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TECHNICAL PAPERS: Bone/Orthopedic

Microstructural Mechanics of Collagen Gels in Confined Compression: Poroelasticity, Viscoelasticity, and Collapse

[+] Author and Article Information
Preethi L. Chandran, Victor H. Barocas

Department of Biomedical Engineering, University of Minnesota, 312 Church St SE, Minneapolis, MN 55455

J Biomech Eng 126(2), 152-166 (May 04, 2004) (15 pages) doi:10.1115/1.1688774 History: Received June 13, 2003; Revised November 03, 2003; Online May 04, 2004
Copyright © 2004 by ASME
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References

Veis,  A., 1982, “Collagen Fibrillogenesis,” Connect. Tissue Res., 10, pp. 11–24.
Holmes,  D. F., Graham,  H. K., Trotter,  J. A., and Kadler,  K. E., 2001, “STEM/TEM Studies of Collagen Fibril Assembly,” Micron, 32, pp. 273–85.
Kadler,  K. E., Holmes,  D. F., Graham,  H., and Starborg,  T., 2000, “Tip-Mediated Fusion Involving Unipolar Collagen Fibrils Accounts for Rapid Fibril Elongation, the Occurrence of Fibrillar Branched Networks in Skin and the Paucity of Collagen Fibril Ends in Vertebrates,” Matrix Biol., 19, pp. 359–65.
Kadler,  K. E., Holmes,  D. F., Trotter,  J. A., and Chapman,  J. A., 1996, “Collagen Fibril Formation,” Biochem. J., 316, pp. 1–11.
Tranquillo, R. T., 1999, “Self-Organization of Tissue-Equivalents: The Nature and Role of Contact Guidance,” Biochemical Society Symposia., 65, pp. 27–42.
Allen,  T. D., Schor,  S. L., and Schor,  A. M., 1984, “An Ultrastructural Review of Collagen Gels, a Model System for Cell-Matrix, Cell-Basement Membrane and Cell-Cell Interactions,” Scan Electron Microsc., 375–90.
Roeder,  B. A., Kokini,  K., Surgis,  J. E., Robinson,  J. P., and Voytik-Harbin,  S. L., 2002, “Tensile Mechanical Properties of Three-Dimensional Type I Collagen Extracellular Matrices with Varied Microstructure,” J. Biomech. Eng., 124, pp. 214–223.
Grinnell,  F., and Lamke,  C. R., 1984, “Reorganization of Hydrated Collagen Lattices by Human Skin Fibroblasts,” J. Cell. Sci., 66, pp. 51–63.
Guidry,  C., and Grinnell,  F., 1986, “Contraction of Hydrated Collagen Gels by Fibroblasts: Evidence of Two Mechanisms by Which Collagen Fibrils are Stabilized,” Coll. Relat. Res., 6, pp. 515–529.
Bell, E., Ivarsson, B., and Merrill, C., 1979, “Production of a Tissue-Like Structure by Contraction of Collagen Lattices by Human Fibroblasts of Different Proliferative Potential In Vivo,” Proceedings of the National Academy of Sciences of the USA, 76, pp. 1274-8.
Elsdale,  T., and Bard,  J., 1972, “Collagen Substrata for Studies on Cell Behavior,” J. Cell Biol., 54, pp. 626–37.
Stopak,  D., and Harris,  A. K., 1982, “Connective Tissue Morphogenesis by Fibroblast Traction. I. Tissue Culture Observations,” Dev. Biol., 90, pp. 383–98.
Auger,  F. A., Rouabhia,  M., Goulet,  F., Berthod,  F., Moulin,  V., and Germain,  L., 1998, “Tissue-Engineered Human Skin Substitutes Developed from Collagen-Populated Hydrated Gels: Clinical and Fundamental Applications,” Med. Biol. Eng. Comput., 36, pp. 801–812.
Wakatsuki,  T., Kolodney,  M. S., Zahalak,  G. I., and Elson,  E. L., 2000, “Cell Mechanics Studied by a Reconstituted Model Tissue,” Biophys. J., 79, pp. 2353–2368.
Grodzinsky,  A. J., Levenston,  M. E., Jin,  M., and Frank,  E. H., 2000, “Cartilage Tissue Remodeling in Response to Mechanical Forces,” Annual Review of Biomedical Engineering, 2 , pp. 691–713.
Guilak,  F., and Mow,  V. C., 2000, “The Mechanical Environment of the Chondrocyte: A Biphasic Finite Element Model of Cell-Matrix Interactions in Articular Cartilage,” J. Biomech., 33, pp. 1663–73.
Mow,  V. C., Wang,  C. C., and Hung,  C. T., 1999, “The Extracellular Matrix, Interstitial Fluid and Ions as a Mechanical Signal Transducer in Articular Cartilage,” Osteoarthritis Cartilage, 7, pp. 41–58.
Barocas,  V. H., Moon,  A. G., and Tranquillo,  R. T., 1995, “The Fibroblast-Populated Microsphere Assay of Cell Traction Force—Part 2. Measurement of the Cell Traction Coefficient,” J. Biomech. Eng., 117, pp. 161–170.
Parsons,  J. W., and Coger,  R. N., 2002, “A New Device for Measuring the Viscoelastic Properties of Hydrated Matrix Gels,” J. Biomech. Eng., 124, pp. 145–54.
Velegol,  D., and Lanni,  F., 2001, “Cell Traction Forces on Soft Biomaterials. I. Microrheology of Type I Collagen Gels,” Biophys. J., 81, pp. 1786–92.
Ferry, J. D., 1970, Viscoelastic Properties of Polymers, Wiley.
