Effect of collagen fibre orientation on the Poisson's ratio and stress relaxation of skin: an ex vivo and in vivo study

Abstract

During surgical treatment skin undergoes extensive deformation, hence it must be able to withstand large mechanical stresses without damage. Therefore, understanding the mechanical properties of skin becomes important. A detailed investigation on the relationship between the three-dimensional deformation response of skin and its microstructure is conducted in the current study. This study also discloses the underlying science of skin viscoelasticity. Deformation response of skin is captured using digital image correlation, whereas micro-CT, scanning electron microscopy and atomic force microscopy are used for microstructure analysis. Skin shows a large lateral contraction and expansion (auxeticity) when stretched parallel and perpendicular to the skin tension lines, respectively. Large lateral contraction is a result of fluid exudation from the tissue, while large rotation of the stiff collagen fibres in the loading direction explains the skin auxeticity. During stress relaxation, lateral contraction and fluid effluxion from skin reveal that tissue volume loss is the intrinsic science of skin viscoelasticity. Furthermore, the results obtained from in vivo study on human skin show the relevance of the ex vivo study to physiological conditions and stretching of the skin during its treatments.

Keywords: Poisson's ratio; auxeticity; digital image correlation; micro-CT; skin collagen fibre; stress relaxation.

Figure 1.

(a) Schematic shows the rectangle specimens extracted from the dorsal portion of the pig skin with marked orientations to skin tension line (STL). Circle numbers 1–5 in blue circles represent the random locations of five specimens that were excised parallel to STLs, whereas circle numbers 1–4 in green circles represent the random locations of four specimens that were excised perpendicular to STLs. These specimens were used for microstructural assessment. (b) A typical specimen with dimensions (gauge length and width) and random-sized black dots. (c) A schematic of an experimental set-up coupled with the DIC system, where two identical cameras were mounted perpendicular to each other. Camera 1 captures the deformation of the skin in X–Y plane, and camera 2 captures deformation in the Y–Z plane. (d) In vivo stretching experiment on human back skin. Note: here, the direction of stretching and direction perpendicular to stretching were nomenclatures as yy and xx, respectively.

Figure 2.

The schematic description of experimental pipeline which was used in this study.

Figure 3.

(a) Ramp and hold portions of experiment at different strain levels. (b) Stress–strain curve (average value) of parallel and perpendicular specimens. Map of the engineering strain in X–Y (left column) and Y–Z (right column) planes at the end of ramp (20% strain level) for (c) parallel and (d) perpendicular specimens. The black rectangular boxes represent the area of interest over which the average value of strain was measured.

Figure 4.

(a) Micro-CT slices of the skin in X–Y (left) and Y–Z (right) planes. The white rectangle represents an area of interest. (b) The upper figure represents the schematic of sections obtained from the dermis in X–Y and Y–Z planes, and the bottom figures present the post-processed images of skin slices.

Figure 5.

(a) The trend of Poisson's ratio (average value) for parallel and perpendicular specimens when plotted against applied strain. The linear correlation between Poisson's ratio (b) ${\nu }_{xy}$ and (c) ${\nu }_{yz}$ and applied strain for parallel specimens. Note: in perpendicular specimens, ${\nu }_{xy}$ and applied strain were not found correlated; however, the trend for ${\nu }_{yz}$ was found similar to parallel specimens (electronic supplementary material, figure 3S(g)). Comparison of Poisson's ratio (${\nu }_{xy}$) (X–Y plane) among the different strain levels in (d) parallel specimens and (e) perpendicular specimens. (f) Comparison of Poisson's ratio (${\nu }_{yz}$) (Y–Z plane) among different strain levels in parallel and perpendicular specimens. Note: *p < 0.05 and **p < 0.01.

Figure 6.

Comparison of relative change in stress (mean ± 1 s.d.) among different hold strains (e.g. 5%, 10%, 15% and 20%) for (a) parallel specimens and (b) perpendicular specimens. Comparison of increase in Poisson's ratio in X–Y plane (${\nu }_{xy}$) during stress relaxation for (c) parallel and (d) perpendicular specimens. (e) Comparison of increase in Poisson's ratio in Y–Z plane (${\nu }_{yz}$) during stress relaxation for parallel and perpendicular specimens. Note: *p < 0.05 and **p < 0.01.

Figure 7.

Map of engineering strain when human skin is stretched (a,b) parallel and (c,d) perpendicular to STL The trend of engineering strains (${\epsilon }_{xx}$ and ${\epsilon }_{yy}$) when stretched (e) parallel and (f) perpendicular to STL.

Figure 8.

Histograms of collagen fibres orientations in X–Y plane (a) parallel specimens and (b) perpendicular specimens, and in Y–Z plane (c) parallel specimens and (d) perpendicular specimens. Note: collagen orientation is presented in half hemisphere of 180°.

Figure 9.

AFM images of collagen fibrils configuration in (a) X–Y and (b) Y–Z planes. High magnification images show the almost parallel arrangement of collagen fibrils within the collagen fibres. This trend was found similar in both the planes.

Figure 10.

(a) SEM micrograph of collagen fibre. High magnified micrograph of collagen fibres in pig dermis, superimposed by the simplified representation of curved collagen fibres. Photograph of white paper (b) without wrinkles, (c) with undeformed wrinkles (d) with deformed wrinkles (movie of white paper deformation is provided in electronic supplementary material, video-2).

Figure 11.

(a) The representative volumetric element (RVE) model of collagen fibril and matrix assembly. The collagen fibrils assembled in parallel and staggered manner inside the soft matrix. The RVE with tetrahedron mesh is presented in electronic supplementary material, figure 7S(a). (b) A cross-sectional view RVE at undeformed state. Cross-sectional view of RVE at deformed states corresponding to applied strain (c) 0.02 (d) 0.04 (e) 0.06. The three-dimensional view of RVE in deformed state is provided in electronic supplementary material, figure 7S(c,d). All neighbouring collagen fibrils except unconnected fibrils (two left side) come close to each other under the stretching of RVE.