Quantitative description of collagen structure in the articular cartilage of the young and adult equine distal metacarpus

Animal Biology

Volumn 58, Issue 4, 2008, Pages 353-370

  Van Turnhout, Mark C ^a   Haazelager, Monique B ^a   Gijsen, Merel A L ^a   Schipper, Henk ^a   Kranenbarg, Sander ^a   Van Leeuwen, Johan L ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Articular cartilage; Collagen structure; Equine; Mechanobiology; QPLM; SEM

Indexed keywords

BONE; COLLAGEN; MODELING; POLARIZATION; QUANTITATIVE ANALYSIS;

ANIMALIA; EQUIDAE;

EID: 66849101234     PISSN: 15707555     EISSN: 15707563     Source Type: Journal    
DOI: 10.1163/157075608X383674     Document Type: Article

References (56)

1. Alhadlaq, H., Xia, Y., Moody, J. & Matyas, J. (2004) Detecting structural changes in early experimental osteoarthritis of tibial cartilage by microscopic magnetic resonance imaging and polarised light microscopy, Ann. Rheum. Dis., 63, 709-717.
2. Arokoski, J.P., Hyttinen, M.M., Helminen, H.J. & Jurvelin, J.S. (1999) Biomechanical and structural characteristics of canine femoral and tibial cartilage , J. Biomed. Mater. Res., 48, 99-107.
3. Arokoski, J.P., Hyttinen, M.M., Lapveteläinen, T., Takács, P., Kosztáczky, B., Modis, L., Kovanen, V. & Helminen, H.J. (1996) Decreased birefringence of the superfi cial 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, 253-264.
4. Bennett, S.H. (1950) Methods applicable to the study of both fresh and fi xed materials - the microscopical investigation of biological materials with polarized light , in McClung Jones , R. (Ed.), McClung's handbook of microscopical technique, Cassel and company limited , chap. IX, 3rd ed. , 591 - 677 .
5. Benninghoff , A. ( 1925 ) Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zweiter Teil: Der Aufbau des Gelenkknorpels in seinen Beziehungen zur Funktion , Z. Zellforsch., 2, 783-862.
6. Bi, X., Li, G., Doty, S. & Camacho, N. (2005) A novel method for determination of collagen orientation in cartilage by Fourier transform infrared imaging spectroscopy (FT-IRIS) , Osteoarthritis Cartilage 13, 1050-1058.
7. Bland, Y.S. & Ashhurst, D.E. (1996a) Changes in the content of the fi brillar collagens and the expression of their mRNAs in the menisci of the rabbit knee joint during development and ageing , Histochem. J. 28, 265-274.
8. Bland, Y.S. & Ashhurst, D.E. (1996b) Development and ageing of the articular cartilage of the rabbit knee joint: distribution of the fi brillar collagens , Anat. Embryol. (Berl), 194, 607-619.
9. Brama, P., Karssenberg, D., Barneveld, A. & van Weeren, P. (2001) Contact areas and pressure distribution on the proximal articular surface of the proximal phalanx under sagittal plane loading , Equine Vet. J., 33, 26-32.
10. Brama, P., Tekoppele, J., Bank, R., Barneveld, A., Firth, E. & van Weeren, P. (2000a) T e influence of strenuous exercise on collagen characteristics of articular cartilage in T oroughbreds age 2 years , Equine Vet. J., 32, 551-554.
11. Brama, P., TeKoppele, J., Bank, R., Barneveld, A. & van Weeren, P. (2000b) Functional adaptation of equine articular cartilage: the formation of regional biochemical characteristics up to age one year , Equine Vet. J., 32, 217-221.
12. Brama, P., TeKoppele, J., Bank, R., Barneveld, A. & van Weeren, P. (2002) Development of biochemical heterogeneity of articular cartilage: influences of age and exercise , Equine Vet. J., 34, 265-269.
13. Brama, P., Tekoppele, J., Bank, R., Karssenberg, D., Barneveld, A. & van Weeren, P. (2000c) Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint , Equine Vet. J., 32, 19-26.
14. Brama, P., TeKoppele, J., Bank, R., van Weeren, P. & Barneveld, A. (1999) Influence of diff erent exercise levels and age on the biochemical characteristics of immature equine articular cartilage , Equine Vet. J. Suppl., 55-61.
15. Brommer, H., Brama, P., Laasanen, M., Helminen, H., van Weeren, P. & Jurvelin, J. (2005) Functional adaptation of articular cartilage from birth to maturity under the influence of loading: a biomechanical analysis , Equine Vet. J., 37, 148-154.
16. Clark, J.M. (1985) T e organization of collagen in cryofractured rabbit articular cartilage: a scanning electron microscopic study , J. Orthop. Res., 3, 17-29.
