Mechanics of a two-fiber model with one nested fiber network, as applied to the collagen-fibrin system

David Nedrelow, Danesh Bankwala, Jeffrey D. Hyypio, Victor Lai, Victor H Barocas

Research output: Contribution to journalArticle

Abstract

The mechanical behavior of collagen-fibrin (col-fib) co-gels is both scientifically interesting and clinically relevant. Collagen-fibrin networks are a staple of tissue engineering research, but the mechanical consequences of changes in co-gel composition have remained difficult to predict or even explain. We previously observed fundamental differences in failure behavior between collagen-rich and fibrin-rich co-gels, suggesting an essential change in how the two components interact as the co-gel's composition changes. In this work, we explored the hypothesis that the co-gel behavior is due to a lack of percolation by the dilute component. We generated a series of computational models based on interpenetrating fiber networks. In these models, the major network component percolated the model space but the minor component did not, instead occupying a small island embedded within the larger network. Each component was assigned properties based on a fit of single-component gel data. Island size was varied to match the relative concentrations of the two components. The model predicted that networks rich in collagen, the stiffer component, would roughly match pure-collagen gel behavior with little additional stress due to the fibrin, as seen experimentally. For fibrin-rich gels, however, the model predicted a smooth increase in the overall network strength with added collagen, as seen experimentally but not consistent with an additive parallel model. We thus conclude that incomplete percolation by the low-concentration component of a co-gel is a major determinant of its macroscopic properties, especially if the low-concentration component is the stiffer component. Statement of significance: Models for the behavior of fibrous networks have useful applications in many different fields, including polymer science, textiles, and tissue engineering. In addition to being important structural components in soft tissues and blood clots, these protein networks can serve as scaffolds for bioartificial tissues. Thus, their mechanical behavior, especially in co-gels, is both interesting from a materials science standpoint and significant with regard to tissue engineering.

Original languageEnglish (US)
Pages (from-to)306-315
Number of pages10
JournalActa Biomaterialia
Volume72
DOIs
StatePublished - May 1 2018

Fingerprint

Mechanics
Fibrin
Collagen
Gels
Fibers
Tissue Engineering
Tissue engineering
Islands
Tissue
Space Simulation
Tissue Scaffolds
Network components
Engineering research
Textiles
Materials science
Scaffolds (biology)
Chemical analysis
Blood Proteins
Polymers
Thrombosis

Keywords

  • Biomechanics
  • Composite
  • Computational
  • Failure
  • Multiscale
  • Solid
  • Tissue

Cite this

Mechanics of a two-fiber model with one nested fiber network, as applied to the collagen-fibrin system. / Nedrelow, David; Bankwala, Danesh; Hyypio, Jeffrey D.; Lai, Victor; Barocas, Victor H.

In: Acta Biomaterialia, Vol. 72, 01.05.2018, p. 306-315.

Research output: Contribution to journalArticle

@article{37efaccc03744d6a9d7b989fb06d8b63,
title = "Mechanics of a two-fiber model with one nested fiber network, as applied to the collagen-fibrin system",
abstract = "The mechanical behavior of collagen-fibrin (col-fib) co-gels is both scientifically interesting and clinically relevant. Collagen-fibrin networks are a staple of tissue engineering research, but the mechanical consequences of changes in co-gel composition have remained difficult to predict or even explain. We previously observed fundamental differences in failure behavior between collagen-rich and fibrin-rich co-gels, suggesting an essential change in how the two components interact as the co-gel's composition changes. In this work, we explored the hypothesis that the co-gel behavior is due to a lack of percolation by the dilute component. We generated a series of computational models based on interpenetrating fiber networks. In these models, the major network component percolated the model space but the minor component did not, instead occupying a small island embedded within the larger network. Each component was assigned properties based on a fit of single-component gel data. Island size was varied to match the relative concentrations of the two components. The model predicted that networks rich in collagen, the stiffer component, would roughly match pure-collagen gel behavior with little additional stress due to the fibrin, as seen experimentally. For fibrin-rich gels, however, the model predicted a smooth increase in the overall network strength with added collagen, as seen experimentally but not consistent with an additive parallel model. We thus conclude that incomplete percolation by the low-concentration component of a co-gel is a major determinant of its macroscopic properties, especially if the low-concentration component is the stiffer component. Statement of significance: Models for the behavior of fibrous networks have useful applications in many different fields, including polymer science, textiles, and tissue engineering. In addition to being important structural components in soft tissues and blood clots, these protein networks can serve as scaffolds for bioartificial tissues. Thus, their mechanical behavior, especially in co-gels, is both interesting from a materials science standpoint and significant with regard to tissue engineering.",
keywords = "Biomechanics, Composite, Computational, Failure, Multiscale, Solid, Tissue",
author = "David Nedrelow and Danesh Bankwala and Hyypio, {Jeffrey D.} and Victor Lai and Barocas, {Victor H}",
year = "2018",
month = "5",
day = "1",
doi = "10.1016/j.actbio.2018.03.053",
language = "English (US)",
volume = "72",
pages = "306--315",
journal = "Acta Biomaterialia",
issn = "1742-7061",
publisher = "Elsevier BV",

