Pattern formation in fiber-reinforced tubular tissues: Folding and segmentation during epithelial growth

Abstract

Constrained growth processes in living materials result in a complex distribution of residual strains, which in certain geometries may induce a bifurcation in the elastic stability. In this work, we investigate the combined effects of growth and material anisotropy in the epithelial pattern formation of tubular tissues. In order to represent the structural organization of most organs, we adopt a strain energy density which accounts for the presence of a nonlinear reinforcement made of cross-ply fibers distributed inside a ground matrix. Using a canonical transformation in mixed polar coordinates, we transform the nonlinear elastic boundary value problem into a variational formulation, performing a straightforward derivation of the Euler–Lagrange equations for perturbations in circumferential and longitudinal directions. The corresponding curves of marginal stability are obtained numerically: the results demonstrate that both the three-dimensional distribution of residual strains and the mechanical properties of fiber reinforcements within the tissue are fundamental to determine the emergence of a specific instability pattern. In particular, different proportions of axial and circumferential residual strains can model the epithelial formation of mucosal folds in the esophagus and of plicae circulares in the small intestine. The theoretical predictions are compared with morphological data for embryonic intestinal tissues, suggesting that the volumetric growth of the epithelium can also drive the early stages of villi morphogenesis.