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Journal of Biomechanics 47 (2014) 24672474

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Journal of Biomechanics
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www.JBiomech.com

Deformation of articular cartilage during static loading


of a knee joint Experimental and nite element analysis
K.S. Halonen a,n, M.E. Mononen a,b, J.S. Jurvelin a, J. To
yrs a,b, J. Salo b, R.K. Korhonen a
a
b

Department of Applied Physics, University of Eastern Finland, POB 1627, FI-70211 Kuopio, Finland
Diagnostic Imaging Centre, Kuopio University Hospital, Kuopio, Finland

art ic l e i nf o

a b s t r a c t

Article history:
Accepted 3 April 2014

Novel conical beam CT-scanners offer high resolution imaging of knee structures with i.a. contrast media,
even under weight bearing. With this new technology, we aimed to determine cartilage strains and
meniscal movement in a human knee at 0, 1, 5, and 30 min of standing and compare them to the subjectspecic 3D nite element (FE) model. The FE model of the volunteer's knee, based on the geometry
obtained from magnetic resonance images, was created to simulate the creep. The effects of collagen
bril network stiffness, nonbrillar matrix modulus, permeability and uid ow boundary conditions on
the creep response in cartilage were investigated. In the experiment, 80% of the maximum strain in
cartilage developed immediately, after which the cartilage continued to deform slowly until the 30 min
time point. Cartilage strains and meniscus movement obtained from the FE model matched adequately
with the experimentally measured values. Reducing the bril network stiffness increased the mean
strains substantially, while the creep rate was primarily inuenced by an increase in the nonbrillar
matrix modulus. Changing the initial permeability and preventing uid ow through noncontacting
surfaces had a negligible effect on cartilage strains. The present results improve understanding of the
mechanisms controlling articular cartilage strains and meniscal movements in a knee joint under
physiological static loading. Ultimately a validated model could be used as a noninvasive diagnostic tool
to locate cartilage areas at risk for degeneration.
& 2014 Elsevier Ltd. All rights reserved.

Keywords:
Knee joint
Articular cartilage
Meniscus
Creep
Finite element analysis
Computed tomography
Magnetic resonance imaging

1. Introduction
Occupying nearly 80% of the wet weight (Buckwalter et al.,
2005), interstitial uid is the dominant constituent of articular
cartilage. Primarily with the help of collagen network (6080%
of the dry weight (Buckwalter et al., 2005; Mow et al., 1990)),
interstitial uid pressure helps the tissue to carry high instantaneous loads (Mow et al., 1990). During creep loading the uid
slowly redistributes and proteoglycans (PGs) (2040% of the dry
weight (Buckwalter et al., 2005; Mow et al., 1990)) take the main
role in resisting compressive loads at equilibrium, i.e. when the
uid ow has ceased (Bader et al., 1992; Mansour, 2004). This
creep behavior has been extensively studied in in vitro studies
(Armstrong and Mow, 1982; Ateshian et al., 1997; Boschetti, 2004;
Kempson et al., 1970; Li et al., 2008; Mow et al., 1980) and in situ
studies (Herberhold et al., 1999; Kb et al., 1998). Yet, to our
knowledge, the in vivo creep behavior of cartilage within a knee
joint has only been examined during short-term loading (Eckstein
et al., 2005; Hosseini et al., 2010, 2012).

Corresponding author. Tel.: 358 50 3580102; fax: 358 17 162585.


E-mail address: kimmo.halonen@uef. (K.S. Halonen).

http://dx.doi.org/10.1016/j.jbiomech.2014.04.013
0021-9290/& 2014 Elsevier Ltd. All rights reserved.

