

  4. Weinstein GD, Boucek RJ. Collagen and elastin of human dermis. J Invest Dermatol. 1960; 35:227–9.

    Article  Google Scholar 

  5. Elsner P, Berardesca E, Wilhelm KP, Maibach HI. Bioengineering of the skin-skin biomechanics. Boca Raton: CRC Press, 2002.

    Google Scholar 

  6. Pope FM, Martin GR, Lichtenstein JR, Penttinen R, Gerson B, Rowe DW, McKusick VA. Patients with Ehlers-Danlos Syndrome Type IV lack Type III collagen. Proc Nat Acad Sci USA. 1975; 72:1314–6.

    Article  Google Scholar 

  7. Byers PH, Holbrook K, McGillivray B, MacLeod PM, Lowry RB. Clinical and ultrastructure heterogeneity of Type IV Ehlers-Danlos Syndrome. Hum Genet. 1979; 47:141–50.

    Article  Google Scholar 

  8. Yen JL, Lin SP, Chen MR, Niu DM. Clinical features of Ehlers-Danlos Syndrome. J Formos Med Assoc. 2006; 105:475480.

    Google Scholar 

  9. Alexander H, Cook TH. Accounting for natural tension in the mechanical testing of human skin. J Invest Dermatol. 1977; 69:310–4.

    Article  Google Scholar 

  10. Larrabee WF, Sutton D. A finite element model of skin deformation II: an experimental model of skin deformation. Laryngoscope. 1986;96:406–12.

    Google Scholar 

  11. Mahmud J, Holtb C, Evansb S, Nor Fazli Adull Manan NFA, Chizari M. A parametric study and simulations in quantifying human skin. Procedia Eng, 2012; 41:1580–6.

    Article  Google Scholar 

  12. Pailler-Mattei C Bec S, Zahouani H. In vivo measurements of the elastic mechanical properties of human skin by indentation tests. Med Eng Phys. 2008; 30:599–606.

    Article  Google Scholar 

  13. Evans SL, Holt CA. Measuring the mechanical properties of human skin in vivo using digital image correlation and finite element modelling. J Strain Anal. 2009; 44:337–45.

    Article  Google Scholar 

  14. Liang X, Boppart SA. Biomechanical properties of in vivo human skin from dynamic optical coherence elastography. IEEE T Biomed Eng, 2010; 57:953–9.

    Article  Google Scholar 

  15. Flynn C, Taberner A, Nielsen P. Mechanical characterisation of in vivo human skin using 3D force-sensitive micro-robot and finite element analysis. Biomech Model Mechan. 2011; 10:27–38.

    Article  Google Scholar 

  16. Veronda DR, Westmann RA. Mechanical characterization of skin-finite deformations. J Biomech. 1970; 3:111–24.

    Article  Google Scholar 

  17. Ridge MD, Wright V. Mechanical properties of skin: a bioengineering study of skin structure. J Appl Phys. 1966; 21:1602–6.

    Google Scholar 

  18. Ridge MD, Wright V. The directional effects skin. J Invest Dermatol. 1966; 46:341–6.

    Article  Google Scholar 

  19. Karimi A, Navidbakhsh M. Measurement of the uniaxial mechanical properties of rat skin using different stress-strain definitions. Skin Res Technol. 2014; 21:149–157.

    Article  Google Scholar 

  20. Shadwick RE, Russell AP, Lauff RF. The structure and mechanical design of rhinoceros dermal armour. Philos T Roy Soc B. 1992; 337:419–28.

    Article  Google Scholar 

  21. Ankersen J, Birkbeck AE, Thomson RD, Vanezis P. Puncture resistance and tensile strength of skin simulants. P I Mech Eng H. 1999; 213:493–501.

    Article  Google Scholar 

  22. Shergold OA, Fleck NA, Radford D. The uniaxial stress versus strain response of pig skin and silicon rubber at low and high strain rates. Int J Impact Eng. 2006; 32:1384–402.

    Article  Google Scholar 

  23. Lim J, Hong J, Chen WW, Weerasooriya T. Mechanical response of pig skin under dynamic tensile loading, Int J Impact Eng. 2011; 38:130–5.

