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Computer Methods in Biomechanics and Biomedical


Engineering
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Finite element analysis of the meniscectomised tibio-


femoral joint: implementation of advanced articular
cartilage models
ab ac a a
Lorenza Mattei , Eleonora Campioni , Mario Alberto Accardi & Daniele Dini
a
Department of Mechanical Engineering, Imperial College London, South Kensington
Campus, Exhibition Road, London SW7 2AZ, UK
b
Department of Civil and Industrial Engineering, University of Pisa, Largo Lucio Lazzarino 1,
Pisa 56122, Italy
c
Department of Mechanical and Civil Engineering, University of Modena and Reggio Emilia,
Via Vignolese, 905/b, 41125 Modena, Italy
Published online: 01 Mar 2013.

To cite this article: Lorenza Mattei, Eleonora Campioni, Mario Alberto Accardi & Daniele Dini (2014) Finite element analysis
of the meniscectomised tibio-femoral joint: implementation of advanced articular cartilage models, Computer Methods in
Biomechanics and Biomedical Engineering, 17:14, 1553-1571, DOI: 10.1080/10255842.2012.758253

To link to this article: http://dx.doi.org/10.1080/10255842.2012.758253

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Computer Methods in Biomechanics and Biomedical Engineering, 2014
Vol. 17, No. 14, 1553– 1571, http://dx.doi.org/10.1080/10255842.2012.758253

Finite element analysis of the meniscectomised tibio-femoral joint: implementation of advanced


articular cartilage models
Lorenza Matteia,b*, Eleonora Campionia,c, Mario Alberto Accardia and Daniele Dinia
a
Department of Mechanical Engineering, Imperial College London, South Kensington Campus, Exhibition Road, London SW7 2AZ, UK;
b
Department of Civil and Industrial Engineering, University of Pisa, Largo Lucio Lazzarino 1, Pisa 56122, Italy; cDepartment of
Mechanical and Civil Engineering, University of Modena and Reggio Emilia, Via Vignolese, 905/b, 41125 Modena, Italy
(Received 21 May 2012; final version received 10 December 2012)

The article presents advanced computer simulations aimed at the accurate modelling of human tibio-femoral joints (TFJs) in
terms of anatomy, physiological loading and constitutive behaviour of the tissues. The main objective of this research is to
demonstrate the implications that the implementation of different articular cartilage models have on the prediction of the
joint response. Several biphasic material constitutive laws are tested using a finite element package and compared to the
monophasic linear elastic description, often still used to predict the instantaneous response of the cartilage in 3D knee
models. Thus, the importance of adequately capturing the contribution of the interstitial fluid support is proved using a
simplified 3D model; subsequently, a biphasic poroviscoelastic non-linear constitutive law is implemented to study the
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response of a patient-specific TFJ subjected to simplified walking cycles. The time evolution of stresses, pore pressure,
contact areas and joint displacements is captured and compared with existing meniscectomised knee models. Contact
pressures and areas obtained using the developed numerical simulations are in agreement with the existing experimental
evidence for meniscectomised human knee joints. The results are then used to predict the most likely site for the origin of
mechanical damage, i.e. the medial cartilage surface for the specific case analysed in the present contribution. Finally, future
research directions are suggested.
Keywords: articular cartilage; biphasic; fluid load support; tibio-femoral joint; finite element modelling; osteoarthritis

1. Introduction hereditary or inflammatory factors (Buckwalter and


Osteoarthritis (OA) is a degenerative joint condition, Martin 2006). The latter is the subject of our investigation
which causes irreversible damage to the structural and the in the present contribution. In particular, meniscectomy is
mechanical integrity of articular cartilage (AC). Osteoar- well recognised as risk factor for secondary OA in the knee
thritic AC differs from healthy AC in that mechanically, it (Papalia et al. 2011) causing a severe change in the knee
tends to gradually become softer, and visually, fibrillation contact mechanics. As for example, the loss of the medial
and shallow fissures on the surface start to occur meniscus leads to a decrease of up to 75% and an increase
(Buckwalter and Mankin 1998, Knecht et al. 2006). of up to 300% in contact area and contact stress,
Eventually, at the later stages of the pathology, ulceration respectively (Kurosawa et al. 1980; Baratz et al. 1986; Ihn
and full AC loss occur. Consequently, osteoarthritic AC et al. 1993; McDermott and Amis 2006). Many clinical
loses its fundamental capability to protect bone extremities studies have highlighted the significant incidence of OA
and to attenuate loads, causing pain and limiting patient’s after meniscectomy, which can be observed both in the
life quality. short- and long-term follow-up (Roos et al. 2001; Englund
This pathology is today of great interest since it is and Lohmander 2004; Petty and Lubowitz 2010), and
thought to affect 85% of people by the age of 55 affects both young (McNicholas et al. 2000) and older
(Fergusson 1987; Wilson et al. 2005b) and recognised as patients (Crevoisier et al. 2001). In addition to this, it has
the primary cause of joint replacement surgery. At present, been demonstrated that total meniscectomy causes higher
a well-accepted classification distinguishes between incidence of degenerative change compared to partial
primary and secondary OA. Primary OA is referred to as meniscectomy (Hede et al. 1992; McGinty et al. 1997).
OA that develops in apparently normal joints with absence In vitro studies on animals have confirmed this evidence:
of any joint degeneration (e.g. healthy ligaments and meniscectomy-induced OA models revealed biological,
menisci) and with no predisposing factors (Buckwalter and biochemical and biomechanical degradation of knee AC
Martin 2006), and prevails in older adults. Secondary OA centrally, and osteophyte formation peripherally (LeRoux
can be triggered by abnormal and excessive stresses in the et al. 2000; Appleyard et al. 2003; Oakley et al. 2004;
tissue (Wilson et al. 2005b) caused by trauma, injury, Young et al. 2006; Song et al. 2008).

*Corresponding author. Email: l.mattei@ing.unipi.it


q 2013 Taylor & Francis
1554 L. Mattei et al.

