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PII: S0021-9290(16)30549-8
DOI: http://dx.doi.org/10.1016/j.jbiomech.2016.05.002
Reference: BM7719
To appear in: Journal of Biomechanics
Received date: 8 September 2015
Revised date: 17 April 2016
Accepted date: 2 May 2016
Cite this article as: K.S. Halonen, M.E. Mononen, J. Töyräs, H. Kröger, A.
Joukainen and R.K. Korhonen, Optimal graft stiffness and pre-strain restore
normal joint motion and cartilage responses in ACL reconstructed knee, Journal
of Biomechanics, http://dx.doi.org/10.1016/j.jbiomech.2016.05.002
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Optimal graft stiffness and pre-strain restore normal
joint motion and cartilage responses in ACL
reconstructed knee
Corresponding author:
Kimmo Halonen
Department of Applied Physics, University of Eastern Finland
POB 1627, FI-70211 Kuopio, Finland
Tel. +358 50 3580102
Fax. +358 17 162585
E-mail: kimmo.halonen@uef.fi
Abstract
Anterior cruciate ligament (ACL) rupture leads to abnormal loading of the knee joint and
increases the risk of osteoarthritis. It is unclear how different ACL reconstruction techniques
affect knee joint motion and mechanics. As the in vivo measurement of knee joint loading is
not possible, we used finite element analysis to assess the outcome of ACL reconstruction
techniques.
1
Effects of different ACL reconstruction techniques on knee joint mechanics were studied
using six models during gait; with 1) healthy ACL, 2) ACL rupture, 3) single bundle ACL
Early in the gait, the ACL rupture caused substantially increased tibial translation in the
anterior direction as well as a smaller but increased lateral translation and internal tibial
rotation. ACL rupture substantially reduced average stresses and strains, while local peak
stresses and strains could be either increased or decreased. Single bundle and double bundle
reconstructions restored joint motion close to normal levels. However, cartilage strains and
stresses were elevated during the entire gait cycle. Models with modulated graft stiffness and
pre-strain restored the joint motion and cartilage stresses and strains close to the normal,
healthy levels.
Results suggest that rather than the choice of reconstruction technique, stiffness and pre-
strain of the ACL reconstruction affect the motion and mechanics of the operated knee. We
suggest that an optimal choice of graft properties might help restore normal knee joint
Keywords: Anterior cruciate ligament, reconstruction, graft, knee joint, articular cartilage,
gait, finite element analysis
1. Introduction
Anterior cruciate ligament (ACL) is an essential structure of the knee, providing stability to
the joint during its movement. ACL rupture is a common, often sports-related injury, which if
left untreated, has been shown to greatly increase the risk of osteoarthritis (OA) in the knee
articular cartilage (Barenius et al., 2014; Kessler et al., 2008). Even though the mechanism
2
behind the development of OA in relation to the ACL injury is not fully understood, the
altered motion of the knee and cartilage stresses are believed to be major causes (Kessler et
al., 2008; Tsoukas et al., 2015). In ACL reconstruction, an autograft, harvested from the
al., 2008). A recent high quality randomized controlled trial, comparing conservative
treatment with early ACL reconstruction, showed similar clinical follow-up results between
the groups at five years. However, 51% of the conservative rehabilitation-only treatment
group had gone through reconstructive surgery during the 5-year follow-up (Frobell et al.,
2013).
Single bundle and double bundle techniques are the most common ACL reconstruction
techniques (Meredick et al., 2008). In the single bundle reconstruction technique, a graft is
harvested either from the central part of the patellar tendon or from gracilis and
semitendinosus tendons (Herrington et al., 2005). Two insertion holes are drilled, one into
femur and the other into tibia. The graft is then tensioned and fastened with special bone
screws (Kim et al., 2013). In the double bundle reconstruction technique, two grafts, usually
folded gracilis and semitendinosus tendons, are inserted into the knee to mimic the anterior-
medial (AM) and posterior-lateral (PL) bundles of a healthy ACL. Though the causality
mechanism of ACL rupture and secondary OA is not known, the ability to preserve knee joint
function seems to be important for minimizing the risk of OA (Barenius et al., 2014; Kessler
et al., 2008). Therefore a means to assess and optimize the outcome of ACL reconstruction is
needed.
