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Mechanics Reveals the Biological Trigger in Wrinkly Fingers

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Abstract

Fingertips wrinkle due to long exposure to water. The biological reason for this morphological change is unclear and still not fully understood. There are two main hypotheses for the underlying mechanism of fingertip wrinkling: the ‘shrink’ model (in which the wrinkling is driven by the contraction of the lower layers of skin, associated with the shrinking of the underlying vasculature), and the ‘swell’ model (in which the wrinkling is driven by the swelling of the upper layers of the skin, associated with osmosis). In reality, contraction of the lower layers of the skin and swelling of the upper layers will happen simultaneously. However, the relative importance of these two mechanisms to drive fingertip wrinkling also remains unclear. Simulating the swelling in the upper layers of skin alone, which is associated with neurological disorders, we found that wrinkles appeared above an increase of volume of \({\approx } 10\%.\) Therefore, the upper layers can not exceed this swelling level in order to not contradict in vivo observations in patients with such neurological disorders. Simulating the contraction of the lower layers of the skin alone, we found that the volume have to decrease a \({\approx } 20\%\) to observe wrinkles. Furthermore, we found that the combined effect of both mechanisms leads to pronounced wrinkles even at low levels of swelling and contraction when individually they do not. This latter results indicates that the collaborative effect of both hypothesis are needed to induce wrinkles in the fingertips. Our results demonstrate how models from continuum mechanics can be successfully applied to testing hypotheses for the mechanisms that underly fingertip wrinkling, and how these effects can be quantified.

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References

  1. Ambrosi, D., G. A. Ateshian, E. M. Arruda, S. C. Cowin, J. Dumais, A. Goriely, G. A. Holzapfel, J. D. Humphrey, R. Kemkemer, E. Kuhl, J. E. Olberding, L. A. Taber, and K. Garikipati. Perspectives on biological growth and remodeling. J. Mech. Phys. Solids 59:863–883, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Balbi, V., E. Kuhl, and P. Ciarletta. Morphoelastic control of gastro-intestinal organogenesis: theoretical predictions and numerical insights. J. Mech. Phys. Solids 78:493–510, 2014.

    Article  Google Scholar 

  3. Ben Amar, M., and P. Ciarletta. Swelling instability of surface-attached gels as a model of soft tissue growth under geometric constraints. J. Mech. Phys. Solids 58(7):935–954, 2010.

    Article  CAS  Google Scholar 

  4. Ben Amar, M., and A. Goriely. Growth and instability in elastic tissues. J. Mech. Phys. Solids 53(10):2284–2319, 2005.

    Article  CAS  Google Scholar 

  5. Ben Amar, M., and F. Jia. Anisotropic growth shapes intestinal tissues during embryogenesis. Proc. Natl Acad. Sci. USA 110(26):10525–10530, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Blugerman, G., M. D. Paul, D. Schavelzon, R. S. Mulholland, M. Sandhoffer, P. Lisborg, A. Rusciani, M. Divaris, and M. Kreindel. In: Radio-frequency Assisted Liposuction (RFAL), Advanced Techniques in Liposuction and Fat Transfer, edited by N. Serdev. InTech. doi:10.5772/20831.

  7. Braham, J., M. Sadeh, and I. Sarovapinhas. Skin wrinkling on immersion of hands: a test of sympathetic function. Arch. Neurol. 36(2):113–114, 1979.

    Article  CAS  PubMed  Google Scholar 

  8. Bryan, F. Dynamic mechanical testing of human skin ‘in vivo’. J. Biomech. 6(3):559–558, 1970.

    Google Scholar 

  9. Budday, S., C. Raybaud, and E. Kuhl. A mechanical model predicts morphological abnormalities in the developing human brain. Sci. Rep. 4:5644, 2014a.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Budday, S., P. Steinmann, and E. Kuhl. The role of mechanics during brain development. J. Mech. Phys. Solids 72:75–92, 2014b.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Cao, Y., and J. W. Hutchinson. From wrinkles to creases in elastomers: the instability and imperfection-sensitivity of wrinkling. Proc. R. Soc. A 468(2137):94–115, 2012.

    Article  Google Scholar 

  12. Changizi, M., R. Weber, R. Kotecha, and J. Palazzo. Are wet-induced wrinkled fingers primate rain treads? Brain Behav. Evol. 77:286–290, 2011.

    Article  PubMed  Google Scholar 

  13. Chaudhry, H. R., B. Bukiet, T. Findley, and A. B. Ritter. Evaluation of residual stress in rabbit skin and the relevant material constants. J. Theor. Biol. 2:191–195, 1998.

    Article  Google Scholar 

  14. Ciarletta, P., and M. Ben Amar. Pattern formation in fiber-reinforced tubular tissues: folding and segmentation during epithelial growth. J. Mech. Phys. Solids 60(3):525–537, 2012a.

    Article  Google Scholar 

  15. Ciarletta, P., and M. Ben Amar. Peristaltic patterns for swelling and shrinking of soft cylindrical gels. Soft Matter 8(6):1760, 2012b.