Secondary OA, being mechanically induced, has of user-defined material subroutines, which are often not
recently become the subject of many biomechanical and readily available or simple to code and usually are linked to
biomedical engineering studies. To this aim, finite element high computational costs.
method (FEM) is certainly an invaluable tool for studying The aim of the research presented in this article is
stresses and strains distribution within healthy or injured threefold: (i) to develop a patient-specific meniscectomised
knee joints, and investigating the onset of AC damage. knee joint model to be used to assess the contact stresses
However, this can only be successful if suitable and induced by realistic loading histories; (ii) to perform a
realistic constitutive models of AC are employed. In the critical comparison between linear elastic and readily
last decades, a plethora of advanced constitutive models available biphasic constitutive models applied to the study
for AC has been proposed and numerically implemented of joint biomechanics and (iii) to estimate the likelihood of
using FEM in order to describe the unique mechanical AC damage to occur and the location of damage initiation.
behaviour of AC dictated by its biphasic nature (Mow et al. To serve this purpose, a realistic FE model of the tibio-
1980), flow-dependent and flow-independent viscoelasti- femoral joint (TFJ) contact following total meniscectomy
cities (DiSilvestro, Zhu and Suh 2001, DiSilvestro, Zhu, has been reconstructed from MRI and CT scans of a human
Wong, et al. 2001) and its strong structural and mechanical knee joint. This model is used to provide further evidence
anisotropy mainly due to fibril reinforcement (Wilson et al. that linear elastic constitutive laws should not be used to
2005a; Julkunen et al. 2008; Li et al. 2009; Hosoda et al. model AC if the instantaneous response of the tissue is
2010). under investigation. Indeed this topic is still the object of an
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Although a linear elastic model is a long way away active debate in the scientific community, as confirmed by
from an accurate representation of AC, it has been largely recent publications (Li and Gu 2011). On the other hand,
adopted in the study of knee biomechanics. Indeed, the biphasic constitutive descriptions should be used, and here
high non-linearity of both realistic knee geometries and AC a number of biphasic laws are tested using a commercial
mechanical behaviour lead to define a numerical problem package to establish which one provides the best results in
of very complex nature and computationally expensive. comparison with the existing experimental evidence
Consequently, the linear elastic model was adopted to collected on cartilage samples tested under physiological
model AC in several patient-specific finite element (FE) conditions. It should be noted that, although the
models of the knee used for investigating stresses and incorporation of fibril-reinforced non-linear models have
strains of native (Bendjaballah et al. 1997, Donahue et al. already been successfully attempted for 2D configurations
2002; Beillas et al. 2004; Moglo and Shirazi-Adl 2005; by our group (Accardi and Dini 2009), the non-linearity in
Pena et al. 2006; Papaioannou et al. 2008; Guo et al. 2009) the elastic behaviour of the solid constituents of the AC
and meniscectomised (Bendjaballah et al. 1995; Pena et al. tissue is not explicitly modelled in the research presented
2005, 2008; Shirazi and Shirazi-Adl 2009; Yang et al. here. This is due to the fact that the incorporation of the non-
2010) joints. Only very recently, sophisticated biphasic linear response due to the AC fibrils network requires user-
constitutive models of AC have been implemented in defined material description to be implemented in the
human knee FE models. The fibril-reinforced model adopted FE package (Gu and Li 2011; Kazemi et al. 2011;
proposed by Li et al. (2009) has been implemented in knee Mononen et al. 2012); this in turn implies that (a) the model
FE models1 (Gu and Li 2011; Kazemi et al. 2011) in order is not as readily portable as those developed using the
to investigate the effect of pore pressure and fibres constitutive laws tested in this study (which do not require
orientation in contact mechanics of both healthy and user-defined materials for their implementation), (b) the
meniscectomised knee joints (Kazemi et al. 2011). The computational time increases significantly, especially if
effect of the fibril pattern has also been investigated by also the viscoelastic contribution of the fibrils network is
Mononem et al. (2012) for both healthy and osteoarthritic considered and (c) simulating repeated loading cycles
AC in the human knee. In this case, the fibril-reinforced under physiological conditions is difficult, even using
poroviscoelastic model described in Wilson et al. (2005a), reasonably large computational resources. Therefore, also
Julkunen et al. (2008) and Mononen et al. (2011) was bearing in mind that one of our aims was to simulate
adopted for AC. The models mentioned above simulated realistic loading scenarios, simpler biphasic models, which
compression loads with the femur in full extension, i.e. a still capture the fluid-induced non-linearity and the
fast loading ramp followed by a constant load. The viscoelasticity of the solid matrix, and provide stress
maximum load was relatively low in the models described maps for repeated loading cycles in a reasonable amount of
by Gu and Li (2011) and by Kazemi et al. (2011), being CPU time, have been favoured in this study.
36 N and 300 N (in 1 s), respectively, whilst a physiological The paper is outlined as follows. First, in Section 2, we
load of 1000 N (in 1 s) was applied in the model described introduce and thoroughly discuss different AC constitutive
by Mononen et al. (2012). In addition, the majority of these models. These models include: (i) the monophasic
models rely on the implementation of laws for the homogeneous, isotropic and linear elastic model (M),
description of the tissue’s constitutive behaviour by means (ii) the biphasic isotropic model with linear permeability
Computer Methods in Biomechanics and Biomedical Engineering 1555