Strains in the knee joint cartilage have been measured in vivo during static loading (Halonen
et al., 2014; Hosseini et al., 2010). However, during dynamic gait loading, direct assessment
of stresses and strains in articular cartilage is not possible, but they can be simulated with
finite element (FE) modeling (Bae et al., 2012; Peña et al., 2006; Shirazi et al., 2008). In
3
previous FE studies, ACL rupture has either been modeled using a fixed flexion angle
(Huang et al., 2012; Peña et al., 2005) or a simple linear elastic material model for cartilage
(Moglo and Shirazi-Adl, 2003; Yao et al., 2005). Simulation of gait is obviously more
relevant when assessing the risk of OA. In order to study the effect of changes in the ACL on
the knee motion and cartilage responses, implementation of the gait as forces and moments is
properties have an influence when assessing risk locations and mechanisms of damage in
joints (Brody, 2014; Hosseini et al., 2014). However, for instance changes in collagen fibril
strains (high strains may lead to damage and OA (Butler et al. 1978; Wang 2007)) due to
injury and/or reconstruction have not been shown before. Furthermore, these complex
properties may also have an effect on other parameters, such as fluid pressure and maximum
principal stress, the latter one describing typically tissue failure (Danso et al. 2014; Mononen
et al. 2016).
In this study, we simulated the effect of ACL rupture and reconstruction techniques on the
knee joint motion as well as stresses and strains in the tibial articular cartilage during the
stance phase of gait. A model with ACL deficiency as well as two most common (Herrington
et al., 2005) reconstruction models, single bundle and double bundle ACL reconstructions,
were compared with the healthy knee joint model. We hypothesized that, due to the way the
double bundle technique mimics the anatomy of a healthy ACL, it would preserve the knee
motion better than the single bundle, but cause similar stresses and strains in the tibial
articular cartilage (as a consequence of the graft stiffness). We also hypothesized that the
reduced stiffness and pre-strain of the graft would cause decreased stresses and strains in the
cartilage. The reduced stiffness and pre-strain were tested on both the single bundle and
4
2. Materials and methods
Gait analysis
Analysis of the subject’s gait pattern was conducted in a motion analysis laboratory and is
described in detail in Klodowski et al. (2015) and Halonen et al. (2016). The final gait input
(Fig. 2 a-c) for the FE model (see below) included the quadriceps forces as well as knee joint
moments and translational forces, excluding the extension-flexion angle, which was defined
as rotation. Similar implementation of the gait data into the FE model was done recently
It has been reported that the passive internal-external moment is approximately 10-20% of
the measured ones (Adouni et al., 2012). Another study by Tanska et al. (2015) found the best
match with experimental studies (Benoit et al., 2006; Kabada et al., 1990; Reinschmidt et al.,
1997) by implementing 10% of the internal-external moment in the knee joint FE model. In
this study, the supporting effect of muscles and other tissues were accounted for by using
50% of the total varus-valgus and internal-external moments within the knee, which was
found to produce knee rotations that matched the observed ones well (Halonen et al., 2016)
(better than when implementing 20% of the measured values (Adouni et al., 2012) – this was
also tested). The difference most likely arises from the use of patella and quadriceps forces in
contrast to the model without patella (such as in the model of Tanska et al. (2015)). In
addition, the resulting amplitudes of the moments were in accordance with experimental
The subject’s knee was imaged with an MR scanner (a clinical 3.0 T scanner, Philips) using
3D fast spin-echo sequence (VISTA) (in-plane resolution = 0.5 mm, slice thickness = 0.5
5
mm, TR = 1300 ms, TE = 32.3 ms). The knee geometry (Fig. 3a) was obtained by
segmentation in Mimics v.15.01 (Materialise). The geometry was imported into Abaqus v.
6.12-3 (Dassault Systèmes Simulia) and meshed. The femoral cartilage and menisci were
meshed with four element layers. By using the ‘subdivide’ option and TIE constraint, tibial
cartilage was meshed more densely at the superficial zone than at the deep zone in order to
improve convergence and accuracy of the implementation of the collagen fibril architecture.
The element type was set as C3D8P (Halonen et al., 2014) and the number of elements for
femoral, tibial and patellar cartilages and menisci was 8980, 20710, 738 and 9300,
respectively. Frictionless surface-to-surface contact was defined for all contacting surfaces.
