Incomplete Restoration of Immobilization Induced Softening of Young Beagle Knee Articular Cartilage After 50-Week Remobilization

The aim of this study was to characterize the biomechanical and structural changes in canine knee cartilage after an initial 11-week immobilization and subsequent remobilization period of 50 weeks. Cartilage from the immobilized and remobilized knee was compared with the tissue from age-matched control animals. Compressive stiffness, in the form of instant shear modulus (ISM) and equilibrium shear modulus (ESM) of articular cartilage, was investigated using an in situ indentation creep technique. The local variations in cartilage of glycosaminoglycan (GAG) concentration were measured with a microspectrophotometer after safranin O staining of histological sections. Using a computer-based quantitative polarized light microscopy method, collagen-related optical retardation, Γ, of cartilage zones were performed to investigate the collagen network of cartilage. Macroscopically, cartilage surfaces of the knee joint remained intact both after immobilization and remobilization periods. Immobilization caused significant softening of the lateral femoral and tibial cartilages, as expressed by ESM (up to 30 %, p < 0.05). Remobilization restored the biomechanical properties of cartilage in the lateral condyle of tibia, but in the lateral condyle of femur ESM remained 15 % below the control level (p = 0.05). The instant shear modulus was not changed either after immobilization or remobilization. The GAG content of the cartilage was slightly decreased after immobilization, especially in the superficial zone of cartilage, but the change was not statistically significant. After remobilization the intensity of safranin O content rose to control level. Neither immobilization nor remobilization had any effect on the Γ value of collagen fibril network either in the superficial or the deep zone at any of the test points. The changes of ESM were positively correlated with the alterations in GAG content of the superficial and deep zones after immobilization and remobilization. This confirms the key role of protoglycans in the regulation of the equilibrium stiffness of articular cartilage. As a conclusion, immobilization of the joint of a young individual may cause long-term, if not permanent, alterations of cartilage biomechanical properties. This may predispose joint to degenerative changes later in life.

Articular cartilage - biomechanical properities - indentation test - immobilization - remobilization

