On the load bearing mechanism of the human intervertebral disc

W. Ehlers, B. Markert & N. Karajan

Institute of Applied Mechanics (CE), University of Stuttgart, Germany

ABSTRACT: The spinal discs are part of the load bearing system of our body. They serve as shock absorbers,
transmit loads and enable the motion between the vertebrae. In order to get a more detailed insight into the
functioning of the intervertebral disc (IVD) in vivo, which is apparently impossible by standard examination
methods, numerical simulations provide an elegant and cost-effective alternative. Accordingly, this requires an
appropriate theoretical model, which is capable of describing the physiological behaviour of charged hydrated
tissues. This includes the electro-chemomechanical couplings as well as the viscoelastic and anisotropic prop-
erties of the extracellular matrix. In order to meet these requirements, the established Theory of Porous Media
(TPM) can be applied, which allows the description of multicomponent continua with internal interactions and is
proven to yield stable implementations within the mixed finite element method (FEM). The overall possibilities
offered by this approach are finally shown in a numerical analysis of a human IVD accounting for the essential
inhomogeneities within its realistic anatomic structure.

1 INTRODUCTION Ehlers (2002), where the constitutive assumptions,

Currently, most models that describe the IVD as a
soft biological tissue are restricted to single-phase
materials, which are not capable of describing
the electro-chemomechanical behaviour of charged
hydrated tissues, see, e.g., Eberlein et al. (2004) for
references. Moreover, the available models are often
limited to small strains or to finite strains but purely
elastic skeleton deformations without considering any
of the occurring inhomogeneities. In fact, these types
of naturally grown materials undergo large viscoelastic
deformations, where the extracellular matrix exhibits
so-called intrinsic viscoelastic properties (Iatridis et al.
1996, Ehlers & Markert 2001). These flowindepen-
dent viscoelastic effects are strongly coupled with the
dissipative phenomena resulting from the interstitial
fluid flow and the electrochemical (osmotic and elec-
trostatic) swelling mechanisms. Furthermore, their
inner structure and thus, the associated physical prop-
erties are inhomogeneously distributed over the 3-d
anatomic shape of the tissue. In addition, anisotropic
properties may occur due to embedded collagen fibers
and orientation-dependent hydraulic and electrolytic
conductivities. Another difficulty arises in the appli-
cation of the numerical model. It is often difficult
to obtain reliable experimental data to fit the needed
material parameters and to define realistic boundary
conditions for boundary-value problems (BVP).
The goal of this contribution is to present a con-
sistent theoretical framework based on the Theory of
Porous Media (TPM), see, e.g., de Boer (2000) or
necessary to cover all relevant tissue properties, are
merged in a modular manner. This actually allows for
a concise representation of the resulting system of
coupled partial differential equations, which can be
efficiently treated within the FEM and thus, enables
the numerical solution of even large 3-d problems at
suitable computational costs. Here, special attention
is drawn on the arising inhomogeneous fiber rein-
forcement as well as on the consideration of swelling
phenomena.
2 TISSUE PROPERTIES
The intervertebral disc is a sophisticated cushion-like
structure embedded in between two adjacent vertebrae
constituting 20 to 30% of the entire spine height. On
the macroscale, it is composed of three significant sub-
structures. In the center of the disc, a gel structure is
found, known as the nucleus pulposus (NP), which
exhibits a fluid-like behaviour and covers about 30 to
50% of the cross sectional area. The portion of the IVD
that becomes gradually prominent within the periph-
ery of the NP forms the outer boundary, known as the
anulus fibrosus (AF). At this, the AF appears as a lami-
nate structure surrounding the NP. Marchand &Ahmed
(1990) observed that the anulus consists of 15 to 26 lay-
ers of discontinuous concentric lamellae, each having
string-like structures embedded, known as the collagen
fibers. This natural fiber reinforcement runs obliquely
around the AF, whereas the direction of the fibers is

