Table of Contents Author Guidelines Submit a Manuscript
Computational and Mathematical Methods in Medicine
Volume 2013, Article ID 164146, 14 pages
http://dx.doi.org/10.1155/2013/164146
Research Article

Superficial Collagen Fibril Modulus and Pericellular Fixed Charge Density Modulate Chondrocyte Volumetric Behaviour in Early Osteoarthritis

1Department of Applied Physics, University of Eastern Finland, P.O. Box 1627, 70211 Kuopio, Finland
2Fischell Department of Bioengineering, A.J. Clark School of Engineering, University of Maryland, College Park, MD 20742, USA
3Department of Clinical Neurophysiology, Kuopio University Hospital, 70211 Kuopio, Finland
4Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada T2N 1N4
5Mechanical and Manufacturing Engineering, Schulich School of Engineering, University of Calgary, Calgary, AB, Canada T2N 1N4

Received 18 October 2012; Revised 7 January 2013; Accepted 22 January 2013

Academic Editor: C. C. Van Donkelaar

Copyright © 2013 Petri Tanska et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. P. A. Arokoski, J. S. Jurvelin, U. Väätäinen, and H. J. Helminen, “Normal and pathological adaptations of articular cartilage to joint loading,” Scandinavian Journal of Medicine and Science in Sports, vol. 10, no. 4, pp. 186–198, 2000. View at Google Scholar · View at Scopus
  2. J. A. Buckwalter and H. J. Mankin, “Articular cartilage. Part II: degeneration and osteoarthrosis, repair, regeneration, and transplantation,” Journal of Bone and Joint Surgery A, vol. 79, no. 4, pp. 612–632, 1997. View at Google Scholar · View at Scopus
  3. S. Saarakkala, P. Julkunen, P. Kiviranta, J. Mäkitalo, J. S. Jurvelin, and R. K. Korhonen, “Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics,” Osteoarthritis and Cartilage, vol. 18, no. 1, pp. 73–81, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. R. L. Sah, A. S. Yang, A. C. Chen et al., “Physical properties of rabbit articular cartilage after transection of the anterior cruciate ligament,” Journal of Orthopaedic Research, vol. 15, no. 2, pp. 197–203, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Yoshioka, R. D. Coutts, D. Amiel, and S. A. Hacker, “Characterization of a model of osteoarthritis in the rabbit knee,” Osteoarthritis and Cartilage, vol. 4, no. 2, pp. 87–98, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Guilak, A. Ratcliffe, N. Lane, M. P. Rosenwasser, and V. C. Mow, “Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis,” Journal of Orthopaedic Research, vol. 12, no. 4, pp. 474–484, 1994. View at Publisher · View at Google Scholar · View at Scopus
  7. X. Bi, X. Yang, M. P. G. Bostrom, and N. P. Camacho, “Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage,” Biochimica et Biophysica Acta, vol. 1758, no. 7, pp. 934–941, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. L. G. Alexopoulos, M. A. Haider, T. P. Vail, and F. Guilak, “Alterations in the mechanical properties of the human chondrocyte pericellular matrix with osteoarthritis,” Journal of Biomechanical Engineering, vol. 125, no. 3, pp. 323–333, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. L. G. Alexopoulos, G. M. Williams, M. L. Upton, L. A. Setton, and F. Guilak, “Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage,” Journal of Biomechanics, vol. 38, no. 3, pp. 509–517, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. R. K. Korhonen, P. Julkunen, J. S. Jurvelin, and S. Saarakkala, “Structural and compositional changes in peri- and extracellular matrix of osteoarthritic cartilage modulate chondrocyte morphology,” Cellular and Molecular Bioengineering, vol. 4, no. 3, pp. 484–494, 2011. View at Google Scholar
  11. J. P. G. Urban and M. T. Bayliss, “Regulation of proteoglycan synthesis rate in cartilage in vitro: influence of extracellular ionic composition,” Biochimica et Biophysica Acta, vol. 992, no. 1, pp. 59–65, 1989. View at Google Scholar · View at Scopus
  12. J. P. G. Urban, A. C. Hall, and K. A. Gehl, “Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes,” Journal of Cellular Physiology, vol. 154, no. 2, pp. 262–270, 1993. View at Publisher · View at Google Scholar · View at Scopus