(BL), (iii) the biphasic isotropic model with non-linear through the ECM, which is controlled by the permeability.
permeability (BNL), (iv) the biphasic poroviscoelastic Indeed, in porous media, the permeability is such that it is
model with non-linear permeability (BPVNL) and (v) the not constant but decreases with compressive strain due to
transversely isotropic biphasic model with non-linear the reduction of the porous matrix void ratio (the ratio
permeability (BTINL). The effect of the implementation of between the fluid and solid fractions). As a consequence,
different AC models in a simplified 3D configuration is then water can move in and out of the tissue, therefore varying,
explored in Section 3. In Section 4, a patient-specific FE as a function of the applied load/strain history, the fraction
model of the TFJ is developed in order to compare the effect of the load supported by the solid and the fluid constituents.
of monophasic and biphasic models of AC on the joint The flow-independent viscoelasticity corresponds to the
mechanical response, and to investigate the effect of intrinsic viscoelasticity of the solid matrix and it is mainly
physiological loading –unloading cycles when reproducing due to the PGs and the collagen fibrils. The latter show a
simplified walking conditions. Finally, the results obtained strain-dependent stiffness response, characterised by
from the models described in Sections 3 and 4 are discussed increasing stiffness with increasing tensile strain (Mak
in Section 5, and conclusions are drawn in Section 6. 1986). In AC tissue, a swelling behaviour is also observed,
mainly caused by the negative charge of the PGs, which
induces a chemical expansion phenomenon (due to the
2. Constitutive models for AC repulsion force between the tightly packed PGs) and the
This section describes the constitutive laws and the osmotic swelling (due to the higher ionic concentration of
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methods employed in this study to investigate the the ECM with respect to the surrounding synovial fluid)
mechanical response of AC; this is done in order to (Grodzinsky et al. 1981; Lai et al. 1991).
explore the suitability of the existing constitutive material In the literature, many material models of AC can be
behaviours to study realistic TFJ geometries. found (Wilson et al. 2005b), ranging from the relatively
The anatomical structures to be considered and modelled simple biphasic models to models considering more or less
when analysing the human joints under investigation consist explicitly all the main components of the tissue, such as
of menisci, ligament, muscles, cortical bone, trabecular bone the fibril-reinforced models (Li et al. 1999, Soulhat et al.
and the AC. In this study, the presence of the ligaments and 1999, Wilson et al. 2005a; Li et al. 2009) and triphasic
the muscles were reproduced implicitly using ad hoc models (Lai et al. 1991; Wu and Herzog 2002; Lu et al.
boundary conditions (BCs), while the presence of the menisci 2010). In this study, only some of the existing biphasic AC
was ignored as our focus is placed on the meniscectomised models are considered and implemented in a commercial
knee joints. As far as the mechanical properties of the FE software package. These models, while not explicitly
materials modelled are concerned, the femur and the tibia modelling the microstructural features of AC, are chosen
extremities are assumed to be composed of only epiphyseal as they allow a realistic representation of the tissue’s
surface bone, which has mechanical properties in the range mechanical response. They are relatively simple to
between the cortical and trabecular bones’ properties. These implement as they do not require the implementation of
are, therefore, modelled as homogeneous, isotropic and linear user defined material descriptions and enable to run
elastic, with a Young’s modulus of 5 GPa and a Poisson’s ratio simulations of 3D non-linear models at a relatively low
of 0.3 (Beillas et al. 2004). computational cost.
The real focus of this study is the AC tissue, a very The AC models, which have been considered in this
complex material with a unique mechanical behaviour study and implemented in the models described in
mainly due to its biphasic nature. In its most common Sections 3 and 4, are briefly described below.
representation, it consists of two distinct phases (Mow et al.
1980): a porous solid matrix phase and an interstitial fluid
phase. The solid matrix, often referred to as extra cellular 2.1 Monophasic model
matrix (ECM), is mainly composed of a collagen fibril The monophasic model is the simplest model considered
network, proteoglycans (PGs) and glycoproteins (Schneck by researchers in this field (Bendjaballah et al. 1995, 1997;
and Bronzino 2002). The interstitial fluid phase contains Donahue et al. 2002, 2003; Bei and Fregly 2004; Beillas
approximately 75% water (Rieppo et al. 2004). The AC et al. 2004; Pena et al. 2005, 2008; Papaioannou et al.
components, including the proportion of interstitial fluid, 2008): here, AC is modelled as a single solid phase, which
are distributed in different quantities and with different is considered as linear elastic, homogenous, isotropic and
architectures within the AC thickness, making the tissue almost incompressible. The model is thus characterised by
strongly inhomogeneous and anisotropic. In addition, AC only two mechanical parameters: the Young’s modulus
exhibits a significant viscoelastic response, which in turn is and the Poisson’s ratio. In particular, instantaneous (i.e.
characterised by both flow-dependent and flow-indepen- dynamic) values of these two parameters are employed to
dent components. The flow-dependent viscoelasticity is represent the constitutive behaviour of the material; these
caused by the frictional drag force caused by the fluid flow are termed Eins and nins, respectively. The instantaneous
1556 L. Mattei et al.

Young’s modulus is extrapolated from indentation or It should be noted that the non-linear permeability law
compression curves obtained instantaneously after the proposed by Lai et al. (1981) provides a good description
load application on the AC and takes into account both the of the AC response only for small strains. Its adoption in
response of the solid and the fluid constituent. Conse- this study is justified by the fact that the AC tissue
quently, it accounts for the stiffness changes induced by modelled by the authors undergoes small deformations.
the interstitial fluid pressurisation of AC and increases However, a generalised form of this non-linear per-
with the strain rate. If enough time is allowed, however, meability law has been proposed by Holmes and Mow
equilibrium conditions are reached and Eins and nins (1990); since its validity has been demonstrated for both
correspond to the solid matrix parameters Eeq and neq. small and finite strains, such formulation should be
adopted when larger loads are applied and larger strains
are computed.
2.2 Biphasic linear model
The BL model is the most basic of the biphasic models,
which was initially developed by Torzilli and Mow 2.4 Biphasic poroviscoelastic non-linear model
(1976a, 1976b). It is the backbone of all the more The BPVNL model takes into account both the flow-
advanced AC models. The tissue is assumed to be dependent and the flow-independent contributions to the
constituted by a linear elastic, homogenous, isotropic and viscoelastic tissue response. The BPVNL model was first
almost incompressible solid phase and an incompressible analytically formulated by Mak (1986) and implemented
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fluid phase. The permeability is assumed to be constant (to numerically using two different methods, namely the
which the linearity of the model is due), hence independent continuous (Fung 1972) and the discrete (Suh and Bai
of the void ratio. All the biphasic models use the Young’s 1998) spectrum algorithms. The latter is more widely used
modulus evaluated at equilibrium, Eeq. for the viscoelastic approximation as it saves significant
The BL model is acceptable as a general approxi- memory and CPU time, being equally reliable; thus, it is
mation of the AC mechanical behaviour since it enables to adopted in this study, where minimising the use of
capture the main characteristics of the tissue due to its computational resources is imperative. The discrete
biphasic nature. Furthermore, it is fairly simple to spectrum algorithm describes viscoelastic properties
implement using FEM and not too computationally using the reduced relaxation function G(t) written as a
expensive. However, although capable of dealing with series of combinations of discrete relaxations function Gi
the long-term creep and stress relaxation of AC during
confined compression, this model shows non-negligible X
Nd