    Article  Google Scholar 

  24. Zak M, Kuropka P, Kobielarz M, Dudek A, Kaleta-Kuratewicz K, Szotek S. Determination of the mechanical properties of the skin of pig foetuses with respect to its structure. Acta Bioeng Biomech. 2011; 13:37–43.

    Google Scholar 

  25. Ni Annaidh A, Bruyere K, Destrade M, Gilchrist MD, Ottenio M. Characterization of the anisotropic mechanical properties of excised human skin. J Mech Behav Biomed. 2012; 5:139–48.

    Article  Google Scholar 

  26. Lanir Y, Fung YC. Two-dimensional mechanical properties of rabbit skin-I experimental system. J Biomech. 1974; 7:29–34.

    Article  Google Scholar 

  27. Lanir Y, Fung YC. Two-dimensional mechanical properties of rabbit skin-II experimental results. J Biomech. 1974; 7:171–82.

    Article  Google Scholar 

  28. Schneider DC, Davison TM, Nahum AM. In vitro biaxial stressstrain response of human skin. Arch Otolaryngol. 1984; 110:329–33.

    Article  Google Scholar 

  29. Reihsner R, Balogh B, Menzel EJ. Two-dimensional elastic properties of human skin in terms of an incremental model at the in vivo configuration. Med Eng Phys. 1995; 4:304–13.

    Article  Google Scholar 

  30. Jor JWY, Nash MP, Nielsen PMF, Hunter PJ. Estimating material parameters of a structurally based constitutive relation for skin mechanics. Biomech Model Mechan. 2010; 10:767–78.

    Article  Google Scholar 

  31. Dick JC. The tension and resistance to stretching of human skin and other membranes, with results from a series of normal and oedematous cases. J Physiol. 1951; 112:102–13.

    Article  Google Scholar 

  32. Tonge TK, Atlan LS, Voo LM, Nguyen TD. Full-field bulge test for planar anisotropic tissues: Part I-experimental methods applied to human skin tissue. Acta Biomater. 2013; 9:5913–23.

    Article  Google Scholar 

  33. Zhou B, Xu F, Chen CQ, Lu TJ. Strain rate sensitivity of skin tissue under thermomechanical loading. Philos T Roy Soc A. 2014; 368:679–90.

    Article  MATH  Google Scholar 

  34. Li WG, Going J, Hill NA, Luo XY. Breaking analysis of artificial elastic tubes and human artery. Int J Appl Mech. 2013; 5:55–66.

    Article  Google Scholar 

  35. Holzapfel GA, Gasser TC, Ogden RW. A new constitutive framework for arterial wall mechanics and a comparative study of material models. J Elasticity Phys Sci Solids. 2000; 61:1–48.

    Article  MathSciNet  MATH  Google Scholar 

  36. Cox HT. The cleavage lines of the skin. Brit J Surg. 1941; 29:234–40.

    Article  Google Scholar 

  37. Gibson T, Kendi RM, Craik JE. The mobile micro-architectures of dermal collagen. Brit J Surg. 1965; 52:764–70.

    Article  Google Scholar 

  38. Tregear RT. The mechanical properties of skin. J Soc Cosmet Chem. 1969; 20:467–77.

    Google Scholar 

  39. Carr KE. Scanning electron microscopy studies of human skin. Brit J Plast Surg. 1970; 23:66–72.

    Article  Google Scholar 

  40. Papa CM, Farber B. Direct scanning electron microscopy. Arch Dermatol. 1971; 104:262–70.

    Article  Google Scholar 

  41. Dawber R, Shuster S. Scanning electron microscopy of dermis fibrous tissue networks in normal skin, solar elastosis and pseudo-xanthoma elasticum. Brit J Dermatol. 1971; 84:130–4.

    Article  Google Scholar 

  42. Brown IA. Scanning electron microscopy of human dermal fibrous tissue. J Anatomy. 1972; 113:159–68.

    Google Scholar 

  43. Brown IA. A scanning electron microscopy study of the effects of uniaxial tension on human skin. Brit J Dermatol. 1973; 89:383–93.

