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research-article

An Agent-Based Discrete Collagen Fiber Network Model of Dynamic Traction Force-Induced Remodeling

[+] Author and Article Information
James W. Reinhardt

Department of Biomedical Engineering, The Ohio State University, 270 Bevis Hall, 1080 Carmack Rd., Columbus, OH 43210
james.reinhardt@nationwidechildrens.org

Keith Gooch

Department of Biomedical Engineering, The Ohio State University, 270 Bevis Hall, 1080 Carmack Rd., Columbus, OH 43210; Dorothy M. Davis Heart & Lung Research Institute, The Ohio State University, 473 W. 12th Ave., Columbus, OH 43210
gooch.20@osu.edu

1Corresponding author.

ASME doi:10.1115/1.4037947 History: Received May 11, 2017; Revised September 11, 2017

Abstract

We developed an agent-based model that incorporates repetitively applied traction force within a discrete fiber network to understand how microstructural properties of the network influence mechanical properties and traction force-induced remodeling. An important difference between our model and similar finite-element models is that by implementing more biologically-realistic dynamic traction, we can explore a greater range of matrix remodeling. Here, we validated our model by reproducing qualitative trends observed in three sets of experimental data reported by others: tensile and shear testing of cell-free collagen gels, collagen remodeling around a single isolated cell, and collagen remodeling between pairs of cells. In response to tensile and shear strain, simulated acellular networks exhibited biphasic stress-strain curves indicative of strain-stiffening. Our data support the notion that strain-stiffening might occur as individual fibrils successively align along the axis of strain and become engaged in tension. In simulations with a single, contractile cell, peak collagen displacement occurred closest to the cell and decreased with increasing distance. In simulations with two cells, compaction of collagen between cells appeared inversely related to the initial distance between cells. Further analysis revealed strain energy was relatively uniform around the outer surface of cells separated by 250 microns, but became increasingly non-uniform as the distance between cells decreased. This pattern was partly attributable to the pattern of collagen compaction. These findings are of interest because fibril alignment, density, and strain energy may each contribute to contact guidance during tissue morphogenesis.

Copyright (c) 2017 by ASME
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