Characterization of cartilage metabolic response to static and dynamic stress using a mechanical explant test system

Torzilli, Peter A.; Grigiene, Rita; Huang, Charles; Friedman, Steven M.; Doty, Stephen B.; Boskey, Adele L.; Lust, George

Affiliations

¹Laboratory for Soft Tissue Research, The Hospital for Special Surgery, NY 10021, U.S.A

²Cornell University Veterinary College, Ithaca, New York, U.S.A.

Abstract and keywords

Experimenting with crack propagation in human cortical tissue is a necessary prerequisite for developing a cracking model. A three-point bending test on a shaft section of a notched human long bone is presented. A procedure for carrying out the experimental test, including unloading/reloading cycles, is implemented. The results obtained are analyzed regarding the physical mechanisms which occur in the different phases of the test, and during the cycles. The prominent role of cracking is highlighted. In addition a hypothesis is proposed concerning the potential effect of initial internal residual stresses, due to bone remodelling, on the significant residual notch openings after unloading and on the cycles’ shape.

Keywords: Cartilage; Mechanical load; Metabolism

Links

DOI: 10.1016/S0021-9290(96)00117-0

PubMed: 8970918

WoS: A1997VY60300001

History

Revised: 1997-07-16

Cited Works (24)

Year	Entry
1986	Schneiderman R, Keret D, Maroudas A. Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J Orthop Res. 1986;4(4):393-408.
1989	Sah RL-Y, Kim Y-J, Doong J-YH, Grodzinsky AJ, Plass AHK, Sandy JD. Biosynthetic response of cartilage explants to dynamic compression. J Orthop Res. 1989;7(5):619-636.
1992	Buschmann MD, Gluzband YA, Grodzinsky AJ, Kimura JH, Hunziker EB. Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix. J Orthop Res. November 1992;10(6):745-758.
1980	Palmoski MJ, Colyer RA, Brandt KD. Joint motion in the absence of normal loading does not maintain normal articular cartilage. Arthritis Rheum. March 1980;23(3):325-334.
1992	Parkkinen JJ, Lammi MJ, Helminen HJ, Tammi M. Local stimulation of proteoglycan synthesis in articular cartilage explants by dynamic compression in vitro. J Orthop Res. 1992;10(5):610-620.
1984	Palmoski MJ, Brandt KD. Effects of static and cyclic compressive loading on articular cartilage plugs in vitro. Arthritis Rheum. June 1984;27(6):675-681.
1989	Behrens F, Kraft EL, Oegema TR Jr. Biochemical changes in articular cartilage after joint immobilization by casting or external fixation. J Orthop Res. 1989;7(3):335-343.
1976	McDevitt CA, Muir H. Biochemical changes in the cartilage of the knee in experimental and natural osteoarthritis in the dog. J Bone Joint Surg. February 1976;58B(1):94-103.
