On the biomechanics and mechanobiology of growing skin

Abstract

Skin displays an impressive functional plasticity, which allows it to adapt gradually to environmental changes. Tissue expansion takes advantage of this adaptation, and induces a controlled in situ skin growth for defect correction in plastic and reconstructive surgery. Stretches beyond the skin’s physiological limit invoke several mechanotransduction pathways, which increase mitotic activity and collagen synthesis, ultimately resulting in a net gain in skin surface area. However, the interplay between mechanics and biology during tissue expansion remains unquantified. Here we present a continuum model for skin growth that summarizes the underlying mechanotransduction pathways collectively in a single phenomenological variable, the strain-driven area growth. We illustrate the governing equations for growing biological membranes, and demonstrate their computational solution within a nonlinear finite element setting. In displacement-controlled equi-biaxial extension tests, the model accurately predicts the experimentally observed histological, mechanical, and structural features of growing skin, both qualitatively and quantitatively. Acute and chronic elastic uniaxial stretches are 25% and 10%, compared to 36% and 10% reported in the literature. Acute and chronic thickness changes are −28% and −12%, compared to −22% and −7% reported in the literature. Chronic fractional weight gain is 3.3, compared to 2.7 for wet weight and 3.3 for dry weight reported in the literature. In two clinical cases of skin expansion in pediatric forehead reconstruction, the model captures the clinically observed mechanical and structural responses, both acutely and chronically. Our results demonstrate that the field theories of continuum mechanics can reliably predict the mechanical manipulation of thin biological membranes by controlling their mechanotransduction pathways through mechanical overstretch. We anticipate that the proposed skin growth model can be generalized to arbitrary biological membranes, and that it can serve as a valuable tool to virtually manipulate living tissues, simply by means of changes in the mechanical environment.

Mathematical and computational modelling of skin biophysics: a review

“…An attractive feature of computational models is the ability to quantify physical parameters required to obtain a specific outcome. For example, Prof. Kuhl's group at Stanford University has pioneered the development of mechanobiological adaptation models for skin to optimize the outcome of reconstructive surgery procedures in children [61][62][63][64][65][66][67] Streamline plots representing the maximum (coloured) and minimum (white) principal strain vectors in a finite deformation 2D plane-strain image-based finite-element model of the skin subjected to 20% in-plane compression (adapted from [20]). Grey arrows indicate the direction and location of the applied load.…”

Characterization of human skin through skin expansion

“…Skin growth was not considered although an overview on the mechanobiology underlying skin growth sustains that tensile stress applied to skin appears to stimulate skin growth [Silver et al 2003]. Researchers recently are looking for a model to describe the growth of the skin under tensile stress, establishing computational models for stretch-induced skin growth under expansion [Buganza Tepole et al 2011] and also patient-specific finite element simulation of skin growth in situ [Zöllner et al 2012]. …”

Explicit finite deformation analysis of isogeometric membranes

“…The implementation of more suitable anisotropic hyperelastic models to represent the passive and adaptive behaviour of biological membrane structures [10,55,62,63] in the present IGA framework is under way. Figure 10.…”