  13. M. D. Buschmann, E. B. Hunziker, Y. J. Kim, and A. J. Grodzinsky, “Altered aggrecan synthesis correlates with cell and nucleus structure in statically compressed cartilage,” Journal of Cell Science, vol. 109, no. 2, pp. 499–508, 1996. View at Google Scholar · View at Scopus
  14. T. M. Quinn, A. J. Grodzinsky, M. D. Buschmann, Y. J. Kim, and E. B. Hunziker, “Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants,” Journal of Cell Science, vol. 111, no. 5, pp. 573–583, 1998. View at Google Scholar · View at Scopus
  15. M. D. Buschmann, Y. A. Gluzband, A. J. Grodzinsky, and E. B. Hunziker, “Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture,” Journal of Cell Science, vol. 108, no. 4, pp. 1497–1508, 1995. View at Google Scholar · View at Scopus
  16. R. B. Lee, R. J. Wilkins, S. Razaq, and J. P. G. Urban, “The effect of mechanical stress on cartilage energy metabolism,” Biorheology, vol. 39, no. 1-2, pp. 133–143, 2002. View at Google Scholar · View at Scopus
  17. F. Guilak, L. G. Alexopoulos, M. L. Upton et al., “The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage,” Annals of the New York Academy of Sciences, vol. 1068, no. 1, pp. 498–512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Julkunen, W. Wilson, J. S. Jurvelin, and R. K. Korhonen, “Composition of the pericellular matrix modulates the deformation behaviour of chondrocytes in articular cartilage under static loading,” Medical and Biological Engineering and Computing, vol. 47, no. 12, pp. 1281–1290, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Guilak, W. R. Jones, H. P. Ting-Beall, and G. M. Lee, “The deformation behavior and mechanical properties of chondrocytes in articular cartilage,” Osteoarthritis and Cartilage, vol. 7, no. 1, pp. 59–70, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. S. K. Han, S. Federico, and W. Herzog, “A depth-dependent model of the pericellular microenvironment of chondrocytes in articular cartilage,” Computer Methods in Biomechanics and Biomedical Engineering, vol. 14, no. 7, pp. 657–664, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. C. A. Poole, “Articular cartilage chondrons: form, function and failure,” Journal of Anatomy, vol. 191, no. 1, pp. 1–13, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. S. M. Turunen, S.-K. Han, W. Herzog, and R. K. Korhonen, “Cell deformation behavior in mechanically loaded rabbit articular cartilage 4 weeks after anterior cruciate ligament transection,” Osteoarthritis Cartilage, vol. 21, no. 3, pp. 505–513, 2013. View at Publisher · View at Google Scholar
  23. S. K. Han, R. Seerattan, and W. Herzog, “Mechanical loading of in situ chondrocytes in lapine retropatellar cartilage after anterior cruciate ligament transection,” Journal of the Royal Society Interface, vol. 7, no. 47, pp. 895–903, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. R. K. Korhonen, P. Julkunen, W. Wilson, and W. Herzog, “Importance of collagen orientation and depth-dependent fixed charge densities of cartilage on mechanical behavior of chondrocytes,” Journal of Biomechanical Engineering, vol. 130, no. 2, Article ID 021003, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Tanska, P. Julkunen, and R. K. Korhonen, “Collagen fibrils of articular cartilage modulate cell deformations in early osteoarthritis,” in Transactions of the Orthopaedic Research Society, vol. 36, p. 2174, 2011. View at Google Scholar
  26. R. K. Korhonen and W. Herzog, “Depth-dependent analysis of the role of collagen fibrils, fixed charges and fluid in the pericellular matrix of articular cartilage on chondrocyte mechanics,” Journal of Biomechanics, vol. 41, no. 2, pp. 480–485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. C. C. van Donkelaar and W. Wilson, “Mechanics of chondrocyte hypertrophy,” Biomech Model Mechanobiol, vol. 11, no. 5, pp. 655–664, 2011. View at Publisher · View at Google Scholar