1990	Eberhardt AW, Keer LM, Lewis JL, Vithoontien V. An analytical model of joint contact. J Biomech Eng. November 1990;112(4):407-413.
1994	Guilak F, Meyer BC, Ratcliffe A, Mow VC. The effects of matrix compression on proteoglycan metabolism in articular cartilage explants. Osteoarthritis Cartilage. June 1994;2(2):91-101.
1991	Brown TD, Pope DF, Hale JE, Buckwalter JA, Brand RA. Effects of osteochondral defect size on cartilage contact stress. J Orthop Res. 1991;9(4):559-567.
1977	Repo RU, Finlay JB. Survival of articular cartilage after controlled impact. J Bone Joint Surg. December 1977;59A(8):1068-1076.
1989	Gray ML, Pizzanelli AM, Lee RC, Grodzinsky AJ, Swann DA. Kinetics of the chondrocyte biosynthetic response to compressive load and release. Biochim Biophys Acta. June 27, 1989;991(3):415-425.
1988	Gray ML, Pizzanelli AM, Grodzinsky AJ, Lee RC. Mechanical and physicochemical determinants of the chondrocyte biosynthetic response. J Orthop Res. November 1988;6(6):777-792.
1980	Mow VC, Kuei SC, Lai WM, Armstrong CG. Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J Biomech Eng. February 1980;102(1):73-84.
1980	Kurosawa H, Fukubayashi T, Nakajima H. Load-bearing mode of the knee joint: physical behavior of the knee joint with or without menisci. Clin Orthop Relat Res. June 1980;149:283-290.
1986	Jurvelin J, Kiviranta I, Tammi M, Helminen JH. Softening of canine articular cartilage after immobilization of the knee joint. Clin Orthop Relat Res. June 1986;207:246-252.
1973	Pond MJ, Nuki G. Experimentally-induced osteoarthritis in the dog. Ann Rheum Dis. July 1973;32(4):387-388.
1990	O'Hara BP, Urban JP, Maroudas A. Influence of cyclic loading on the nutrition of articular cartilage. Ann Rheum Dis. July 1990;49(7):536-539.
1983	Hascall VC, Handley CJ, McQuillan DJ, Hascall GK, Robinson H, Lowther DA. The effect of serum on biosynthesis of proteoglycans by bovine articular cartilage in culture. Arch Biochem Biophys. July 1, 1983;224(1):206-223.
1991	Sah RL-Y, Doong J-YH, Grodzinsky AJ, Plaas AHK, Sandy JD. Effects of compression on the loss of newly synthesized proteoglycans and proteins from cartilage explants. Arch Biochem Biophys. April 1991;286(1):209-29.
1985	Lippiello L, Kaye C, Neumata T, Mankin HJ. In vitro metabolic response of articular cartilage segments to low levels of hydrostatic pressure. Connect Tissue Res. 1985;13(2):99-107.
1991	Hall AC, Urban JPG, Gehl KA. The effects of hydrostatic pressure on matrix synthesis in articular cartilage. J Orthop Res. January 1991;9(1):1-10.
1982	Jones IL, Klämfeldt A, Sandström T. The effect of continuous mechanical pressure upon the turnover of articular cartilage proteoglycans in vitro. Clin Orthop Relat Res. May 1982;165:283-289.