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Copyright 2005 Taylor & Francis Group plc, London, UK
alternating within successive layers. Furthermore, the
upper and lower faces of the IVD are covered with a
layer of hyaline cartilage, known as the cartilaginous
end plates (CEP).
On the microscale, the biochemical composition of
the IVD is rather complex. Generally, the interverte-
bral disc is composed of a charged hydrated extra-
cellular matrix consisting of proteoglycans (PGs),
glycosaminoglycans (GAGs) and embedded collagen
fibers as well as an ionized interstitial fluid includ-
ing dissolved electrolytes. Besides these free movable
solutes, there are further chemically active negative
charges attached to the long chained PG and GAG
molecules within the solid matrix. Their distribution is
highest within the NP reaching 10 to 20% of the overall
dry weight and decreases towards the outer periphery
of the AF. Hence, the fixed charges density (FCD) is
also highest in the center of the IVD, which corre-
sponds to measurements performed by Iatridis et al.
(2003) and Urban & Holm (1986). However, a differ-
ent distribution is observed regarding the obiquitious
collagen. Out of the several different types of colla-
gen, there are two main groups to be found within the
IVD. Firstly, this is collagen of type I, which is well
organized and forms parallel fiber bundles within the
AF, having a diameter of approximately 2 to 10 m.
In contrast, collagen fibers of type II are of a much
smaller diameter, ranging from 20 to 200 nm, and form
a loose network of fibrils mostly present in the nucleus
pulposus.
However, the intervertebral disc is not uniform in
many of its aspects. Firstly, there is the inhomoge-
neous distribution of collagen type I, which yields
a varying alignment within the lamellae of the AF.
This variation can be expressed in terms of a fiber
angle 0 between the fiber and the axial direction of
the spine. Eberlein et al. (2001) measured an anterior
fiber angle of 0 = 67 as well as a posterior angle
of 0 = 43 and discovered an almost linear relation-
ship of the two angles in circumferential direction,
whereas this linearity stays constant in radial direc-
tion. Furthermore, Marchand & Ahmed (1990) found
a decrease of the embedded collagen fibers of type
I as one moves towards the NP. Secondly, there is a
variation concerning the discontinuities in the lamellar
structure of the AF. A detailed study was performed by
Tsuji et al. (1993) elaborating the structural variation
of the anterior and posterior parts of the AF in terms
of the number of continuous and discontinuous fiber
bundles. At this, all anterior parts consist of mostly
complete fiber bundles, whereas the posterior part is
composed of a very complex structure having several
incomplete and discontinuous lamellar bundles.
The differences in continuity as well as in the num-
ber of embedded fiber bundles finally leads to an
inhomogeneous mechanical behaviour of the lamel-
lae, when pulled in fiber direction. Hence, it is the
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Copyright 2005 Taylor & Francis Group plc, London, UK
superimposed effect of the structural inhomogeneities,
which finally predicts the stress-strain relationship
of the fibers at any point in the AF. In a compre-
hensive study, Eberlein et al. (2004) measured these
mechanical variations by performing tensile tests in
fiber direction on single lamellae taken from differ-
ent regions of the AF. The results show an exponential
stress-strain behaviour of the collagen fibers, where
the overall stiffness of fibers found within the periph-
ery of the AF is about three times greater than the
values found close to the NP. Moreover, there is also
a variation in the circumferential direction classify-
ing the posterior part being weaker as the anterior
parts. This behaviour is in good accordance with the
qualitative findings of Skaggs et al. (1994).
3 THEORY OF POROUS MEDIA (TPM)
The TPM is a macroscopic continuum theory, which is
based on the theory of mixtures extended by the con-
cept of volume fractions. Proceeding from a binary
mixture consisting of solid and fluid constituents
denoted by = {S, F}, the solid phase is extended by
incorporating the volume-free fixed negative charges
fc (Ehlers et al. 2002). Furthermore, the interstitial
fluid F is composed of water as a liquid solvent with
dissolved electrolytes (Na+ Cl ) providing mobile
ions. In this context, it is assumed that all constituents
are in a state of ideal disarrangement. Following
this, the prescription of a real or a virtual averaging pro-
cess over a representative elementary volume (REV)
leads to a model of superimposed and interacting
continua, i.e., the homogenized or smeared model.
Particularly in the case of soft biological tissues, the
tiny mobile ions are assumed to diffuse rapidly through
the liquid and by themselves do not give rise to con-
centration gradients. Hence, the intervertebral disc is
always immediately in electrochemical equilibrium, so
that the arising osmotic properties can be sufficiently
described without considering the ion concentrations
(or electrochemical potentials) as additional unknowns
(degrees of freedom) of the process, cf. Lanir (1987).
Moreover, the volume fractions n = dv /dv (partial
volume per bulk volume ) serve as describing
physical quantities consistent with the saturation con-
straint n = nS + nF = 1, where n fc 0. Exploiting the
definition of the volume fractions n , a partial den-
sity = dm /d (constituent mass m ) and a material
or realistic density R = dm /dv can be defined
for each constituent , which are related to each
other via = n R underlining the macroscopic
compressibility of porous materials.
In the framework of superimposed continua, each
spatial point x of the current configuration is simulta-
neously occupied by material points P of all con-
stituents. Following this, all particles proceed from
different reference positions X , which leads to indi- tensors T as well as the interaction term p F = p S
vidual motion and velocity fields for each constituent, need to be defined. From general thermodynamical
reading x = (X , t) and x
= d (X , t)/dt, respec- considerations (Ehlers 1993), these assumptions read
tively.Therein, ()
denotes the material time derivative
following the motion of . Describing multipha-
sic materials, it is convenient to express the solid
in a Lagrangean setting via the displacement vec-
tor uS = x XS and the overall fluid in a modified Therein, I is the identity tensor and ()E denotes the
Eulerian setting relative to the deforming solid skele- so-called extra terms governed by the solid defor-
ton through the seepage velocity wF = xF
xS
. Fur- mation state and the fluid viscosity. As is usual in
thermore, the fixed charges are assumed to move with hydraulics, the fluid extra stress can be neglected,
the solid skeleton described by the solid deformation TFE 0, which can be deduced from a dimensional
gradient given through FS = x/XS . analysis. Furthermore, p can be interpreted as the
The model under consideration is assumed to be entire pore pressure introducing a third independent
composed of materially incompressible constituents, scalar field variable. Thus, an extra equation needs to
which are incapable of an internal mass production be generated, which is achieved by inserting the con-
or exchange, thereby excluding biochemical reactions stitutive assumption p FE = (nF )2 FR (K F )1 wF into
and growth processes. Moreover, assuming quasi- the specific fluid momentum balance. This leads to
static conditions and excluding thermal effects yields Darcys well-known filter law
the corresponding volume, concentration and momen-
tum balances of the constituents (cf. Ehlers et al.
2002):