The nite element (FE) modeling allows the simulation of internal


strains and stresses within the knee joint during daily activities
such as standing or walking (Bae et al., 2012; Bendjaballah et al.,
1995; Donahue et al., 2002; Pea et al., 2006; Shirazi et al., 2008).
It can also be used to study mechanisms that control tissue responses
in mechanically loaded knee joints. In terms of the constituents of
articular cartilage, past 3D models of knee joints have included
collagen brils (Adouni et al., 2012; Gu and Li, 2011; Halonen et al.,
2013; Mononen et al., 2012; Shirazi et al., 2008; Shirazi and ShiraziAdl, 2009), strain-dependent permeability (Halonen et al., 2013;
Mononen et al., 2012), nonbrillar matrix mimicking the effect of
PGs (Halonen et al., 2013; Mononen et al., 2012; Shirazi et al., 2008;
Shirazi and Shirazi-Adl, 2009) and uid ow through free surfaces (Gu
and Li, 2011). To our knowledge, only Kazemi et al. (2011) simulated
the creep behavior of articular cartilage in a 3D knee joint geometry,
with their main focus on the analysis of uid pressure under a load of
300 N. However, they did not investigate how the uid ow through
noncontacting surfaces or different mechanical properties (specically
the nonbrillar matrix, collagen brils and permeability) of cartilage
affect the in vivo creep response under physiological joint loads.
In computed tomography arthrography (CTa), a contrast agent
is injected into the synovial cavity of a joint, causing a clear
contrast between cartilage and its surroundings, thus, giving

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K.S. Halonen et al. / Journal of Biomechanics 47 (2014) 24672474

geometrical information of the tissue when imaged (De Filippo


et al., 2009). In human cadaver studies, CTa has been shown to
assess cartilage thickness with even better accuracy than MRI
(El-Khoury et al., 2004; Llopis et al., 2012).
Being less tightly attached to the joint capsule, the lateral
meniscus is more mobile than the medial meniscus (Masouros
et al., 2008). While the meniscal movement has been well studied
during exion (Thompson et al., 1991; Tienen et al., 2005; Vedi
et al., 1999), the displacement of menisci is not well known during
static loading of a human knee.
This study aims to evaluate in vivo strains of articular cartilage
in a knee joint during 30 min of standing and compare the results
to the subject-specic FE model. The model is further used to
study the effect of the collagen brils, nonbrillar matrix and
internal uid ow and ow through noncontacting surfaces on the
creep response in cartilage. This study provides new information
about the mechanical behavior of articular cartilage and meniscal
movement in a knee joint during static loading, while taking a step
towards validating the FE model of a knee joint.

2. Materials and methods


The workow of both the experiment and the simulations is represented in Fig. 1.

2.1. Experimental setup


In order to determine the cartilage thickness (El-Khoury et al., 2004; Llopis
et al., 2012), an ioxaglate-based isotonic contrast agent solution of Hexabrix

(Mallinckrodt Inc., USA) (53% of the total volume) and distilled water (47% of the
total volume) was prepared to match the osmolarity of synovial uid (300 mOsm/L)
in the knee joint (Bertram and Krawetz, 2012). The left knee of a healthy 28-yearold volunteer (m 82 kg) was imaged using CTa (voxel size 0.2  0.2  0.2 mm3)
(Verity, Planmed, Finland). First, the imaging was conducted during light
cartilagecartilage contact (12.8 72.8% of body weight, BW), then immediately
after introducing 47.1 72.3% of BW, then subsequently 1, 5 and 30 min after the
initial contact. A creep time of 30 min was chosen because the preliminary test
showed that it was the last time point when the cartilage surfaces were
distinguishable. It took  25 s to complete each imaging step and approximately
35 s to prepare for the next one. Imaging under light cartilagecartilage contact
was conducted in order to obtain information about initial cartilage thicknesses
and locations of menisci. A custom made Linux program and a Wii Balance Board
(Nintendo, Japan) were used to monitor the weight distribution during the experiment. In order to control the load on the knee joint the subject wore harnesses
fastened to the ceiling (Fig. 2a). A quick-release lever was used to increase the load
from 12.8% to 47.1% of BW instantaneously.
In CTa images, femoral and tibial cartilages as well as menisci were manually
segmented using Mimics v.15.01 (Materialise, Belgium). At femoro-tibial contact
areas the cartilagecartilage interface was determined to be in the halfway point of
contrast agent lm between articulating surfaces (Fig. 2b, blue line). Local cartilage
thickness was determined in Matlab v. R2012a (MathWorks Inc., USA) by calculating the minimum distance between the vertices on the cartilage surface and the
cartilagebone interface of the 3D surface mesh (Stammberger et al., 1999). The
image stacks were manually co-registered on Analyze v. 10.0 (Biomedical Imaging
Source, MN) by rotating the stacks so that the edges of tibia bone in the reference
stack (before the load application) matched to those in all subsequent measurement points. This was done in order to enable the comparison of cartilage thickness
maps in the analysis of engineering strains in cartilage (cartilage deformation
divided by the initial thickness). CTa resolution and the subject's relatively thin
femoral cartilage caused some areas of the femoral cartilage to appear only 5 pixels
thick in the images, resulting in one pixel to cause a maximum error of 20% of the
tissue thickness (average error being 14.3%). The corresponding maximum and
average errors in the tibial cartilage were 6.7% and 4.4%, respectively. Therefore
only the thicker tibial cartilage was analyzed.