deviations from the tissue’s experimental response. The GðtÞ ¼ G1 þ Gi e2t=ti ; ð2Þ
i¼0
model becomes even more inaccurate when applied to
unconfined compression tests, mainly due to the fact that where ti is the discrete relaxation time constant and G1 ¼
the anisotropy of the tissue is neglected. As a consequence, Gð1Þ ¼ 1 (Suh and Bai 1998). According to Suh and Bai
the BL model tends to underestimate the stresses in the (1998) in the implementation of Equation (2), it can be
tissue, and this might constitute a severe limitation when assumed that Gi ¼ G  for each given i, where G  is the
investigating damage initiation (Armstrong et al. 1984; discrete spectrum magnitude and is
Brown and Singerman 1986).
 ¼ G0 2 1 ;
G ð3Þ
Nd þ 1
2.3 Biphasic non-linear model
The BNL model combines the BL model with a non-linear where G0 ¼ Gð0Þ. Furthermore ti can be considered
permeability law, thus reproducing the flow-dependent equally distributed with a logarithmic interval between the
viscoelasticity of the tissue. Lai et al. (1981) were the first to short-term and long-term relaxation time constants, i.e. ts
propose a non-linear law to be used to account for the and tL, and thus
change in permeability related to the deformation of  
t
the porous matrix by specifying a relationship between the N d ¼ log L : ð4Þ
permeability and the void ratio. This law was later revisited ts
by Van der Voet (1997), assuming the following form:
It is worth noting that three additional parameters, i.e.
   ts and tL, are necessary to characterise the biphasic
1þe M G,
k ¼ k0 ; ð1Þ poroviscoelastic materials with respect to the BNL model.
1 þ e0
The BPVNL model is capable of representing the
where k0 and M are material constants, and e and e0 the tissue’s response and reproducing the experimental data
initial and the current void ratio, respectively. obtained using confined and unconfined compression, and
Computer Methods in Biomechanics and Biomedical Engineering 1557

indentation tests. In particular, it can predict simul- Table 1. Mechanical parameters for the BL and the BNL
taneously lateral displacements and reaction forces during models of AC (DiSilvestro, Zhu, Wong, et al. 2001).
unconfined compression tests (DiSilvestro, Zhu, Wong,
Model Type Mechanical Parameters
et al. 2001), also for different strain rates (DiSilvestro, Zhu
and Suh 2001). Although this model does include the Eeq (MPa) 0.421
neq 0.28
fundamental characteristic of the flow-independent vis- k0 (m4/N s) 6.9 10215
BL, BNL
coelasticity, it does not capture anisotropy and the r* (g/cm3) 1
compression – tension non-linearity of the tissue. e0* 4
BNL M* 5

2.5 Biphasic transversely isotropic non-linear model


As previously discussed, AC is highly anisotropic mainly fluid non-linear behaviour captured by using the permeability
because of collagen fibres aligned in specific directions law given in Equation (1). Furthermore, three BPVNL
within the AC thickness. The modelling of AC full models, characterised by different relaxation functions
anisotropy is a challenging numerical task. However, as (BPVNLa, BPVNLb and BPVNLc), were implemented in
stated by Donzelli et al. (1999), the BTINL model is suitable order to investigate the role of the viscoelasticity of the solid
to capture the AC anisotropy without explicitly accounting phase on the AC mechanical response. Collagen fibrils
for the collagen network. A transversely isotropic material oriented parallel to the AC surface, i.e. running in x and z
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can be defined as a special case of an orthotropic material; directions, were considered in the BTINL model.
namely, its mechanical properties are invariant with respect The mechanical properties characterising each model
to rotations about an axis, called axis of symmetry, which is (see Tables 1– 3) were extracted from experimental studies
normal to the plane of isotropy (Ting 1996). In AC, the plane reported in the literature and used to calibrate the
of isotropy is thought to be aligned with the superficial parameters to be adopted for the numerical implementation.
collagen fibrils, which run parallel to the AC surface. This For the monophasic model, Eins ¼ 10 MPa and nins ¼ 0.46
assumption allows the stresses in the tissue to be obtained by were chosen from the ranges of values reported in literature,
manipulating the elastic stiffness matrix to account for the i.e. 4 –20 MPa and 0.45– 0.48, respectively (Bendjaballah
planar isotropy. By invoking symmetries, it can be shown et al. 1995, 1997; Donahue et al. 2002, 2003; Bei and Fregly
that only five independent material parameters are required 2004; Beillas et al. 2004; Pena et al. 2005, 2008;
in order to characterise the model (see Section 2.6). Papaioannou et al. 2008). The parameters of the biphasic
This model, as shown using direct comparison with models BL, BNL, BPVNLa and BTINL were taken from
experimental data in (DiSilvestro, Zhu and Suh 2001), is DiSilvestro, Zhu, Wong, et al. (2001). This allowed us to use
capable of capturing both lateral displacements and a consistent set of parameters, i.e. derived from the same
reaction forces produced by an unconfined compression AC samples set, for different AC models and, consequently,
test, but it does not capture the evolution of these two to perform a direct and rigorous comparison between the
variables simultaneously. This is probably caused by the implemented models. It should be noted that the parameters
absence of the viscoelasticity of the solid matrix. M and e0 were not reported in DiSilvestro, Zhu, Wong, et al.
(2001) and consequently they were estimated from other
literature sources (Suh and Bai 1998; Wilson et al. 2003;
2.6 Material parameters Han et al. 2005; Pawaskar et al. 2010). The properties of the
In summary, five constitutive models of AC were used in this BPVNLb and BPVNLc models were taken from DiS-
study: M, BL, BNL, BPVNL and BTINL. It should be noted ilvestro and Suh (2001) and Suh and Bai (1998),
that the non-linearity (hence the acronym ending in NL) respectively, assuming the same values of M and e0 used
included in the BNL, BPVNL and BTINL models refers to the for the other models.
Table 2. Mechanical parameters for the BPVNL models of AC (BPVNLa, DiSilvestro, Zhu, Wong, et al. 2001; BPVNLb, DiSilvestro
and Suh 2001; BPVNLc, Suh and Bai 1998), in addition to the marked parameters (*) of Table 1.

Mechanical Parameters
Model Type BPVNLa BPVNLb BPVNLc
Eeq (MPa) 0.55 0.63 0.7
neq 0.24 0.1 0
k0 (m4/N s) 0.9 10215 1.72 10215 2 10215
BPVNL 
G 15.180 17.692 10.21
ts (s) 0.45 0.62 0.001
tL (s) 95.9 85.1 10
1558 L. Mattei et al.