relating the hydraulic gradient i to the filter velocity

fc
Herein, c m is the molar concentration of the fixed
charges, T is the partial Cauchy stress tensor and
b is the body force. Furthermore, p represents the
momentum production term satisfying the conserva-
tion constraint p S + p F = 0. Combining the specific
volume and momentum balances for the solid and
the fluid phases yields the respective balances of the
overall mixture as
Moreover, the specific volume balance of the solid
skeleton as well as the concentration balance of the
fixed charges can be analytically integrated from initial
quantities ()0S leading to
4 CONSTITUTIVE SETTING
In order to close the materially independent set of
equations for the extended two phase model, con-
stitutive assumptions for the partial Cauchy stress
nF wF . Herein, KF is the Darcy permeability tensor
and FR = FR g is the effective fluid weight (g = |b|
is the gravitation constant).
However, the introduced entire pore pressure
p = P + is constitutively decomposed into hydraulic
and osmotic contributions, respectively. Herein, in
the sense of continuum thermodynamics, P is under-
stood as a Lagrangean multiplier, whereas is directly
related to the deformation of the solid skeleton via the
fc
molar concentration change c m . Due to the assumption
of Lanir (1987), chemical equilibrium expressed by the
Donnan equation is not limited to the domain bound-
ary. Following this and exploiting the electroneutral-
ity condition for the internal and external solutions,
cf. Huyghe & Janssen (1997), yields the local col-
loid osmotic pressure (Donnan osmosis) expressed
through
where R is the universal gas constant, is the absolute
temperature and c m , denotes the molar concentration
of the monovalent external salt solution.
The final constitutive assumption concerns the
solid Cauchy extra stress tensor TSE describing the
purely mechanical contribution of the extracellular
matrix. Proceeding from the evaluation of the entropy
inequality one has