Fig. 1. Workow chart of the experiment and FE simulations.

K.S. Halonen et al. / Journal of Biomechanics 47 (2014) 24672474

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Fig. 2. (a) Experimental setup. Initially 12.8% of the subject's BW was applied on the knee joint (i.e. No contact), then the load was instantaneously increased to 47.1% of BW.
The harnesses attached to ceiling enabled the subject to maintain a stance that mimics two-legged standing while exerting approximately half of the BW on the knee joint.
The load on the knee was monitored with the Balance Board during the experiment. (b) Coronal view of a CECT image from the lateral tibial compartment at 30 min after
contact. The lines indicate the segmented cartilages at different time points. Red line indicates the initial cartilage thickness (12.8% of BW), green the thickness right after
introducing 47.1% of BW onto the knee and blue the thickness after 30 min. (c) FE model of the subject's left knee joint, constructed from MR images. (For interpretation of
the references to color in this gure legend, the reader is referred to the web version of this article.)

2.2. Finite element model


2.2.1. Model geometry and material properties
A model geometry was created from MR images of the subject's knee joint.
Articular cartilage was dened as bril-reinforced poroviscoelastic (FRPVE)
(Julkunen et al., 2007; Wilson et al., 2004, 2005) and menisci as bril reinforced
poroelastic (FRPE) (Dabiri and Li, 2013; Makris et al., 2011). Meniscal attachments
and ligaments were dened as linearly or nonlinearly elastic (Momersteeg et al.,
1995; Villegas et al., 2007). See Supplementary Appendix A for more details.
2.2.2. Boundary conditions
Node-to-surface contact was dened between master and slave surfaces.
Femoral cartilage was dened as a master surface to the tibial cartilage and
menisci, and the tibial cartilage was dened as a master surface to the menisci.
Bones were dened as rigid by xing the cartilagebone interface. A reference
point (Fig. 2c), used to move the femur, was dened at halfway between the
femoral epicondyles (Cappozzo et al., 1995; Halonen et al., 2013; Mononen et al.,
2012). The ligaments' femoral attachments and the femoral bonecartilage surface
were coupled to the reference point. In the simulations, all translations, rotations
and loads were applied through the reference point. Creep simulations consisted of
three steps. In the rst step (0.1 s), the femoral cartilage was rst brought into a
light contact with the tibial cartilage. In the second step (0.1 s), the following
actions were implemented simultaneously: stretching of the ligaments (see below),
rotation of the femur to the initial position of the knee measured from CTa images,
application of an axial force of 47.1% of BW (386 N) and external moment of
788 N mm (Kutzner et al., 2010). In the nal step (1 min of creep), the uid ow
through noncontacting surfaces was allowed.
The force exerted by the ligaments on the cartilage was simulated by stretching
the bottom anchorage points of the springs by 1.5 mm. The pre-elongation was
determined by matching the resultant reaction forces to those presented in the
literature. The total tibial reaction force with 47.1% BW loading was 880 N (107% of
BW), which is in good agreement with those obtained from experiments (Komistek
et al., 1997; Kutzner et al., 2010). Due to the CTa's limited eld of view (FOV), an
accurate determination of the varusvalgus and extensionexion angles proved to
be challenging. Especially a slight change in the varusvalgus angle greatly
inuenced the lateralmedial load distribution. Therefore the valgus angle was
adjusted to reproduce similar contact area to that observed in the experiments.
During creep, the orientation of the knee was approximately 3.51 valgus and 61
exion.
2.2.3. Simulations
Tissue creep was simulated with the FE model using physiological loads only
during the rst minute for two reasons: most of the cartilage strains occurred
during the rst seconds after the load application, and excessive strains occurred in
the surface elements under prolonged physiological loads (see more details in
Section 4). First, after implementing the material properties of cartilage (Table 1),
the creep behavior was simulated and compared to the experimental data. To
examine the effect of PGs, collagen brils and uid ow on cartilage strains, a
parametric study (Table 2) was conducted. For this aim, the following parameters
were varied: (1) nonbrillar matrix modulus Em (mimicking the PGs), (2) initial and

