In situ deformation of cartilage in cyclically loaded tibiofemoral joints by displacement-encoded MRI.

OBJECTIVES Cartilage displacement and strain patterns were documented noninvasively in intact tibiofemoral joints in situ by magnetic resonance imaging (MRI). This study determined the number of compressive loading cycles required to precondition intact joints prior to imaging, the spatial distribution of displacements and strains in cartilage using displacement-encoded MRI, and the depth-dependency of these measures across specimens. DESIGN Juvenile porcine tibiofemoral joints were cyclically compressed at one and two times body weight at 0.1 Hz to achieve a quasi-steady state load-displacement response. A 7.0 T MRI scanner was used for displacement-encoded imaging with stimulated echoes and a fast spin echo acquisition (DENSE-FSE) in eight intact joints. Two-dimensional displacements and strains were determined throughout the thickness of the tibial and femoral cartilage and then normalized over the tissue thickness. RESULTS Two-dimensional displacements and strains were heterogeneous through the depth of femoral and tibial cartilage under cyclic compression. Strains in the loading direction were compressive and were maximal in the middle zone of femoral and tibial cartilage, and tensile strains were observed in the direction transverse to loading. CONCLUSIONS This study determined the depth-dependent displacements and strains in intact juvenile porcine tibiofemoral joints using displacement-encoded imaging. Displacement and strain distributions reflect the heterogeneous biochemistry of cartilage and the biomechanical response of the tissue to compression in the loading environment of an intact joint. This unique information about the biomechanics of cartilage has potential for comparisons of healthy and degenerated tissue and in the design of engineered replacement tissues.

[1]  H. Wen,et al.  DENSE: displacement encoding with stimulated echoes in cardiac functional MRI. , 1999, Journal of magnetic resonance.

[2]  Jon D. Szafranski,et al.  Chondrocyte mechanotransduction: effects of compression on deformation of intracellular organelles and relevance to cellular biosynthesis. , 2004, Osteoarthritis and cartilage.

[3]  C. Herberhold,et al.  An MR‐based technique for quantifying the deformation of articular cartilage during mechanical loading in an intact cadaver joint , 1998, Magnetic resonance in medicine.

[4]  A. Grodzinsky,et al.  Cartilage tissue remodeling in response to mechanical forces. , 2000, Annual review of biomedical engineering.

[5]  R L Spilker,et al.  An evaluation of three-dimensional diarthrodial joint contact using penetration data and the finite element method. , 2001, Journal of biomechanical engineering.

[6]  V. Mow,et al.  Indentation Determined Mechanoelectrochemical Properties and Fixed Charge Density of Articular Cartilage , 2004, Annals of Biomedical Engineering.

[7]  M. Hull,et al.  An MRI-based method to align the compressive loading axis for human cadaveric knees. , 2007, Journal of biomechanical engineering.

[8]  Won C Bae,et al.  Depth-dependent biomechanical and biochemical properties of fetal, newborn, and tissue-engineered articular cartilage. , 2007, Journal of biomechanics.

[9]  C. Herberhold,et al.  In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading. , 1999, Journal of biomechanics.

[10]  D. Schurman,et al.  Mechanoregulation of human articular chondrocyte aggrecan and type II collagen expression by intermittent hydrostatic pressure in vitro , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[11]  V C Mow,et al.  Contact analysis of biphasic transversely isotropic cartilage layers and correlations with tissue failure. , 1999, Journal of biomechanics.

[12]  A. Fowden,et al.  The effects of birth weight on basal cardiovascular function in pigs at 3 months of age , 2002, The Journal of physiology.

[13]  D L Butler,et al.  Functional tissue engineering: the role of biomechanics. , 2000, Journal of biomechanical engineering.

[14]  Kyriacos A. Athanasiou,et al.  Principles of Cell Mechanics for Cartilage Tissue Engineering , 2004, Annals of Biomedical Engineering.

[15]  D. R. Carter,et al.  In vitro stimulation of articular chondrocyte mRNA and extracellular matrix synthesis by hydrostatic pressure , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[16]  J Töyräs,et al.  Indentation diagnostics of cartilage degeneration. , 2008, Osteoarthritis and cartilage.

[17]  Y P Huang,et al.  Ultrasonic measurement of depth-dependent transient behaviors of articular cartilage under compression. , 2005, Journal of biomechanics.

