Advertisement

Multiscale Characterisation of Skin Mechanics Through In Situ Imaging

  • Jean-Marc AllainEmail author
  • Barbara Lynch
  • Marie-Claire Schanne-Klein
Chapter
  • 564 Downloads
Part of the Studies in Mechanobiology, Tissue Engineering and Biomaterials book series (SMTEB, volume 22)

Abstract

The complex mechanical properties of skin have been studied intensively over the past decades. They are intrinsically linked to the structure of the skin at several length scales, from the macroscopic layers (epidermis, dermis and hypodermis) down to the microstructural organization at the molecular level. Understanding the link between this microscopic organization and the mechanical properties is of significant interest in the cosmetic and medical fields. Nevertheless, it only recently became possible to directly visualize the skin’s microstructure during mechanical assays, carried out on the whole tissue or on isolated layers. These recent observations have provided novel information on the role of structural components of the skin in its mechanical properties, mainly the collagen fibers in the dermis, while the contribution of others, such as elastin fibers, remains elusive. In this chapter we present current methods used to observe skin’s microstructure during a mechanical assay, along with their strengths and limitations, and we review the unique information they provide on the link between structure and function of the skin.

References

  1. 1.
    Lanir Y, Fung YC (1974) Two-dimensional mechanical properties of rabbit skin—II. Experimental results. J Biomech 7:171–182.  https://doi.org/10.1016/0021-9290(74)90058-X CrossRefGoogle Scholar
  2. 2.
    Tong P, Fung Y-C (1976) The stress-strain relationship for the skin. J Biomech 9:649–657.  https://doi.org/10.1016/0021-9290(76)90107-X CrossRefGoogle Scholar
  3. 3.
    Veronda DR, Westmann RA (1970) Mechanical characterization of skin—finite deformations. J Biomech 3:111–124CrossRefGoogle Scholar
  4. 4.
    Affagard J-S, Wijanto F, Allain J-M (2017) Improving the experimental protocol for a more accurate identification of a given mechanical behaviour in a single assay: application to skin. Strain 53:e12236.  https://doi.org/10.1111/str.12236 CrossRefGoogle Scholar
  5. 5.
    Edwards C, Marks R (1995) Evaluation of biomechanical properties of human skin. Clin Dermatol 13:375–380.  https://doi.org/10.1016/0738-081X(95)00078-T CrossRefGoogle Scholar
  6. 6.
    Jor JWY, Nash MP, Nielsen PMF, Hunter PJ (2010) Estimating material parameters of a structurally based constitutive relation for skin mechanics. Biomech Model Mechanobiol 10:767–778.  https://doi.org/10.1007/s10237-010-0272-0 CrossRefGoogle Scholar
  7. 7.
    Edsberg LE, Mates RE, Baier RE, Lauren M (1999) Mechanical characteristics of human skin subjected to static versus cyclic normal pressures. J Rehabil Res Dev 36(2):133–141Google Scholar
  8. 8.
    Wang Y, Marshall KL, Baba Y et al (2013) Hyperelastic material properties of mouse skin under compression. PLoS One 8:e67439.  https://doi.org/10.1371/journal.pone.0067439 CrossRefGoogle Scholar
  9. 9.
    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 10:651–661.  https://doi.org/10.1007/s10237-010-0263-1 CrossRefGoogle Scholar
  10. 10.
    Bonod-Bidaud C, Roulet M, Hansen U et al (2012) In vivo evidence for a bridging role of a collagen V subtype at the epidermis–dermis interface. J Investig Dermatol 132:1841–1849CrossRefGoogle Scholar
  11. 11.
    Oxlund H, Manschot J, Viidik A (1988) The role of elastin in the mechanical properties of skin. J Biomech 21:213–218.  https://doi.org/10.1016/0021-9290(88)90172-8 CrossRefGoogle Scholar
  12. 12.
    Eshel H, Lanir Y (2001) Effects of strain level and proteoglycan depletion on preconditioning and viscoelastic responses of rat dorsal skin. Ann Biomed Eng 29:164–172.  https://doi.org/10.1114/1.1349697 CrossRefGoogle Scholar
  13. 13.
    Agache PG, Monneur C, Leveque JL, De Rigal J (1980) Mechanical properties and Young’s modulus of human skin in vivo. Arch Dermatol Res 269:221–232.  https://doi.org/10.1007/BF00406415 CrossRefGoogle Scholar
  14. 14.
