Fibrillar structure and elasticity of hydrating collagen: A quantitative multiscale approach

It is well known that hydration of collagenous tissues leads to their swelling, as well as to softening of their elastic behavior. However, it is much less clear which microstructural and micromechanical “rules” are involved in this process. Here, we develop a theoretical approach cast in analytical mathematical formulations, which is experimentally validated by a wealth of independent tests on collagenous tissues, such as X-ray diffraction, vacuum drying, mass measurements, and Brillouin light scattering. The overall emerging picture is the following: air-drying leaves water only in the gap zones between the triple-helical collagen molecules; upon re-hydration, the extrafibrillar space is established at volumes directly proportional to the hydration-induced swelling of the (micro) fibrils, until the maximum equatorial distance between the long collagen molecules is reached. Thereafter, the volume of the fibrils stays constant, and only the extrafibrillar volume continues to grow. At all these hydration stages, the elastic behavior is governed by the same, hydration-invariant mechanical interaction pattern of only two, interpenetrating mechanical phases: transversely isotropic molecular collagen and isotropic water (or empty pores in the vacuum-dried case). ► General rules for hydration-induced collagen swelling and softening are identified. ► Fibrillar volume swelling is quantified from X-ray diffraction data. ► Fibrillar elasticity is quantified from Brillouin light scattering. ► Extrafibrillar space grows proportional to fibril swelling. ► Transversely isotropic elasticity of molecular collagen is hydration-independent.