Table 3. Mechanical parameters for the BTINL model of AC contact regions. The bone is represented by a prismatic part
(DiSilvestro, Zhu, Wong, et al. 2001), in addition to the marked characterised by a square base (16 mm £ 16 mm) and
parameters (*) of Table 1. height of 25 mm. Only a quarter of the model was
Model Type Mechanical Parameters simulated since symmetric kinematic BCs were invoked
(Section 3.3).
Ex ¼ Ez 1.7
Eeq (MPa) Ey 0.421
nxy ¼ nyx 0.09
BTINL neq 3.2 Mesh
nxz ¼ nyz 0.01
Geq (GPa) Gxz ¼ Gyz 0.84 Hexahedral elements were employed to mesh both the AC
k0 (m4/N s) – 0.5 10215 and the bone. Different element types were used for each
tissue/model: linear 3D stress (C3D8R) for bone, quadratic
3D stress (C3D20R) for monophasic AC and quadratic
All the AC constitutive models were implemented in pore fluid/stress (C3D20RP) for biphasic AC. It is worth
the simplified TFJ FE model, whilst only the monophasic noting that hexahedral elements are a requirement for soils
and the BPVNLb models were adopted in the patient- consolidation analyses performed by Abaqus; in addition,
specific TFJ model, as explained in Section 5. The FE the quadratic order used for the AC elements was chosen
models were developed using the FE package Abaqus 6.9, in order to achieve better accuracy and avoid convergence
using predefined material models. issues. This is in accordance with the mesh sensitivity
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study performed in this work (here not detailed for


brevity); a thorough investigation tackling convergence
3. Three-dimensional simplified FE model of the TFJ and accuracy issues was also carried out to select the
element size required to correctly capture the AC
3.1 Model description behaviour. On the basis of such analysis, which showed
As a first step towards the implementation of an advanced that the results are relatively insensitive to the choice of
AC material model in realistic 3D knee geometries, a 3D prismatic element base size, two mesh densities were
simplified FE model of the TFJ has been developed, selected: their topologies are depicted in Figure 1(b), with
reproducing the realistic local anatomy of the joint. the finer one employed in the simplified 3D model to
Simulations are, therefore, performed with the aim of maximise accuracy and the coarser one used in the full 3D
identifying the optimal mesh and the most reliable knee joint model to achieve an optimal compromise
constitutive law for AC to then be implemented in the between accuracy and computational cost.2
patient-specific FE model presented in Section 4. The
simplified 3D model of the TFJ depicted in Figure 1(a) is
geometrically representative of a single knee compartment 3.3 Boundary conditions
and is constituted by two interacting spherical layers of AC Surface interactions: Two different surface interactions
bonded to two prismatic substrates representing the occur in the TFJ: the bone–AC and the AC–AC interactions
equivalent bone structures. An average thickness of the (Figure 2(a)). The bone–AC interaction was modelled as a
AC layers of 2.5 mm (Li et al. 2005; Liu et al. 2010) and tie constraint (i.e. no relative motion). This was thought to be
curvature radius of 200 mm were selected as they a reasonable assumption since the AC surface is strongly
correspond to the equivalent radius of curvature and bonded to the correspondent bone surface where the AC
cartilage thickness observed in the most heavily loaded TFJ tidemark lies. The AC–AC interaction was modelled as a

3D geometry 3D mesh

Rigid surface
×RP AC mesh
• AC elements:
Femoral
2 × 2 × 0.625 mm3
bone
• Element layers: 4
AC
AC
AC mesh
Tibial • AC elements:
bone Y 2 × 2 × 0.3125 mm3
• Element layers: 8
Z X
(a) (b)
Figure 1. Simplified model of the TFJ: geometry of a quarter of a single compartment (a) and two examples of mesh (b).
Computer Methods in Biomechanics and Biomedical Engineering 1559

Surface interactions &


Loading conditions Pore pressure BCs for AC
kinematic BCs

Vertical load
RP-reference
point ×RP
Free draining
10

Load (N)
Tied
bone/AC 5
Frinctionless
surfaces
contact 0
0 200 400
Time (s) Sealed
Y
Kinematic
Z X Built-in simmetry BCs
(a) (b) (c)

Figure 2. Scheme of the BCs applied to simplified TFJ model. The global coordinate system is shown on the bottom-left.

frictionless (considering only normal stresses at the contact 4. Patient-specific FE model of the TFJ
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surface) and hard contact (the contact is ‘total’ when it is 4.1 Model description
detected), taking into account the possibility of finite sliding
In this study, a bicompartmental total meniscectomised
between the surfaces.
knee joint has been modelled with the aim to investigate
Kinematic and loading conditions: The lower transversal
the development of secondary OA. Consequently, the
section of the tibial bone was built-in while the femur
anatomical structures of interest are the femur/tibia bone,
kinematics was driven by the kinematics of a reference point
the AC, the ligaments and the muscles. As the stabilising
(RP) linked to the top rigid surface, as depicted in Figure 2(a).
and the load transfer functions of ligaments and muscles
The vertical translation of the RP was left as unconstrained, were reproduced by ad hoc BCs, the patient-specific model
since this degree of freedom (DoF) was indirectly controlled consists of the femur/tibia bone extremities and AC, which
by the vertical load; all the other DoFs were fixed. The is modelled as a surface layer perfectly bonded to the bone.
loading cycle consisted in a vertical load of 10 N applied to The model geometry was obtained from high-resolution
the rigid surface using a ramp of 15 s, then kept constant for medical images of a 75-year old female patient, with a body
450 s (Figure 2(b)), which resulted in a maximum load of weight of 65 kg, who had previously undergone a
80 N applied to the entire knee. Although such conditions do bicompartmental total meniscectomy surgery. The hard and
not reproduce the physiological conditions later adopted for soft tissue reconstructions were based on CT and MRI scans,
the patient-specific TFJ model, they were chosen for a respectively (Figure 3(a)). The 2D scans were later combined
number of reasons. First of all, the loading protocol for the surface rendering by means of the AVIZO package.
simulated conditions similar to those of mechanical tests The final model consists of six deformable parts, as shown
carried out to extrapolate AC material properties used in this in Figure 3(b): the two articulating bone extremities of the
study (Table 3): for example, DiSilvestro, Zhu, Wong, et al. femur and the tibia, the lateral femoral AC (LFAC), the medial
(2001) prescribed a strain rate of 0.001 s-1 whilst here (see femoral AC (MFAC), the lateral tibial AC (LTAC) and the
Section 5.1) the loading conditions resulted in a strain rate in medial tibial AC (MTAC). A rigid body, corresponding to the
the range 0.002 – 0.007 s-1 at the end of the load upper transversal slice of the femur (coloured in grey in Figure
ramp. Secondly, the simulation of low loads allowed to 3(c)), was also included to enable the application of uniform
compare AC constitutive models and to gain insights into the loads on the upper bone cross section.
transient mechanical response of AC avoiding numerical
difficulties and high computational costs; a similar approach
has also been adopted in other studies presented in the recent 4.2 Mesh
literature (Gu and Li 2011). The reconstructed geometry was imported in Abaqus
BCs for the pore pressure of the biphasic AC: When where all remaining phases of preprocessing, solving and
the AC is modelled as a biphasic material, pore pressure postprocessing of FE analysis were executed.
BCs are implemented to regulate the fluid flow in and out The geometric parts were individually meshed as
of the tissue. As indicated in Figure 2(c), a sealed portrayed in Figure 3(c). The mesh characteristics are
condition (i.e. no fluid flow) at the bone– AC interfaces, detailed in Table 4. The bone and the AC were meshed
and a free-draining condition (i.e. zero pore pressure) on with tetrahedral and hexahedral elements, respectively
the external AC surfaces were employed. (see Section 3.2). The dimension of the bone elements
1560 L. Mattei et al.