    Kvistedal YA, Nielsen PMF (2009) Estimating material parameters of human skin in vivo. Biomech Model Mechanobiol 8:1–8.  https://doi.org/10.1007/s10237-007-0112-z CrossRefGoogle Scholar
  15. 15.
    Hendriks FM, Brokken D, Oomens CWJ, Baaijens FPT (2004) Influence of hydration and experimental length scale on the mechanical response of human skin in vivo, using optical coherence tomography. Skin Res Technol 10:231–241.  https://doi.org/10.1111/j.1600-0846.2004.00077.x CrossRefGoogle Scholar
  16. 16.
    Pailler-Mattéi C, Zahouani H (2006) Analysis of adhesive behaviour of human skin in vivo by an indentation test. Tribol Int 39:12–21.  https://doi.org/10.1016/j.triboint.2004.11.003 CrossRefGoogle Scholar
  17. 17.
    Groves RB (2011) Quantifying the mechanical properties of skin in vivo and ex vivo to optimise microneedle device design. Cardiff University, CardiffGoogle Scholar
  18. 18.
    Abrahams M (1967) Mechanical behaviour of tendon in vitro. Med Biol Eng 5:433–443CrossRefGoogle Scholar
  19. 19.
    Elsheikh A, Alhasso D, Rama P (2008) Biomechanical properties of human and porcine corneas. Exp Eye Res 86:783–790.  https://doi.org/10.1016/j.exer.2008.02.006 CrossRefGoogle Scholar
  20. 20.
    Holzapfel GA, Sommer G, Gasser CT, Regitnig P (2005) Determination of layer-specific mechanical properties of human coronary arteries with nonatherosclerotic intimal thickening and related constitutive modeling. Am J Physiol Heart Circ Physiol 289:H2048–H2058.  https://doi.org/10.1152/ajpheart.00934.2004 CrossRefGoogle Scholar
  21. 21.
    Ottenio M, Tran D, Ní Annaidh A et al (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 CrossRefGoogle Scholar
  22. 22.
    Pensalfini M, Haertel E, Hopf R et al (2018) The mechanical fingerprint of murine excisional wounds. Acta Biomater 65:226–236.  https://doi.org/10.1016/j.actbio.2017.10.021 CrossRefGoogle Scholar
  23. 23.
    Samani A, Zubovits J, Plewes D (2007) Elastic moduli of normal and pathological human breast tissues: an inversion-technique-based investigation of 169 samples. Phys Med Biol 52:1565–1576.  https://doi.org/10.1088/0031-9155/52/6/002 CrossRefGoogle Scholar
  24. 24.
    Diridollou S, Vabre V, Berson M et al (2001) Skin ageing: changes of physical properties of human skin in vivo. Int J Cosmet Sci 23:353–362CrossRefGoogle Scholar
  25. 25.
    Belkoff SM, Haut RC (1991) A structural model used to evaluate the changing microstructure of maturing rat skin. J Biomech 24:711–720CrossRefGoogle Scholar
  26. 26.
    Brown IA (1973) Scanning electron-microscope study of effects of uniaxial tension on human skin. Br J Dermatol 89:383–393CrossRefGoogle Scholar
  27. 27.
    Hoath SB, Leahy DG (2003) The organization of human epidermis: functional epidermal units and phi proportionality. J Investig Dermatol 121:1440–1446.  https://doi.org/10.1046/j.1523-1747.2003.12606.x CrossRefGoogle Scholar
  28. 28.
    Ní Annaidh A, Bruyère K, Destrade M et al (2012) Characterization of the anisotropic mechanical properties of excised human skin. J Mech Behav Biomed Mater 5:139–148.  https://doi.org/10.1016/j.jmbbm.2011.08.016 CrossRefGoogle Scholar
  29. 29.
    Shergold OA, Fleck NA, Radford D (2006) The uniaxial stress versus strain response of pig skin and silicone rubber at low and high strain rates. Int J Impact Eng 32:1384–1402.  https://doi.org/10.1016/j.ijimpeng.2004.11.010 CrossRefGoogle Scholar
  30. 30.
    Lynch B, Bancelin S, Bonod-Bidaud C et al (2016) A novel microstructural interpretation for the biomechanics of mouse skin derived from multiscale characterization. Acta Biomater 50:302–311.  https://doi.org/10.1016/j.actbio.2016.12.051 CrossRefGoogle Scholar
  31. 31.
