Abstract
Macro-cracks on the surface of articular cartilage are one of the hallmarks of early osteoarthritis and joint damage initiation. Macro-cracks negatively affect cartilage mechanobiology and load bearing capacity. The aim of this study was to quantify the changes in transient and steady-state force response of healthy cartilage in the presence of macro-cracks when compressed. Ten macro-cracks were created on the surface of intact articular cartilage. The force–time responses of intact cartilage and cartilage with macro-cracks (n = 22) were compared for multiple nominal axial compressive strain levels and strain rates. Experiments were simulated using a fiber-reinforced biphasic finite element model to gain insight into the possible mechanisms contributing to changes in the mechanical response of articular cartilage when introducing macro-cracks. We found a significant reduction in the transient and steady-state load bearing capacity of cartilage samples following the introduction of macro-cracks. Two mechanisms were identified as potential causes of this reduction: (1) an increase in permeability and associated decrease in fluid pressure, and (2) damage of the structural integrity of the solid matrix. The first cause was predicted by the finite element model, while the second cause was not.
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References
Abramson SB, Attur M, Amin AR, Clancy R (2001) Nitric oxide and inflammatory mediators in the perpetuation of osteoarthritis. Curr Rheumatol Rep 3(6):535–541
Centers for Disease Control and Prevention (CDC) (2010) Prevalence of doctor-diagnosed arthritis and arthritis-attributable activity limitation—United States, 2007–2009. MMWR 59(39):1261–1265
Chen C-T, Burton-Wurster N, Lust G, Bank RA, Tekoppele JM (1999) Compositional and metabolic changes in damaged cartilage are peak-stress, stress-rate, and loading-duration dependent. J Orthop Res 17(6):870–879. https://doi.org/10.1002/jor.1100170612
Chin-Purcell MV, Lewis JL (1996) Fracture of articular cartilage. J Biomech Eng 118(4):545–556
Chu CR, Williams AA, Coyle CH, Bowers ME (2012) Early diagnosis to enable early treatment of pre-osteoarthritis. Arthritis Res Ther 14(3):212. https://doi.org/10.1186/ar3845
Comper WD, Williams RPW, Zamparo O (1990) Water transport in extracellular matrices. Connect Tissue Res 25(2):89–102. https://doi.org/10.3109/03008209009006984
Davis MA, Ettinger WH, Neuhaus JM, Cho SA, Hauck WW (1989) The association of knee injury and obesity with unilateral and bilateral osteoarthritis of the knee. Am J Epidemiol 130(2):278–288
Ewers BJ, Dvoracek-Driksna D, Orth MW, Haut RC (2001) The extent of matrix damage and chondrocyte death in mechanically traumatized articular cartilage explants depends on rate of loading. J Orthop Res Off Publ Orthop Res Soc 19(5):779–784. https://doi.org/10.1016/S0736-0266(01)00006-7
Ewers BJ, Jayaraman VM, Banglmaier RF, Haut RC (2002) Rate of blunt impact loading affects changes in retropatellar cartilage and underlying bone in the rabbit patella. J Biomech 35(6):747–755. https://doi.org/10.1016/S0021-9290(02)00019-2
Farquhar T, Xia Y, Mann K, Bertram J, Burton-Wurster N, Jelinski L, Lust G (1996) Swelling and fibronectin accumulation in articular cartilage explants after cyclical impact. J Orthop Res 14(3):417–423. https://doi.org/10.1002/jor.1100140312
Goldring MB, Goldring SR (2007) Osteoarthritis. J Cell Physiol 213(3):626–634. https://doi.org/10.1002/jcp.21258
Howell DS, Pelletier JP (1993) Etiopathogenesis of osteoarthritis. In: McCarty DJ, Koopman WJ (eds) Arthritis and allied conditions: a textbook of rheumatology, 12th edn. Lea & Febiger, Philadelphia, pp 1723–1734
Howell DS, Sapolsky AI, Pita JC, Woessner JF (1976) The pathogenesis of osteoarthritis. Semin Arthritis Rheum 5(4):365–383. https://doi.org/10.1016/0049-0172(76)90015-9
Jeffrey JE, Gregory DW, Aspden RM (1995) Matrix damage and chondrocyte viability following a single impact load on articular cartilage. Arch Biochem Biophys 322(1):87–96. https://doi.org/10.1006/abbi.1995.1439
Komeili A, Abusara Z, Federico S, Herzog W (2018) A compression system for studying depth dependent mechanical properties of articular cartilage under dynamic loading conditions. Med Eng Phys 60:103–108. https://doi.org/10.1016/j.medengphy.2018.07.004
Lewis JL, Johnson SL (2001) Collagen architecture and failure processes in bovine patellar cartilage. J Anat 199(Pt 4):483–492
Lewis JL, Deloria LB, Oyen-Tiesma M, Thompson RC, Ericson M, Oegema TR (2003) Cell death after cartilage impact occurs around matrix cracks. J Orthop Res Off Publ Orthop Res Soc 21(5):881–887. https://doi.org/10.1016/S0736-0266(03)00039-1
Li L, Soulhat J, Buschmann M, Shirazi-Adl A (1999) Nonlinear analysis of cartilage in unconfined ramp compression using a fibril reinforced poroelastic model. Clin Biomech 14(9):673–682. https://doi.org/10.1016/S0268-0033(99)00013-3
Maroudas A (1979) Physicochemical properties of articular cartilage. Adult Articul Cartil 2:215–290