}

TY - JOUR

T1 - Mechanics of a two-fiber model with one nested fiber network, as applied to the collagen-fibrin system

AU - Nedrelow, David

AU - Bankwala, Danesh

AU - Hyypio, Jeffrey D.

AU - Lai, Victor

AU - Barocas, Victor H

PY - 2018/5/1

Y1 - 2018/5/1

N2 - The mechanical behavior of collagen-fibrin (col-fib) co-gels is both scientifically interesting and clinically relevant. Collagen-fibrin networks are a staple of tissue engineering research, but the mechanical consequences of changes in co-gel composition have remained difficult to predict or even explain. We previously observed fundamental differences in failure behavior between collagen-rich and fibrin-rich co-gels, suggesting an essential change in how the two components interact as the co-gel's composition changes. In this work, we explored the hypothesis that the co-gel behavior is due to a lack of percolation by the dilute component. We generated a series of computational models based on interpenetrating fiber networks. In these models, the major network component percolated the model space but the minor component did not, instead occupying a small island embedded within the larger network. Each component was assigned properties based on a fit of single-component gel data. Island size was varied to match the relative concentrations of the two components. The model predicted that networks rich in collagen, the stiffer component, would roughly match pure-collagen gel behavior with little additional stress due to the fibrin, as seen experimentally. For fibrin-rich gels, however, the model predicted a smooth increase in the overall network strength with added collagen, as seen experimentally but not consistent with an additive parallel model. We thus conclude that incomplete percolation by the low-concentration component of a co-gel is a major determinant of its macroscopic properties, especially if the low-concentration component is the stiffer component. Statement of significance: Models for the behavior of fibrous networks have useful applications in many different fields, including polymer science, textiles, and tissue engineering. In addition to being important structural components in soft tissues and blood clots, these protein networks can serve as scaffolds for bioartificial tissues. Thus, their mechanical behavior, especially in co-gels, is both interesting from a materials science standpoint and significant with regard to tissue engineering.

AB - The mechanical behavior of collagen-fibrin (col-fib) co-gels is both scientifically interesting and clinically relevant. Collagen-fibrin networks are a staple of tissue engineering research, but the mechanical consequences of changes in co-gel composition have remained difficult to predict or even explain. We previously observed fundamental differences in failure behavior between collagen-rich and fibrin-rich co-gels, suggesting an essential change in how the two components interact as the co-gel's composition changes. In this work, we explored the hypothesis that the co-gel behavior is due to a lack of percolation by the dilute component. We generated a series of computational models based on interpenetrating fiber networks. In these models, the major network component percolated the model space but the minor component did not, instead occupying a small island embedded within the larger network. Each component was assigned properties based on a fit of single-component gel data. Island size was varied to match the relative concentrations of the two components. The model predicted that networks rich in collagen, the stiffer component, would roughly match pure-collagen gel behavior with little additional stress due to the fibrin, as seen experimentally. For fibrin-rich gels, however, the model predicted a smooth increase in the overall network strength with added collagen, as seen experimentally but not consistent with an additive parallel model. We thus conclude that incomplete percolation by the low-concentration component of a co-gel is a major determinant of its macroscopic properties, especially if the low-concentration component is the stiffer component. Statement of significance: Models for the behavior of fibrous networks have useful applications in many different fields, including polymer science, textiles, and tissue engineering. In addition to being important structural components in soft tissues and blood clots, these protein networks can serve as scaffolds for bioartificial tissues. Thus, their mechanical behavior, especially in co-gels, is both interesting from a materials science standpoint and significant with regard to tissue engineering.

KW - Biomechanics

KW - Composite

KW - Computational

KW - Failure

KW - Multiscale

KW - Solid

KW - Tissue

UR - http://www.scopus.com/inward/record.url?scp=85045056210&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85045056210&partnerID=8YFLogxK

U2 - 10.1016/j.actbio.2018.03.053

DO - 10.1016/j.actbio.2018.03.053

M3 - Article

VL - 72

SP - 306

EP - 315

JO - Acta Biomaterialia

JF - Acta Biomaterialia

SN - 1742-7061

ER -