    Bismuth C, Gerin C, Viguier E et al (2014) The biomechanical properties of canine skin measured in situ by uniaxial extension. J Biomech 47:1067–1073.  https://doi.org/10.1016/j.jbiomech.2013.12.027 CrossRefGoogle Scholar
  32. 32.
    Fung YC (1993) Biomechanics. Mechanical properties of living tissues, 2nd edn. Springer, New YorkGoogle Scholar
  33. 33.
    Kang G, Wu X (2011) Ratchetting of porcine skin under uniaxial cyclic loading. J Mech Behav Biomed Mater 4:498–506.  https://doi.org/10.1016/j.jmbbm.2010.12.015 CrossRefGoogle Scholar
  34. 34.
    Kiss M-O, Hagemeister N, Levasseur A et al (2009) A low-cost thermoelectrically cooled tissue clamp for in vitro cyclic loading and load-to-failure testing of muscles and tendons. Med Eng Phys 31:1182–1186.  https://doi.org/10.1016/j.medengphy.2009.06.008 CrossRefGoogle Scholar
  35. 35.
    Diani J, Fayolle B, Gilormini P (2009) A review on the Mullins effect. Eur Polym J 45:601–612.  https://doi.org/10.1016/j.eurpolymj.2008.11.017 CrossRefGoogle Scholar
  36. 36.
    Langer K (1978) On the anatomy and physiology of the skin – I. The cleavability of cutis. Br J Plast Surg 31:3–8CrossRefGoogle Scholar
  37. 37.
    Leyva-Mendivil MF, Lengiewicz J, Limbert G (2018) Skin friction under pressure. The role of micromechanics. Surf Topogr Metrol Prop 6:014001.  https://doi.org/10.1088/2051-672X/aaa2d4 CrossRefGoogle Scholar
  38. 38.
    Leyva-Mendivil MF, Lengiewicz J, Page A et al (2017) Skin microstructure is a key contributor to its friction behaviour. Tribol Lett 65.  https://doi.org/10.1007/s11249-016-0794-4
  39. 39.
    Leyva-Mendivil MF, Lengiewicz J, Page A et al (2017) Implications of multi-asperity contact for shear stress distribution in the viable epidermis – an image-based finite element study. Biotribology 11:110–123.  https://doi.org/10.1016/j.biotri.2017.04.001 CrossRefGoogle Scholar
  40. 40.
    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.  https://doi.org/10.1016/j.jmbbm.2015.05.010 CrossRefGoogle Scholar
  41. 41.
    Park AC, Baddiel CB (1972) Rheology of stratum corneum. A molecular interpretation of the stress-strain curve. J Soc Cosmet Chem 23:3–12Google Scholar
  42. 42.
    Bancelin S, Lynch B, Bonod-Bidaud C et al (2015) Ex vivo multiscale quantitation of skin biomechanics in wild-type and genetically-modified mice using multiphoton microscopy. Sci Rep 5:17635.  https://doi.org/10.1038/srep17635 CrossRefGoogle Scholar
  43. 43.
    Ventre M, Mollica F, Netti PA (2009) The effect of composition and microstructure on the viscoelastic properties of dermis. J Biomech 42:430–435.  https://doi.org/10.1016/j.jbiomech.2008.12.004 CrossRefGoogle Scholar
  44. 44.
    Geerligs M, van Breemen L, Peters G et al (2011) In vitro indentation to determine the mechanical properties of epidermis. J Biomech 44:1176–1181.  https://doi.org/10.1016/j.jbiomech.2011.01.015 CrossRefGoogle Scholar
  45. 45.
    Geerligs M, Peters GWM, Ackermans PAJ et al (2010) Does subcutaneous adipose tissue behave as an (anti-)thixotropic material? J Biomech 43:1153–1159.  https://doi.org/10.1016/j.jbiomech.2009.11.037 CrossRefGoogle Scholar
  46. 46.
    Gerhardt L-C, Schmidt J, Sanz-Herrera JA et al (2012) A novel method for visualising and quantifying through-plane skin layer deformations. J Mech Behav Biomed Mater 14:199–207.  https://doi.org/10.1016/j.jmbbm.2012.05.014 CrossRefGoogle Scholar
  47. 47.
    Lamers E, van Kempen THS, Baaijens FPT et al (2013) Large amplitude oscillatory shear properties of human skin. J Mech Behav Biomed Mater 28:462–470.  https://doi.org/10.1016/j.jmbbm.2013.01.024 CrossRefGoogle Scholar
  48. 48.
