0
TECHNICAL PAPERS

Tensile Mechanical Properties of Three-Dimensional Type I Collagen Extracellular Matrices With Varied Microstructure

[+] Author and Article Information
Blayne A. Roeder

School of Mechanical Engineering, Purdue University, West Lafayette, IN 47907-1288e-mail: blayne@ecn.purdue.edu

Klod Kokini

School of Mechanical Engineering/Department of Biomedical Engineering, Purdue University, West Lafayette, IN 47907-1288 e-mail: kokini@ecn.purdue.edu

Jennifer E. Sturgis

Department of Basic Medical Sciences, Purdue University, West Lafayette, IN 47907-1515e-mail: jennie@flowcyt.cyto.purdue.edu

J. Paul Robinson, Sherry L. Voytik-Harbin

Department of Basic Medical Sciences/Department of Biomedical Engineering, Purdue University, West Lafayette, IN 47907-1515

J Biomech Eng 124(2), 214-222 (Mar 29, 2002) (9 pages) doi:10.1115/1.1449904 History: Received May 31, 2001; Revised October 08, 2001; Online March 29, 2002
Copyright © 2002 by ASME
Your Session has timed out. Please sign back in to continue.

References

Ingber, D., 2000, “Mechanical and Chemical Determinants of Tissue Development,” Principles of Tissue Engineering, 2nd Edition, eds., R. P. Lanza et al., Academic Press, Inc., San Diego, CA, pp. 101–110.
Chiquet,  M., 1999, “Regulation of Extracellular Gene Expression by Mechanical Stress,” Matrix Biology, 18, pp. 417–426.
Bateman, J. F., Lamande, S. R., and Ramshaw, J. A. M., 1996, “Collagen Superfamily,” Extracellular Matrix Vol. 2., Molecular Components and Interaction, ed., W. D. Comper, Harwood Academic Publishers, The Netherlands, pp. 22–67.
Veis, A., and George A., 1994, “Fundamentals of Interstitial Collagen Assembly,” Extracellular Matrix Assembly and Structure, eds., P. D. Urchenco et al., Academic Press, Inc., San Diego, CA, pp. 15–45.
Wood,  G. C., and Keech,  M. K., 1960, “The Formation of Fibrils from Collagen Solutions. The Effect of Experimental Conditions: Kinetic and Electron Microscopic Studies,” Biochem. J., 75, pp. 588–598.
Voytik-Harbin,  S. L., 2001, “Three-Dimensional Extracellular Matrix Substrates for Cell Culture,” Methods Cell Biol., 63, pp. 561–581.
Parry,  D. A., 1988, “The Molecular and Fibrillar Structure of Collagen and its Relationship to the Mechanical Properties of Connective Tissue,” Biophys. Chem., 29, pp. 195–209.
Yannas,  I. V., and Burke,  J. F., 1980, “Design of an Artificial Skin. I Basic Design Principles,” J. Biomed. Mater. Res., 14, pp. 65–81.
Matsuda,  K., Suzuki,  S., Isshiki,  N., Yoshioka,  K., Okada,  T., and Ikada,  Y., 1990, “Influence of Glycosaminoglycans on the Collagen Sponge Component of a Bilayer Artificial Skin,” Biomaterials, 11, pp. 351–355.
Matsuda,  K., Suzuki,  S., Issihiki,  N., and Ikada,  Y., 1993, “Re-freeze Dried Bilayer Artificial Skin,” Biomaterials, 14, pp. 1030–1035.
Chen,  C. S., Yannas,  I. V., and Spector,  M., 1995, “Pore Strain Behavior of Collagen Glycosaminoglycan Analogues of Extracellular Matrix,” Biomaterials, 16, pp. 777–783.
Pins,  G. D., Huang,  E. K., Christiansen,  D. L., and Silver,  F. H., 1997, “Effects of Static Axial Strain on the Tensile Properties and Failure Mechanisms of Self-Assembled Collagen Fibers,” J. Appl. Polym. Sci., 63, pp. 1429–1440.
Pins,  G. D., Christiansen,  D. L., Patel,  R., and Silver,  F. H., 1997, “Self-Assembly of Collagen Fibers. Influence of Fibrillar Alignment and Decorin on Mechanical Properties,” Biophys. J., 73, pp. 2164–2172.
Silver,  F. H., Christiansen,  D. L., Snowhill,  P. B., and Chen,  Y., 2000, “Role of Storage on Changes in the Mechanical Properties of Tendon and Self-Assembled Collagen Fibers,” Connect. Tissue Res.,41, pp. 155–164.
Law,  J. K., Parsons,  J. R., Silver,  F. H., and Weiss,  A. B., 1989, “An Evaluation of Purified Reconstituted Type I Collagen Fibers,” J. Biomed. Mater. Res., 23, pp. 961–977.
Dunn,  M. G., Avasarala,  P. N., and Zawadsky,  J. P., 1993, “Optimization of Extruded Collagen Fibers for ACL Reconstruction,” J. Biomed. Mater. Res., 27, pp. 1545–1552.
Christensen,  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 Biology, 19, pp. 409–420.