Graessley, W. W., 1974, The Entanglement Concept in Polymer Rheology, Berlin; New York: Springer-Verlag.
Tower,  T. T., Neidert,  M. R., and Tranquillo,  R. T., “Fiber Alignment Imaging During Mechanical Testing of Soft Tissues,” Ann. Biomed. Eng., 30 (10), pp. 1221–1233.
Ozerdem,  B., and Tozeren,  A., 1995, “Physical Response of Collagen Gels to Tensile Strain,” ASME J. Biomech. Eng., 117, pp. 397–401.
Agoram,  B., and Barocas,  V. H., 2001, “Coupled Macroscopic and Microscopic Scale Modeling of Fibrillar Tissues and Tissue Equivalents,” J. Biomech. Eng., 123, pp. 362–9.
Voytik-Harbin,  S. L., Roeder,  B. A., Sturgis,  J. E., Kokini,  K., and Robinson,  J. P., 2003, “Simultaneous Mechanical Loading and Confocal Reflection Microscopy for Three-Dimensional Microbiomechanical Analysis of Biomaterials and Tissue Constructs,” Microscopy and Microanalysis, 9, pp. 74–85.
Knapp,  D. M., Barocas,  V. H., Moon,  A. G., Yoo,  K., Petzold,  L. R., and Tranquillo,  R. T., 1997, “Rheology of Reconstituted Type I Collagen Gel in Confined Compression,” J. Rheol., 41, pp. 971–993.
Harrigan,  T. P., 1987, “Cartilage is Poroelastic but not Biphasic,” J. Biomech., 20, pp. 827–9.
Mow,  V. C., Kuei,  S. C., Lai,  W. M., and Armstrong,  C. G., 1980, “Biphasic Creep and Stress Relaxation of Articular Cartilage in Compression: Theory and Experiments,” J. Biomech. Eng., 102, pp. 73–84.
Simon,  B. R., Coats,  R. S., and Woo,  S. L., 1984, “Relaxation and Creep Quasilinear Viscoelastic Models for Normal Articular Cartilage,” J. Biomech. Eng., 106, pp. 159–64.
Girton,  T. S., Barocas,  V. H., and Tranquillo,  R. T., 2002, “Confined Compression of a Tissue-Equivalent: Collagen Fibril and Cell Alignment in Response to Anisotropic Strain,” J. Biomech. Eng., 124, pp. 568–575.
Barocas,  V. H., and Tranquillo,  R. T., 1997, “An Anisotropic Biphasic Theory of Tissue-Equivalent Mechanics: The Interplay Among Cell Traction, Fibrillar Network Deformation, Fibril Alignment, and Cell Contact Guidance,” J. Biomech. Eng., 119, pp. 137–145.
Dembo,  M., and Harlow,  F., 1986, “Cell Motion, Contractile Networks, and the Physics of Interpenetrating Reactive Flow,” Biophys. J., 50, pp. 109–121.
Armstrong,  C. G., Lai,  W. M., and Mow,  V. C., 1984, “An Analysis of the Unconfined Compression of Articular Cartilage,” J. Biomech. Eng., 106, pp. 165–173.
Tower,  T. T., and Tranquillo,  R. T., 2001, “Alignment Maps in Tissues: II. Fast Harmonic Analysis for Imaging,” Biophys. J. 81, 2964–297.
Wolman,  M., and Kasten,  F. H., 1986, “Polarized Light Microscopy in the Study of the Molecular Structure of Collagen and Reticulin,” Histochemistry, 85, pp. 41–9.
Collett, E., 1993, Polarized Light: Fundamentals and Applications, Marcel Dekker, New York.
Fuller, G. G., 1995, Optical Rheometry of Complex Fluids, Oxford University Press, New York.
Roska,  F. J., and Ferry,  J. D., 1982, “Studies of Fibrin Film. I. Stress Relaxation and Birefringence,” Biopolymers, 21, pp. 1811–32.
Chapuis,  J. F., LucarzBietry,  A., Agache,  P., and Humbert,  P., 1996, “A Mechanical Study of Tense Collagen Lattices,” Eur. J. Dermatol., 6, pp. 56–60.
Puxkandl,  R. , Zizak,  I., Paris,  O., Keckes,  J., Tesch,  W., Bernstorff,  S., Purslow,  P., and Fratzl,  P., 2002, “Viscoelastic Properties of Collagen: Synchrotron Radiation Investigations and Structural Model,” Philosophical Transactions of the Royal Society of London–Series B: Biological Sciences., 357(1418), pp. 191–197.
Moon, A. G., 1992, Ph.D. thesis in Chemical Engineering; Minneapolis, MN: University of Minnesota.
Cheung,  D. T., and Nimri,  M. E., 1982, “Mechanism of Crosslinking of Proteins by Glutaraldehyde II. Reaction with Monomeric and Polymeric Collagen,” Connect. Tissue Res., 10(2), pp. 201–216.
Pineri,  M. H., Escoubes,  M., Roche,  G., 1978, “Water-Collagen Interactions: Calorimetric and Mechanical Experiments,” Biopolymers, 17(12), pp. 2799–2815.
Traore,  A., Foucat,  L., Renou,  J. P., 2000, “1H-nmr Study of Water Dynamics in Hydrated Collagen: Transverse Relaxation-Time and Diffusion Analysis,” Biopolymers, 53(6), pp. 476–483.
Christiansen,  D. L., Huang,  E. K., and Silver,  F. H., 2000, “Assembly of Type I Collagen: Fusion of Fibril Subunits and the Influence of Fibril Diameter on Mechanical Properties,” Matrix Biol., 19, pp. 409–420.
Hsu,  S., Jamieson,  A. M., and Blackwell,  J., 1994, “Viscoelastic Studies of Extracellular Matrix Interactions in a Model Native Collagen Gel System,” Biorheology, 31, pp. 21–36.