    Pensalfini M, Weickenmeier J, Rominger M et al (2018) Location-specific mechanical response and morphology of facial soft tissues. J Mech Behav Biomed Mater 78:108–115.  https://doi.org/10.1016/j.jmbbm.2017.10.021 CrossRefGoogle Scholar
  49. 49.
    Vogt M (2005) Development and evaluation of a high-frequency ultrasound-based system for in vivo strain imaging of the skin. IEEE Trans Ultrason Ferroelect Freq Contr 52:11CrossRefGoogle Scholar
  50. 50.
    Montagna W, Parakkal PF (1974) The structure and function of skin, 3rd edn. Academic Press, New York.  https://doi.org/10.1016/C2012-0-01604-3
  51. 51.
    Naylor EC, Watson REB, Sherratt MJ (2011) Molecular aspects of skin ageing. Maturitas 69:249–256.  https://doi.org/10.1016/j.maturitas.2011.04.011
  52. 52.
    Carrino DA, Önnerfjord P, Sandy JD et al (2003) Age-related changes in the proteoglycans of human skin: specific cleavage of decorin to yield a major catabolic fragment in adult skin. J Biol Chem 278:17566–17572.  https://doi.org/10.1074/jbc.M300124200 CrossRefGoogle Scholar
  53. 53.
    Li Y, Liu Y, Xia W et al (2013) Age-dependent alterations of decorin glycosaminoglycans in human skin. Sci Rep 3:2422.  https://doi.org/10.1038/srep02422 CrossRefGoogle Scholar
  54. 54.
    Langton AK, Graham HK, McConnell JC et al (2017) Organization of the dermal matrix impacts the biomechanical properties of skin. Br J Dermatol 177:818–827.  https://doi.org/10.1111/bjd.15353 CrossRefGoogle Scholar
  55. 55.
    Puxkandl R, Zizak I, Paris O et al (2002) Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc B Biol Sci 357:191–197.  https://doi.org/10.1098/rstb.2001.1033 CrossRefGoogle Scholar
  56. 56.
    Reconditi M, Brunello E, Linari M et al (2011) Motion of myosin head domains during activation and force development in skeletal muscle. Proc Natl Acad Sci 108:7236–7240.  https://doi.org/10.1073/pnas.1018330108 CrossRefGoogle Scholar
  57. 57.
    Lynch B (2016) Multiscale biomechanics of skin: experimental investigation of the role of the collagen microstructure. Ecole polytechniqueGoogle Scholar
  58. 58.
    Zipfel WR, Williams RM, Webb WW (2003) Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 21:1369–1377.  https://doi.org/10.1038/nbt899 CrossRefGoogle Scholar
  59. 59.
    Decencière E, Tancrède-Bohin E, Dokládal P et al (2013) Automatic 3D segmentation of multiphoton images: a key step for the quantification of human skin. Skin Res Technol 19:115–124.  https://doi.org/10.1111/srt.12019 CrossRefGoogle Scholar
  60. 60.
    Lynch B, Bancelin S, Bonod-Bidaud C et al (2017) A novel microstructural interpretation for the biomechanics of mouse skin derived from multiscale characterization. Acta Biomater 50:302–311.  https://doi.org/10.1016/j.actbio.2016.12.051 CrossRefGoogle Scholar
  61. 60.
    Gusachenko I, Tran V, Goulam Houssen Y et al (2012) Polarization-resolved second-harmonic generation in tendon upon mechanical stretching. Biophys J 102:2220–2229.  https://doi.org/10.1016/j.bpj.2012.03.068 CrossRefGoogle Scholar
  62. 61.
    Goulam Houssen Y, Gusachenko I, Schanne-Klein M-C, Allain J-M (2011) Monitoring micrometer-scale collagen organization in rat-tail tendon upon mechanical strain using second harmonic microscopy. J Biomech 44:2047–2052.  https://doi.org/10.1016/j.jbiomech.2011.05.009 CrossRefGoogle Scholar
  63. 62.
    Keyes JT, Haskett DG, Utzinger U et al (2011) Adaptation of a planar microbiaxial optomechanical device for the tubular biaxial microstructural and macroscopic characterization of small vascular tissues. J Biomech Eng 133:075001CrossRefGoogle Scholar
  64. 63.
    Krasny W, Magoariec H, Morin C, Avril S (2017) Kinematics of collagen fibers in carotid arteries under tension-inflation loading. J Mech Behav Biomed Mater 77:718–726.  https://doi.org/10.1016/j.jmbbm.2017.08.014 CrossRefGoogle Scholar
  65. 64.
