Many load-bearing soft tissues exhibit mechanical anisotropy. In order to understand the behavior of natural tissues and to create tissue engineered replacements, quantitative relationships must be developed between the tissue structures and their mechanical behavior. We used a novel collagen gel system to test the hypothesis that collagen fiber alignment is the primary mechanism for the mechanical anisotropy we have reported in structurally anisotropic gels. Loading constraints applied during culture were used to control the structural organization of the collagen fibers of fibroblast populated collagen gels. Gels constrained uniaxially during culture developed fiber alignment and a high degree of mechanical anisotropy, while gels constrained biaxially remained isotropic with randomly distributed collagen fibers. We hypothesized that the mechanical anisotropy that developed in these gels was due primarily to collagen fiber orientation. We tested this hypothesis using two mathematical models that incorporated measured collagen fiber orientations: a structural continuum model that assumes affine fiber kinematics and a network model that allows for nonaffine fiber kinematics. Collagen fiber mechanical properties were determined by fitting biaxial mechanical test data from isotropic collagen gels. The fiber properties of each isotropic gel were then used to predict the biaxial mechanical behavior of paired anisotropic gels. Both models accurately described the isotropic collagen gel behavior. However, the structural continuum model dramatically underestimated the level of mechanical anisotropy in aligned collagen gels despite incorporation of measured fiber orientations; when estimated remodeling-induced changes in collagen fiber length were included, the continuum model slightly overestimated mechanical anisotropy. The network model provided the closest match to experimental data from aligned collagen gels, but still did not fully explain the observed mechanics. Two different modeling approaches showed that the level of collagen fiber alignment in our uniaxially constrained gels cannot explain the high degree of mechanical anisotropy observed in these gels. Our modeling results suggest that remodeling-induced redistribution of collagen fiber lengths, nonaffine fiber kinematics, or some combination of these effects must also be considered in order to explain the dramatic mechanical anisotropy observed in this collagen gel model system.
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e-mail: ThomopoulosS@wudosis.wustl.edu
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October 2007
Technical Papers
Collagen Fiber Alignment Does Not Explain Mechanical Anisotropy in Fibroblast Populated Collagen Gels
Stavros Thomopoulos,
Stavros Thomopoulos
Department of Orthopaedic Surgery,
e-mail: ThomopoulosS@wudosis.wustl.edu
Washington University School of Medicine
, 1 Barnes-Jewish Hospital Plaza, Suite 11300, Campus Box 8233, St. Louis, MO 63110
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Gregory M. Fomovsky,
Gregory M. Fomovsky
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027
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Preethi L. Chandran,
Preethi L. Chandran
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027
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Jeffrey W. Holmes
Jeffrey W. Holmes
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027
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Stavros Thomopoulos
Department of Orthopaedic Surgery,
Washington University School of Medicine
, 1 Barnes-Jewish Hospital Plaza, Suite 11300, Campus Box 8233, St. Louis, MO 63110e-mail: ThomopoulosS@wudosis.wustl.edu
Gregory M. Fomovsky
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027
Preethi L. Chandran
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027
Jeffrey W. Holmes
Department of Biomedical Engineering,
Columbia University
, New York, NY 10027J Biomech Eng. Oct 2007, 129(5): 642-650 (9 pages)
Published Online: February 15, 2007
Article history
Received:
January 25, 2006
Revised:
February 15, 2007
Citation
Thomopoulos, S., Fomovsky, G. M., Chandran, P. L., and Holmes, J. W. (February 15, 2007). "Collagen Fiber Alignment Does Not Explain Mechanical Anisotropy in Fibroblast Populated Collagen Gels." ASME. J Biomech Eng. October 2007; 129(5): 642–650. https://doi.org/10.1115/1.2768104
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