Collagen pp 133-154 | Cite as

Viscoelasticity, Energy Storage and Transmission and Dissipation by Extracellular Matrices in Vertebrates

  • F.H. Silver
  • W.J. Landis


The extracellular matrix (ECM) of vertebrates is an important biological mechanotransducer that prevents premature mechanical failure of tissues and stores and transmits energy created by muscular deformation. It also transfers large amounts of excess energy to muscles for dissipation as heat, and in some cases, the ECM itself dissipates energy locally. Beyond these functions, ECMs regulate their size and shape as a result of the changing external loads. Changes in tissue metabolism are transduced into increases or decreases in synthesis and catabolism of the components of ECMs. Viscoelasticity is an important feature of the mechanical behavior of ECMs. This parameter, however, complicates the understanding of ECM behavior since it contains both viscous and elastic contributions in most real-time measurements made on vertebrate tissues.

The purpose of this chapter is to examine how time-dependent (viscous) and timeindependent (elastic) mechanical behaviors of an ECMare related to the hierarchical structure of vertebrate tissues and the macromolecular components found in specific tissues. In most ECMs, energy storage is believed to involve elastic stretching of collagen triple helices found in the cross-linked collagen fibrils comprising vertebrate connective tissues, and energy dissipation is believed to involve sliding of such collagen fibrils by each other during tissue deformation. It may be concluded that viscoelasticity differs markedly among different ECMs and is related to ECM hierarchical structure at the molecular and supramolecular levels of any particular vertebrate tissue.


