Maturation of collagen fibril network structure in tibial and femoral cartilage of rabbits

Osteoarthritis and Cartilage

Volumn 18, Issue 3, 2010, Pages 406-415

  Julkunen, P ^a   Iivarinen, J ^b   Brama, P A ^c   Arokoski, J ^a,b   Jurvelin, J S ^b   Helminen, H J ^b  

^a KUOPIO UNIVERSITY HOSPITAL   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Anisotropy; Articular cartilage; Collagen; Maturation; Polarized light microscopy

Indexed keywords

COLLAGEN; PROTEOGLYCAN;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANISOTROPY; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CONTROLLED STUDY; DEVELOPMENT; FEMALE; FEMUR; GENE REGULATORY NETWORK; MATURATION; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN STRUCTURE; RABBIT; STRUCTURE ANALYSIS; THICKNESS; TIBIA; TISSUE GROWTH;

AGE FACTORS; AGING; ANIMALS; ANISOTROPY; CARTILAGE, ARTICULAR; COLLAGEN; FEMALE; FEMUR; MICROSCOPY, POLARIZATION; RABBITS; STATISTICS AS TOPIC; TIBIA;

EID: 76549094981     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2009.11.007     Document Type: Article

References (50)

1. Jeffery A.K., Blunn G.W., Archer C.W., and Bentley G. Three-dimensional collagen architecture in bovine articular cartilage. J Bone Joint Surg [Br] 73 (1991) 795-801
2. Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Function. Z Zellforsch Mikrosk Anat 2 (1925) 783-862
3. Julkunen P., Kiviranta P., Wilson W., Jurvelin J.S., and Korhonen R.K. Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model. J Biomech 40 (2007) 1862-1870
4. Julkunen P., Korhonen R.K., Nissi M.J., and Jurvelin J.S. Mechanical characterization of articular cartilage by combining magnetic resonance imaging and finite-element analysis-a potential functional imaging technique. Phys Med Biol 53 (2008) 2425-2438
5. Brommer H., Brama P.A., Laasanen M.S., Helminen H.J., van Weeren P.R., and Jurvelin J.S. Functional adaptation of articular cartilage from birth to maturity under the influence of loading: a biomechanical analysis. Equine Vet J 37 (2005) 148-154
6. Brama P.A., Tekoppele J.M., Bank R.A., Barneveld A., and van Weeren P.R. Functional adaptation of equine articular cartilage: the formation of regional biochemical characteristics up to age one year. Equine Vet J 32 (2000) 217-221
7. Rieppo J., Hyttinen M.M., Halmesmäki E., Ruotsalainen H., Vasara A., Kiviranta I., et al. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. Osteoarthritis Cartilage 17 (2009) 448-455
8. Armstrong C.G., and Mow V.C. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. J Bone Joint Surg Am 64 (1982) 88-94
9. Simunek Z., and Muir H. Changes in the protein-polysaccharides of pig articular cartilage during prenatal life, development and old age. Biochem J 126 (1972) 515-523
10. Kiviranta P., Rieppo J., Korhonen R.K., Julkunen P., Töyräs J., and Jurvelin J.S. Collagen network primarily controls the Poisson's ratio of bovine articular cartilage in compression. J Orthop Res 24 (2006) 690-699
11. Nieminen M.T., Rieppo J., Töyräs J., Hakumaki J.M., Silvennoinen J., Hyttinen M.M., et al. T2 relaxation reveals spatial collagen architecture in articular cartilage: a comparative quantitative MRI and polarized light microscopic study. Magn Reson Med 46 (2001) 487-493
12. Grunder W. MRI assessment of cartilage ultrastructure. NMR Biomed 19 (2006) 855-876
13. Nissi M.J., Rieppo J., Töyräs J., Laasanen M.S., Kiviranta I., Jurvelin J.S., et al. T(2) relaxation time mapping reveals age- and species-related diversity of collagen network architecture in articular cartilage. Osteoarthritis Cartilage 14 (2006) 1265-1271