References

• 1 Armstrong C G, Mow V C. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content.  J Bone Joint Surg. 1982;  64A 88-94
• 2 Arokoski J, Hyttinen M, Helminen H J, Jurvelin J. Biomechanical and structural characteristics of canine femoral and tibial cartilage.  J Biomed Materials Res. 1999;  48 (2) 99-107
• 3 Arokoski J, Jurvelin J, Kiviranta I, Tammi M, Helminen H J. Softening of the lateral condylar articular cartilage in the canine knee joint after long distance (up to 40 km/day) running training lasting one year.  Int J Sports Med. 1994;  15 254-260
• 4 Arokoski J P, Hyttinen M M, Lapveteläinen T, Takacs P, Kosztaczky B, Modis L, Kovanen V, Helminen H J. 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. 1996;  55 253-264
• 5 Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Erste Mitteilung: Die modellierenden und formerhaltenen Faktoren des Knorpelreliefs.  Zeitschrift für die gesamte Anatomie Abt. 1. 1925;  76 43-63
• 6 Buckwalter J, Mankin H. Articular cartilage: Degeneration and osteoarthritis, repair, regeneration, and transplantation.  J Bone Joint Surg. 1997;  79A 612-632
• 7 Haapala J, Arokoski J, Hyttinen M, Lammi M, Tammi M, Kovanen V, Helminen H J, Kiviranta I. Remobilization does not fully restore immobilization induced articular cartilage atrophy.  Clin Orthop Rel Res. 1999;  362 218-229
• 8 Hayes W C, Keer L M, Hermann G, Mockros L F. A mathematical analysis for indentation tests of articular cartilage.  J Biomech. 1972;  5 541-551
• 9 Heikkinen L M, Panula H E, Lyyra T, Olkkonen H, Kiviranta I, Nevalainen T, Helminen H J. Electromechanical film sensor device for dynamic force recording from canine limbs.  Scand J Anim Sci. 1997;  24 85-92
• 10 Jurvelin J, Arokoski J, Hunziker E, Helminen H J. Topographical variation in the elastic modulus and Poisson's ratio of canine knee articular cartilage. Jyväskylä, Finland; In XVth Congress of the International Society of Biomechanics 1995: 440-441
• 11 Jurvelin J, Kiviranta I, Arokoski J, Tammi M, Helminen H J. Indentation study of the biomechanical properties of articular cartilage in the canine knee.  Engineering in Medicine. 1987;  16 15-22
• 12 Jurvelin J, Kiviranta I, Säämänen A-M, Tammi M, Helminen H J. Indentation stiffness of young canine knee articular cartilage - influence of strenuous joint loading.  J Biomech. 1990;  23 1239-1246
• 13 Jurvelin J, Kiviranta I, Säämänen A-M, Tammi M, Helminen H J. Partial restoration of immobilization-induced softening of canine articular cartilage after remobilization of the knee (stifle) joint.  J Orthop Res. 1989;  7 352-358
• 14 Jurvelin J, Kiviranta I, Tammi M, Helminen H J. Effect of physical exercise on indentation stiffness of articular cartilage in the canine knee.  Int J Sports Med. 1986;  7 106-110
• 15 Jurvelin J, Kiviranta I, Tammi M, Helminen H J. Softening of canine articular cartilage after immobilization of the knee joint.  Clin Orthop. 1986;  207 246-252
• 16 Jurvelin J, Säämänen A-M, Arokoski J, Helminen H J, Kiviranta I, Tammi M. Biomechanical properties of the canine knee articular cartilage as related to matrix proteoglycans and collagen.  Engineering in Medicine. 1988;  17 157-162
• 17 Kempson G E, Muir H, Swanson S AV, Freeman M AR. Correlations between stiffness and the chemical constituents of cartilage on the human femoral head.  Biochim Biophys Acta. 1970;  215 70-77
• 18 Kiraly K, Lapveteläinen T, Arokoski J, Törrönen K, Modis L, Kiviranta I, Helminen H J. Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage with microspectrophotometry.  Histochem J. 1996;  28 577-590
• 19 Kiviranta I, Jurvelin J, Tammi M, Säämänen A-M, Helminen H J. Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with safranin O.  Histochemistry. 1985;  82 249-255
• 20 Mak A F, Lai W M, Mow V C. Biphasic indentation of articular cartilage: Part I. Theoretical analysis.  J Biomech. 1987;  20 703-714
• 21 Mizrahi J, Maroudas A, Lanir Y, Ziv I, Webber T J. The “instantaneous” deformation of cartilage: effects of collagen fiber orientation and osmotic stress.  Biorheology. 1986;  23 311-330
• 22 Mow V C, Holmes M H, Lai W M. Fluid transport and mechanical properties of articular cartilage: a review.  J Biomech. 1984;  17 377-394
• 23 Muir I HM. The chemistry of the ground substance of joint cartilage. In: Sokoloff L (ed) The joints and synovial fluid. New York; Academic Press 1980: 27-94
• 24 Müller F J, Setton L A, Manicourt D H, Mow V C, Howell D S, Pita H. Centrifugal and biochemical comparison of proteoglycan aggregates from articular cartilage in experimental joint disuse and joint instability.  J Orthop Res. 1994;  12 498-508
• 25 NIH: Institute of Laboratory Animal Resources, National Research Council .Guide for care and use of laboratory animals. Bethesda; NIH publication, US Government Printing Office 1985 78 - 23
• 26 Sandy J D, Adams M E, Billingham M EJ, Plaas A, Muir H. In vivo and in vitro stimulation of chondrocyte biosynthetic activity in early experimental osteoarthritis.  Arthritis Rheum. 1984;  27 388-397
• 27 Setton L A, Mow V C, Müller F J, Pita J C, Howell D S. Mechanical behaviour and biochemical composition of canine knee cartilage following periods of joint disuse and disuse with remobilization.  Osteoarthritis Cartilage. 1997;  5 1-16
• 28 Venn G, Billingham M EJ, Hardingham T E. Increased proteoglycan synthesis in cartilage in experimental canine osteoarthritis does not reflect a permanent change in chondrocyte phenotype.  Arthritis Rheum. 1995;  38 525-532