Articular Cartilage Strain Curve Elastic Stress Viscoelastic Behavior Viscous Stress 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander R M (1983) Animal Mechanics (2nd ed.). Blackwell Scientific, Oxford, UK.Google Scholar
  2. Alexander R M (1984) Elastic energy stores in running vertebrates. A. Zool. 24, 85–94.Google Scholar
  3. Arnoczky S P (1992) Gross and vascular anatomy of the meniscus and its role in meniscal healing, regeneration, and remodeling. In: Mow V C, Arnoczky S P, and Jackson D W (Eds.), Knee Meniscus: Basic and Clinical Foundations, Raven Press, New York, pp. 1–14.Google Scholar
  4. Birk D E, Zycband E I, Winkelmann D A, Trelstad R L (1989) Collagen fibrillogenesis in situ: Fibril segments are intermediates in matrix assembly. Proc. Natl. Acad. Sci. U S A 86:4549–4553.CrossRefGoogle Scholar
  5. Christiansen D L, Huang E K, Silver F H (2000) Assembly of type I collagen: Fusions of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 19:409–420.CrossRefGoogle Scholar
  6. Dunn M G, Silver F H (1983) Viscoelastic behavior of human connective tissue: Relative contribution of viscous and elastic components. Connect. Tissue Res. 12: 59–70.CrossRefGoogle Scholar
  7. Freeman J W, Silver, F H (2004a) Analysis of mineral deposition in turkey tendons and self-assembled collagen fibers using mechanical techniques. Connect. Tissue Res. 45: 131–141.CrossRefGoogle Scholar
  8. Freeman J W, Silver F H (2004b) Elastic energy storage in unimineralized and mineralized extracellular matrices (ECMs): A comparison between molecular modeling and experimental measurements. J. Theor. Biol. 229: 371–381.CrossRefGoogle Scholar
  9. Freeman J W, Silver F H (2005) The effects of prestrain on in vitro mineralization of self-assembled collagen fibers. Connect. Tissue Res. 46: 107–155.CrossRefGoogle Scholar
  10. Landis W J, Silver, F H (2002) The structure and function of normally mineralizing tendons. Comp. Biochem. Physiol. A, 133: 1135–1157.CrossRefGoogle Scholar
  11. Landis W J, Silver F H, Freeman J (2006) Collagen as a scaffold for biomimetic mineralization of vertebrate tissues. J. Mater. Chem. 16: 1495–1503.CrossRefGoogle Scholar
  12. McBride D J (1984) Hind Limb Extensor Tendon Development in the Chick: A Light and Transmission Electron Microscopic Study. M.S. Thesis in Physiology, Rutgers University, Piscataway, NJ.Google Scholar
  13. McBride D J, Hahn R, Silver F H (1985) Morphological characterization of tendon development during chick embryogenesis: Measurement of birefringence retardation. Int. J. Biol. Macromol. 7: 71–76.CrossRefGoogle Scholar
  14. McBride D J, Trelstad R L, Silver, F H (1988) Structural and mechanical assessment of developing chick tendon. Int. J. Biol. Macromol. 10: 194–200.CrossRefGoogle Scholar
  15. Mosler E, Folkhard W, Knorzer E., Nemetschek-Gansler H, Nemetschek T H, Koch M H (1985) Stress-induced molecular arrangement in tendon collagen. J. Mol. Biol. 182: 589–596.CrossRefGoogle Scholar
  16. Paterlini M G, Nemethy G, Scheraga H A (1995) The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers 35: 607–619.CrossRefGoogle Scholar
  17. Rigby B J (1964) Effect of cyclic extension on the physical properties of tendon collagen and its possible relation to biological aging of collagen. Nature 202: 1072–1074.CrossRefGoogle Scholar
  18. Schoenfeld A, Landis W J, Kay D. (2007) Meniscal tissue engineering. Am. J. Orthop. 36:614–620.Google Scholar
  19. Seehra G P, Silver F H (2006) Viscoelastic properties of acid- and alkaline-treated human dermis: A correlation between total surface charge and elastic modulus. Skin Res. Technol. 12:190–198.CrossRefGoogle Scholar
  20. Silver, F H (2006) Mechanosensing and Mechanochemical Transduction in Extracellular Matrix: Biological, Chemical, Engineering and Physiological Aspects, Springer, New York.Google Scholar
  21. Silver F H, Birk D E (1984) Molecular structure of collagen in solution: Comparison of types I, II, III, and V. Int. J. Biol. Macromol. 6: 125–132.CrossRefGoogle Scholar
  22. Silver F H, Bradica G (2002) Mechanobiology of cartilage: how do internal and external stresses affect mechanochemical transduction and elastic energy storage? Biomechanics & Modeling in Mechanobiology 1: 1–19.CrossRefGoogle Scholar
  23. Silver F H, Christiansen D L (1999) Biomaterials Science and Biocompatibility, Chapter 6, Springer, New York.Google Scholar
  24. Silver F H, Siperko L M (2003) Mechanosensing and mechanochemical transduction. Crit. Rev. Biomed. Eng. 31: 255–331.CrossRefGoogle Scholar
  25. Silver F H, Christiansen D L, Snowhill P, Chen Y (2000) Role of storage on changes in the mechanical properties of tendon and self-assembled collagen fibers. Connect. Tissue Res. 41: 155–164.CrossRefGoogle Scholar
  26. Silver F H, Christiansen D L, Snowhill P B, Chen Y (2001a) Transition from viscous to elastic-based dependency of mechanical properties of self-assembled type I collagen fibers. J. Appl. Polym. Sci. 79: 134–142.CrossRefGoogle Scholar
  27. Silver F H, Freeman J W, Horvath I, Landis W J (2001b) Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules 2: 750–756.CrossRefGoogle Scholar
  28. Silver F H, Freeman J, DeVore D (2001c) Viscoelastic properties of human skin and processed dermis. Skin Res. Technol. 7: 18–25.CrossRefGoogle Scholar
  29. Silver F H, Horvath I, Foran D (2001d) Viscoelasticity of the vessel wall: Role of collagen and elastic fibers. Crit. Rev. Biomed. Eng. 29: 279–301.Google Scholar
  30. Silver F H, Bradica G, Tria A (2001e) Relationship among biomechanical, biochemical and cellular changes associated with osteoarthritis. Crit. Rev. Biomed. Eng. 29: 373–391.Google Scholar
  31. Silver F H, Bradica G, Tria A (2001f) Viscoelastic behavior of osteoarthritic cartilage. Connect. Tissue Res. 42: 223–233.CrossRefGoogle Scholar
  32. Silver F H, Seehra P, Freeman J W, DeVore D (2002a) Viscoelastic properties of young and old human dermis: Evidence that elastic energy storage occurs in the flexible regions of collagen and elastin. J. Appl. Polym. Sci. 86: 1978–1985.CrossRefGoogle Scholar
  33. Silver F H, Bradica G, Tria A (2002b) Elastic energy storage in human articular cartilage: Estimation of the elastic spring constant for type II collagen and changes associated with osteoarthritis. Matrix Biol. 21: 129–137.CrossRefGoogle Scholar
  34. Silver F H, Ebrahimi A, Snowhill P B (2002c) Viscoelastic properties of self-assembled type I collagen fibers: Molecular basis of elastic and viscous behaviors. Connect. Tissue Res. 43: 1–12.CrossRefGoogle Scholar
  35. Silver F H, Horvath I, Foran D J (2002d) Mechanical implications of the domain structure of fibril forming collagens: Comparison of the molecular and fibrillar flexibility of α -chains found in types I, II and III collagens. J. Theor. Biol. 216: 243–254.CrossRefGoogle Scholar
  36. Silver F H, Siperko L M, Seehra G P (2002e) Mechanobiology of force transduction in dermis. Skin Res. Technol. 8: 1–21.Google Scholar
  37. Silver F H, DeVore D, Siperko L M (2003a) Invited Review: Role of mechanophysiology in aging of ECM: Effects of changes in mechanochemical transduction. J. Appl. Physiol. 95: 2134–2141.Google Scholar
  38. Silver F H, Snowhill P B, Foran D (2003b) Mechanical behavior of vessel wall: A comparative study of aorta, vena cava, and carotid artery. Ann. Biomed. Eng. 31: 793–803.CrossRefGoogle Scholar
  39. Silver F H, Freeman J, Seehra G P (2003c) Collagen self-assembly and development of matrix mechanical properties. J. Biomech. 36: 1529–1553.CrossRefGoogle Scholar
  40. Silver F H, Bradica G., Tria A (2004) Do changes in mechanical properties of articular cartilage alter mechanochemical transduction and promote osteoarthritis? Matrix Biol. 23: 467–476.CrossRefGoogle Scholar
  41. Snowhill P B, Silver F H (2005) A mechanical model of porcine vascular tissues-Part II: Stress–strain and mechanical properties of juvenile porcine blood vessels. Cardiovasc. Eng. 5:157–169.CrossRefGoogle Scholar
  42. Snowhill P B, Foran D J, Silver F H (2004) A mechanical model of porcine vascular tissues-Part I. Determination of macromolecular component arrangement and volume fractions. Cardiovasc. Eng. 4: 281–294.CrossRefGoogle Scholar
  43. Wilson A M, McGuigan M P, Su A, van den Bogert A J (2001) Horses damp the spring in their step. Nature 414: 895–899.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • F.H. Silver
  • W.J. Landis

There are no affiliations available

Personalised recommendations