Figures

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Confined compression chamber
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15 mm Collagen gel before for compression testing. (a) Intensity map. The piston region appears black at the right of the image, and the bar in the lower right is 1 mm. (b) Birefringence map. The magnitude of each vector is scaled to represent the retardation along the extinction angle, averaged over pixels. The piston region shows no optical activity. (c) Retardation profile vs. position along length of the sample. Retardation is averaged over a width of three 3 pixels at y=64 (see 2a).
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Response to 10% Step Compression (0.02 sec) in 5 mm gel. (a) Stress response to step compression. (b) Retardation, (c) orientation and (d) concentration profiles along the length of the chamber, before and immediately (3 s) after compression. The arrows in 3b show the translation of profile features. Bulk (intact) and near-piston (collapsed) regions are marked A and B, respectively.
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Stress Relaxation after 10% Step Compression in 5 mm gel. (a) Stress response during relaxation. (b) Retardation, (c) orientation and (d) concentration profiles along the length of the chamber, at different stages of stress relaxation. The time points of the profiles in (b)–(d) are marked on the stress response plot (a). The birefringence profiles (b and c) in the bulk relax to original state. The near-piston region gets compressed against the piston (b, c and d)
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Piston retraction after Relaxation of 10% Step Compression of 5 mm gel. Retardation is shown along the length of the chamber, before and after compression (as in 3b) and after piston retraction. The retardation profile after retraction (gray open diamonds) shows near complete recovery of the original state (black solid diamonds) in the bulk but not in the near-piston region.
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Response to 10% Step Compression in 15 mm gel. (a) Stress response during compression and relaxation. (b) Retardation profiles along the length of the chamber, at different stages of stress relaxation. The corresponding time points are marked on the stress response plot (a).
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Response to Ramp (0.1%/s) Compression in 5 mm gel. (a) Stress response during compression and relaxation. (b) Retardation, (c) orientation, and (d) concentration profiles along the length of the chamber, before and during compression. The compression is initially greater towards the piston but soon gets transmitted throughout. The retardation and orientation change everywhere in proportion to the gel strain (shown by the translation of profile features). The corresponding time points are marked on the stress response plot (a).
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Stress Relaxation after Ramp (0.1%/s) Compression in 5 mm gel. (a) Stress response during compression and relaxation. (b) Retardation, (c) orientation, and (d) concentration profiles along the length of the chamber, at different stages of stress relaxation. The gel moves away from the piston. The corresponding time points are marked on the stress response plot (a).
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Ramp (0.1%/s) Compression in 15 mm gel. (a) Stress response during compression and relaxation. (b) Retardation profiles along the length of the chamber, during ramp and at different stages of stress relaxation. The corresponding time points are marked on the stress response plot (a).
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Stress Evolution in Step vs. Ramp Compression of 5 mm gel. A logarithmic time scale is used to resolve the short-time data for step compression. The peak stress was higher in the step case, but the long-time stress was higher in the ramp case.
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Center-of-Mass (COM) Motion of 5 mm Gel in Step vs. Ramp Compression. In both cases, the COM was displaced toward the closed end of the cup during compression. During relaxation, the COM moved toward the piston in the step case but away from the piston in the ramp case.

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