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Year	Entry
2001	Brown TD. Devices and techniques for in vitro mechanical stimulation of bone cells. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:27-1–27-22.
2003	Hu JCY, Athanasiou KA. The role of mechanical forces in tissue engineering of articular cartilage. In: Guilak F, Butler DL, Goldstein SA, Mooney DJ, eds. Functional Tissue Engineering. New York, NY: Inc., Springer-Verlag; 2003:227-242.
2000	Soltz MA, Ateshian GA. Interstitial fluid pressurization during confined compression cyclical loading of articular cartilage. Ann Biomed Eng. February 2000;28(2):150-159.
2001	Elder SH, Goldstein SA, Kimura JH, Soslowsky LJ, Spengler DM. Chondrocyte differentiation is modulated by frequency and duration of cyclic compressive loading. Ann Biomed Eng. June 2001;29(6):476-482.
2004	AufderHeide AC, Athanasiou KA. Mechanical stimulation toward tissue engineering of the knee meniscus. Ann Biomed Eng. August 2004;32(8):1161-1174.
2006	Aufderheide AC, Athanasiou KA. A direct compression stimulator for articular cartilage and meniscal explants. Ann Biomed Eng. September 2006;34(9):1463-1474.
2002	Hunter CJ, Imler SM, Malaviya P, Nerem RM, Levenston ME. Mechanical compression alters gene expression and extracellular matrix synthesis by chondrocytes cultured in collagen I gels. Biomaterials. February 15, 2002;23(4):1249-1259.
1999	Carver SE, Heath CA. Increasing extracellular matrix production in regenerating cartilage with intermittent physiological pressure. Biotechnol Bioeng. 1999;62(2):166-174.
1999	Carver SE, Heath CA. Influence of intermittent pressure, fluid flow, and mixing on the regenerative properties of articular chondrocytes. Biotechnol Bioeng. 1999;65(3):274-281.
2003	Wong M, Carter DR. Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone. July 2003;33(1):1-13.
2000	Brown TD. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech. January 2000;33(1):3-14.
2000	Guilak F, Mow VC. The mechanical environment of the chondrocyte: a biphasic finite element model of cell–matrix interactions in articular cartilage. J Biomech. December 2000;33(12):1663-1673.
2024	Rich MJ, Burnash S, Krishnan RR, Chubinskaya S, Loeser RF, Polacheck WJ, Diekman BO. Use of a novel magnetically actuated compression system to study the temporal dynamics of axial and lateral strain in human osteochondral plugs. J Biomech. January 2024;162:111887.
1999	Torzilli PA, Grigiene R, Borrelli J Jr, Helfet DL. Effect of impact load on articular cartilage: cell metabolism and viability, and matrix water content. J Biomech Eng. October 1999;121(5):433-441.
2000	Elder SH, Kimura JH, Soslowsky LJ, Lavagnino M, Goldstein SA. Effect of compressive loading on chondrocyte differentiation in agarose cultures of chick limb-bud cells. J Orthop Res. January 2000;18(1):78-86.
2003	Angele P, Yoo JU, Smith C, Mansour J, Jepsen KJ, Nerlich M, Johnstone B. Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res. May 2003;21(3):451-457.
2003	Chen C-T, Bhargava M, Lin PM, Torzilli PA. Time, stress, and location dependent chondrocyte death and collagen damage in cyclically loaded articular cartilage. J Orthop Res. September 2003;21(5):888-898.
2003	Darling EM, Athanasiou KA. Articular cartilage bioreactors and bioprocesses. Tissue Eng. February 2003;9(1):9-26.
2000	Soltz MA. Investigation of a Boundary Friction Model for Articular Cartilage: Effects of Interstitial Fluid Pressurization and Surface Topography [PhD thesis]. Columbia University; 2000.
2002	Sun D. Theoretical and Experimental Investigations of the Mechano-Electrochemical Properties of Articular Cartilage, a Charged -Hydrated -Soft, Biological Tissue [PhD thesis]. Columbia University; 2002.
2003	Mauck RL. Functional Tissue Engineering of Articular Cartilage: The Effect of Physical Forces on the in Vitro Growth of Engineered Constructs [PhD thesis]. Columbia University; 2003.
2012	Khanarian NT. Scaffold Design and Optimization for Osteochondral Interface Tissue Engineering [PhD thesis]. Columbia University; 2012.
2014	Tan AR. Towards Clinical Use of Engineered Tissues for Cartilage Repair [PhD thesis]. Columbia University; 2014.
2017	Roach BL. Modulation of the in Vitro Mechanical and Chemical Environment for the Optimization of Tissue-Engineered Articular Cartilage [PhD thesis]. Columbia University; 2017.