The master surfaces were determined as a surface, whereas the slave surfaces were defined as
a node surface (CNS). The master-to-slave interactions were: femoral cartilage to tibial
cartilage and menisci, menisci to tibia, patellar cartilage to femoral cartilage. A convergence
test for the model was conducted in our previous work (Halonen et al., 2014).
Fibril-reinforced poroviscoelastic (FRPVE) material (Wilson et al., 2004; Wilson et al., 2005)
was defined for the cartilages and menisci. For cartilages, depth-dependent arcade-like
collagen fibril architecture with split-line patterns was implemented. The FRPVE material
model is well validated vs. experiments in previous studies (Wilson et al., 2004; Wilson et al.,
2005; Julkunen et al., 2007; Halonen et al., 2014), and it allows for instance the evaluation of
fibril strains. Find more details about the material model and its time-dependent response to
compressive and tensile loading from the Supplementary material. Only circumferential
collagen fibrils were implemented into the menisci. See our previous papers for more details
of the materials in the knee joint model (Halonen et al., 2013; Mononen et al., 2012). Split-
line architecture was implemented in the superior-inferior direction in the patellar cartilage
6
The ACL and posterior cruciate ligament (PCL) were segmented from the MR images, and
the exact insertion sites in femur and tibia were determined (Fig. 3b-d). Two experienced
orthopaedic surgeons were consulted in the segmentation as well as the insertion sites for the
single bundle and double bundle ACL reconstruction techniques. The healthy ACL consisted
bundles were included in the PCL (Makris et al., 2000). In the single bundle and double
bundle ACL reconstructions, the graft was set as approximately 6-8 mm in diameter. The
exact locations of femoral and tibial graft insertion sites are presented in Fig. 3b-c.
The ligaments were assumed to be in tension at their normal length obtained from MRI, so
that a pre-strain of 5% was applied to the ACL and PCL and 4% to the LCL and MCL
(Gantoi et al., 2013). The pre-strains were implemented using the nonlinear spring response
option in Abaqus. Ligament stiffness values were k=201 Nmm-1 for ACL and k=258 Nmm-1
for PCL. For MCL and LCL, the stiffness values were k=114 Nmm-1 and k=134 Nmm-1,
gracilis/semitendinosus graft with a stiffness of k=715 Nmm-1 (Kim et al., 2003). A review
study by Herrington et al. (2005) showed no significant differences between the outcomes of
reconstructions using patellar tendon grafts and gracilis/semitendinosus grafts. Therefore only
Linear springs without pre-strains were used to represent meniscal attachments and tendons.
The combined total spring constant of each meniscal horn attachment was 350 Nmm-1
(Villegas et al., 2007). The stiffness values used for quadriceps tendon and patellar tendon
were 475 Nmm-1 and 545 Nmm-1, respectively (Schatzmann et al., 1998). In order to omit the
compression resistance of linear springs, the lateral and medial patellofemoral ligaments
(LPFL and MPFL, respectively) were defined as linearly elastic truss elements with no
7
compressive stiffness. The elastic modulus was defined as 17 MPa for LPFL and 19 MPa for
MPFL (Atkinson et al., 2000). The Poisson’s ratio was set to 0.499.
Six models with varying ACL properties were created (see also Fig. 3):
1. Healthy ACL model with anatomically accurate insertion sites and AM and PL
3. Single bundle ACL reconstruction model, consisting of a single bundle (k=715 Nmm-
1
, 5% pre-strain).
Nmm-1, 5% pre-strain).
6. ACL reconstruction model with less pre-strain (k=715 Nmm-1, 2% pre-strain (change
1) In the first step, the femoral cartilage was brought into light contact with the patellar
and tibial cartilages as well as the menisci. The cartilage-bone interface of the tibial
2) In the second step, the femur was rotated from its position in the MR images (9°
flexion) to the initial position (5.73° flexion) at the beginning of the stance phase of
gait, observed in the motion analysis. Boundary conditions for translations and
internal-external and varus-valgus rotations were removed, and initial forces and
8
moments (at the beginning of stance phase of gait) were implemented into the model
through the reference point, i.e. the midpoint between the epicondyles of femur,
directions) and extension-flexion rotation were implemented (Fig. 2a-c). All femoral
forces, moments and rotations with respect to tibia were implemented through the
reference point (see step 2). The quadriceps force followed the direction of the distal-
To assess the effect of the ACL rupture as well as the single bundle and double bundle
reconstruction techniques, tibial rotations with respect to femur were determined from the
reference point described above as a function of the gait. Furthermore, reaction forces
through the joint as well as stresses, strains, contact pressures and fluid pressures of tibial
cartilage in all models were determined and compared with the healthy knee joint model.