  28. F. Guilak, A. Ratcliffe, and V. C. Mow, “Chondrocyte deformation and local tissue strain in articular cartilage: a confocal microscopy study,” Journal of Orthopaedic Research, vol. 13, no. 3, pp. 410–421, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. S. K. Han, P. Colarusso, and W. Herzog, “Confocal microscopy indentation system for studying in situ chondrocyte mechanics,” Medical Engineering and Physics, vol. 31, no. 8, pp. 1038–1042, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Király, M. M. Hyttinen, T. Lapveteläinen et al., “Specimen preparation and quantification of collagen birefringence in unstained sections of articular cartilage using image analysis and polarizing light microscopy,” Histochemical Journal, vol. 29, no. 4, pp. 317–327, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Rieppo, J. Hallikainen, J. S. Jurvelin, I. Kiviranta, H. J. Helminen, and M. M. Hyttinen, “Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage,” Microscopy Research and Technique, vol. 71, no. 4, pp. 279–287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Rieppo, M. M. Hyttinen, E. Halmesmaki et al., “Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation,” Osteoarthritis and Cartilage, vol. 17, no. 4, pp. 448–455, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Mäkitalo, S. Saarakkala, L. Rieppo, S. K. Han, W. Herzog, and R. K. Korhonen, “Can collagen fibrillation or proteoglycan depletion of cartilage explain changed deformation behavior of chondrocytes 9 weeks after anterior cruciate ligament transaction?” in Transactions of the Orthopaedic Research Society, vol. 36, p. 2026, 2011. View at Publisher · View at Google Scholar
  34. I. Kiviranta, J. Jurvelin, and M. Tammi, “Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O,” Histochemistry, vol. 82, no. 3, pp. 249–255, 1985. View at Google Scholar · View at Scopus
  35. K. Király, T. Lapveteläinen, J. Arokoski et al., “Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry,” Histochemical Journal, vol. 28, no. 8, pp. 577–590, 1996. View at Google Scholar · View at Scopus
  36. H. E. Panula, M. M. Hyttinen, J. P. A. Arokoski et al., “Articular cartilage superficial zone collagen birefringence reduced and cartilage thickness increased before surface fibrillation in experimental osteoarthritis,” Annals of the Rheumatic Diseases, vol. 57, no. 4, pp. 237–245, 1998. View at Google Scholar · View at Scopus
  37. J. Rieppo, J. Töyräs, M. T. Nieminen et al., “Structure-function relationships in enzymatically modified articular cartilage,” Cells Tissues Organs, vol. 175, no. 3, pp. 121–132, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. S. M. Turunen, M. J. Lammi, S. Saarakkala et al., “The effect of collagen degradation on chondrocyte volume and morphology in bovine articular cartilage following a hypotonic challenge,” Biomechanics and Modeling in Mechanobiology. In press. View at Publisher · View at Google Scholar
  39. W. Wilson, C. C. Van Donkelaar, B. Van Rietbergen, and R. Huiskes, “A fibril-reinforced poroviscoelastic swelling model for articular cartilage,” Journal of Biomechanics, vol. 38, no. 6, pp. 1195–1204, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Benninghoff, “Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion—Erste Mitteilung: die modellierenden und formerhaltenden Faktoren des Knorpelreliefs,” Zeitschrift für Anatomie und Entwicklungsgeschichte, vol. 76, no. 1–3, pp. 43–63, 1925. View at Publisher · View at Google Scholar · View at Scopus
  41. W. Wilson, J. M. Huyghe, and C. C. van Donkelaar, “A composition-based cartilage model for the assessment of compositional changes during cartilage damage and adaptation,” Osteoarthritis and Cartilage, vol. 14, no. 6, pp. 554–560, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. A. van der Voet, “A comparison of finite element codes for the solution of biphasic poroelastic problems,” Proceedings of the Institution of Mechanical Engineers, vol. 211, no. 2, pp. 209–211, 1997. View at Google Scholar · View at Scopus
  43. J. M. Huyghe, G. B. Houben, M. R. Drost, and C. C. van Donkelaar, “An ionised/non-ionised dual porosity model of intervertebral disc tissue,” Biomech Model Mechanobiol, vol. 2, no. 1, pp. 3–19, 2003. View at Google Scholar
  44. W. M. Lai, J. S. Hou, and V. C. Mow, “A triphasic theory for the swelling and deformation behaviors of articular cartilage,” Journal of Biomechanical Engineering, vol. 113, no. 3, pp. 245–258, 1991. View at Google Scholar · View at Scopus
  45. N. P. Camacho, P. West, P. A. Torzilli, and R. Mendelsohn, “FTIR microscopic imaging of collagen and proteoglycan in bovine cartilage,” Biopolymers, vol. 62, no. 1, pp. 1–8, 2001. View at Google Scholar