    Benoit A, Latour G, Schanne-Klein M-C, Allain J-M (2015) Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure. J Mech Behav Biomed Mater 60:93–105.  https://doi.org/10.1016/j.jmbbm.2015.12.031 CrossRefGoogle Scholar
  66. 65.
    Mauri A, Ehret AE, Perrini M et al (2015) Deformation mechanisms of human amnion: quantitative studies based on second harmonic generation microscopy. J Biomech 48:1606–1613.  https://doi.org/10.1016/j.jbiomech.2015.01.045 CrossRefGoogle Scholar
  67. 66.
    Mauri A, Perrini M, Mateos JM et al (2013) Second harmonic generation microscopy of fetal membranes under deformation: normal and altered morphology. Placenta 34:1020–1026.  https://doi.org/10.1016/j.placenta.2013.09.002 CrossRefGoogle Scholar
  68. 67.
    Jayyosi C, Affagard J-S, Ducourthial G et al (2017) Affine kinematics in planar fibrous connective tissues: an experimental investigation. Biomech Model Mechanobiol 16(4):1459–1473.  https://doi.org/10.1007/s10237-017-0899-1 CrossRefGoogle Scholar
  69. 68.
    Jayyosi C, Coret M, Bruyère-Garnier K (2016) Characterizing liver capsule microstructure via in situ bulge test coupled with multiphoton imaging. J Mech Behav Biomed Mater 54:229–243.  https://doi.org/10.1016/j.jmbbm.2015.09.031 CrossRefGoogle Scholar
  70. 69.
    Alavi SH, Ruiz V, Krasieva T et al (2013) Characterizing the collagen fiber orientation in pericardial leaflets under mechanical loading conditions. Ann Biomed Eng 41:547–561.  https://doi.org/10.1007/s10439-012-0696-z CrossRefGoogle Scholar
  71. 70.
    Ban E, Franklin JM, Nam S et al (2018) Mechanisms of plastic deformation in collagen networks induced by cellular forces. Biophys J 114:450–461.  https://doi.org/10.1016/j.bpj.2017.11.3739 CrossRefGoogle Scholar
  72. 71.
    Vader D, Kabla A, Weitz D, Mahadevan L (2009) Strain-induced alignment in collagen gels. PLoS One 4:e5902.  https://doi.org/10.1371/journal.pone.0005902 CrossRefGoogle Scholar
  73. 72.
    Cheng VWT, Screen HRC (2007) The micro-structural strain response of tendon. J Mater Sci 42:8957–8965.  https://doi.org/10.1007/s10853-007-1653-3 CrossRefGoogle Scholar
  74. 73.
    Jayyosi C, Fargier G, Coret M, Bruyère-Garnier K (2014) Photobleaching as a tool to measure the local strain field in fibrous membranes of connective tissues. Acta Biomater 10:2591–2601.  https://doi.org/10.1016/j.actbio.2014.02.031 CrossRefGoogle Scholar
  75. 74.
    Nesbitt S, Scott W, Macione J, Kotha S (2015) Collagen fibrils in skin orient in the direction of applied uniaxial load in proportion to stress while exhibiting differential strains around hair follicles. Materials 8:1841–1857.  https://doi.org/10.3390/ma8041841 CrossRefGoogle Scholar
  76. 75.
    Bischoff JE (2006) Reduced parameter formulation for incorporating fiber level viscoelasticity into tissue level biomechanical models. Ann Biomed Eng 34:1164–1172.  https://doi.org/10.1007/s10439-006-9124-6 CrossRefGoogle Scholar
  77. 76.
    Manschot JFM, Brakkee AJM (1986) The measurement and modelling of the mechanical properties of human skin in vivo—II. The model. J Biomech 19:517–521CrossRefGoogle Scholar
  78. 77.
    Lynch B, Bonod-Bidaud C, Ducourthial G et al (2017) How aging impacts skin biomechanics: a multiscale study in mice. Sci Rep 7:13750.  https://doi.org/10.1038/s41598-017-13150-4 CrossRefGoogle Scholar
  79. 78.
    Krasny W, Morin C, Magoariec H, Avril S (2017) A comprehensive study of layer-specific morphological changes in the microstructure of carotid arteries under uniaxial load. Acta Biomater 57:342–351.  https://doi.org/10.1016/j.actbio.2017.04.033 CrossRefGoogle Scholar
  80. 79.
