Cartilage Mechanical Response under Dynamic Compression at Physiological Stress Levels Following Collagenase Digestion

The objective of this study was to test the hypothesis that enzymatic degradation by collagenase significantly reduces dynamic moduli and increases compressive strains of bovine articular cartilage under physiological compressive stress levels and loading frequencies. Twenty-seven distal femoral cartilage plugs (3 mm diameter) were loaded in a custom apparatus under load control, with a load up to 40 N and loading frequencies of 0.1, 1, 10, and 40 Hz, before and after incubation in physiological buffered saline containing various concentrations of collagenase (0, 2, and 10 U/mL). Collagenase digestion reduced the equilibrium Young’s modulus by 49% with 2 U/mL and 61% with 10 U/mL, while the decrease in dynamic modulus at 40 Hz was in the range of 13–20% with 2 U/mL and 24–33% with 10 U/mL, relative to respective controls. The amplitudes of dynamic compressive strains increased from 22 ± 6% to 26 ± 8% at 0.1 Hz and 9.6 ± 3.3% to 13.5 ± 3.2% at 40 Hz, with 10 U/mL collagenase. This experimental study serves to confirm that collagen contributes significantly to the dynamic compressive properties of cartilage, by demonstrating that collagenase digestion impairs these properties, under stress amplitudes and frequencies which are representative of physiological loading conditions.

[1]  G E Kempson,et al.  The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage. , 1976, Biochimica et biophysica acta.

[2]  G. Vunjak‐Novakovic,et al.  Bioreactor studies of native and tissue engineered cartilage. , 2002, Biorheology.

[3]  Xiaohong Bi,et al.  Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage. , 2006, Biochimica et biophysica acta.

[4]  A. Grodzinsky,et al.  Biosynthetic response of cartilage explants to dynamic compression , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[5]  V C Mow,et al.  Effects of proteoglycan extraction on the tensile behavior of articular cartilage , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[6]  V C Mow,et al.  Finite deformation biphasic material properties of bovine articular cartilage from confined compression experiments. , 1997, Journal of biomechanics.

[7]  Mark R. DiSilvestro,et al.  Biphasic Poroviscoelastic Characteristics of Proteoglycan-Depleted Articular Cartilage: Simulation of Degeneration , 2002, Annals of Biomedical Engineering.

[8]  David Rubin,et al.  Introduction to Continuum Mechanics , 2009 .

[9]  R W Mann,et al.  Contact pressures from an instrumented hip endoprosthesis. , 1989, The Journal of bone and joint surgery. American volume.

[10]  V C Mow,et al.  The role of flow-independent viscoelasticity in the biphasic tensile and compressive responses of articular cartilage. , 2001, Journal of biomechanical engineering.

[11]  V. Mow,et al.  A transversely isotropic biphasic model for unconfined compression of growth plate and chondroepiphysis. , 1998, Journal of biomechanical engineering.

[12]  H. Nötzli,et al.  Deformation of articular cartilage collagen structure under static and cyclic loading , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[13]  L. Bonassar,et al.  The role of cartilage streaming potential, fluid flow and pressure in the stimulation of chondrocyte biosynthesis during dynamic compression. , 1995, Journal of biomechanics.

[14]  J Mizrahi,et al.  The "instantaneous" deformation of cartilage: effects of collagen fiber orientation and osmotic stress. , 1986, Biorheology.

[15]  Albert C. Chen,et al.  Mechanical compression modulates proliferation of transplanted chondrocytes , 2000, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[16]  R K Korhonen,et al.  Biomechanical properties of knee articular cartilage. , 2003, Biorheology.

[17]  K J Gooch,et al.  IGF-I and mechanical environment interact to modulate engineered cartilage development. , 2001, Biochemical and biophysical research communications.

[18]  V C Mow,et al.  Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments , 1993, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[19]  G. Vunjak‐Novakovic,et al.  Frontiers in tissue engineering. In vitro modulation of chondrogenesis. , 1999, Clinical orthopaedics and related research.

[20]  Antonios G. Mikos,et al.  Frontiers in tissue engineering , 1998 .

[21]  G A Ateshian,et al.  Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. , 2000, Journal of biomechanical engineering.

[22]  L. S. Matthews,et al.  Load bearing characteristics of the patello-femoral joint. , 1977, Acta orthopaedica Scandinavica.

[23]  R W Farndale,et al.  A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. , 1982, Connective tissue research.

[24]  A Shirazi-Adl,et al.  A fibril-network-reinforced biphasic model of cartilage in unconfined compression. , 1999, Journal of biomechanical engineering.

[25]  L. Bonassar,et al.  Changes in cartilage composition and physical properties due to stromelysin degradation. , 1995, Arthritis and rheumatism.

[26]  Seonghun Park,et al.  Cartilage interstitial fluid load support in unconfined compression. , 2003, Journal of biomechanics.

[27]  B. Obradovic,et al.  Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue‐engineered cartilage , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[28]  H. Stegemann,et al.  Determination of hydroxyproline. , 1967, Clinica chimica acta; international journal of clinical chemistry.

[29]  G A Ateshian,et al.  A Conewise Linear Elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. , 2000, Journal of biomechanical engineering.

[30]  C. Herberhold,et al.  In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading. , 1999, Journal of biomechanics.

[31]  G. Ateshian,et al.  Cartilage interstitial fluid load support in unconfined compression following enzymatic digestion. , 2004, Journal of biomechanical engineering.

[32]  Seonghun Park,et al.  Dynamic response of immature bovine articular cartilage in tension and compression, and nonlinear viscoelastic modeling of the tensile response. , 2006, Journal of biomechanical engineering.

[33]  L. Setton,et al.  Osteoarthritis-like changes and decreased mechanical function of articular cartilage in the joints of mice with the chondrodysplasia gene (cho). , 2003, Arthritis and rheumatism.

[34]  G A Ateshian,et al.  Mechanical response of bovine articular cartilage under dynamic unconfined compression loading at physiological stress levels. , 2004, Osteoarthritis and cartilage.

[35]  H. Helminen,et al.  Characterization of enzymatically induced degradation of articular cartilage using high frequency ultrasound. , 1999, Physics in medicine and biology.

[36]  Y. Zheng,et al.  Measurement of the layered compressive properties of trypsintreated articular cartilage: An ultrasound investigation , 2006, Medical and Biological Engineering and Computing.

[37]  E B Hunziker,et al.  Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. , 1999, Archives of biochemistry and biophysics.