14. Brama P.A., TeKoppele J.M., Bank R.A., Barneveld A., and van Weeren P.R. Development of biochemical heterogeneity of articular cartilage: influences of age and exercise. Equine Vet J 34 (2002) 265-269
15. Julkunen P., Harjula T., Iivarinen J., Marjanen J., Seppänen K., Närhi T., et al. Biomechanical, biochemical and structural correlations in immature and mature rabbit articular cartilage. Osteoarthritis Cartilage 17 (2009) 1626-1636
16. Hunziker E.B., Kapfinger E., and Geiss J. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthritis Cartilage 15 (2007) 403-413
17. Brama P.A., Tekoppele J.M., Bank R.A., Karssenberg D., Barneveld A., and van Weeren P.R. Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint. Equine Vet J 32 (2000) 19-26
18. Jurvelin J.S., Arokoski J.P., Hunziker E.B., and Helminen H.J. Topographical variation of the elastic properties of articular cartilage in the canine knee. J Biomech 33 (2000) 669-675
19. Julkunen P., Harjula T., Marjanen J., Helminen H.J., and Jurvelin J.S. Comparison of single-phase isotropic elastic and fibril-reinforced poroelastic models for indentation of rabbit articular cartilage. J Biomech 42 (2009) 652-656
20. Kiviranta P., Lammentausta E., Töyräs J., Kiviranta I., and Jurvelin J.S. Indentation diagnostics of cartilage degeneration. Osteoarthritis Cartilage 16 (2008) 796-804
21. Kiviranta P., Lammentausta E., Töyräs J., Nieminen H.J., Julkunen P., Kiviranta I., et al. Differences in acoustic properties of intact and degenerated human patellar cartilage during compression. Ultrasound Med Biol 35 (2009) 1367-1375
22. Julkunen P., Korhonen R.K., Herzog W., and Jurvelin J.S. Uncertainties in indentation testing of articular cartilage: a fibril-reinforced poroviscoelastic study. Med Eng Phys 30 (2008) 506-515
23. Korhonen R.K., Julkunen P., Wilson W., and Herzog W. Importance of collagen orientation and depth-dependent fixed charge densities of cartilage on mechanical behavior of chondrocytes. J Biomech Eng 130 (2008) 021003
24. Quinn T.M., Hunziker E.B., and Hauselmann H.J. Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee. Osteoarthritis Cartilage 13 (2005) 672-678
25. Buschmann M.D., Hunziker E.B., Kim Y.J., and Grodzinsky A.J. Altered aggrecan synthesis correlates with cell and nucleus structure in statically compressed cartilage. J Cell Sci 109 Pt 2 (1996) 499-508
26. Buschmann M.D., Kim Y.J., Wong M., Frank E., Hunziker E.B., and Grodzinsky A.J. Stimulation of aggrecan synthesis in cartilage explants by cyclic loading is localized to regions of high interstitial fluid flow. Arch Biochem Biophys 366 (1999) 1-7
27. Quinn T.M., Grodzinsky A.J., Buschmann M.D., Kim Y.J., and Hunziker E.B. Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J Cell Sci 111 Pt 5 (1998) 573-583
28. Rieppo J., Hallikainen J., Jurvelin J.S., Kiviranta I., Helminen H.J., and Hyttinen M.M. Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage. Microsc Res Tech 71 (2008) 279-287
29. Király K., Hyttinen M.M., Lapveteläinen T., Elo M., Kiviranta I., Dobai J., et al. Specimen preparation and quantification of collagen birefringence in unstained sections of articular cartilage using image analysis and polarizing light microscopy. Histochem J 29 (1997) 317-327
30. Xia Y. Averaged and depth-dependent anisotropy of articular cartilage by microscopic imaging. Semin Arthritis Rheum 37 (2008) 317-327
31. Kuroki H., Nakagawa Y., Mori K., Kobayashi M., Yasura K., Okamoto Y., et al. Maturation-dependent change and regional variations in acoustic stiffness of rabbit articular cartilage: an examination of the superficial collagen-rich zone of cartilage. Osteoarthritis Cartilage 14 (2006) 784-792
32. Brama P.A., Holopainen J., van Weeren P.R., Firth E.C., Helminen H.J., and Hyttinen M.M. Effect of loading on the organization of the collagen fibril network in juvenile equine articular cartilage. J Orthop Res 27 (2009) 1226-1234