Table 1
Material parameters implemented for cartilage and menisci.
Material properties

Femoral
cartilage

Tibial cartilage

Menisci

E0 (MPa)

0.92a
150a

0.18a
23.6a

28b

1062a
0.215a
6a
0.15d
5.09a
0.80.15ze

1062a
0.106a
18a
0.15d
15.64a
0.80.15ze

0.5b
1.25c
0.36b
5.09
0.72c

E (MPa)
(MPa s)
Em (MPa)
k0 (10  15 m4/N s)
vm
M
nf

E0 initial bril network modulus, E strain-dependent bril network modulus,


damping coefcient, Em nonbrillar matrix modulus, k0 initial permeability,
vm Poisson's ratio, M exponential term for the strain-dependent permeability,
nf uid fraction, and z normalized depth.
a

Julkunen et al. (2007).


Dabiri and Li (2013).
c
Makris et al. (2011).
d
Wilson et al. (2003).
e
Mow and Guo (2002).
b

strain-dependent bril network moduli (E0, E) and the damping coefcient of the
viscoelastic brils () and (3) initial permeability (k0). To study the effect of uid
ow boundary conditions, the ow at cartilage and meniscus surfaces was rst
allowed through noncontacting surfaces and then inhibited. The mean cartilage
engineering strains were determined by averaging the strains at nodes. The strains
were obtained similarly to the experiment: the initial Euclidian distance between
the contact area surface node and the closest node in the cartilagebone interface
was calculated. The minimum distance between the new position of the surface
node (during loading of the knee joint) and cartilagebone interface node was
calculated and the strain was obtained by dividing the deformation with the initial
thickness.
Due to not being able to simulate the full 30 min with physiological loads,
creep simulations with an axial load of 50 N were conducted. See Supplementary
Appendix B.

3. Results
3.1. Experiment
During the loading experiment, the anterior horn of the lateral
meniscus was moved instantly after the initial contact, and the

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K.S. Halonen et al. / Journal of Biomechanics 47 (2014) 24672474

Table 2
Minimum and maximum values of the material parameters used in the
parametric study.
Parameter

Reference model

Min

Max

E0 (MPa)
E (MPa)
(MPa s)
Em (MPa)
k0 (10  15 m4/N s)
Fluid ow (noncontact surfaces)

0.18
23.6
1062
0.106
18
Yes (P 0)

0.1
13.6
700
0.106
1e  6
No

1
50
2000
1
1e 6

E0 initial bril network modulus, E strain-dependent bril network modulus,


damping coefcient, Em nonbrillar matrix modulus, k0 initial permeability,
and P uid pressure.

Table 3
Cartilage deformation during 30 min of standing (47.1% BW).
Time after
contact [min]

0
1
5
30

Lateral tibial compartment

Medial tibial compartment

Mean strain
[%]

Maximum
strain [%]

Mean strain
[%]

Maximum
strain [%]

9
10
10
12

24
26
23
30

5
6
10
10

29
19
32
39

3.2. Computational analysis


In the FE model, medial meniscal movement was slightly
different than that in the experiment (Fig. 3b). The reference
FE model, i.e. with the material parameters for femoral and tibial
cartilage and menisci obtained from the literature (Table 1),
slightly underestimated the experimentally measured mean
strains of cartilage, while the model with the reduced bril
stiffness improved the t (Fig. 5). The peak strains were 17% for
the lateral and 13% for the medial tibial compartment at 1 min
(corresponding experimental values were 26% and 19%, respectively). In the parametric study (Fig. 6), a change in the bril
network stiffness (E0, E and ; Table 2) shifted the creep response
the most (Fig. 6a). The difference in mean strains between the
model with the lowest and highest bril network stiffness was
1.4%-units for both lateral and medial compartments during the
entire loading period. Increasing the value of the nonbrillar
matrix modulus Em from 0.106 to 1.0 MPa (Table 2) decreased
the slope of the creep curve the most: the absolute difference in
the mean strains increased from 0.3%-units (0 min) to 0.5%-units
(1 min) in the lateral and from 0.3%-units (0 min) to 0.6%-units
(1 min) in the medial compartment (Fig. 6b). A twelve orders of
magnitude variation in the permeability caused a negligible effect
on mean strains (Fig. 6c). Prevention of the uid ow through
cartilage surfaces in the model, compared to the model with uid
ow through the noncontacting surfaces, decreased strains only
minimally (Fig. 6d).

