On the tear resistance of skin

Abstract

Tear resistance is of vital importance in the various functions of skin, especially protection from predatorial attack. Here, we mechanistically quantify the extreme tear resistance of skin and identify the underlying structural features, which lead to its sophisticated failure mechanisms. We explain why it is virtually impossible to propagate a tear in rabbit skin, chosen as a model material for the dermis of vertebrates. We express the deformation in terms of four mechanisms of collagen fibril activity in skin under tensile loading that virtually eliminate the possibility of tearing in pre-notched samples: fibril straightening, fibril reorientation towards the tensile direction, elastic stretching and interfibrillar sliding, all of which contribute to the redistribution of the stresses at the notch tip.

Figure 1. Tear resistance of skin in comparison to bone materials.

(a–d) The sequence of events where rabbit skin, containing an edge notch or tear (of a length half the lateral specimen dimension), is strained under uniaxial tensile loading; the notch does not propagate but progressively yawns open under tensile loading. (e) Schematic illustration of skin with a pre-crack under loading; the crack does not propagate but instead blunts. (f) Corresponding schematic of bone (transverse orientation) with a notch under loading; the crack (white line) often propagates in a zig-zag pattern with multiple crack deflections. (g–j) The deformation of a central notch in skin loaded in tension. Distortion of a central notch as specimen of rabbit skin is extended uniaxially. There is no increase in the initial length of the cut. (k,l) The notch root radius increases with axial extension of the specimen, with a consequent decrease in stress concentration. This is enabled by local straightening and stretching of fibres and by interfibrillar sliding. Scale bar in (a–d), (g–j) is 10 mm.

Figure 2. Evolution of fibril and fibre configuration during tensile extension.

(a) Disordered arrangement of curved collagen fibres (SEM). (b) High magnification of a, collagen fibrils (~50 nm diameter) comprising each fibre (~1–10 μm diameter; SEM). (c,d) Collagen fibrils in section plane parallel to skin surface including detail of sectioned fibrils (inset in c) and wavy structure (TEM). (e) Collagen fibrils at notched side are delaminated, aligning close to the tension direction after loading. The loading direction is shown by the arrow, (f) collagen fibrils at unnotched side are delaminated/relaxed after loading/unloading. (g–j) Schematic of mechanisms of fibril deformation and failure under tension: (g) original configuration; (h,i) straightening and reorientation of fibres with projected length in tensile direction increasing from L₀ to L₁, and L₂ (j) separation into fibrils; elastic stretching through the increase in collagen d spacing from d₀ to d₃, and sliding (schematically shown by S), increasing length in tensile direction to L₃. R₀−R₂ are the radii of curvature of collagen during stretching. Scale bars in a–f and the picture inset in c are 50 μm, 500 nm, 500 nm, 500 nm, 1 μm, 2 μm and 200 nm, respectively.

Figure 3. Experimental and predicted tensile response of a wavy structure simulating collagen in skin.

(a) Stress-strain curves of rabbit skin in longitudinal (parallel to backbone, perpendicular to Langer’s lines) and transverse (perpendicular to backbone) orientations, at strain rates of 10⁻¹ (red band) and 10⁻³ s⁻¹ (blue band). Skin displays higher strength at higher strain rates. Inset shows tensile response of latex, with much higher tensile strains determined by the degree of vulcanization. (b) Modelling of stress-strain curves of skin with Castigliano's therom (dashed lines) and by experiments using steel wire, composed of segments of circles (full lines). (c) Steel wire before and after stretching. The wire curvature (shown in schematic drawing) is defined by the central angle θ₀ (~30° to 130°), which determines the maximum strain. Experimental and mathematical predictions indicate good agreement reflecting the characteristic response of skin.

Figure 4. Viscosity and hierarchical structure.

(a) Effect of viscosity on the stress-strain response of a non-linear elastic material. (b) Effect of strain rate, at a constant viscosity, purely elastic response at 10⁻³ s⁻¹. (c) Actual skin has a hierarchical structure spanning the nanoscale of twisted peptide chains to the microscale of wavy collagen and elastin fibres. The proposed wire model only addresses structure at the ~50 nm to 10 μm dimensions, as depicted by levels II and III in the schematic. Blue dots in II represent hydrogen bonds and water molecules.

Figure 5. SAXS analysis of skin in tension.

Variation in SAXS peak-intensity, orientation angle, collagen fibril d-spacing and full-width-at-half-maximum (FWHM), from tensile tests on rabbit skin. (a–d) Diffraction patterns: arcs show orientations of fibrils, images of the sample shown at top-right corners, (a) collagen fibrils randomly oriented to tensile axis, shown by constant intensity of diffraction pattern circles, (b) fibrils become gradually aligned in tension direction, (c) fibrils aligned along tensile axis, (d) fibrils fractured and relaxed. (e) During tensile test, 13 stress-strain data points (black dots) were recorded at 5 s intervals; four stages were identified. (f) Angle of normal to the tensile axis (black dots) versus intensity of fibrils (blue dots) as a function of strain, and (g) d-spacing (black dots) and FWHM (blue dots) of fibrils as a function of strain. Four stages: I-toe and II-heel, curved collagen fibrils straighten, rotate, stretch (d-spacing increases), III-linear, fibrils continue to rotate and stretch, orienting completely along tensile axis (angle=0°), but also slide and delaminate; IV-fracture, fibrils fracture and curl back (angle deviates from 0°, d-spacing, FWHM and intensity decrease).

Figure 6. Mechanistic stages of the tensile loading of skin.

SEM images (a–d) and schematic drawings (e–h) of the mechanisms during the four stages of tensile loading of rabbit skin, black arrows in a and e represent the direction of tension testing. (a,e) Curved collagen fibrils are oriented along the tensile axis; (b,f) collagen fibrils are straightening, larger and larger amount of the fibrils re-orient close to the tensile axis; (c,g) collagen fibrils are stretching, sliding, delaminating and orientated completely along the tensile axis; (d,h) collagen fibrils are fractured and curled back. Scale bars in a–d are 20, 20, 20, 50 μm, respectively.