17. Clark, J.M. (1991) Variation of collagen fi ber alignment in a joint surface: a scanning electron microscope study of the tibial plateau in dog, rabbit, and man , J. Orthop. Res., 9, 246-257.
18. Firth, E. & Greydanus, Y. (1987) Cartilage thickness measurement in foals, Res. Vet. Sci., 42, 35-46.
19. Han, B., Cole, A., Shen, Y., Brodie, T. & Williams, J. (2002) Early alterations in the collagen meshwork and lesions in the ankles are associated with spontaneous osteoarthritis in guinea-pigs , Osteoarthritis Cartilage, 10, 778-784.
20. Helminen, H.J., Hyttinen, M.M., Lammi, M.J., Arokoski, J.P., Lapveteläinen, T., Jurvelin, J., Kiviranta, I. & Tammi , M.I. ( 2000 ) Regular joint loading in youth assists in the establishment and strengthening of the collagen network of articular cartilage and contributes to the prevention of osteoarthrosis later in life: a hypothesis , J. Bone Miner. Metab., 18, 245-257.
21. Hodge, W., Fijan, R., Carlson, K., Burgess, R., Harris, W. & Mann, R. (1986) Contact pressures in the human hip joint measured in vivo , Proc. Natl. Acad. Sci. U.S.A., 83, 2879-2883.
22. Hughes, L., Archer, C. & ap Gwynn, I. (2005) T e ultrastructure of mouse artic-ular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review , Eur. Cell Mater., 9, 68-84.
23. Hunziker, E., Kapfinger, E. & Geiss, J. (2007a) Corrigendum to "T e 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], Osteoarthritis Cartilage.
24. Hunziker, E., Kapfinger, E. & Geiss, J. (2007b) T e structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development, Osteoarthritis Cartilage, 15, 403-413, corrigendum in Hunziker et al. (2007a).
25. Hyttinen, M., Arokoski, J., Parkkinen, J., Lammi, M., Lapveteläinen, T., Mauranen, K., Király, K., Tammi, M. & Helminen, H. (2001) Age matters: collagen birefringence of superfi cial articular cartilage is increased in young guinea-pigs but decreased in older animals after identical physiological type of joint loading , Osteoarthritis Cartilage, 9, 694-701.
26. Julkunen, P., Kiviranta, P., Wilson, W., Jurvelin, J.S. & Korhonen, R.K. (2007) Characterization of articular cartilage by combining microscopic analysis with a fi bril-reinforced fi nite-element model , J. Biomech., 40, 1862-1870.
27. Kääb, M., ap Gwynn, I. & Nötzli, H. (1998) Collagen fi bre arrangement in the tibial plateau articular cartilage of man and other mammalian species , J. Anat., 193 (Pt 1), 23-34.
28. Kim, A., Lakshman, N. & Petroll, W.M. (2006) Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase , Exp. Cell Res., 312, 3683-3692.
29. Király, K., Hyttinen, M., Lapveteläinen, T., Elo, M., Kiviranta, I., Dobai, J., Modis, L., Helminen, H. & Arokoski, J. (1997) Specimen preparation and quantifi cation of collagen birefringence in unstained sections of articular cartilage using image analysis and polarizing light microscopy , Histochem. J., 29, 317-327.
30. Király, K., Hyttinen, M., Parkkinen, J., Arokoski, J., Lapveteläinen, T., Törrönen, K. Kiviranta, I. & Helminen , H. ( 1998 ) Articular cartilage collagen birefringence is altered concurrent with changes in proteoglycan synthesis during dynamic in vitro loading , Anat. Rec. 251, 28-36.
31. Kiviranta, P., Rieppo, J., Korhonen, R.K., Julkunen, P., Töyräs, J. & Jurvelin, J.S. (2006) Collagen network primarily controls Poisson's ratio of bovine articular cartilage in compression , J. Orthop. Res. 24, 690-699.
32. Korhonen, R., Wong, M., Arokoski, J., Lindgren, R., Helminen, H., Hunziker, E. & Jurvelin, J. (2002) Importance of the superfi cial tissue layer for the indentation stiff ness of articular cartilage , Med. Eng. Phys., 24, 99-108.
33. Li, C., Pruitt, L.A. & King, K.B. (2006) Nanoindentation diff erentiates tissue-scale functional properties of native articular cartilage , J. Biomed. Mater. Res. A, 78, 729-738.
34. Massoumian, F., Juškaitis, R., Neil, M. & Wilson, T. (2003) Quantitative polarized light microscopy, J. Microsc., 209, 13-22.
35. Murray, R., Birch, H., Lakhani, K. & Goodship, A. (2001) Biochemical composition of equine carpal articular cartilage is influenced by short-term exercise in a site-specifi c manner , Osteoarthritis Cartilage, 9, 625-632.
36. Oldenbourg, R. & Mei, G. (1995) New polarized light microscope with precision universal compensator, J. Microsc., 180, 140-147.