Miller,  E. J., and Rhodes,  E. K., 1982, “Preparation and Characterization of Different types of Collagen,” Methods Enzymol., 82, pp. 33–64.
Özerdem,  B., and Tözeren,  A., 1995, “Physical Response of Collagen Gels to Tensile Strain,” ASME J. Biomech. Eng., 117, pp. 397–401.
Knapp,  D. M., Barocas,  V. H., and Moon,  A. G., Yoo,  K., Petzold,  L. R., Tranquillo,  R. T., 1997, “Rheology of Reconstituted Type I Collagen Gel in Confined Compression,” J. Rheol., 41, pp. 971–993.
Osborne,  C. S., Barbenel,  J. C., Smith,  D., Savakis,  M., and Grant,  M. H., 1998, “Investigation into the Tensile Properties of Collagen/Chondroitin-6-sulphate Gels: The Effect of Crosslinking Agents and Diamines,” Med. Biol. Eng. Comput., 36, pp. 129–134.
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.
Voytik-Harbin,  S. L., Rajwa,  B., and Robinson,  J. P., 2000, “3D Imaging of Extracellular Matrix and Extracellular Matrix-Cell Interactions,” Methods Cell Biol., 63, pp. 583–597.
Brightman,  A. O., Rajwa,  B. P., Sturgis,  J. E., McCallister,  M. E., Robinson,  J. P., and Voytik-Harbin,  S. L., 2000, “Time-Lapse Confocal Reflection Microscopy of Collagen Fibrillogenesis and Extracellular Matrix Assembly In Vitro,” Biopolymers, 54, pp. 222–234.
Kolodney,  M. S., and Wysolmerski,  R. B., 1992, “Isometric Contraction by Fibroblasts and Endothelial Cells in Tissue Culture: A Quantitative Study,” J. Cell Biol., 117, pp. 73–82.
Delvoye,  P., Wiliquet,  P., Leveque,  J. L., Nusgens,  B. V., and Lapiere,  C. M., 1991, “Measurement of Mechanical Forces Generated by Skin Fibroblasts Embedded in a Three Dimensional Collagen Gel,” J. Invest. Dermatol., 97, pp. 898–902.
Benkherourou,  M., Rochas,  C., Tracqui,  P., Tranqui,  L., and Guméry,  P. Y., 1999, “Standardization of a Method for Characterizing Low-Concentration Biogels: Elastic Properties of Low Concentration Agarose Gels,” ASME J. Biomech. Eng., 121, pp. 184–187.
Baer,  E., Cassidy,  J. J., and Hiltner,  A., 1991, “Hierarchical Structure of Collagen Composite Systems,” Pure Appl. Chem., 63, pp. 961–973.
Birk D. E., Silver F. H., and Trelstad R. L., 1991, “Matrix Assembly,” The Cell Biology of the Extracellular Matrix, 2nd Edition, ed., E. D. Hay, Academic Press, Inc., New York, pp. 221.
Voytik-Harbin,  S. L., Brightman,  A. O., Waisner,  B. Z., Robinson,  J. P., and Lamar,  C. H., 1998, “Small Intestinal Submucosa: A Tissue-Derived Extracellular Matrix that Promotes Tissue-Specific Growth and Differentiation of Cells In Vitro,” Tissue Eng., 4, pp. 157–174.
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., 1, pp. 375–390.
Abrahams,  M., 1967, “Mechanical Behavior of Tendon In Vitro,” Med. Biol. Eng., 5, pp. 433–443.
Diamant,  J., Keller,  A., Baer,  E., Litt,  M., and Arridge,  R. G. C., 1972, “Collagen; Ultrastructure and its Relation to Mechanical Properties as a Function of Aging,” Proc. R. Soc. London, Ser. B, 180, pp. 293–315.
Folkhard,  W. E., Mosler,  E., Geerken,  E., Knorzer,  E., Nemetschek-Gonsler,  H., Nemetschek,  T., and Koch,  M. H., 1986, “Quantitative Analysis of the Molecular Sliding Mechanism in Native Tendon Collagen—Time-Resolved Dynamic Studies Using Synchrotron Radiation,” Int. J. Biol. Macromol., 9, pp. 169–175.
Fung, Y. C., 1993, Biomechanics: Mechanical Properties of Living Tissues, Springer-Verlag, New York, NY.
Haut,  R. C., and Little,  R. W., 1972, “A Constitutive Equation for Collagen Fibers,” J. Biomech., 5, pp. 423–430.
Kato,  Y. P., Christiansen,  D. L., Hahn,  R. A., Shieh,  S-J., Goldstein,  J. D., and Silver,  F. H., 1989, “Mechanical Properties of Collagen Fibers: A Comparison of Reconstituted and Rat Tail Tendon Fibers,” Biomaterials, 10, pp. 38–42.
Comper,  W. D., and Veis,  A., 1977, “Characterization of Nuclei in In Vitro Collagen Fibril Formation,” Biopolymers, 16, pp. 2133–2142.
Snowden,  J. M., and Swann,  D. A., 1979, “The Formation and Thermal Stability of In Vitro Assemble Fibrils From Acid-Soluble and Pepsin Treated Collagens,” Biochim. Biophys. Acta, 580, pp. 372–381.
Callister, W. D., Jr., 1994, Material Science and Engineering: An Introduction, John Wiley and Sons, New York, NY.