Abaqus/standard with soils consolidation (*SOILS) analysis was used in all simulations. This
3. Results
Compared with the healthy ACL model (Fig. 4a), an increase of up to 542% in the anterior
translation of tibia relative to femur was observed in the model with the ACL rupture. The
change was most prominent during the heel strike and lowest between ipsilateral heelrise and
contralateral heelstrike. Lateral tibial translation was also increased in the model with the
ACL rupture (compared with the healthy joint, Fig. 4c), and an increase of up to 261% in the
9
internal rotation was observed (Fig. 4e). Single bundle and double bundle reconstruction
models showed slightly smaller or similar joint motion as simulated for the healthy knee joint
model. The best fit in rotations and translations was observed between the weakened (softer)
single bundle reconstruction model and the healthy knee joint model (Fig. 4). The weakened
double bundle reconstruction model showed a similar response in all observed parameters
with the weakened single bundle model (results not shown). Correspondingly, the double
bundle reconstruction model with reduced pre-strain also showed a similar response in all
observed parameters with the single bundle model with reduced pre-strain (results not
shown).
During the first peak force of gait, the ACL rupture shifted the contact pressure and therefore
maximum principal strain areas (peak strain 17.8%) in the posterior direction in both lateral
and medial tibial cartilage (Fig. 5b), compared with the healthy joint model (peak strain
13.8%) (Fig. 5a). The same behavior was observed in fibril strain, fluid pressure and
maximum principal stress (Figs. 6 and 7). The maximum difference between the normal,
healthy joint model and that with the ACL rupture was observed in maximum principal stress
(51%)
Similar maximum principal strains were seen in both single bundle and double bundle ACL
reconstruction models (peak values 14.9% and 14.8%, respectively) (Fig. 5c, d). Compared
with the healthy ACL model, the strains were slightly increased in both reconstruction
models, particularly in the anterior direction of the joint surface. The same behavior was
observed in other parameters (Figs. 6 and 7). The weakened single bundle model and the
single bundle model with less graft pre-strain produced similar maximum principal strains
(peak values 13.8% and 14.6%, respectively) (Fig. 5e, f). Those strains, as well as all the
other analyzed parameters were similar to those in the normal, healthy joint model (Fig. 5, 6
and 7). The maximum difference in parameters between the model with less pre-strain and
10
the healthy joint model was 18% in maximum principal stress. Compared with the healthy
joint model, the maximum difference in the model with the weakened graft was only 10%, in
Same trend was observed in the quantitative analysis of average reaction forces (Fig. 8),
contact pressures, maximum principal strains, fibril strains, fluid pressures and maximum
principal stresses during the entire stance phase of gait (Fig. 9). Lowest values in all
parameters were observed in the ACL rupture model throughout the whole gait apart from the
contact pressure, which showed a small increase during the first 10% of the stance. The
maximum difference between the normal, healthy joint model and that with the ACL rupture
was observed in fibril strains and maximum principal stresses, which were both reduced by
up to 80% at 10% of the stance. Throughout the stance phase, the double bundle
reconstruction model produced stresses and strains very similar to those in the single bundle
model, which were elevated compared with the healthy ACL model with the maximum
difference in fluid pressure (79% at 10% of the stance). Apart from the very end of the
stance, the weakened (softer) single bundle reconstruction showed stresses and strains most
similar to those in the healthy ACL model, with a maximum difference in fibril strains (10%
at 5% of stance). The single bundle reconstruction model with reduced pre-strain slightly
increased contact pressures, strains and stresses during the first 50% of stance compared with
the healthy ACL model. The maximum difference was in contact pressure (37% at 5% of the
stance).