[18]  G. Navon,et al.  Multinuclear NMR and MRI studies of the maturation of pig articular cartilage , 2006, Magnetic resonance in medicine.

[19]  M. Hull,et al.  Toward an MRI-based method to measure non-uniform cartilage deformation: an MRI-cyclic loading apparatus system and steady-state cyclic displacement of articular cartilage under compressive loading. , 2003, Journal of biomechanical engineering.

[20]  Walter Herzog,et al.  An articular cartilage contact model based on real surface geometry. , 2005, Journal of biomechanics.

[21]  M. Hull,et al.  Quasi-steady-state displacement response of whole human cadaveric knees in a MRI scanner. , 2009, Journal of biomechanical engineering.

[22]  M. Hull,et al.  Articular cartilage deformation determined in an intact tibiofemoral joint by displacement‐encoded imaging , 2009, Magnetic resonance in medicine.

[23]  D. Carter,et al.  Articular cartilage MR imaging and thickness mapping of a loaded knee joint before and after meniscectomy. , 2006, Osteoarthritis and cartilage.

[24]  G. Ateshian,et al.  An automated approach for direct measurement of two-dimensional strain distributions within articular cartilage under unconfined compression. , 2002, Journal of biomechanical engineering.

[25]  W Herzog,et al.  The Mechanical Behaviour of Chondrocytes Predicted with a Micro-structural Model of Articular Cartilage , 2007, Biomechanics and modeling in mechanobiology.

[26]  Dawn M Elliott,et al.  Human Internal Disc Strains in Axial Compression Measured Noninvasively Using Magnetic Resonance Imaging , 2007, Spine.

[27]  Seonghun Park,et al.  Inhomogeneous cartilage properties enhance superficial interstitial fluid support and frictional properties, but do not provide a homogeneous state of stress. , 2003, Journal of biomechanical engineering.

[28]  T. Aigner,et al.  Roles of chondrocytes in the pathogenesis of osteoarthritis. , 2002, Current opinion in rheumatology.

[29]  M. Hull,et al.  A finite element model of the human knee joint for the study of tibio-femoral contact. , 2002, Journal of biomechanical engineering.

[30]  W M Lai,et al.  An asymptotic solution for the contact of two biphasic cartilage layers. , 1994, Journal of biomechanics.

[31]  Gerard A Ateshian,et al.  Two-dimensional strain fields on the cross-section of the bovine humeral head under contact loading. , 2008, Journal of biomechanics.

[32]  Y. Zheng,et al.  Extraction of mechanical properties of articular cartilage from osmotic swelling behavior monitored using high frequency ultrasound. , 2007, Journal of biomechanical engineering.

[33]  Gerard A. Ateshian,et al.  A Paradigm for Functional Tissue Engineering of Articular Cartilage via Applied Physiologic Deformational Loading , 2004, Annals of Biomedical Engineering.

[34]  M. Hull,et al.  Heterogeneous three‐dimensional strain fields during unconfined cyclic compression in bovine articular cartilage explants , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[35]  Harry E Rubash,et al.  In Vivo Articular Cartilage Contact Kinematics of the Knee , 2005, The American journal of sports medicine.

[36]  Frederick H Epstein,et al.  Displacement‐encoded cardiac MRI using cosine and sine modulation to eliminate (CANSEL) artifact‐generating echoes , 2004, Magnetic resonance in medicine.

[37]  Walter Herzog,et al.  An improved solution for the contact of two biphasic cartilage layers , 1997 .

[38]  Albert C. Chen,et al.  Depth‐dependent confined compression modulus of full‐thickness bovine articular cartilage , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[39]  F Eckstein,et al.  In vivo cartilage deformation after different types of activity and its dependence on physical training status , 2005, Annals of the rheumatic diseases.

[40]  Mgd Marc Geers,et al.  Computing strain fields from discrete displacement fields in 2D-solids , 1996 .

[41]  Jeffrey H Walton,et al.  Displacement encoding for the measurement of cartilage deformation , 2008, Magnetic resonance in medicine.

[42]  T. Stammberger,et al.  Patellar cartilage deformation in vivo after static versus dynamic loading. , 2000, Journal of biomechanics.

[43]  H. Weinans,et al.  In vivo imaging of cartilage degeneration using microCT-arthrography. , 2007, Osteoarthritis and cartilage.