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Copyright 2005 Taylor & Francis Group plc, London, UK
Therein, SE is the extra solid Kirchhoff stress, while
CS = FTS FS is the right Cauchy-Green deformation
tensor of the solid skeleton. Hence, it is possible to cap-
ture the intrinsic viscoelastic and anisotropic effects
in terms of an admissible ansatz for the solid strain
required. Eliminating the seepage velocity by use of
the Darcy filter law (5) yields a concise representa-
tion of the respective balance relations by means of the
primary variables uS and p. Subsequently, weighted by
independent test functions and integrated over the spa-
energy function W S . This is accomplished by a consti- tial domain  with the surface , one finds the weak
tutive split of W S into purely isotropic and anisotropic forms of the mixture volume (MV) and the mixture
contributions, viz.: momentum (MM) balances:

Herein, the isotropic part can be further split into an

equilibrium (EQ) and a non-equilibrium (NEQ) part
yielding a finite viscoelastic material law based on a
generalized Maxwell model as is described in Ehlers
et al. (2002) and Markert (2005). However, the focus
of this paper lies on the description of the osmotic
swelling pressure, the influence of the collagen fibers
and their inhomogeneous distribution. Therefore, only
a purely elastic compressible Neo-Hookean material
S
law is used for WISO reading
Therein, uS and p are the corresponding test func-
tions, q denotes the efflux of the interstitial fluid over
where S0 is the classical ground-state shear modulus,
I1 = tr(CS ) is the first principal invariant of CS , and
JS = detFS is the solid Jacobian. Furthermore, U S (JS )
is an arbitrary volumetric response function, which
characterizes the macroscopic compressibility of the
porous material (cf. Eipper 1998).
Moreover, the anisotropic contribution has to
describe a locally orthotropic fiber reinforcement,
since the fibers within neighbouring layers are
mechanically equivalent. Here, an ansatz in accor-
dance to Holzapfel & Gasser (2001) is chosen via
where 1 and 2 denote material parameters, and a0
and b0 represent the unit fiber vectors defined in
the undeformed state. Note that the mixed invariants
I4 = a0 CS a0 and I6 = b0 CS b0 describe the squared
stretches in fiber direction and, hence, have a clear
physical interpretation (Spencer 1984). Like in rope-
theory, the collagen fibers are assumed to carry loads
only under tension. Therefore, the restriction {I4 , I6 }
1 must hold, which simultaneously satisfies the
material stability criterion (keyword: polyconvexity).
5 NUMERICAL MODELLING AND
EXAMPLE
For the numerical treatment within the FEM, weak
forms of the governing multi-field equations (2) are
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Copyright 2005 Taylor & Francis Group plc, London, UK
the surface , and t = (TSE pI) n is the external
load vector acting on the entire mixture, where n is
the outward oriented unit surface normal. Note that
the spatial discretization has to be carried out using
stable mixed finite elements, such as the Taylor-Hood
element with a quadratic approximation of uS and a
linear approximation of p.
Furthermore, the numerical approximation of
equation (11) demands discrete fiber vectors a0 and
b0 to be initially computed at every Gauss point (GP)
of the mixed finite elements representing the AF. Due
to the irregular geometry of the IVD, it is rather incon-
venient to define a closed mathematical distribution
function. Hence, the fiber vectors are defined with an
algorithm based on tangential planes, which are com-
puted at points resulting from a GP projection onto
the outer surface of the IVD. As depicted in Figure 1,
the fibers are then distributed with a circumferentially
67
59