4. Discussion
We investigated the effect of ACL rupture and reconstruction techniques on the femoral
rotations and tibial cartilage response during the stance phase of gait. The healthy knee joint
11
model showed very similar translations and rotations as those reported in a bone-pin study by
Benoit et al., (2007) a dual fluoroscopy study by Kozanek et al. (2009). Ruptured ACL
caused a substantially increased tibial translation in the anterior direction, and a small shift in
the lateral direction. The internal tibial rotation was also increased due to the ACL rupture.
Although knee joint forces were reduced compared with the healthy knee joint, the ACL
rupture shifted the stress and strain areas in the tibial cartilage, especially in the medial tibial
plateau. The single bundle and double bundle ACL reconstruction models were able to
restore the translational and rotational motions of the knee, but they increased the forces,
stresses and strains experienced by the joint and cartilage. The weakened single and double
bundle reconstruction (softer graft) models and those with less graft pre-strain produced the
most similar rotations, translations, reaction forces, stresses and strains compared with the
It is known that ACL rupture increases anterior tibial translation and internal tibial rotation
(Beynnon et al., 2002; Zhang et al., 2003), the first one being primary and the latter one
secondary restraint (Nigg and Herzog, 2007). This phenomenon was observed in our model
with the ACL rupture. The magnitude of translation in ACL-deficient knees was very similar
to those in the experimental studies (Kvist and Gillquist, 2001; Sonesson and Kvist, 2015).
with healthy knees) has been reported than what was observed in this study (Kvist and
Gillquist, 2001; Sonesson and Kvist, 2015). The differences arise possibly due to different
testing protocols (e.g. only flexion in Kvist et al. (2001)). In addition, in those studies the
ACL-deficient knee is usually compared with the contralateral healthy knee, whereas in our
model it was the same knee that had its ACL removed. Despite this, the simulated increase in
anterior tibial translation in the ACL-deficient model was similar to that reported by Zhang et
al. (2003). In addition to these increased motions, the ACL rupture model showed slightly
12
increased lateral tibial translation. This might contribute to the increased peak stresses and
Even though the average stresses, strains, fluid pressures and contact pressures decreased due
to the ACL rupture, the tibiofemoral contact area shifted toward posterior direction. This
caused elevated values in all analyzed parameters in the posterior direction and decreased
values in the anterior direction. This could expose the posterior side of the medial tibial
It has been suggested that the double bundle reconstruction is able to replicate the function of
the ACL better than the single bundle (Yagi et al., 2002), which mainly mimics the AM
bundle of a healthy ACL (Woo et al., 2002). In our study, both simulated techniques were
able to restore the rotational and translational joint movements close to the normal levels.
This was against our hypothesis, as we expected the double bundle method (mimicking the
AM and PL bundles of a healthy ACL) to perform better than the single bundle. However, the
results are in accordance with the results by Meredick et al. (2008). Further, the differences in
stresses and strains between the single bundle and double bundle techniques were found to be
minimal, which is in accordance with the hypothesis. Though, and in accordance with Yagi et
al. (2002), stresses, strains and fluid pressures experienced by cartilage were slightly lower in
the model with the double bundle than that with the single bundle.
The results suggest that in order to restore the forces within the joint and stresses and strains
of cartilage, the stiffness of the graft plays a crucial role. Throughout all analyses, the models
with modulated properties of the single bundle reconstruction (softer graft and less pre-strain)
produced the best match with the normal, healthy joint model. This is consistent with our
hypothesis. With the chosen material parameters, the graft stiffness rather than the graft pre-
strain had more influence on the restoration of the normal, healthy knee joint motion.