4. Discussion
Fig. 3. (a) Meniscal movement during the experiment. (b) FE model shows the
meniscus displacement at the tibial cartilage surface at 60 s after the application of
load (47.1% of BW). Red and green lines represent meniscal movement in the FE
model before and after cartilagecartilage contact. After the contact, the menisci
remained stationary till the end of analysis. (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this article.)

entire lateral meniscus moved toward the anterior-lateral direction. After the initial contact, the meniscus remained relatively
stationary (Fig. 3a). The anterior horn of the medial meniscus
moved slightly toward the medial direction.
In the lateral and medial compartments, most of the measured peak strains were observed instantly after the loading:
24% and 29% in the lateral and medial compartments, respectively, when the peak strains at 30 min were 30% and 39%
(Table 3), respectively. However, cartilage continued to deform
throughout the entire loading duration (Fig. 4; Table 3). Peak
cartilage strains of 30% and 39% were observed in the lateral
and medial tibial compartments, respectively (Table 3). Highest
mean strains over the femoro-tibial contact area were 12% and
10% for the lateral and medial tibial compartments, respectively
(Table 3).

4.1. Summary
Articular cartilage strains and meniscal movements were measured during static loading of a volunteer's knee (standing)
and compared to the results obtained from the FE model of the
subject's knee joint. Excluding the anterior horn of the lateral
meniscus, the menisci remained nearly stationary during the
entire experiment. After the cartilage was compressed instantly,
a slow creep response until the end of the experiment was
observed. Higher average tissue strains of cartilage were measured
in the lateral than in the medial tibial compartment. The FE model
matched adequately the experimental data. The model was further
used to evaluate mechanisms that control the creep response of
cartilage in a knee joint (uid ow, collagen, and PGs). In the
model, collagen brils primarily controlled cartilage strains, while
PGs affected the creep rate. Fluid velocity and ow out from
cartilage to the joint space were found to have negligible effects on
strains.
4.2. Experiment
During the experiment, only the anterior horn of the lateral
meniscus moved during the loading, while the medial meniscus

K.S. Halonen et al. / Journal of Biomechanics 47 (2014) 24672474

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Fig. 4. Engineering strains in the tibial cartilage analyzed from CTa images of the subject's knee, before contact (12.8% of BW) vs. 0, 1, 5 and 30 min after contact (47.1%
of BW).

Fig. 5. Mean engineering strains in the cartilage contact area at (a) medial and (b) lateral tibial compartments. The FE model with the material parameters obtained from the
literature (Julkunen et al. 2007; Table 1) and a model with reduced collagen bril network stiffness (Table 2). Experimental data is also shown.

remained relatively stationary supporting the knee joint, distributing the load and reducing stresses on the medial tibial cartilage.
This is in agreement with clinical ndings suggesting that the
anterior horn of lateral meniscus is less susceptible to mechanical
damage compared to the posterior horn of medial meniscus (Kan
et al., 2010), thus implying that efforts should be made to preserve
the functional role of the medial posterior meniscus. If the lateral
meniscus is damaged, however, the risk of OA is 60% higher than in
the case of a damaged medial meniscus (Englund and Lohmander,
2004).
Tibial cartilage experienced over 70% of the maximum strain
during the rst seconds after implementing a load of  50% of BW.
Although conducted with 100% of BW, the study by Hosseini et al.
(2010) shows a similar tendency; 80% of the peak strains occurred

at 20 s after the load application, after which the rate of creep fell
close to zero during the 5 min experiment. On the other hand and
in contrast to Hosseini et al. (2010), our results indicate that tibial
cartilage continued to deform in compression during the entire
30 min of experimentation. Hosseini et al. (2010) also reported
peak strains of 11% for lateral and 9% for medial compartments at
20 s, where as we observed peak strains of 26% and 19% for lateral
and medial tibial cartilages after 1 min of loading. These differences between studies might arise from the analysis techniques.
Hosseini et al. (2010) calculated the cartilage strains based on
the penetration of femoral and tibial cartilage meshes into each
other, divided by the distance between femur and tibia. This
represents the average and combined strain of both the tibial
and femoral cartilages, i.e. due to thicker and softer tibial cartilage