  46. K. Potter, L. H. Kidder, I. W. Levin, E. N. Lewis, and R. G. Spencer, “Imaging of collagen and proteoglycan in cartilage sections using fourier transform infrared spectral imaging,” Arthritis & Rheumatism, vol. 44, no. 4, pp. 846–855, 2001. View at Google Scholar
  47. P. Julkunen, P. Kiviranta, W. Wilson, J. S. Jurvelin, and R. K. Korhonen, “Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model,” Journal of Biomechanics, vol. 40, no. 8, pp. 1862–1870, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Guilak, G. R. Erickson, and H. P. Ting-Beall, “The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes,” Biophysical Journal, vol. 82, no. 2, pp. 720–727, 2002. View at Google Scholar · View at Scopus
  49. W. M. Lai, D. D. Sun, G. A. Ateshian, X. E. Guo, and V. C. Mow, “Electrical signals for chondrocytes in cartilage,” Biorheology, vol. 39, no. 1-2, pp. 39–45, 2002. View at Google Scholar · View at Scopus
  50. M. Likhitpanichkul, X. E. Guo, and V. C. Mow, “The effect of matrix tension-compression nonlinearity and fixed negative charges on chondrocyte responses in cartilage,” MCB Molecular and Cellular Biomechanics, vol. 2, no. 4, pp. 191–204, 2005. View at Google Scholar · View at Scopus
  51. V. C. Mow and A. Ratcliffe, “Structure and function of articular cartilage and meniscus,” in Basic Orthopaedic Biomechanics & Mechano-Biology, V. C. Mow and R. Huiskes, Eds., pp. 181–258, Lippincott Williams & Wilkins, Philadelphia, PA, USA, 2005. View at Google Scholar
  52. P. J. Basser, R. Schneiderman, R. A. Bank, E. Wachtel, and A. Maroudas, “Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique,” Archives of Biochemistry and Biophysics, vol. 351, no. 2, pp. 207–219, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. A. I. Maroudas, “Balance between swelling pressure and collagen tension in normal and degenerate cartilage,” Nature, vol. 260, no. 5554, pp. 808–809, 1976. View at Google Scholar · View at Scopus
  54. A. Maroudas and C. Bannon, “Measurement of swelling pressure in cartilage and comparison with osmotic pressure of constituent proteoglycans,” Biorheology, vol. 18, no. 3-6, pp. 619–632, 1981. View at Google Scholar · View at Scopus
  55. H. J. Mankin, H. Dorfman, L. Lippiello, and A. Zarins, “Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data,” Journal of Bone and Joint Surgery A, vol. 53, no. 3, pp. 523–537, 1971. View at Google Scholar · View at Scopus
  56. H. J. Mankin, M. E. Johnson, and L. Lippiello, “Biochemical and metabolic abnormalities in articular cartilage from osteoarthritic human hips. III. Distribution and metabolism of amino sugar-containing macromolecules,” Journal of Bone and Joint Surgery A, vol. 63, no. 1, pp. 131–139, 1981. View at Google Scholar · View at Scopus
  57. G. Venn, M. E. J. Billingham, and T. E. Hardingham, “Increased proteoglycan synthesis in cartilage in experimental canine osteoarthritis does not reflect a permanent change in chondrocyte phenotype,” Arthritis and Rheumatism, vol. 38, no. 4, pp. 525–532, 1995. View at Publisher · View at Google Scholar · View at Scopus
  58. J. D. Sandy, M. E. Adams, and M. E. J. Billingham, “In vivo and in vitro stimulation of chondrocyte biosynthetic activity in early experimental osteoarthritis,” Arthritis and Rheumatism, vol. 27, no. 4, pp. 388–397, 1984. View at Google Scholar · View at Scopus
  59. I. Youn, J. B. Choi, L. Cao, L. A. Setton, and F. Guilak, “Zonal variations in the three-dimensional morphology of the chondron measured in situ using confocal microscopy,” Osteoarthritis and Cartilage, vol. 14, no. 9, pp. 889–897, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. P. G. Bush and A. C. Hall, “Passive osmotic properties of in situ human articular chondrocytes within non-degenerate and degenerate cartilage,” Journal of Cellular Physiology, vol. 204, no. 1, pp. 309–319, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. J. M. Huyghe and W. Wilson, “On the thermodynamical admissibility of the triphasic theory of charged hydrated tissues,” Journal of Biomechanical Engineering, vol. 131, no. 4, Article ID 044504, 5 pages, 2009. View at Publisher · View at Google Scholar