2005	Pritchard SE. Interleukin-1 Initiates Intracellular Calcium Transients in Articular Chondrocytes and Modulates Their Response to Osmotic Stress: The Role of F-Actin and TRPV4 [PhD thesis]. Duke University; 2005.
2006	Davis BH. Cell Survival and Metabolism Under Hypoxia and Nutrient Deprivation: Roles in Cardiac Cell Therapy [PhD thesis]. Duke University; 2006.
2001	Hunter CJ. Mechanical Stimulation of an in Vitro Articular Cartilage Defect Repair Model [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; October 2001.
2015	Giorgi M. Mechanobiological Predictions of Fetal Joint Morphogenesis [PhD thesis]. Imperial College London; April 2015.
2013	Vernon LL. Articular Cartilage Response Following Impact Injury [PhD thesis]. University of Miami; August 2013.
2008	Wheeler CA. Cartilage Response to in Vitro Models of Injury in Combination With Growth Factor and Antioxidant Treatments [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; February 2008.
2001	Dvoracek-Driksna DM. Effects of Mechanical Impact on a Bovine Articular Cartilage Explant System [Master's thesis]. East Lansing, MI: Michigan State University; 2001.
2005	Rundell SA. Investigation of the Acute Injury Response of Articular Cartilage in Vitro and in Vivo: Analysis of Various Therapeutic Treatments [Master's thesis]. East Lansing, MI: Michigan State University; 2005.
2006	Martin LM. Blunt Force Injury to Cartilage: Some Effects of Exercise and a Nutraceutical [Master's thesis]. East Lansing, MI: Michigan State University; 2006.
2015	Kaviani R. Effect of Dynamic Loading Parameters on the Biomechanics and Biology of in Vitro Modulated Growth Plate Explants [PhD thesis]. École polytechnique de Montréal; December 2015.
2009	Fan CY. Effects of Intermittent Static and Dynamic Tension on Articular Chondrocytes in High Density Culture [Master's thesis]. Queen's University; March 2009.
2010	Usprech JF. A Therapeutic Dose of Adenosine Triphosphate (ATP) for Cartilage Tissue Engineering [Master's thesis]. Queen's University; September 2010.
2004	Darling EM. Phenotype of Passaged, Zonal Articular Chondrocytes [PhD thesis]. Houston, TX: Rice University; July 2004.
2005	Hu J. Chondrocyte Self -Assembly and Culture in Bioreactors [PhD thesis]. Houston, TX: Rice University; April 2005.
2005	Scott CC. Interferometry of Chondrocytes and Impact of Articular Cartilage [PhD thesis]. Houston, TX: Rice University; August 2005.
2006	Aufderheide AC. Mechanical Stimulation Towards Tissue Engineering of the Knee Meniscus [PhD thesis]. Houston, TX: Rice University; June 2006.
2007	Koay EJ. Chondrocyte Biomechanics and Chondrogenesis [PhD thesis]. Houston, TX: Rice University; December 2007.
2010	Kalpakci KN. Interspecies Characterization and Tissue Engineering of the Temporomandibular Joint Disc [PhD thesis]. Houston, TX: Rice University; May 2010.
2005	Gushue DL. Frontal Plane Knee Joint Biomechanics: Implications in Experimental Animal Models and Childhood Obesity [PhD thesis]. University of Rochester; 2005.
2010	Holguin N. Low-Level Vibrations Maintain the Intervertebral Disc During Unloading [PhD thesis]. Stony Brook, NY: Stony Brook University; December 2010.
2007	McMahon LA. The Effect of Cyclic Tensile Loading and Growth Factors on the Chondrogenic Differentiation of Bone-Marrow Derived Mesenchymal Stem Cells in a Collagen-Glycosaminoglycan Scaffold [PhD thesis]. Trinity College Dublin; September 2007.
2002	Li KW. Regulation of Chondrocytes by Static and Dynamic Loading in Articular Cartilage Repair [PhD thesis]. San Diego (UCSD), University of California; 2002.
2006	Nugent GE. Biomechanical Regulation of Articular Cartilage Metabolism of Proteoglycan 4 and Articular Surface Integrity [PhD thesis]. San Diego (UCSD), University of California; 2006.
2012	Nguyen QT. Mechanobiology and Biomechanics of Articular Cartilage Repair [PhD thesis]. San Diego (UCSD), University of California; 2012.
1998	Elder SH. Effects of Compressive Loading on Chondrocyte Differentiation in a Novel Chick Limb Bud Cell-Agarose Model of Chondrogenesis [PhD thesis]. University of Michigan; 1998.
2013	Henak CR. Cartilage and Labrum Mechanics in the Normal and Pathomorphologic Human Hip [PhD thesis]. University of Utah; August 2013.