Two-dimensional strain fields on the cross-section of the bovine humeral head under contact loading
Introduction
Despite a wealth of studies on the biomechanics of articular cartilage, it is interesting that detailed measurements of the strain distribution in articular layers under physiological loading conditions have yet to be reported. Here, physiological loading conditions refer to relatively rapid loading rates (but not impact loading) and contact stress magnitudes achieved during normal activities of daily living. Load magnitudes (Cooney and Chao, 1977; Paul, 1976; Poppen and Walker, 1978; Rydell, 1973) and articular contact tractions (Ahmed and Burke, 1983; Ahmed et al., 1983; Brown and Shaw, 1983, Brown and Shaw, 1984; Clark et al., 2002; Huberti and Hayes, 1984, Huberti and Hayes, 1988; Matthews et al., 1977) have been reported for a number of activities of daily living. However, there are only a few reports of measurements of relative cartilage deformation under physiological conditions, using radiographic techniques (Armstrong et al., 1979), ultrasound (Macirowski et al., 1994) and magnetic resonance imaging, (Eckstein et al., 1999, Eckstein et al., 2000), typically reporting relative deformations ranging from 6% to 20%. In contrast, the relative change in thickness of cartilage under prolonged static loading is on the order of 57% (Herberhold et al., 1998, Herberhold et al., 1999). However, this type of loading is not physiological and large changes in thickness under static conditions are not representative of in vivo cartilage deformation.
Cartilage deformation, as measured by change in thickness, has been characterized under various loading conditions using radiographic methods (Armstrong et al., 1979; Wayne et al., 1998), ultrasound (Macirowski et al., 1994; Suh et al., 2001), cryofixation followed by scanning electron microscopy (Kaab et al., 1998), chemical fixation followed by light microscopy (Clark et al., 2003), and magnetic resonance imaging (Eckstein et al., 2000; Herberhold et al., 1998, Herberhold et al., 1999).
Local strain measurements in articular cartilage explants have been reported under equilibrium static loading conditions using optical methods, by tracking distances between cells or cell nuclei (Guilak et al., 1995; Schinagl et al., 1996, Schinagl et al., 1997) or with digital image correlation (DIC) (Bae et al., 2003; Canal et al., 2003; Erne et al., 2005; Wang et al., 2002, Wang et al., 2003). These studies have yielded valuable insights into the equilibrium properties of the tissue, but the equilibrium response is not representative of physiologic loading conditions, and the explant geometry used in these studies was not representative of the articular geometry. More recently, strain fields in cartilage explants have been reported using magnetic resonance tagging (Neu et al., 2005) under steady-state dynamic loading. This approach holds great promise for delivering three-dimensional (3D) dynamic strain measurements in situ but has only been applied to small explants to date.
The objective of this study is to complement these valuable literature findings by providing a detailed experimental assessment of the two-dimensional (2D) cartilage strain distribution on the cross-section of immature and mature bovine humeral heads subjected to contact loading at a physiological loading rate. Mature and immature joints are compared to explore whether significant differences may arise due to the well-recognized evolution in material properties (Kempson, 1991; Williamson et al., 2003) and composition (Front et al., 1989; Garg and Swann, 1981; Wachtel et al., 1995) with age. The strain measurement method employed in this study, which uses DIC, builds upon our earlier application in the study of cartilage explants under static loading (Wang et al., 2002). The characterization of localized strains from experiments can aid in the understanding of the biomechanics of articular cartilage under physiological loading conditions, the structure–function relationships of this tissue, and the interpretation of degenerative and acute failure patterns observed in osteoarthritis and traumatic injuries. It also sets the stage for refining constitutive models of articular cartilage.