2D medical images 3D geometry 3D mesh

Rigid body
Femur (F)

Deformable
MRI scans bodies
Lateral Medial
for soft tissue femoral AC femoral AC
(LFAC) (MFAC)
Lateral Medial
tibial AC tibial AC
(LTAC) (MTAC)
Y
CT scans
for hard tissue Z X
Tibia (T)
(a) (b) (c)

Figure 3. Reconstruction of 3D geometry of a patient specific TFJ from CT (hard tissue) and MRI (soft tissue) scans (a) (with permission
from M. Tuncer, Imperial College London); geometric parts of the model (b); model meshing (c).
Downloaded by [University of Hull] at 05:34 30 May 2014

varied along the Y-axis, with the elements progressively approaching contact, therefore allowing the surfaces to
reducing in size in the regions adjacent the contact region. reach a relative position that ensures maximum contact area
The mesh of the AC sections was chosen according to the and minimum contact pressure. The lower transversal
mesh sensitivity analysis performed using the simplified section of the tibia was built-in, while the femur kinematics
model described in Section 3, in order to guarantee both was driven by the kinematics of the femoral rigid part,
accuracy and low computational cost. Thus, four layers of whose RP was positioned between the two femoral
prismatic elements of varying thickness and with a square condyles (Figure 4(a)). As for the simplified TFJ model,
base characterised by edge dimensions of about 1.5 – the vertical translation of the RP was controlled via the
2.5 mm were adopted for the discretisation of the AC vertical load. The abduction/adduction, i.e. the rotation of
tissue. It is worth noting that this mesh refinement was the rigid part of the femur around the Z-axis, was
exploited also in other literature studies on 3D FEM knee considered free whilst all the other DoFs were fixed. The
modelling (Gu and Li 2011; Kazemi et al. 2011). full extension of the TFJ was chosen as the initial condition,
since this is considered one of the most critical loading
conditions. All simulations were executed in load control.
4.3 Boundary conditions A physiological vertical load was applied to the femoral
Surface interactions: The surface interactions were rigid part and transmitted, as a homogenously distributed
modelled as described in Section 3.3. The resulting model pressure, to the upper transversal section of the femoral
was composed of four pairs of tied surfaces at the AC– deformable part. The loading cycle, which was repeatedly
bone interfaces, and two contact pairs, in the medial applied to the joint for five times during the simulations, is
(MFAC – MTAC) and in the lateral (LFAC – LTAC) illustrated in Figure 4(b). This corresponds to a simplified
compartments (Figure 4(a)). representation of the vertical load evolution observed
Kinematic and loading conditions: The kinematic and during a gait cycle, which is characterised by a double peak
loading BCs were chosen in order to simulate the during the stance phase and a constant low value during the
adaptation mechanism of the articulating surfaces swing phase. This is in agreement with both the predictions

Table 4. Main characteristics of the mesh of the patient specific TFJ model.

Elements Nodes
Part
Geometry Dimension (mm) Type Geometric order Number Number
Femur 5768 24636
Tibia Tetrahedral 1.5 – 4 (edge) 3D stress Linear 5508 23590

LFAC 592 3143


MFAC 924 4776
LTAC Hexahedral 1.5– 2.5 (edge) þ 4 layers 3D stress/pore fluid-stress Quadratic 680 3547
MTAC 684 3580
Computer Methods in Biomechanics and Biomedical Engineering 1561

Surface interactions &


Loading conditions Pore pressure BCs for AC
kinematic BCs

Vertical load

1st Peak 2nd Peak LFAC


RP 1000
Sealed
800

Tied

Load (N)
600
LTAC Free
bone/AC
surfaces 400 draining

200 End
Start
Frinctionless cycle cycle
0
contact 0 0.2 0.4 0.6 0.8 1
Y Time (s)

Z X Built-in
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(a) (b) (c)

Figure 4. Scheme of the BCs applied to patient-specific TFJ model. The global coordinate system is shown on the left-bottom.

