Cargando…

Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model

While it is known that musculotendon units adapt to their load environments, there is only a limited understanding of tendon adaptation in vivo. Here we develop a computational model of tendon remodeling based on the premise that mechanical damage and tenocyte-mediated tendon damage and repair proce...

Descripción completa

Detalles Bibliográficos
Autores principales: Young, Stuart R., Gardiner, Bruce, Mehdizadeh, Arash, Rubenson, Jonas, Umberger, Brian, Smith, David W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5042511/
https://www.ncbi.nlm.nih.gov/pubmed/27684554
http://dx.doi.org/10.1371/journal.pcbi.1005106
_version_ 1782456604909633536
author Young, Stuart R.
Gardiner, Bruce
Mehdizadeh, Arash
Rubenson, Jonas
Umberger, Brian
Smith, David W.
author_facet Young, Stuart R.
Gardiner, Bruce
Mehdizadeh, Arash
Rubenson, Jonas
Umberger, Brian
Smith, David W.
author_sort Young, Stuart R.
collection PubMed
description While it is known that musculotendon units adapt to their load environments, there is only a limited understanding of tendon adaptation in vivo. Here we develop a computational model of tendon remodeling based on the premise that mechanical damage and tenocyte-mediated tendon damage and repair processes modify the distribution of its collagen fiber lengths. We explain how these processes enable the tendon to geometrically adapt to its load conditions. Based on known biological processes, mechanical and strain-dependent proteolytic fiber damage are incorporated into our tendon model. Using a stochastic model of fiber repair, it is assumed that mechanically damaged fibers are repaired longer, whereas proteolytically damaged fibers are repaired shorter, relative to their pre-damage length. To study adaptation of tendon properties to applied load, our model musculotendon unit is a simplified three-component Hill-type model of the human Achilles-soleus unit. Our model results demonstrate that the geometric equilibrium state of the Achilles tendon can coincide with minimization of the total metabolic cost of muscle activation. The proposed tendon model independently predicts rates of collagen fiber turnover that are in general agreement with in vivo experimental measurements. While the computational model here only represents a first step in a new approach to understanding the complex process of tendon remodeling in vivo, given these findings, it appears likely that the proposed framework may itself provide a useful theoretical foundation for developing valuable qualitative and quantitative insights into tendon physiology and pathology.
format Online
Article
Text
id pubmed-5042511
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-50425112016-10-27 Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model Young, Stuart R. Gardiner, Bruce Mehdizadeh, Arash Rubenson, Jonas Umberger, Brian Smith, David W. PLoS Comput Biol Research Article While it is known that musculotendon units adapt to their load environments, there is only a limited understanding of tendon adaptation in vivo. Here we develop a computational model of tendon remodeling based on the premise that mechanical damage and tenocyte-mediated tendon damage and repair processes modify the distribution of its collagen fiber lengths. We explain how these processes enable the tendon to geometrically adapt to its load conditions. Based on known biological processes, mechanical and strain-dependent proteolytic fiber damage are incorporated into our tendon model. Using a stochastic model of fiber repair, it is assumed that mechanically damaged fibers are repaired longer, whereas proteolytically damaged fibers are repaired shorter, relative to their pre-damage length. To study adaptation of tendon properties to applied load, our model musculotendon unit is a simplified three-component Hill-type model of the human Achilles-soleus unit. Our model results demonstrate that the geometric equilibrium state of the Achilles tendon can coincide with minimization of the total metabolic cost of muscle activation. The proposed tendon model independently predicts rates of collagen fiber turnover that are in general agreement with in vivo experimental measurements. While the computational model here only represents a first step in a new approach to understanding the complex process of tendon remodeling in vivo, given these findings, it appears likely that the proposed framework may itself provide a useful theoretical foundation for developing valuable qualitative and quantitative insights into tendon physiology and pathology. Public Library of Science 2016-09-29 /pmc/articles/PMC5042511/ /pubmed/27684554 http://dx.doi.org/10.1371/journal.pcbi.1005106 Text en © 2016 Young et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Young, Stuart R.
Gardiner, Bruce
Mehdizadeh, Arash
Rubenson, Jonas
Umberger, Brian
Smith, David W.
Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title_full Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title_fullStr Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title_full_unstemmed Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title_short Adaptive Remodeling of Achilles Tendon: A Multi-scale Computational Model
title_sort adaptive remodeling of achilles tendon: a multi-scale computational model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5042511/
https://www.ncbi.nlm.nih.gov/pubmed/27684554
http://dx.doi.org/10.1371/journal.pcbi.1005106
work_keys_str_mv AT youngstuartr adaptiveremodelingofachillestendonamultiscalecomputationalmodel
AT gardinerbruce adaptiveremodelingofachillestendonamultiscalecomputationalmodel
AT mehdizadeharash adaptiveremodelingofachillestendonamultiscalecomputationalmodel
AT rubensonjonas adaptiveremodelingofachillestendonamultiscalecomputationalmodel
AT umbergerbrian adaptiveremodelingofachillestendonamultiscalecomputationalmodel
AT smithdavidw adaptiveremodelingofachillestendonamultiscalecomputationalmodel