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Biomechanical properties of knee articular cartilage

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Biorheology 40 (2003) 133–140 133
IOS Press

Biomechanical properties of knee articular

cartilage
M.S. Laasanen a,b , J. Töyräs a , R.K. Korhonen a,b , J. Rieppo b , S. Saarakkala a,b ,
M.T. Nieminen b , J. Hirvonen a and J.S. Jurvelin a,∗
a Department of Clinical Physiology and Nuclear Medicine, Kuopio University Hospital,
Kuopio, Finland
b Department of Anatomy, University of Kuopio, Kuopio, Finland

Abstract. Structure and properties of knee articular cartilage are adapted to stresses exposed on it during physiological activ-
ities. In this study, we describe site- and depth-dependence of the biomechanical properties of bovine knee articular cartilage.
We also investigate the effects of tissue structure and composition on the biomechanical parameters as well as characterize
experimentally and numerically the compression–tension nonlinearity of the cartilage matrix. In vitro mechano-optical mea-
surements of articular cartilage in unconfined compression geometry are conducted to obtain material parameters, such as
thickness, Young’s and aggregate modulus or Poisson’s ratio of the tissue. The experimental results revealed significant site-
and depth-dependent variations in recorded parameters. After enzymatic modification of matrix collagen or proteoglycans our
results show that collagen primarily controls the dynamic tissue response while proteoglycans affect more the static properties.
Experimental measurements in compression and tension suggest a nonlinear compression–tension behavior of articular carti-
lage in the direction perpendicular to articular surface. Fibril reinforced poroelastic finite element model was used to capture
the experimentally found compression–tension nonlinearity of articular cartilage.

1. Introduction

The structure and properties of healthy articular cartilage are optimal for its mechanical function in the
joint. Cartilage is permeable, mechanically viscoelastic, consisting of an organic matrix and free inter-
stitial fluid which is mostly water. The most important macromolecules, forming the organic matrix, are
collagens (mainly type II) and proteoglycans (PGs), which make up most of the remaining 20–30% of
the wet weight [31]. Collagens are proteins that form the fibrillar meshwork providing cartilage with its
high tensile stiffness and strength [13,15,31]. Glycosaminoglycans (GAGs) attract water and repel each
other due to their electronegativity, creating a swelling pressure that is restrained by the collagenous
meshwork [5–8,26,38,40,41]. The compressive stiffness of cartilage is positively related to GAG con-
centration and negatively related to the hydration of the tissue [1,14]. Under physiological joint loading,
complex patterns of interstitial compressive, tensional and shear stresses arise in the cartilage matrix.
At high rate dynamic loading, cartilage is virtually incompressible, even though the shape of the matrix
changes [12,43,44].
Cartilage is functionally highly anisotropic. Also a significant depth-dependence in compressive
stiffness of cartilage has been revealed [35]. The elastic modulus of articular cartilage is typically
0.3–1.5 MPa [2,11,30,32]. However, significantly higher in vivo peak stresses up to 18 MPa in joints
*
Address for correspondence: J.S. Jurvelin, Ph.D., Dept. of Clinical Physiology and Nuclear Medicine, P.O. Box 1777, FIN-
70211 Kuopio, Finland. Tel.: +358 17 173 261; Fax: +358 17 173 244; E-mail: Jukka.Jurvelin@uku.fi.

0006-355X/03/$8.00  2003 – IOS Press. All rights reserved

134 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage

during dynamic loads have been measured [10]. This apparent mismatch can be explained by the rel-
atively low permeability of cartilage. Interstitial water cannot be squeezed out from the tissue during
dynamic loading but is pressurized and therefore supports the high physiological stresses. This is the
main reason why the dynamic stiffness of cartilage may be 10 to 20 times higher than the intrinsic mod-
ulus of the matrix [12]. Under long-term loading conditions, fluid flow through the porous matrix takes
place and causes creep or stress–relaxation phenomenon. This process is controlled by the cartilage per-
meability, which depends mostly on the PG concentration [30]. The pressurization and flow mechanisms
protect articular cartilage against excessive strains and mechanical failure [37].
Various theoretical models have been developed to explain the mechanical behavior of articular carti-
lage. The first models were isotropic and elastic [9] and could be applied only to characterize the instan-
taneous or equilibrium responses of cartilage after a stepload application. As a next step the isotropic
biphasic solution [25,29] could also explain the time dependence of the cartilage mechanical behaviour.
In addition to the isotropic solution, transversely isotropic biphasic [28], poroviscoelastic [39], fibril rein-
forced poroelastic [38] or conewise linear elasticity biphasic [36] solutions exist to improve the accuracy
of the theoretical models to predict the cartilage response.
In this study, we describe site- and depth-dependence of the structure and mechanical properties of
articular cartilage in the bovine knee joint. We also characterize experimentally the effects of tissue struc-
ture on the biomechanical response, compression–tension nonlinearity of the tissue and apply numerical
techniques to model the nonlinearity.