37. Oldenbourg, R. (2004) Polarization microscopy with the LC-microscope, in R.D. Goldman & D.L. Spector (Eds.), Live Cell Imaging: A Laboratory Manual, Cold Spring Harbor Laboratory Press , chap. 13, 205-238.
38. Palmer, J.L., Bertone, A.L. & Litsky, A. (1994) Contact area and pressure distribution changes of the equine third carpal bone during loading , Equine Vet. J., 26, 197-202.
39. Petroll, W.M., Cavanagh, H.D., Barry, P., Andrews, P. & Jester, J.V. (1993) Quantitative analysis of stress fi ber orientation during corneal wound contraction , J. Cell Sci., 104, 353-363.
40. Rieppo, J., Töyräs, J., Nieminen, M.T., Kovanen, V., Hyttinen, M.M., Korhonen, R.K., Jurvelin, J.S. & Helminen, H.J. (2003a) Structure-function relationships in enzymatically modifi ed articular cartilage, Cells Tissues Organs, 175, 121-132.
41. Rieppo, J., Hallikainen, J., Jurvelin, J., Helminen, H. & Hyttinen, M. (2003b) Novel quantitative polarization microscopic assessment of cartilage and bone collagen birefringence, orientation and anisotropy, Transactions of the ORS , 28, paper nr. 0570 at the 49th Annual Meeting of the Orthopaedic Research Soceity, New Orleans, Louisiana.
42. Ross, S., Newton, R., Zhou, Y.M., Haffegee, J., Ho, M.W., Bolton, J. & Knight, D. (1997) Quantitative image analysis of birefringent biological material , J. Microsc., 187, 62-67.
43. Saadat , E. , Lan , H. , Majumdar , S. , Rempel , D.M. & King , K.B. ( 2006 ) Long-term cyclical in vivo loading increases cartilage proteoglycan content in a spatially specifi c manner: an infrared microspectro-scopic imaging and polarized light microscopy study , Arthritis. Res. Ter., 8, R147.
44. Schinagl, R.M., Gurskis, D., Chen, A.C. & Sah, R.L. (1997) Depth-dependent confi ned compression modulus of full-thickness bovine articular cartilage , J. Orthop. Res., 15, 499-506.
45. Shribak, M. & Oldenbourg, R. (2003) Techniques for fast and sensitive measurements of two-dimensional birefringence distributions , Appl. Opt., 42, 3009-3017.
46. Speer, D.P. & Dahners, L. (1979) T e collagenous architecture of articular cartilage. Correlation of scanning electron microscopy and polarized light microscopy observations , Clin. Orthop. Relat. Res. 267-275.
47. Ugryumova, N., Attenburrow, D.P., Winlove, C.P. & Matcher, S.J. (2005) T e collagen structure of equine articular cartilage, characterized using polarizationsensitive optical coherence tomography , J. Phys. D: Appl. Phys., 38, 2612-2619.
48. Upton, G.J. & Fingleton, B. (1989) Spatial data analysis by example - Volume 2: Categorical and directional data., Wiley series in probability and mathematical statistics , John Wiley and Sons .
49. Wilson, W., van Donkelaar, C., van Rietbergen, B. & Huiskes, R. (2005a) A fi bril-reinforced poroviscoe-lastic swelling model for articular cartilage , J. Biomech., 38, 1195-1204, erratum in J. Biomech. 38(10):2138-2140, see Wilson et al. (2005b).
50. Wilson, W., van Donkelaar, C., van Rietbergen, B., Ito, K. & Huiskes, R. (2005b) Erratum to "Stresses in the local collagen network of articular cartilage: a poroviscoelastic fi bril-reinforced fi nite element study" [Journal of Biomechanics 37 (2004) 357-366] and "A fi bril-reinforced poroviscoelastic swelling model for articular cartilage" [Journal of Biomechanics 38 (2005) 1195-1204] , J. Biomech. 38, 2138-2140.
51. Wilson, W., Driessen, N., van Donkelaar, C. & Ito, K. (2006a) Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm , Osteoarthritis Cartilage, 14, 1196-1202.
52. Wilson, W., Huyghe, J. & van Donkelaar, C. (2006b) A composition-based cartilage model for the assessment of compositional changes during cartilage damage and adaptation , Osteoarthritis Cartilage, 14, 554-560.
53. Wilson, W., Huyghe, J. & van Donkelaar, C. (2007) Depth-dependent compressive equilibrium properties of articular cartilage explained by its composition , Biomech. Model. Mechanobiol., 6, 43-53.
54. Xia, Y., Ramakrishnan, N. & Bidthanapally, A. (2007) T e depth-dependent anisotropy of articular cartilage by Fourier-transform infrared imaging (FTIRI) , Osteoarthritis Cartilage, 15, 780-788.
55. 2 relaxation in articular cartilage: A microscopic MRI (μ MRI) study, Magn. Reson. Med., 48, 460-469.
56. Xia, Y., Moody, J.B., Alhadlaq, H. & Hu, J. (2003) Imaging the physical and morphological properties of a multi-zone young articular cartilage at microscopic resolution , J. Magn. Reson. Imaging, 17, 365-374.