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in tibial cartilage was calculated by using the minimum distance


method.
Schmidt et al. (1990) also found a rapid increase in cartilage
strain in a tensile creep test, followed by a very slow tissue
elongation up to 25,000 s. We do not know if longer creep time
in our experimental loading conguration would have also led to
longer creep deformation of cartilage. However, our 1 h FE
simulation suggests that the equilibrium was reached within that
time. The difference between the creep times may stem primarily
from the difference in loading conguration; in vitro tension vs.
in vivo compression. The viscoelastic component of collagen brils
dictates the tensile creep, while uid ow controls the creep
response in compression (Li et al., 2005). Since the characteristic
time for collagen brils is longer than that for uid, we believe
that static loading of human knee joint would lead to equilibrium
much faster than that of cartilage in tension (Schmidt et al., 1990).
4.3. Computational analysis

Fig. 6. The effect of (a) bril network stiffness (E0, E and ), (b) nonbrillar matrix
modulus (Em), (c) initial permeability (k0) and (d) uid ow boundary conditions on
mean engineering strains in the lateral and medial tibial compartments. For details,
see Table 2.

compared to the femoral cartilage, the values reported by Hosseini


et al. (2010) might underestimate tibial strains, and consequently,
overestimate femoral strains. In the present study, only the strain

The model was able to capture the experimentally observed


meniscal motion. During the FE simulation, the contact area
between the femoral cartilage and meniscal surfaces increased,
leading to the menisci bearing more weight. Consistently with
Kazemi et al. (2011), this contributed to the decrease in cartilage
stresses as the creep progressed.
The FE model could reproduce the observed mean strains of
cartilage. This was actually quite surprising, considering that the
initial material parameters were obtained from a study in which
bovine cartilage was investigated. Since there were numerous
parameters in the knee joint model, we did not pursue with
nding the optimal t to the experimental curve. With the model,
we rather concentrated nding mechanisms that control cartilage
creep in an intact human knee joint.
Changes in the collagen bril network stiffness shifted the
creep curve drastically. Because the absolute difference in mean
strains as a function of time was nearly constant between the
models with high and low bril network stiffness, the bril
contribution to the mean strains decreased as the creep advanced.
These results are consistent with our earlier ndings (Halonen
et al., 2013) as well as several studies suggesting that the collagen
network primarily controls the dynamic response of cartilage
(Bader et al., 1992; Korhonen et al., 2003; Laasanen et al., 2003;
Mizrahi et al., 1986). The results also suggest that collagen controls
the transient, short-term time points of cartilage creep in the knee.
However, in the simulations with a load of 50 N, high bril
network stiffness reduced mean strains by 27% while low bril
network stiffness increased mean strains by 11% during 30 min of
creep. The substantial change to the creep response suggests that
the collagen bril network contributes strongly to the equilibrium
response as well. This might be due to the fact that in the knee
joint geometry the collagen brils are attached to the bone on the
joint periphery and loading resembles in situ indentation.
The nonbrillar matrix modulus (simulating mainly the effect
of PGs) altered the creep rate the most. However, considering the
10-fold increase in the nonbrillar matrix modulus, its effect was
still minor compared to the shift in the creep curve induced by the
changes in the bril network stiffness. As PGs have mainly been
suggested to contribute to the equilibrium response (Kempson
et al., 1970; Korhonen et al., 2003; Laasanen et al., 2003), its effect
on the longer-term time points of the creep would likely become
even more evident. This is supported by the fact that in the
simulations with a load of 50 N, the reduced slope of the creep
curve induced by the increased nonbrillar matrix modulus
(Table 2) caused a reduction of 31% in mean strains at 30 min.
A variation of twelve orders of magnitude in the initial permeability of articular cartilage had a negligible effect on the creep