Figures

Grahic Jump Location
Construction of the mold used to prepare collagen matrix test specimens (a). Schematic showing the dimensions of the collagen matrix test specimen with polypropylene mesh reinforcement (b).
Grahic Jump Location
Cut away view of the experimental setup used for mechanical testing of collagen matrices. Collagen matrices were tested while submerged in PBS, pH 7.4 at 37°C.
Grahic Jump Location
Representative stress-strain curve of a collagen matrix (2 mg/mL, pH 7.4) tested at a strain rate of 38.5 percent/min. The stress strain curve can be separated into three distinct regions designated “toe,” “linear,” and “failure.” Determinations of linear modulus, failure stress and failure strain are demonstrated.
Grahic Jump Location
Representative 3D reconstructed confocal reflection image of a matrix prepared from purified type I collagen (1 mg/mL, pH 7.4)
Grahic Jump Location
Confocal reflection images comparing the microstructure of collagen matrices prepared at concentrations of 0.3 mg/mL (a), 1 mg/mL (b), 2 mg/mL (c), and 3 mg/mL (d). An increase in fibril density was observed with increasing collagen concentration (10 μm bar is applicable to all images).
Grahic Jump Location
Confocal reflection images comparing the microstructure of collagen matrices (2 mg/mL) prepared at pH of 6.0 (a), 7.0 (b), 8.0 (c), and 9.0 (d). Both fibril diameter and length were affected by pH. Fibrils formed at lower pH were shorter and thicker than those produced at higher pH (10 μm bar is applicable to all images).
Grahic Jump Location
Time-lapse images demonstrating the tensile testing of a collagen matrix (2 mg/mL, pH 7.4) at a strain rate of 38.5 percent/min
Grahic Jump Location
Effect of polymerization time on the linear modulus, failure stress and failure strain of 1.0 mg/mL (▴), 2.0 mg/mL (•), and 3.0 mg/mL (▪) collagen matrices (pH 7.4) tested at a strain rate of 38.5 percent/min. Exponential curve fits are shown for the linear modulus and failure stress data.
Grahic Jump Location
Effect of polymerization time on the linear modulus, failure stress and failure strain of pH 6.0 (▾), pH 7.4 (•), and pH 9.0 (♦) collagen matrices (2.0 mg/mL) tested at a strain rate of 38.5 percent/min. Exponential curve fits are shown for the linear modulus and failure stress data.
Grahic Jump Location
Effect of collagen concentration (0.3–3.0 mg/mL) on the linear modulus (•), failure stress (♦), and failure strain (○) of collagen matrices (pH 7.4) tested at 38.5 percent/min
Grahic Jump Location
Effect of phosphate buffer pH (6.0–9.0) on the linear modulus (•), failure stress (♦), and failure strain (○) of collagen matrices (2 mg/mL) tested at a strain rate of 38.5 percent/min
Grahic Jump Location
Effect of strain rate (19.2–385 percent/min) on the linear modulus (•), failure stress (♦), and failure strain (○) of collagen matrices (2 mg/mL, pH 7.4)
Grahic Jump Location
Comparison of “true” stress (approximated) and “engineering” stress (calculated) as a function of strain for a collagen matrix (2mg/mL, pH 7.4)

Tables

Errata

Discussions

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In