2. Materials and methods

A high number of cartilage samples from different sites of the bovine knee joint (n = 25) were studied
(Fig. 1). Unconfined compression (Fig. 2A), mechano-optical determination of Poisson’s ratio (Fig. 2B)
and finite element modeling (Fig. 2C) were utilized for the characterization of cartilage mechanical
properties. In unconfined compression tests stepwise stress-relaxation protocols were used. Static (equi-
librium or Young’s) modulus of cartilage was derived from the equilibrium response. In addition, high
rate (2 mm/s, 10% strain) stress–strain tests were conducted to obtain cartilage dynamic (instantaneous)
modulus.

2.1. Depth-dependent variation

Patellar osteochondral plug (∅ = 9 mm) was prepared from the knee, within 2 hours post mortem.
A cylindrical cut was made to the plug using a biopsy punch (inner ∅ = 2.7 mm). The plug was mounted
on a biopsy mold with O.C.T compound and frozen at −20◦ C. After freezing the cartilage surface was
trimmed flat with cryomicrotome and uncalcified cartilage layer was cut into ten successive slices [34].

2.2. Topographical variation

Cylindrical samples (n = 29) from the patella, tibia, medial femoral condyle, medial and lateral
patellar groove were detached from the joint using a razor blade and punched with a biopsy punch (∅ =
3.0 mm). Stress relaxation measurements in unconfined compression were conducted to obtain dynamic
and static Young’s modulus, including also an optical measurement of Poisson’s ratio (∅ = 2.0 mm,
punched from the original sample).
 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage 135

MPG

TM

LPG

FMC PAT

Fig. 1. Measurement sites in the bovine knee joint. Medial tibial plateau (TM), lateral (LPG) and medial (MPG) facets of the
patello-femoral groove, medial femoral condyle (FMC) and the patella (PAT).

Fig. 2. A. Measurement geometry for the determination of dynamic and static Young’s modulus. The sample is compressed
between two smooth impermeable metallic platens and the stress–strain response is recorded [42]. B. Measurement geometry
for the determination of Poisson’s ratio. The sample is compressed with micrometer in unconfined geometry and the lateral
deformation is determined optically. From this information Poisson’s ratio can be calculated [12]. C. Articular cartilage
finite element (FE) mesh illustrating the arrangement of spring elements in a poroelastic element. Springs are nonlinear in
vertical plane.

2.3. Effect of tissue composition

Cylindrical (∅ = 4 mm) cartilage samples (n = 18) from the lateral upper quadrant of the patella were
prepared. The samples were divided into three groups. Collagenase type VII (C 0773, Sigma Chemical
Co., St. Louis, MO, USA) was used for type II collagen degradation, chondroitinase ABC (Seikagaku Co.,
Tokyo, Japan) for PG digestion and trypsin (T 0646, Sigma) for combined PG digestion and collagen
degradation. The incubation time (in 37°C, 5% CO2 athmosphere) for collagenase (30 U/ml) and chond-
roitinase ABC (0.1 U/ml) treated samples was 44 h and 90 min for trypsin (1 mg/ml) [42]. To mimic
osteoarthrotic cartilage degradation, the geometry for treatments was designed to allow enzymatic pene-
tration only through the articular surface.
136 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage

2.4. Compression–tension nonlinearity

Osteochondral sample (∅ = 4 mm) was extracted from the peripheral part of the humeral head and
glued with syanoacrylate between smooth metallic platens. Stepwise stress relaxation measurement was
conducted up to 5.4% strain both in compression and in tension perpendicular to articular surface [22].
The measurement geometry was modelled with a FE-technique, using a commercial finite element pack-
age (Abaqus v.5.8, Hibbitt, Karlsson & Sorensen, Inc., Pawtucket, RI, USA). Cartilage was modelled
as biphasic poroelastic (BPE) [29] or modified fibril reinforced biphasic poroelastic (FRBPE) [23] tis-
sue. In both models the cartilage consisted of axisymmetric, quadratic, 8-node elements (CAX8P). In
the FRBPE model collagen fibrils were modeled as linear or nonlinear springs (SPRINGA), which resist
tension only (Fig. 2C). The compressing metallic platens were modeled as analytical rigid bodies. The
nonlinearity of the model was utilized (NLGEOM in Abaqus) and the load was applied incrementally.
The material parameters for cartilage were elastic modulus E = 1.0 MPa and 0.4 MPa, and Poisson’s ra-
tio ν = 0.15 and 0.42 of the drained solid matrix for BPE and FRBPE models, respectively. Permeability
was k = 2 × 10−12 m/s, specific weight of interstitial fluid γ = 9.81 × 103 N/m3 and solid fraction of
the total tissue volume θs = 25% in both models. There was no need for nonlinear springs in horizon-
tal plane but vertical springs had nonlinear behavior. The stiffness of linear and non-linear springs was
EF = 15.3 MPa and EF = 1090ε, respectively, where ε is tensile strain.

3. Results

Cartilage properties showed significant depth-dependent variation from surface to subchondral bone.
The lowest Poisson’s ratios were measured at the superficial and deep cartilage layers, while the highest
values were determined at the transitional layer (Fig. 3). The aggregate and Young’s moduli as well as
PG concentration (indicated by the optical density of safranin O stained sections [17,18,21,33]) reached
maximum values at the deep tissue. Collagen meshwork was less rigorously arranged (indicated by the
quantitative polarized miscroscopy [3,19,27]) and the Poisson’s ratio reached maximum values at the
transitional layer.
Effects of the 3D collagenous meshwork and the PG content on the cartilage dynamic and static stiff-
ness were experimentally studied using selective enzymatic digestions. The measurements suggested that
collagen meshwork was mainly responsible for the dynamic stiffness of the cartilage but had significant
effect on the static properties as well. The PGs were found to mainly affect the static properties of the
cartilage. This was most evident after robust cleavage induced by the trypsin (Fig. 4).
Significant topographical variation of cartilage thickness, dynamic and static modulus and Poisson’s
ratio was revealed in the bovine knee joint (Fig. 5).
FRBPE model could predict the compression–tension nonlinearity of articular cartilage in the direction
perpendicular to articular surface (Fig. 6). Model was able to obtain the equilibrium response of cartilage
both in compression and in tension. On the other hand, BPE model could predict the equilibrium response
of cartilage only in compression.

4. Discussion

Knowledge of the site- and depth-dependent variations in the structural and functional properties of
cartilage matrix is necessary when developing realistic theoretical models for knee joint structure and
 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage 137

Distance from articular surface (µm)

0 300 600 900 1200 1500 1800
1.2 2.2

Birefingence (×10 )
2.0

-3
1.0 1.8

Optical density
0.8 1.6 Birefringence
1.4 Optical density
0.6 1.2
0.4 1.0
0.8
0.2 0.6

Schematic presentation
of cartilage structure

2.5 0.5

2.0 0.4
Modulus (MPa)

Poisson’s ratio
1.5 0.3 Young's modulus
Aggregate modulus
1.0 0.2 Poisson's ratio

0.5 0.1

0.0 0.0
1 2 3 4 5 6 7 8 9 10
Section level (1=surface, 10=deep)

Fig. 3. Depth-dependent variation of the biomechanical characteristics of bovine knee articular cartilage. Poisson’s ratio reached
maximum at the transitional cartilage layer (lower panel), while the aggregate and Young’s modulus reached highest values at the
deep cartilage. Birefringence (from polarized light microscopy) indicates the degree of paraller organized collagen fibrils (upper
panel) [3,19,27]. Optical density (from safranin O stain) indicates the local PG content in tissue [17,18,21,33].