Martin JA, Buckwalter JA (2000) The role of chondrocyte-matrix interactions in maintaining and repairing articular cartilage. Biorheology 37(1–2):129–140
Meachim G, Emery IH (1974) Quantitative aspects of patello-femoral cartilage fibrillation in Liverpool necropsies. Ann Rheum Dis 33(1):39–47
Men Y, Jiang Y, Chen L, Zhang C, Ye J (2017) On mechanical mechanism of damage evolution in articular cartilage. Mater Sci Eng C 78:79–87. https://doi.org/10.1016/J.MSEC.2017.03.289
Morel V, Quinn TM (2004) Cartilage injury by ramp compression near the gel diffusion rate. J Orthop Res Off Publ Orthop Res Soc 22(1):145–151. https://doi.org/10.1016/S0736-0266(03)00164-5
Morel V, Berutto C, Quinn TM (2006) Effects of damage in the articular surface on the cartilage response to injurious compression in vitro. J Biomech 39(5):924–930. https://doi.org/10.1016/j.jbiomech.2005.01.026
Owen JR, Wayne JS (2006) Influence of a superficial tangential zone over repairing cartilage defects: implications for tissue engineering. Biomech Model Mechanobiol 5(2–3):102–110. https://doi.org/10.1007/s10237-006-0022-5
Quinn TM, Grodzinsky AJ, Hunziker EB, Sandy JD (1998) Effects of injurious compression on matrix turnover around individual cells in calf articular cartilage explants. J Orthop Res Off Publ Orthop Res Soc 16(4):490–499. https://doi.org/10.1002/jor.1100160415
Repo RU, Finlay JB (1977) Survival of articular cartilage after controlled impact. J Bone Jt Surg Am Vol 59(8):1068–1076
Rieppo J, Hyttinen MM, Halmesmaki E, Ruotsalainen H, Vasara A, Kiviranta I et al (2009) Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. Osteoarthr Cartil OARS 17(4):448–455. https://doi.org/10.1016/j.joca.2008.09.004
Sadeghi H, Shepherd DET, Espino DM (2015) Effect of the variation of loading frequency on surface failure of bovine articular cartilage. Osteoarthr Cartil 23(12):2252–2258. https://doi.org/10.1016/j.joca.2015.06.002
Sadeghi H, Lawless BM, Espino DM, Shepherd DET (2018) Effect of frequency on crack growth in articular cartilage. J Mech Behav Biomed Mater 77:40–46. https://doi.org/10.1016/j.jmbbm.2017.08.036
Sah RL, Doong JY, Grodzinsky AJ, Plaas AH, Sandy JD (1991) Effects of compression on the loss of newly synthesized proteoglycans and proteins from cartilage explants. Arch Biochem Biophys 286(1):20–29
Schmalzried TP, Szuszczewicz ES, Northfield MR, Akizuki KH, Frankel RE, Belcher G, Amstutz HC (1998) Quantitative assessment of walking activity after total hip or knee replacement. J Bone Jt Surg Am Vol 80(1):54–59
Shen P-C, Shiau A-L, Jou I-M, Lee C-H, Tai M-H, Juan H-Y et al (2011) Inhibition of cartilage damage by pro-opiomelanocortin prohormone overexpression in a rat model of osteoarthritis. Exp Biol Med 236(3):334–340. https://doi.org/10.1258/ebm.2010.010319
Silyn-Roberts H, Broom ND (1990) Fracture behaviour of cartilage-on-bone in response to repeated impact loading. Connect Tissue Res 24(2):143–156
Stok K, Oloyede A (2003) A qualitative analysis of crack propagation in articular cartilage at varying rates of tensile loading. Connect Tissue Res 44(2):109–120
Stok K, Oloyede A (2007) Conceptual fracture parameters for articular cartilage. Clin Biomech 22(6):725–735. https://doi.org/10.1016/j.clinbiomech.2007.03.005
Thambyah A, Broom N (2007) On how degeneration influences load-bearing in the cartilage–bone system: a microstructural and micromechanical study. Osteoarthr Cartil 15(12):1410–1423. https://doi.org/10.1016/j.joca.2007.05.006
Verma P, Dalal K (2011) ADAMTS-4 and ADAMTS-5: key enzymes in osteoarthritis. J Cell Biochem 112(12):3507–3514. https://doi.org/10.1002/jcb.23298
Verteramo A, Seedhom BB (2007) Effect of a single impact loading on the structure and mechanical properties of articular cartilage. J Biomech 40(16):3580–3589. https://doi.org/10.1016/j.jbiomech.2007.06.002
Wieland HA, Michaelis M, Kirschbaum BJ, Rudolphi KA (2005) Osteoarthritis: an untreatable disease? Nat Rev Drug Discov 4(4):331–344. https://doi.org/10.1038/nrd1693
Wilson W, van Donkelaar CC, van Rietbergen B, Huiskes R (2005) A fibril-reinforced poroviscoelastic swelling model for articular cartilage. J Biomech 38(6):1195–1204. https://doi.org/10.1016/j.jbiomech.2004.07.003
Acknowledgements
This work was supported by the Eyes High Postdoctoral Scholarship offered through the University of Calgary, The Canadian Institutes of Health Research (Grant No. FDN-143341) through a Foundation Scheme Grant, The Canada Research Chair Program (Grant No. 950-230603), and the Killam Memorial Chair for Interdisciplinary Research at the University of Calgary (Grant No. 150303).
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Komeili, A., Chau, W. & Herzog, W. Effects of macro-cracks on the load bearing capacity of articular cartilage. Biomech Model Mechanobiol 18, 1371–1381 (2019). https://doi.org/10.1007/s10237-019-01149-x
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DOI: https://doi.org/10.1007/s10237-019-01149-x