K.S. Halonen et al. / Journal of Biomechanics 47 (2014) 24672474

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response during the minute-long simulation. Also the uid ow


boundary condition (either preventing uid ow through cartilage
surfaces or allowing ow through noncontacting surfaces) had a
negligible effect on cartilage creep due to the small amount of free
surfaces. In the knee joint geometry, the vast majority of tibial
cartilage surface is compressed by femoral cartilage and menisci
(Haemer et al., 2012). This led to fairly uniform pore pressure
distribution throughout the depth and width of the cartilage
under the contacting areas a nding consistent with Kazemi
et al. (2011). The creep behavior of cartilage arose just primarily
from a redistribution of uid within cartilage and collagen viscoelasticity. Increase in the permeability in the 50 N simulation with
more free surface areas showed a drastic increase in the mean
strains, which is in agreement with this explanation. A closer
inspection revealed that due to geometry of the cartilage and
underlying bone, after 20 min of creep the uid velocity increased
substantially through the free surface areas. Preventing the uid
ow also substantially reduced the strains at 30 min an effect
also not present in the minute-long simulations with physiological
loads. The results suggest that if most of the cartilage surface is not
free (65% in the studied knee), the uid ow boundary condition is
not an important factor to consider in knee joint models, at least if
short-term loadings are modeled. In their stressrelaxation simulations, Gu and Li (2011) came to the same conclusion.

determination of extensionexion and varusvalgus angles, causing a potential mismatch in the angles between the experiment
and the model.

4.4. Limitations

The nancial support from the Kuopio University Hospital,


Kuopio, Finland (EVO, Grant 5041722), the International Doctoral
Programme in Biomedical Engineering and Medical Physics, Jenny
& Antti Wihuri foundation, Academy of Finland (Grants 269315,
138574 and 218038), and the strategic funding of the University of
Eastern Finland and the European Research Council under the
European Union's Seventh Framework Programme (FP/20072013)/ERC Grant Agreement no. 281180 is acknowledged. Dr.
James Fick is acknowledged for the English review and Juuso
Honkanen for the technical help with the CT. CSC-IT Center for
Science, Finland, is acknowledged for computing resources.

Some limitations of this study must be noted. The substantial


(880 N) load exerted by the ligaments caused excessive element
strains in the tibial cartilage, preventing the simulation of the full
30 min of loading. Because of this and the fact that 80% of the
maximum strains occurred during the rst few seconds after the
application of load, only the rst minute of creep was simulated
with physiological loads and full 30 min was simulated with 50 N
load. As can be seen from aforementioned discussions, the conclusions from the 50 N simulation were consistent with the
conclusions (effects of tissue parameters on longer-term creep
deformation) that were drawn from the 1 min simulation with the
physiological load. Therefore we argue that even though the
absolute strain values would be different than with physiological
loads, the conclusions remain the same. Also, because of the ringlike structure of the applied cone beam CT-scanner, the subject
was unable to stand on both feet. Rather, the weight of the subject
was monitored and kept about 50% of the BW and the other
leg had to be raised as shown in Fig. 2. This may have caused
nonuniform stress distribution between the compartments. In the
FE model, the use of springs to represent ligaments, instead of 3D
solid ligaments, may cause uncertainties for the joint and meniscal
motion. However, we argue that the 3D ligaments mainly affect
the meniscal motion during gait, when certain parts of ligaments
(especially in MCL and LCL) extend and others contract (Thornton
et al., 2007). There are also contacts between ligaments (for
instance between ACL and PCL (Proffen et al., 2012)) that cannot
be modeled using the spring elements. However, in static loading
such as in the present study, the LCL and MCL do not notably affect
the meniscal motion. Rather, the joint movement is mainly
restricted by the ACL, which also experienced the greatest forces
in our model. The manual co-registration of image stacks (see
Section 2) may have slightly inuenced the results. However,
while the iterative closest point algorithm has been successfully
implemented by several groups (Carpenter et al., 2009; van
de Giessen et al., 2009; Zhu and Li, 2011), Dean et al. (2012)
reported no signicant differences between manual and automated co-registration processes. In addition, we did not see signicant operator-dependent differences in manual co-registration.
The limited FOV also caused some uncertainties to the

5. Conclusions
The present study provides novel understanding of the effect of
static loading of human knee joint on articular cartilage strains
and meniscal movement. The study also points out the important
role of collagen on the short-term creep deformation of cartilage
in the knee. The present experimental method could be applied
to characterize the effect of joint disorders on cartilage strains,
meniscus movements, and risk locations in joints. Furthermore, a
valid computational model is a step toward noninvasive diagnostics and could help evaluate possible failure points in joints.

Conicts of interest statement


None.

Acknowledgments

Appendix A. Supplementary information


Supplementary data associated with this article can be found in
the online version at http://dx.doi.org/10.1016/j.jbiomech.2014.04.013.
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