Viscoelastic properties of young and old human dermis: A proposed molecular mechanism for elastic energy storage in collagen and elastin

Abstract

ABSTRACT:We have studied the strain-rate dependency of the viscoelastic mechanical properties of human dermis from young (23-year-old) and old (87-year-old) donors using incremental stress-strain measurements. The elastic spring constant for elastic fibers was found to be strain-rate and age dependent, whereas that for collagen was only age dependent. Fibril lengths were observed to decrease with increased strain rates and age for both elastic and collagen fibers; however, the large decrease in collagen fibril viscosity was hypothesized to be a result of thixotropy that results when neighboring collagen fibrils slide by each other. It is concluded that the elastic spring constant measured for elastic fibers may be higher than previously reported and is consistent with stretching of ␣-helical segments of elastin into a more extended conformation during the initial part of the elastic stress-strain curve. The decrease in the elastic spring constant with increased age observed is consistent with disruption of the elastic fibers and loss of ␣-helical structure. The pH dependency of the elastic modulus reported previously for collagen suggests that charge-charge interactions within and between collagen molecules are involved in energy storage during stretching. Elastic energy storage is consistent with the stretching of charged pairs located in flexible regions of the collagen molecule. Shear thinning, or thixotropy of skin, is hypothesized to reflect breakage of bonds that occur between collagen fibrils. It is hypothesized that both collagen and elastin are complex macromolecules that are hybrids of flexible and rigid regions. The flexible regions reversibly store elastic energy during stretching by breakage of secondary bonds. After stretching, the flexible regions become extended and transfer stress to the rigid regions of these molecules. This prevents premature mechanical failure of collagen and elastic fibers in the dermis.

Tissue Strain Reorganizes Collagen With a Switchlike Response That Regulates Neuronal Extracellular Signal-Regulated Kinase Phosphorylation In Vitro: Implications for Ligamentous Injury and Mechanotransduction

“…4 and 5) may be due to the viscoelastic properties of the neurons and their surrounding collagen matrix [75][76][77]. Viscoelasticity may limit fiber rotation and stretch during rapid NCC stretch because hydrogen bonds between and within the collagen molecules are less likely to break under rapid loading [78,79]. This resistance to fiber movement and deformation may limit fiber realignment toward the loading direction more in the NCCs loaded at 3.5 mm/s than at 0.5 mm/s (Fig.…”

Mechanical Implications of the Domain Structure of Fiber-Forming Collagens: Comparison of the Molecular and Fibrillar Flexibilities of the α1-Chains Found in Types I–III Collagen

“…Previously, we proposed elastic energy is stored in collagen fibers during tensile deformation of tendon, skin, cartilage, mineralizing tendon and selfassembled cross-linked type I collagen (Silver et al, 2000a(Silver et al, , 2001a(Silver et al, -c, 2002). This energy is stored during stretching of the flexible regions in the molecule; these regions coincide with the positive staining bands in the D-period of type I collagen fibril (Silver et al, 2002).…”

“…Of these functions, elastic energy storage is key to normal functioning of skin, tendon, cartilage and vessel wall (Silver 1987;Silver et al, 2000aSilver et al, , b, 2001a. Elastic energy storage appears to involve the polar amino acid residues that are found primarily in the positive staining bands of the collagen D-period (Silver et al, 2002). Although the flexibility of the collagen molecule has been implicated in elastic energy storage, there is little information in the literature to relate molecular properties of the different collagen molecules to the macroscopic mechanical properties.…”

Dermatoporosis: A Chronic Cutaneous Insufficiency/Fragility Syndrome

“…The decrease in the collagen fibril viscosity and length associated with an increase in the strain rate reflects a decrease in the viscosity of skin [20]. The fracture pattern of the collagen fibers can be classified into three main patterns [21]: (1) fracture occurring in a single plane perpendicular to the fiber axis, or ‘smooth fracture’; (2) fracture starting as a smooth fracture but resulting in the splitting of the fiber along the axis, or ‘step fracture’; (3) fracture with a split open end resembling the bristles of a brush, or ‘fibrillation fracture’ [22].…”