    Article  Google Scholar 

  44. Mowafy M, Cassens RG. Microscopic structure of pig skin. J Anim Sci. 1975; 41:1281–90.

    Google Scholar 

  45. Meyer W, Neurand K, Radke B. Collagen fibre arrangement in the skin of the pig. J Anat. 1982; 134:139–48.

    Google Scholar 

  46. Ferdman AG, Yannas IV. Scattering of light from histologic sections: a new method for the analysis of connective tissue. J Invest Dermatol. 1993; 100:710–6.

    Article  Google Scholar 

  47. Vaezy S, Smith LT, Milaninia A, Clark JI. Two-dimensional Fourier analysis of electron micrographs of human skin for quantification of the collagen fiber organization in the dermis. J Electron Microsc. 1995; 44:358–64.

    Google Scholar 

  48. Gogly B, Godeau G, Gilbert S, Legrand JM, Kut C, Pellat B, Goldberg M. Morphometric analysis of collagen and elastic fibers in normal skin and gingiva in relation to age. Clin Oral Invest. 1997; 1:147–52.

    Article  Google Scholar 

  49. Noorlander ML, Melis P, Jonker A, Van Noorden CJF. A quantitative method to determine the orientation of collagen fibers in the dermis. J Histochem Cytochem. 2002; 50:1469–74.

    Article  Google Scholar 

  50. Osman OS, Selway JL, Harikumar PE, Stocker CJ, Wargent ET, Cawthorne MA, Jassim S, Langlands K. A novel method to assess collagen architecture in skin. BMC Bioinformatics. 2013; 14:260–70.

    Article  Google Scholar 

  51. Rawlins JM, Lam WL, Karoo RO, Naylor IL, Sharpe DT. Quantifying collagen type in mature burn scars: a novel approach using histology and digital image analysis. J Burn Care Res. 2006; 27:60–5.

    Article  Google Scholar 

  52. Vardaxis NJ, Brans TA, Boon ME, Kreis RW, Marres LM. Confocal laser scanning microscopy of porcine skin: implications for human wound healing studies. J Anat. 1997; 190:601–11.

    Article  Google Scholar 

  53. van Zuijlen PPM, Ruurda JJB, van Veen HA, van Marle J, van Trier AJM, Groenevelt F, Kreis RW, Middelkoop E. Collagen morphology in human skin and scar tissue: no adaptations in response to mechanical loading at joints. Burns. 2003; 29:423–31.

    Article  Google Scholar 

  54. Verhaegen PD, Schouten HJ, Tigchelaar-Gutter W, van Marle J, van Noorden CJ, Middelkoop E, van Zuijlen PPM. Adaptation of the dermis collagen structure of human skin and scar tissue in response to stretch: an experimental study. Wound Repair Regen. 2012; 20:658–66.

    Article  Google Scholar 

  55. Jor JWY, Nielsen PMF, Nash MP, Hunter PJ. Modelling collagen fibre orientation in porcine skin based upon confocal laser scanning microscopy. Skin Res Technol. 2011; 17:149–59.

    Article  Google Scholar 

  56. O’Brien K, Bhatia A, Tsen F, Chen M, Wong AK, et al. Identification of the critical therapeutic entity in secreted hsp90á that promotes wound healing in newly re-standardized healthy and diabetic pig models. PLoS ONE. 2014; 9(12): e113956. doi:10.1371/journal.pone.0113956.

    Article  Google Scholar 

  57. Ni Annaidh A, Bruyere K, Destrade M, Gilchrist MD, Maurini C, Ottenio M, Saccomandi G. Automated estimation of collagen fibre dispersion in the dermis and its contribution to the anisotropic behaviour of skin. Annals Biomed Eng. 2012; 40:1666–78.

    Article  Google Scholar 

  58. Ribeiro JF, dos Anjos EHM, Mello ML, de Campos Vidal B. Skin collagen fiber molecular order: a pattern of distributional fiber orientation as assessed by optical anisotropy and image analysis. PLoS ONE. 8:e54724. Dio:10.1371/journal.pone.0054724.

  59. Ridge MD, Wright V. The rheology of skin. Brit J Dermatol. 1965; 77:635–49.

    Article  Google Scholar 

  60. Lapeer RJ, Gasson PD, Karri V. Simulating plastic surgery: from human skin tensile tests, through hyperelastic finite element models to real-time haptics. Progress Biophys Mol Biol. 2010; 103:208–16.