Section snippets
Specimen preparation
Humeral heads were dissected from 6-week-old calf joints (N=6) and mature 3-year-old shoulder joints (N=4). All samples were observed to be normal by visual inspection. The humeral heads were sectioned by band saw to create samples with smooth cross-sectional areas of the articular layer and underlying bone. The resulting sample groups were labeled ‘immature’ (n=6) and ‘mature’ (n=6, with two joints providing two samples each). The cartilage layers were kept moist with phosphate buffered saline
Results
The temporal evolution in the axial normal strain Eyy under the prescribed ramp-and-hold loading profile is depicted for a representative immature specimen in Fig. 4a–c, showing that the strain magnitude increased with time after the applied load had reached its peak value at 5 s. Repeatability measurements, illustrated in this representative specimen (Fig. 4a–c, versus d–f), demonstrated that reloading the tissue sample (after a 5 min recovery) and evaluating the strain distribution anew
Discussion
In this study, strain distributions throughout full thickness cross-sections of the articular layer of the bovine humeral head were characterized under physiological loading rates (average contact stresses of ∼1.5–2.0 MPa applied over 5 s) which, for humans, would represent moderate activities of daily living (Ahmed and Burke, 1983; Brown and Shaw, 1983). Both mature and immature joints were analyzed to investigate how age related differences in material properties and composition affect strain
Conflict of interest statement
The authors of this manuscript do not have any conflicts of interest with regard to this study and the materials contained herein.
Acknowledgments
This study was funded by the National Institute of Arthritis, Musculoskeletal and Skin Diseases of the US National Institutes of Health (AR46532). This material is also based upon work supported under a National Science Foundation Graduate Research Fellowship. We would like to thank Ms. Christine Schwaller and Ms. Elizabeth Chorney for their assistance in this study.
References (59)
- et al.
Incompressibility of the solid matrix of articular cartilage under high hydrostatic pressures
Journal of Biomechanics
(1998) - et al.
In vitro contact stress distributions in the natural human hip
Journal of Biomechanics
(1983) - et al.
Contact area and pressure distribution in the feline patellofemoral joint under physiologically meaningful loading conditions
Journal of Biomechanics
(2002) - et al.
In situ chondrocyte deformation with physiological compression of the feline patellofemoral joint
Journal of Biomechanics
(2003) - et al.
Patellar cartilage deformation in vivo after static versus dynamic loading
Journal of Biomechanics
(2000) - et al.
Depth-dependent strain of patellofemoral articular cartilage in unconfined compression
Journal of Biomechanics
(2005) - et al.
In situ measurement of articular cartilage deformation in intact femoropatellar joints under static loading
Journal of Biomechanics
(1999) - et al.
Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model
Journal of Biomechanics
(2007) - et al.
Optical and mechanical determination of Poisson's ratio of adult bovine humeral articular cartilage
Journal of Biomechanics
(1997) Age-related changes in the tensile properties of human articular cartilage: a comparative study between the femoral head of the hip joint and the talus of the ankle joint
Biochimica et Biophysica Acta
(1991)
A fibril reinforced nonhomogeneous poroelastic model for articular cartilage: inhomogeneous response in unconfined compression
Journal of Biomechanics
The nonlinear interaction between cartilage deformation and interstitial fluid flow
Journal of Biomechanics
Nonuniform swelling-induced residual strains in articular cartilage
Journal of Biomechanics
Cartilage interstitial fluid load support in unconfined compression
Journal of Biomechanics
Mechanical response of bovine articular cartilage under dynamic unconfined compression loading at physiological stress levels
Osteoarthritis Cartilage
Type II collagen degradation in articular cartilage fibrillation after anterior cruciate ligament transection in rats
Osteoarthritis Cartilage
An in situ calibration of an ultrasound transducer: a potential application for an ultrasonic indentation test of articular cartilage
Journal of Biomechanics
Age-related changes in collagen packing of human articular cartilage
Biochimica et Biophysica Acta
An analysis of the effects of depth-dependent aggregate modulus on articular cartilage stress-relaxation behavior in compression
Journal of Biomechanics
Optical determination of anisotropic material properties of bovine articular cartilage in compression
Journal of Biomechanics
Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components
Journal of Orthopaedic Research
In-vitro measurement of static pressure distribution in synovial joints—part I: tibial surface of the knee
Journal of Biomechanical Engineering
In-vitro measurement of static pressure distribution in synovial joints—part II: retropatellar surface
Journal of Biomechanical Engineering
Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing and fibrillation on the tensile modulus
Journal of Orthopaedic Research
In vitro measurement of articular cartilage deformations in the intact human hip joint under load
Journal of Bone and Joint Surgery America
An analysis of the unconfined compression of articular cartilage
Journal of Biomechanical Engineering
Equivalence between short-time biphasic and incompressible elastic material responses
Journal of Biomechanical Engineering
Impact responses of the flexed human knee using a deformable impact interface
Journal of Biomechanical Engineering
Blunt injuries to the patellofemoral joint resulting from transarticular loading are influenced by impactor energy and mass
Journal of Biomechanical Engineering
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