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Journal of Biomechanics
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www.JBiomech.com
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).
http://dx.doi.org/10.1016/j.jbiomech.2014.04.013
0021-9290/& 2014 Elsevier Ltd. All rights reserved.
2468
(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.
2469
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.)
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
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
2470
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
Table 3
Cartilage deformation during 30 min of standing (47.1% BW).
Time after
contact [min]
0
1
5
30
Mean strain
[%]
Maximum
strain [%]
Mean strain
[%]
Maximum
strain [%]
9
10
10
12
24
26
23
30
5
6
10
10
29
19
32
39
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
2471
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
2472
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.
2473
determination of extensionexion and varusvalgus angles, causing a potential mismatch in the angles between the experiment
and the model.
4.4. Limitations
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.
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