    Screen HR, Bader DL, Lee DA, Shelton JC (2004) Local strain measurement within tendon. Strain 40:157–163CrossRefGoogle Scholar
  81. 80.
    Hendriks FM, Brokken D, Oomens CWJ et al (2006) The relative contributions of different skin layers to the mechanical behavior of human skin in vivo using suction experiments. Med Eng Phys 28:259–266.  https://doi.org/10.1016/j.medengphy.2005.07.001 CrossRefGoogle Scholar
  82. 81.
    Qi J, Elson DS (2017) Mueller polarimetric imaging for surgical and diagnostic applications: a review. J Biophotonics 10:950–982.  https://doi.org/10.1002/jbio.201600152 CrossRefGoogle Scholar
  83. 82.
    Bancelin S, Nazac A, Ibrahim BH et al (2014) Determination of collagen fiber orientation in histological slides using Mueller microscopy and validation by second harmonic generation imaging. Opt Express 22:22561.  https://doi.org/10.1364/OE.22.022561 CrossRefGoogle Scholar
  84. 83.
    Jacques SL, Ramella-Roman JC, Lee K (2002) Imaging skin pathology with polarized light. J Biomed Opt 7:329.  https://doi.org/10.1117/1.1484498 CrossRefGoogle Scholar
  85. 84.
    German GK, Engl WC, Pashkovski E et al (2012) Heterogeneous drying stresses in stratum corneum. Biophys J 102:2424–2432.  https://doi.org/10.1016/j.bpj.2012.04.045 CrossRefGoogle Scholar
  86. 85.
    Liang X, Graf BW, Boppart SA (2011) In vivo multiphoton microscopy for investigating biomechanical properties of human skin. Cell Mol Bioeng 4:231–238.  https://doi.org/10.1007/s12195-010-0147-6 CrossRefGoogle Scholar
  87. 86.
    Wu KS, van Osdol WW, Dauskardt RH (2006) Mechanical properties of human stratum corneum: effects of temperature, hydration, and chemical treatment. Biomaterials 27:785–795.  https://doi.org/10.1016/j.biomaterials.2005.06.019 CrossRefGoogle Scholar
  88. 87.
    Vyumvuhore R, Tfayli A, Biniek K et al (2015) The relationship between water loss, mechanical stress, and molecular structure of human stratum corneum ex vivo: Relationship between SC water loss, mechanical stress, and molecular structure. J Biophotonics 8:217–225.  https://doi.org/10.1002/jbio.201300169 CrossRefGoogle Scholar
  89. 88.
    Geerligs M (2010) Skin layer mechanics. Technische Universiteit Eindhoven, EindhovenGoogle Scholar
  90. 89.
    Geerligs M, Peters GW, Ackermans PA et al (2008) Linear viscoelastic behavior of subcutaneous adipose tissue. Biorheology 45:677–688.  https://doi.org/10.3233/BIR-2008-0517 CrossRefGoogle Scholar
  91. 90.
    Gefen A (2007) Viscoelastic properties of ovine adipose tissue covering the gluteus muscles. J Biomech Eng 129:924.  https://doi.org/10.1115/1.2800830 CrossRefGoogle Scholar
  92. 91.
    Patel PN, Smith CK, Patrick CW (2005) Rheological and recovery properties of poly(ethylene glycol) diacrylate hydrogels and human adipose tissue. J Biomed Mater Res A 73A:313–319.  https://doi.org/10.1002/jbm.a.30291 CrossRefGoogle Scholar
  93. 92.
    Shoham N, Girshovitz P, Katzengold R et al (2014) Adipocyte stiffness increases with accumulation of lipid droplets. Biophys J 106:1421–1431.  https://doi.org/10.1016/j.bpj.2014.01.045 CrossRefGoogle Scholar
  94. 93.
    Shoham N, Levy A, Shabshin N et al (2017) A multiscale modeling framework for studying the mechanobiology of sarcopenic obesity. Biomech Model Mechanobiol 16:275–295.  https://doi.org/10.1007/s10237-016-0816-z CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Jean-Marc Allain
    • 1
    • 2
    Email author
  • Barbara Lynch
    • 1
  • Marie-Claire Schanne-Klein
    • 3
  1. 1.LMS, Ecole Polytechnique, CNRSPalaiseauFrance
  2. 2.Inria, Université Paris-SaclayPalaiseauFrance
  3. 3.LOB, Ecole Polytechnique, CNRS, INSERMPalaiseauFrance

Personalised recommendations