function. For this reason, variation of the moduli and Poisson’s ratio through cartilage depth was de-
termined using direct mechano-optical measurement. All material properties determined in this study
showed significant depth-dependent variation. Exact structure–function relationship is still open for Pois-
son’s ratio, but factors such as collagen fibril orientation and cross-linking may be important in restricting
lateral expansion of cartilage under compression.
The significant topographical variation in the biomechanical properties, revealed in the present and
some earlier studies, implies that cartilage has adapted its functional properties to prevailing loading
conditions. It also suggests that if the cartilage properties are diagnosed in vivo, it is essential to compare
the measured values with the reference values determined for the same measurement site of the knee joint
in the reference population [24].
It is known that collagen meshwork is predominantly responsible for the tensile and shear properties of
the tissue while the proteoglycans are main determinants of the compressive stiffness [14–16]. In this
study we found, using collagenase digestion, that collagen affects mainly the dynamic stiffness but has an
effect on the equilibrium properties as well. The PG cleavage, using chondroitinase ABC, has only a minor
effect on the dynamic stiffness but a major effect on the static stiffness. Significant cleavage of PGs with
minor simultaneous cleavage of collagens, using trypsin, affected both dynamic and static cartilage
mechanical properties. These results suggest that collagen disruption can be detected via instantaneous
measurement while a long-term equilibrium measurement is needed for sensitive detection of PG
depletion. We find this result important when developing instrumentation for clinical evaluation of
ddddddd
138 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage

-65
Trypsin
Chond.ABC

dynamic modulus (%)

-55 Collagenase

-45

Change in
-35

-25

-15
-40 -60 -80 -100
Change in equilibrium modulus (%)

Fig. 4. Changes in equilibrium and dynamic modulus of articular cartilage after specific cleavage of collagen (by collagenase) or
PG (by chondroitinase ABC) or both (by trypsin) components (mean ± SEM, n = 6). The results suggest that collagens are
mainly responsible for the dynamic (instantaneous) properties, while proteoglycans affect more the static (equilibrium) properties
of articular cartilage. In all cases the change was significant (p < 0.05) (Wilcoxon signed ranks test).

TM FMC PAT LPG MPG

1800
Thickness (µ m )

1600
1400
1200
1000
800
600
21 1.0
Dynamic

modulus (MPa)
modulus (MPa)

Equilibrium 0.8 Equilibrium

Dynamic

14
0.6
0.4
7
0.2
0 0.0
0.50
Poisson's ratio

0.40
0.30
0.20
0.10
TM FMC PAT LPG MPG

Fig. 5. Topographical variation of the biomechanical characteristics (thickness, equilibrium and dynamic modulus, Poisson’s
ratio) of bovine knee articular cartilage (mean ± SD, n = 6 (TM; n = 5)).

cartilage status – collagen degradation is an irreversible process whereas PG-depletion may be restored by
curative actions [4,20].
The significant compression–tension non-linearity was found in the direction perpendicular to articular
surface. The nonlinearity suggests for the use of anisotropic models, such as the models presented by Li et
al. (1999) [23] or Soltz and Ateshian (2000) [36]. However, the present models are still simplifications of
the complex cartilage structure and do not include realistic, depth-dependent orientation and organization
of the collagen fibrils, and thereby, may miss the possible anisotropy in cartilage mechanical properties.
ddddddddddddddddddddddddddddddddddd
 M.S. Laasanen et al. / Biomechanical properties of knee articular cartilage 139
1
-6 -3

-1 3 6
Strain (%)

-3

Load (N)
-5 FRBPE
BPE
Experimental
-7

Fig. 6. The compression–tension nonlinearity of articular cartilage in the direction perpendicular to articular surface, as
demonstrated by experimental equilibrium test and by biphasic poroelastic (BPE) or fibril reinforced biphasic poroelastic
(FRBPE) finite-element models.

Acknowledgments

Financial support from the Technology Development Center (TEKES), Finland, Kuopio University
Hospital, Kuopio, Finland (EVO 5103), Research Foundation of Orion Corporation, Finland and the
Graduate School for Musculoskeletal Diseases, Finland is acknowledged.

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