    Article  CAS  Google Scholar 

  16. Ciarletta, P., M. Ben Amar, and M. Labouesse. Continuum model of epithelial morphogenesis during Caenorhabditis elegans embryonic elongation. Philos. Trans. A 367(1902):3379–3400, 2009.

    Article  CAS  Google Scholar 

  17. Ciarletta, P., V. Balbi, and E. Kuhl. Pattern selection in growing tubular tissues. Phys. Rev. Lett. 113:248101, 2014.

    Article  CAS  PubMed  Google Scholar 

  18. Efimenko, K., M. Rackaitis, E. Manias, A. Vaziri, L. Mahadevan, and J. Genzer. Nested self-similar wrinkling patterns in skins. Nat. Mater. 4(4):293–297, 2005.

    Article  CAS  PubMed  Google Scholar 

  19. Eskandari, M., W. G. Kuschner, and E. Kuhl. Patient-specific airway wall remodeling in chronic lung disease. Ann. Biomed. Eng. 43(10):2538–2551, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Flory, P. J. Thermodynamic relations for high elastic materials. Trans. Faraday Soc. 57:829–838, 1961.

    Article  CAS  Google Scholar 

  21. Flynn, C. O., and B. A. O. McCormack. A three-layer model of skin and its application in simulating wrinkling. Comput. Methods Biomech. Biomed. Eng. 12(2):125–134, 2009.

    Article  Google Scholar 

  22. Flynn, C., and B. A. O. McCormack. Simulating the wrinkling and aging of skin with a multi-layer finite element model. J. Biomech. 43(3):442–448, 2010.

    Article  PubMed  Google Scholar 

  23. Frenzel, H., J. Bohlender, K. Pinsker, B. Wohlleben, J. Tank, S. G. Lechner, D. Schiska, T. Jaijo, F. Rueschendorf, K. Saar, J. Jordan, J. M. Millan, M. Gross, and G. R. Lewin. A genetic basis for mechanosensory traits in humans. PLoS Biol. 10(5):e1001318, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Goektepe, S., O. J. Abilez, and E. Kuhl. A generic approach towards finite growth with examples of athlete’s heart, cardiac dilation, and cardiac wall thickening. J. Mech. Phys. Solids 58(10):1661–1680, 2010.

    Article  Google Scholar 

  25. Goriely, A., and M. Ben Amar. Differential growth and instability in elastic shells. Phys. Rev. Lett. 94(19):198103, 2005.

    Article  PubMed  Google Scholar 

  26. Hendriks, F. M., D. V. Brokken, J. T. W. M. Van Eemeren, C. W. J. Oomens, F. P. T. Baaijens, and J. B. A. M. Horsten. A numerical-experimental method to characterize the non-linear mechanical behaviour of human skin. Skin Res. Technol. 9(3):274–283, 2003.

    Article  CAS  PubMed  Google Scholar 

  27. Hendriks, F. M., D. Brokken, C. W. J. Oomens, D. L. Bader, and F. P. T. Baaijens. 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, 2006.

    Article  CAS  PubMed  Google Scholar 

  28. Himpel, G., E. Kuhl, A. Menzel, and P. Steinmann. Computational modelling of isotropic multiplicative growth. Comput. Model. Eng. Sci. 8(2):119–134, 2005.

    Google Scholar 

  29. Holzapfel, G. Nonlinear Solid Mechanics: A Continuum Approach for Engineering. Chichester: Wiley, 2000.

    Google Scholar 

  30. Huang, Z., W. Hong, and Z. Suo. Evolution of wrinkles in hard films on soft substrates. Phys. Rev. E 70(3):030601, 2004.

    Article  Google Scholar 

  31. Huang, Z. Y., W. Hong, and Z. Suo. Nonlinear analyzes of wrinkles in a film bonded to a compliant substrate. J. Mech. Phys. Solids 53(9):2101–2118, 2005.

    Article  CAS  Google Scholar 

  32. Jones, G. W., and S. J. Chapman. Modeling growth in biological materials. SIAM Rev. 54(1):52–118, 2012.

    Article  Google Scholar 

  33. Kareklas, K., D. Nettle, and T. V. Smulders. Water-induced finger wrinkles improve handling of wet objects. Biol. Lett. 9(2):20120999, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kuhl, E. Growing matter: a review of growth in living systems. J. Mech. Behav. Biomed. Mater. 29:529–543, 2014.

    Article  PubMed  Google Scholar 

  35. Kuhl, E., and P. Steinmann. Theory and numerics of geometrically non-linear open system mechanics. Int. J. Numer. Methods Eng. 58(11):1593–1615, 2003.

    Article  Google Scholar 

  36. Lambert, W. C. Physiology, biochemistry, and molecular biology of the skin. N. Engl. J. Med. 328:1048, 1993.

    Article  Google Scholar 

  37. Lanir, Y., and Y. C. Fung. Two-dimensional mechanical properties of rabbit skin—II. Experimental results. J. Biomech. 2(7):171–174, 1974.