of other musculoskeletal models (Hurwitz et al. 1998; Initially, the difference between the monophasic and the
Shelburne et al. 2006) and the measurements carried out on biphasic AC models was considered. The results reported in
instrumented knee prostheses (Zhao et al. 2007). However, Figure 5 demonstrate that the monophasic material, whose
the peak load, which can reach up to 2.5 BW during the gait, properties have been calibrated as described in Section 2.6,
was here set to 1.5 BW, which corresponds to the maximum seems to be stiffer than the biphasic model, being
force during the gait with the knee in full extension characterised by a lower vertical displacement of the RP
(Lamoreux 1971; Fox and Delp 2010) and is also in line (i.e. indication of soft tissue compression), a lower contact
with the loading protocol used in the experimental tests area and a higher contact pressure. The maximum mismatch
(Fukubayashi and Kurosawa 1980) and in other FE models between the models in terms of contact area and contact
(Bendjaballah et al. 1995; Donahue et al. 2002; Pena et al. pressure are 85% and 450%, respectively, as shown in Figure
2005, 2006; Mononen et al. 2012). It is worth mentioning 5(b) and (c). Direct evidence of the fact that biphasic AC
that the load control can be implemented only when the models are required to predict the realistic transient
joint surfaces are in contact. This condition was guaranteed behaviour of the soft tissue is provided by the constant
by an initial phase of displacement control, which consisted values obtained for both local and global characteristics
of a very small linear vertical displacement applied in 0.1 s. when looking at all the outputs of the monophasic model
BCs for the pore pressure of the biphasic AC: As already displayed in Figure 5 after the load reaches the plateau (see
described in Section 3.3, sealed and free-draining conditions
Figure 2(b)). This is obviously not the case for the biphasic
were imposed at the bone–AC interfaces and on the external
model, whereby the load support is generated by both the
AC surfaces, respectively. In this way, we assumed that the
solid matrix and the fluid phase (Sakai et al. 2012) and their
interstitial fluid could exude from the AC across the free
continuous interaction results in a time-dependent material
surfaces, as illustrated by the fluid velocity vectors computed
response (Figure 5). In particular, the ratio of the fluid/solid
during the simulation and shown in Figure 4(c).
support varies both in time and space within the AC
thickness. This is clearly captured in Figure 6, which portrays
the normalised solid and fluid support components along two
5. Results and discussion node paths extracted under the surface of the bottom AC. The
5.1 Comparison of AC material models simulations, obtained assuming the BPVNLb model for the
This section presents the comparison of the constitutive AC, show that when the load is initially ramped to its
models of the AC implemented in the simplified TFJ maximum value the load is almost entirely supported by the
model. Both global (i.e. vertical displacement of the RP increase in interstitial fluid pressure in the tissue, which
and contact area) and local parameters3 (e.g. stresses, develops due to the very low permeability of AC; gradually,
strains, pore pressure and flow velocity) were monitored as the fluid exudes from the contact zone, a load shift is
for the AC, and the implications that their variations had observed from the fluid to the solid phase. It is worth noting
on the tissue’s response were investigated. that the solid and fluid supports were calculated as the
1562 L. Mattei et al.

0 150
BL BL
Vertical displacement of the RP (mm)

–0.1 BNL BNL


BPVNLa BPVNLa
–0.2 BPVNLb BPVNLb

Contact area (mm2)


BPVNLc BPVNLc
–0.3 100
BTINL BTINL
–0.4 M M

–0.5

–0.6 50

–0.7

–0.8

–0.9 0
0 50 100 150 200 250 300 350 400 450 0 50 100 150 200 250 300 350 400 450
Time (s) Time (s)
(a) (b)
0.8 0.4
BL
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BL
0.7 BNL 0.35 BNL
BPVNLa BPVNLa
BPVNLb
Contact pressure (MPa)

0.6 BPVNLb Pore pressure (MPa) 0.3


BPVNLc BPVNLc
0.5 BTINL 0.25 BTINL
M
0.4 0.2

0.3 0.15

0.2 0.1

0.1 0.05

0 0
0 50 100 150 200 250 300 350 400 450 0 50 100 150 200 250 300 350 400 450
Time (s) Time (s)
(c) (d)

Figure 5. Comparison of the AC models in terms of: vertical displacement of the RP (a); contact area (b); contact pressure (c); pore fluid
pressure (d).

integral of the vertical axial stress and the pore pressure along BL model and smallest for the BPVNLa model, with the
the path of nodes, respectively, and were normalised with BNL and the BTINL producing intermediate results. This
respect to the total load. is due to the fact that the BNL model is stiffer than the BL
We turn now to the differences between the various model because of a lower fluid exudation due to the
biphasic AC models considered in this study. Among the reduction of permeability as a function of the strains
implemented BPVNL models, only the BPVNLa is experienced by the solid matrix; furthermore, the BTINL
considered for the purpose of comparison. As shown by material has a stiffness in the transverse direction higher
the vertical displacement of the RP in Figure 5(a), during than the BNL model. Moreover, with respect to all the
the monotonic application of the load the compression of other models, the matrix of the BPVNLa material is
the tissue increases, more or less linearly, depending on characterised by an additional stiffening due to the
the adopted biphasic model; after the load is held constant viscoelastic behaviour of the solid phase; such effect
at its maximum value, the vertical displacement keeps depends on the strain rate and is partly responsible for the
increasing for all models due to the fluid exudation and, in behaviour displayed in Figure 5(a). The compression of
the case of the BPVNLa, also due to the viscoelastic the AC is directly related to the contact area and the
relaxation of the ECM. The comparison between the contact pressure, depicted in Figure 5(b) and (c),
responses obtained using different biphasic AC models respectively: the higher the strain, the better the adaptation
revealed that the compression of the tissue is largest for the of the articulating surfaces and, thus, the larger the contact
Computer Methods in Biomechanics and Biomedical Engineering 1563

area and the lower the contact pressure. Consequently, the models, even in their simplest form, is certainly a first step
lowest contact area and the highest contact pressure were for achieving more accurate predictions of the stress state
observed for the BPVNLa model, whilst the highest and the onset of damage of AC, as this is bound to be
contact area and the lowest contact pressure for the BL linked to the time-varying response of the tissue under
model. It is worth noting the significant dispersion of the impact loading. The BPVNL model was selected among
local/global parameters predicted by the various biphasic the previously discussed biphasic AC models to be
models. For instance, a relative mismatch of 45.2% was implemented in the patient-specific TFJ model, as it is the
found at the end of the loading cycle between the largest only one that accounts for the flow-independent viscoe-
(BL model) and the smallest (BPVNLa model) contact lasticity, and the predicted mechanical response shows
area, and a relative variation of about 54.5% was very good agreement with several experimental findings
computed between the largest (BPVNLa model) and the obtained from different experimental configurations (e.g.
smallest (BL model) peak contact pressure. The same data confined/unconfined tests) (DiSilvestro and Suh 2001;
dispersion was observed for the pore (i.e. fluid) pressures DiSilvestro, Zhu and Suh 2001; DiSilvestro, Zhu, Wong,
of the biphasic models, compared in Figure 5(d). All et al. 2001).
models clearly show pore fluid pressurisation as the load is
applied; in particular, the highest pore pressure was
observed in the BPVNLa model, whilst the lowest was 5.2 Cartilage mechanical response during simplified
observed in the BL model. When the load is kept constant walking cycles
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at its maximum value, the increase in fluid exuded from