    Article  Google Scholar 

  61. Arruda EM, Boyce MC. A three-dimensional constitutive model for the large stretch behaviour of rubber elastic materials. J Mech Phys Solids. 1993; 41:389–412.

    Article  Google Scholar 

  62. Belkoff SM, Arruda EM, Grosh K. Finite element modelling of human skin using an isotropic, nonlinear elastic constitutive model. J Biomech. 2000; 33:645–52.

    Article  Google Scholar 

  63. Weiss JA, Maker BN, Govindjee S. Finite element implementation of incompressible, transversely isotropic hyperelasticity. Comput Method Appl M. 1996; 135:107–35.

    Article  MATH  Google Scholar 

  64. Groves RB, Coulman SA, Birchall JC, Evans SL. An anisotropic, hyperelastic model for skin: experimental measurements, finite element modelling and identification of parameters for human and murine skin. J Mech Behav Biomed. 2013; 18:167–80.

    Article  Google Scholar 

  65. Gasser TC, Ogden RW, Holzapfel GA. Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J Roy Soc Interface. 2006; 3:15–35.

    Article  Google Scholar 

  66. Tonge TK, Atlan LS, Voo LM, Nguyen TD. Full-field bulge test for planar anisotropic tissues: Part II-a thin shell method for determining material parameters and comparison of two distribution fiber modelling approaches. Acta Biomater. 2013; 9:5926–42.

    Article  Google Scholar 

  67. Tepole AB, Gosain AK, Kuhl E. Computational modelling of skin: using stress profiles as predictor for tissue necrosis in reconstructive surgery. Comput Struct. 2014; 143:32–9.

    Article  Google Scholar 

  68. Belkoff SM, Haut RC. A structural model used to evaluate the changing microstructure of maturing rat skin. J Biomech. 1991; 24:711–20.

    Article  Google Scholar 

  69. Lanir Y. Constitutive equations for fibrous connective tissues. J Biomech. 1983; 16:1–12.

    Article  Google Scholar 

  70. Munoz MJ, Bea JA, Rodriguez JF, Ochoa I, Grasa J, Perez A, del Palomar P, Zaragoza P, Osta R, Doblare M. An experimental study of the mouse skin behaviour: damage and inelastic aspects. J Biomech. 2008; 41:93–9.

    Article  Google Scholar 

  71. Nakagawa N, Matsumoto M, Sakai S. In vivo measurement of the water content in the dermis by confocal Raman spectroscopy. Skin Res Technol. 2010; 16:137–41.

    Article  Google Scholar 

  72. Silver FH, Freeman JW, DeVore D. Viscoelastic properties of human skin and processed dermis. Skin Res Technol. 2001; 7:18–23.

    Article  Google Scholar 

  73. Pioletti DP, Rakotomanana LR. Non-linear viscoelastic laws for soft biological tissues. Eur J Mech A Solid. 2000; 19:749–59.

    Article  MATH  Google Scholar 

  74. Wineman A. Nonlinear viscoelastic solids-a review. Math Mech Solids. 2009; 14:300–66.

    Article  MathSciNet  MATH  Google Scholar 

  75. Fung YC. Biomechanics: mechanical properties of living tissues. New York, Springer, 1993.

    Book  Google Scholar 

  76. Flynn C, Taberner A, Nielsen P. Mechanical characterisation of in vivo human skin using 3D force-sensitive micro-robot and finite element analysis. Biomech Model Mechan. 2011; 10:27–38.

    Article  Google Scholar 

  77. Ahsanizadeh S, Li LP. Visco-hyperelastic constitutive modelling of soft tissues based on short and long-term internal variables. Biomed Eng Online. 2015; 14:1–16.

    Article  Google Scholar 

  78. Ciarletta P, Amar MB. Papillary networks in the dermalepidermal junction of skin: a biomechanical model. Mech Res Commun. 2012; 42:68–75.

    Article  Google Scholar 

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Li, W. Modelling methods for In Vitro biomechanical properties of the skin: A review. Biomed. Eng. Lett. 5, 241–250 (2015). https://doi.org/10.1007/s13534-015-0201-3

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