51
COG
43
w0
Figure 1. Distribution of the varying fiber angle 0 depend-
ing on the polar angle .
varying fiber angle 0 . This is achieved by a linear
regression over the polar angle with respect to the
center of gravity (COG), as is described in Eberlein
et al. (2001) and Eberlein et al. (2004).
Moreover, the overall stiffness variation of the colla-
gen fibers has to be considered locally at every GP. At
this point, the anisotropic stress contribution stemming
from equation (11) is fitted to trilinear material laws
of four distinct regions, which are given by Eberlein
et al. (2004). In particular, these are the anterior inner
(AI) and outer (AO) as well as the posterolateral inner
(PI) and outer (PO) regions, cf. Figure 2. Furthermore,
a linear distribution of the respective material para-
meters 1 and 2 is assumed according to Figure 2,
which can be explained by changes in the morpholog-
ical microstructure of the lamellae discussed by Tsuji
et al. (1993).
The initial FCD distribution is modelled in
a simplified fashion using a constant concentra-
fc
tion of c 0S = 0.10 mol/l within the AF and of
fc
c 0S = 0.26 mol/l within the NP. Accordingly, proceed-
ing from a constant concentration of c m = 0.15 mol/l of
the external solution causes an initial osmotic pressure
of 0 = 0.04 MPa and of 0 = 0.24 MPa in the respec-
tive regions, which yields a prestressed solid skeleton,
i.e., TSE0 = 0 I. In order to compare the influence of the
above described inhomogeneities, equations (12) are
implemented in the FE tool PANDAS (http://www.get-
pandas.com). The corresponding BVP concerns a
simple axial compression test of an L4-L5 motion
segment with removed spinal processes, where a phys-
iological load of 400 N is applied, thus leading to an
external load of t = 0.33 N/mm2 (Fig. 3). Since the
focus lies on the IVD, the vertebrae L4 and L5 are
horizontally cut in parallel having boundary condi-
tions as depicted in Figure 3. The simplified motion
segment is discretized using 7275 20-noded hexahe-
dral elements, each equipped with 27 GPs for the
numerical quadrature. A total number of four simula-
tions is performed using material parameters from the
related literature, see, e.g., Gu et al. (1999), Iatridis
et al. (2003) and Eberlein et al. (2004) among oth-
ers. Overall, the findings presented in Figure 4 are
in good accordance with the experimental results
reported in the related literature, e.g., Nachemson
et al. (1979), Brown et al. (1957) and Wilke et al.
(1999). Moreover, the influences of the osmotic pres-
sure and the inhomogeneities concerning the collagen
fibers become apparent regarding the entire pore pres-
sure p and the relative change in height h, which
is computed at two anterior points within the sagit-
tal plane of the disc (Fig. 3). In particular, neglecting
fc
the attached fixed charges (i.e., c m = 0 = 0) leads
to an underestimation of the entire pore pressure,
which somehow represents a degenerated disc hav-
ing a reduced FCD. Hence, the anulus fibers are not
fully utilized yielding an overall softer response and
thus, a non-physiological bearing mechanism of the
IVD. Furthermore, the differences in h ranging from
0.25 mm to 0.44 mm reveal the necessity of modelling
the fiber inhomogeneities. Note in passing that this
influence is altered concerning the height change as
well as the disc bulge when other regions of the disc are
considered.

AO
AI

b1[MPa] b2[-]

PI w0 = const. w0 = const.
PO b1, b2 = const. b1, b2 = const.
0.77 1.24 1.70 57.0 230.0 370.0 c fc = 0 c fc = 0
h = 0.44 mm h = 0.36 mm
Figure 2. Assumed distribution of the varying fiber stiffness p[MPa]
due to the lamellar microstructure.
0 0.23 0.47 0.70

L4-cut

AF NP AF h w0 = const. w0 = const.
b1, b2 = const. b1, b2 = const.
L5-cut
c fc = 0 c fc = 0
h = 0.37 mm h = 0.25 mm
Figure 3. Uniaxial compression test, where all surfaces are
drained with p = 0, while t = 0.33 N/mm2 is linearly applied Figure 4. Results for four simulations carried out with a
in 1 s. different degree of inhomogeneity.

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Copyright 2005 Taylor & Francis Group plc, London, UK
6 CONCLUSIONS
The above presented results show that the model under
consideration is capable of describing the complex
inhomogeneous and coupled behaviour of the IVD.
Herein, the different characterizing modules, namely
inhomogeneous fibers, permeability, FCD or intrin-
sic viscoelasticity, are easily activated or deactivated,
which yields an efficient tool aiding the study of their
influence on a variety of effects, such as the inter-
stitial fluid flow or the disc bulge. As a next step,
the theoretically introduced material parameters must
be determined by independent experiments involving
more complex deformation modes, such as superim-
posed flexion, lateral bending and torsion. Finally,
together with an appropriate damage model, it is then
possible to describe further degeneration effects and
explore mechanisms leading to disc herniation.
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