This section presents the main results obtained by
the contact zone corresponds to a drastic decrease of the
simulating the patient-specific TFJ contact under simpli-
fluid pressure and an increase of the strain in the solid
fied walking cycles. The comparison between the outputs
matrix.
obtained using the monophasic (M) and one of the
Our results pointed out that the flow-dependent
implemented biphasic models (i.e. BPVNLb) was
viscoelasticity of biphasic AC enables more conformal
considered to shed light on the AC behaviour. The main
contacts and hence allows the load to be distributed over a
findings are reported in Figures 7 –10, which show the
larger area, leading to lower contact pressure and stresses
results obtained by the two models in terms of both global
in the soft tissue. Also the flow-independent viscoelasticity
and local responses3 of the AC (Figure 7), also making use
of BPVNL models is a fundamental aspect of AC
of relevant 3D contour plots (Figures 8 –10) to aid the
behaviour: for high strain rates due to rapidly varying
discussion.
dynamic loading, it enables the stiffening of the soft tissue
thus inhibiting excessive deformations, in agreement with
Murakami et al. (2003). The influential role of the flow-
independent viscoelasticity is also highlighted by means of 5.2.1 Monophasic versus BPVNL AC behaviour during
the comparison between the mechanical responses of walking: implications for the onset of damage and OA
several BPVNL models. Indeed BPVNLa – c models The comparison between monophasic and biphasic AC
predicted quite different values of peak contact pressure response during walking confirms the necessity to
(Figure 5(c)) and peak pore pressure (Figure 5(d)), and implement advanced AC models in order to predict a
also different rates of stress relaxation, all in agreement realistic transient tissue response. During each walking
with their viscoelastic parameters reported in Table 3. For cycle, the mechanical response of both the monophasic
instance, the BPVNLb model predicted higher contact and the biphasic AC reflects the transient behaviour of the
pressures when compared to BPVNLa and BPVNLc, with load: all the curves in Figure 7 are characterised by two
a discrepancy of up to 17.8% and 56%, respectively. peaks that correspond to the two loading peaks. Before
This study has provided further evidence of the need to each loading peak, the compressive strains (Figure 7(a)),
implement biphasic AC models; in particular, we have the contact area (Figure 7(b)) and the contact pressure
highlighted that using biphasic constitutive descriptions to (Figure 7(c)) rapidly increase. In the model characterised
model physiological loading conditions in real TFJ contact by biphasic AC, an increase in the interstitial fluid pressure
geometries allows predicting the realistic transient (Figure 7(d)) and of the magnitude of flow velocity is
mechanical behaviour of the tissues under investigation, recorded, whilst both the void ratio and the permeability
the load shift mechanism and the adaptation of the decrease. The opposite occurs as the load decreases after
contacting surfaces together with the load redistribution. each loading peak. In particular, the fluid pressure remains
Although several TFJ contact studies have made use of the always positive; this suggests a continuous fluid exudation
monophasic elastic model, relying on the fact that at high (fluid flowing out of the tissue), in accordance with the
strain rates a biphasic material would behave as a free-draining BC applied to the AC surface.
monophasic model with a higher instantaneous elastic The differences between the two models appeared to
modulus, the implementation of biphasic constitutive be remarkable: the biphasic AC model predicted a
1564 L. Mattei et al.

1
Solid support – path 2 Node path 2
0.9 Fluid support – path 2
0.8 Solid support – path 3
Fluid support – path 3
Normalized supported load

0.7

0.6

0.5

0.4
Node path 3
0.3

0.2

0.1

0
0 50 100 150 200 250 300 350 400 450
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Time (s)

Figure 6. An example of the temporal evolution of the fluid/solid load support in the biphasic AC. The fluid/solid supports for two node
paths at different depths in the AC thickness are compared.

temporal evolution of the mechanical response of the both the Tresca stress and the contact pressure decrease,
tissue, both within a single and several walking cycles, while the contact area increases.
highlighting the unique capacity of the biphasic material to It can be concluded that the longer one walks, the less
adapt to the load and to redistribute stresses and strains. stressed the tibio-femoral AC is going to be! A mechanism
Figures 7 –9 show a significant variation of the biphasic of load redistribution in the tissue occurs which is
AC response during the first three cycles, and less fundamental to prevent the damage of the solid
variation in the last two cycles. Indeed, the AC behaviour constituents. During the initial loading phase of walking,
approached a pseudo-steady state after about five walking the tissue is subject to the highest stresses. After just a few
cycles, when most of the fluid had exuded and the elastic walking cycles, the AC adapts to the loading cycle and
response of the solid matrix dominates the tissue’s shows a quasi-steady behaviour characterised by higher
behaviour. The value of the pore pressure in the MFAC contact area and lower stresses. The limits of the
decreased by 24.2% between the first peak load of the first monophasic AC model are thus highlighted: it fails to
and the third walking cycle, and by 7.5% between the first account for the load redistribution, and it tends to
peak load of the third and the fifth walking cycle; the overestimate the contact area and underestimate the
corresponding percentage decrements of the Tresca stress maximum instantaneous stresses.
were 23.8% and 7.9%, respectively. In brief, the It should be borne in mind, however, that the stress
compression of the soft tissue continuously increased decrease observed in this study might not necessarily
(Figure 7(a)) and allowed a better adaptation of the occur in every TFJ configuration and loading scenario.
contacting surfaces. This corresponds to increasing contact This is a complex phenomenon dictated by the interplay
areas (Figure 7(b)) and decreasing contact pressures between the variation of interstitial fluid support and the
(Figure 7(c)). Between the first peak load of the first and change in stresses due to the adaptation of the joint. The
the last walking cycle, the variations of the contact balance between the two, which ultimately dictates the
pressure and the contact area in the medial side were overall resulting stress levels, depends upon the contact
2 25.8% and 34.3%, respectively. The load, at first mainly geometry and loading conditions which would vary from
supported by the fluid pressurisation, was gradually joint to joint.
transferred to the solid matrix as the fluid exuded the pore The model presented in this work to study the
pressure decreased (Figure 7(d)); furthermore, the Tresca mechanical response of a full knee joint suffering from a
stress decreased as a consequence of the poroviscoelastic total bicompartmental meniscectomy is motivated by the
stress relaxation (Figure 9). The stress and strains will to investigate the initiation of AC damage and OA
redistribution that characterises the behaviour of the associated with such a procedure (Korkala et al. 1984;
biphasic AC is clearly described by the contour plots in Lanzer and Komenda 1990). Indeed, because of the
Figures 8– 10: during the cyclic application of the load, absence of the menisci, the biomechanics of a healthy knee

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