13
However, it should be noted that this conclusion might change with other choices of the
material parameters. Nonetheless, this result suggests that with optimal stiffness and pre-
strain of the graft, it should be possible to fully restore the normal, healthy joint motion and
mechanics. In order to prevent OA, it would be important to be able to plan the operation and
We also tested if the double bundle technique could achieve a better match with the healthy
ACL by creating a model with weakened double bundle graft. The model showed a similarly
good match with the normal, healthy knee joint model as the weakened single bundle model
It has been shown that the graft loses some of its tension immediately after the operation,
cadaveric study reported a loss of 46% of initial pretension at the end of 1500 extension-
flexion cycles (Arnold et al., 2005). The results of this study emphasize the importance of the
final tension the graft ends up with, as it has an effect on the strains and stresses the articular
cartilage undergoes during daily activities. It is beneficial for the function of the knee that the
This study has a few limitations. Only one subject was included in the study. However, we
emphasize that this is a methodological study, in which the model is first validated and then
applied for further clinical studies with more subjects. Furthermore, these mechanisms we
present here should not depend on the joint geometry or other variables. Obviously, the exact
values of strains and stresses would vary from patient to patient. However, the conclusions
would not change (Räsänen et al., 2013). Location of the ACL reconstruction insertion sites
confirm the real anatomic location of the insertion sites. In the future, the effect of the
14
variation in the locations of the insertion sites of the graft on knee joint motion and
mechanics could be an interesting topic (Nishizawa et al., 2015). It has been shown that
patients with a ruptured ACL exhibit reduced range of motion in flexion (DeVita et al.,
1998). Since this was a simulation study and we obviously did not have information of the
possible change in the subject’s knee motion due to ACL rupture, we decided to keep all
The results may help explain why the risk of post-traumatic OA is or is not increased in
ACL-deficient (or reconstructed) knees. The model shows that in ACL deficient knees,
despite the lack of tension by the ligament, local stresses and strains can be increased due to
changes in knee joint motion. On the other hand, the high stiffness of ACL graft increases the
stresses and strains in the tibial cartilage, therefore likely increasing the risk of post-traumatic
OA. The present study further suggests that, for the outcome of an ACL repair operation, the
stiffness and pre-strain of the reconstructed ACL, rather than the choice of the technique, play
a crucial role in the restoration of the knee joint function and cartilage responses.
Conflicts of interest
None.
Acknowledgements
Medical Physics (iBioMEP), Jenny & Antti Wihuri Foundation, Academy of Finland
(138574, 286526), Sigrid Juselius Foundation, Kuopio University Hospital (VTR, project
5041752), the strategic funding of the University of Eastern Finland and European Research
Council under the European Union’s Seventh Framework Programme (FP/2007-2013), ERC
15
Grant Agreement no. 281180 is acknowledged. CSC-IT Center for Science, Finland, is
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Figure legends
Fig 2. Gait input for the FE model. (a) Internal-external and varus-valgus moments as well as
extension-flexion rotation. The moments are scaled to 50% of the ones obtained from gait
analysis (see text for details). (b) Total quadriceps force and its components. (c) Translational
20
forces. The dashed lines represent ipsilateral heelrise and contralateral heelstrike,
respectively.
Fig 3. (a) Finite element model, sagittal view. (b) Axial view of the tibial attachments of
healthy ACL and PCL (red and blue areas, respectively) as well as the tibial insertions of
simulated single bundle and double bundle ACL reconstruction techniques. (c) Sagittal view
of the femoral attachment of a healthy ACL (red area) and the insertions of simulated single
bundle and double bundle ACL reconstruction techniques. (d) Reference point (see text) and
Fig 4. Tibial translations (a)-(c) and rotations (d)-(e) with respect to femur during the stance
phase of gait. (a) Posterior-anterior translation. (b) Inferior-superior translation. (c) Medial-
lateral translation. (d) Valgus-varus rotation. (e) External-internal rotation. (f) Flexion-
extension rotation. Extension-flexion rotations are identical in all models because they were
Fig 5. Maximum principal strains in tibial cartilage surface during the first peak force of gait
(20% of stance). (a) Healthy ACL. (b) ACL rupture. (c) Single bundle ACL reconstruction.
(d) Double bundle ACL reconstruction. (e) Weakened single bundle ACL reconstruction. (e)
Fig 6. Differences in maximum principal strains (a)-(e) and fibril strains (f)-(j) in the tibial
cartilage surface. Values of the healthy joint model are subtracted from the values of other
Fig 7. Differences in fluid pressures (a)-(e) and maximum principal stresses (f)-(j) in the
tibial cartilage surface. Values of the healthy joint model are subtracted from the values of
other models.
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Fig 8. Tibial reaction forces through the joint surfaces during the stance phase of gait. (a)
Fig 9. Average values of the analyzed parameters in the contact area of the medial tibial
cartilage surface during the stance phase of gait. (a) Contact pressures, (b) maximum
principal strains, (c) fibril strains (d) fluid pressures and (e) maximum principal stresses.
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Figure 1
Figure 2 REVISED
Figure 3 REVISED
Figure 4 REVISED
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9