33. Hughes L.C., Archer C.W., and ap Gwynn I. The ultrastructure of mouse articular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review. Eur Cell Mater 9 (2005) 68-84
34. Hyttinen M.M., Arokoski J.P., Parkkinen J.J., Lammi M.J., Lapveteläinen T., Mauranen K., et al. Age matters: collagen birefringence of superficial articular cartilage is increased in young guinea-pigs but decreased in older animals after identical physiological type of joint loading. Osteoarthritis Cartilage 9 (2001) 694-701
35. Guilak F., Sah R.L., and Setton L.A. Physical regulation of cartilage metabolism. In: Mow V.C., and Hayes W.C. (Eds). Basic Orthopaedic Biomechanics (1997), Lippincott-Raven, Philadelphia 179-207
36. Jin H., and Lewis J.L. Determination of Poisson's ratio of articular cartilage by indentation using different-sized indenters. J Biomech Eng 126 (2004) 138-145
37. Urban J.P. The chondrocyte: a cell under pressure. Br J Rheumatol 33 (1994) 901-908
38. Muir H. The chondrocyte, architect of cartilage. Biomechanics, structure, function and molecular biology of cartilage matrix macromolecules. Bioessays 17 (1995) 1039-1048
39. Arokoski J.P., Hyttinen M.M., Lapveteläinen T., Takacs P., Kosztaczky B., Modis L., et al. Decreased birefringence of the superficial zone collagen network in the canine knee (stifle) articular cartilage after long distance running training, detected by quantitative polarised light microscopy. Ann Rheum Dis 55 (1996) 253-264
40. Korhonen R.K., Wong M., Arokoski J., Lindgren R., Helminen H.J., Hunziker E.B., et al. Importance of the superficial tissue layer for the indentation stiffness of articular cartilage. Med Eng Phys 24 (2002) 99-108
41. Wei X., Räsänen T., and Messner K. Maturation-related compressive properties of rabbit knee articular cartilage and volume fraction of subchondral tissue. Osteoarthritis Cartilage 6 (1998) 400-409
42. Arokoski J.P., Hyttinen M.M., Helminen H.J., and Jurvelin J.S. Biomechanical and structural characteristics of canine femoral and tibial cartilage. J Biomed Mater Res 48 (1999) 99-107
43. Williams G.M., Klisch S.M., and Sah R.L. Bioengineering cartilage growth, maturation, and form. Pediatr Res 63 (2008) 527-534
44. Hunziker E.B. Articular cartilage structure in humans and experimental animals. In: Kuettner K. (Ed). Articular Cartilage and Osteoarthritis (1992), Raven Press, New York 183-197
45. Saarakkala S., Julkunen P., Kiviranta P., Mäkitalo J., Jurvelin J.S., and Korhonen R.K. Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics. Osteoarthritis Cartilage 18 (2010) 73-81
46. Puelacher W.C., Kim S.W., Vacanti J.P., Schloo B., Mooney D., and Vacanti C.A. Tissue-engineered growth of cartilage: the effect of varying the concentration of chondrocytes seeded onto synthetic polymer matrices. Int J Oral Maxillofac Surg 23 (1994) 49-53
47. Waldman S.D., Spiteri C.G., Grynpas M.D., Pilliar R.M., and Kandel R.A. Long-term intermittent shear deformation improves the quality of cartilaginous tissue formed in vitro. J Orthop Res 21 (2003) 590-596
48. Wilson W., Driessen N.J., van Donkelaar C.C., and Ito K. Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. Osteoarthritis Cartilage 14 (2006) 1196-1202
49. Responte D.J., Natoli R.M., and Athanasiou K.A. Collagens of articular cartilage: structure, function, and importance in tissue engineering. Crit Rev Biomed Eng 35 (2007) 363-411
50. Jurvelin J.S., Räsänen T., Kolmonen P., and Lyyra T. Comparison of optical, needle probe and ultrasonic techniques for the measurement of articular cartilage thickness. J Biomech 28 (1995) 231-235