    Article  Google Scholar 

  38. Lee, E. H. Elastic-plastic deformation at finite strains. J. Appl. Mech. 36(1):1–6, 1969.

    Article  Google Scholar 

  39. Li, B., Y. P. Cao, X. Q. Feng, and H. Gao. Surface wrinkling of mucosa induced by volumetric growth: theory, simulation and experiment. J. Mech. Phys. Solids 59(4):758–774, 2011.

    Article  Google Scholar 

  40. Lin, H. T., T. F. Hong, and W. L. Li. Grip performance affected by water-induced wrinkling of fingers. Tribol. Lett. 58(3):1–9, 2015a.

    Article  CAS  Google Scholar 

  41. Liu, Y., X. Yang, Y. Cao, Z. Wang, B. Chen, J. Zhang, and H. Zhang. Dehydration of core/shell fruits. Comput. Graph. 47:68–77, 2015b.

    Article  Google Scholar 

  42. Marsden, J. E., and T. J. R. Hughes. Mathematical Foundations of Elasticity. Mineola: Dover Publications, 1983.

    Google Scholar 

  43. Menzel, A., and E. Kuhl. Frontiers in growth and remodeling. Mech. Res. Commun. 42:1–14, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mora, T., and A. Boudaoud. Buckling of swelling gels. Eur. Phys. J. E 20(2):119–124, 2006.

    Article  CAS  PubMed  Google Scholar 

  45. Motala, M. J., D. Perlitz, C. M. Daly, P. Yuan, R. G. Nuzzo, G. Ralph, and J. K. Hsia. Programming matter through strain. Extrem. Mech. Lett. 3:8–16, 2015.

    Article  Google Scholar 

  46. Moulton, D. E., and A. Goriely. Circumferential buckling instability of a growing cylindrical tube. J. Mech. Phys. Solids 59(3):525–537, 2011.

    Article  Google Scholar 

  47. O’Riain, S. New and simple test of nerve function in hand. Br. Med. J. 3(5881):615–616, 1973.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Riks, E. An incremental approach to the solution of snapping and buckling problems. Int. J. Solids Struct. 15(7):529–551, 1979.

    Article  Google Scholar 

  49. Rodriguez, E. K., A. Hoger, and A. D. McCulloch. Stress-dependent finite growth in soft elastic tissues. J. Biomech. 27(4):455–467, 1994.

    Article  CAS  PubMed  Google Scholar 

  50. Saez, P. On the theories and numerics of continuum models for adaptation processes in biological tissues. Arch. Comput. Methods Eng. doi:10.1007/s11831-014-9142-8.

  51. Stoop, N., R. Lagrange, D. Terwagne, P. M. Reis, and J. Dunkel. Curvature-induced symmetry breaking determines elastic surface patterns. Nat. Mater. 14(3):337–342, 2015.

    Article  CAS  PubMed  Google Scholar 

  52. Tong, P., and Y. C. Fung. The stress-strain relationship for the skin. J. Biomech. 9(10):649–657, 1976.

    Article  CAS  PubMed  Google Scholar 

  53. Wempner, G. A. Discrete approximations related to nonlinear theories of solids. Int. J. Solids Struct. 11:1581–1599, 1971.

    Article  Google Scholar 

  54. Wilder-Smith, E. P. V. Water immersion wrinkling-physiology and use as an indicator of sympathetic function. Clin. Auton. Res., 14(2):125–131, 2004.

    Article  PubMed  Google Scholar 

  55. Wilder-Smith, E. P. V., and A. Chow. Water-immersion wrinkling is due to vasoconstriction. Muscle Nerve 27(3):307–311, 2003.

    Article  PubMed  Google Scholar 

  56. http://www.muffler.123dapp.com/123C-3D-Model/Finger-Index/866442. Accessed 01 September 2016.

  57. Yin, J., G. J. Gerling, and X. Chen. Mechanical modeling of a wrinkled fingertip immersed in water. Acta Biomater. 6(4):1487–1496, 2010.

    Article  PubMed  Google Scholar 

  58. Zang, J., X. Zhao, Y. Cao, and J. W. Hutchinson. Localized ridge wrinkling of stiff films on compliant substrates. J. Mech. Phys. Solids 60(7):1265–1279, 2012.

    Article  CAS  Google Scholar 

  59. Zhao, Y., X. Han, G. Li, C. Lu, Y. Cao, X. Q. Feng, et al. Effect of lateral dimension on the surface wrinkling of a thin film on compliant substrate induced by differential growth/swelling. J. Mech. Phys. Solids 83:129–145, 2015.

    Article  CAS  Google Scholar 

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Correspondence to P. Sáez.

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Associate Editor Sean S. Kohles oversaw the review of this article.

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Sáez, P., Zöllner, A.M. Mechanics Reveals the Biological Trigger in Wrinkly Fingers. Ann Biomed Eng 45, 1039–1047 (2017). https://doi.org/10.1007/s10439-016-1764-6

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