Jtam-A4.dvi


JOURNAL OF THEORETICAL

AND APPLIED MECHANICS

52, 3, pp. 677-686, Warsaw 2014

EFFECT OF SUPPORT ON MECHANICAL PROPERTIES OF THE

INTERVERTEBRAL DISC IN LONG-TERM COMPRESSION TESTING

Małgorzata Żak
Wrocław University of Technology, Department of Mechanical Engineering, Wrocław, Poland

e-mail: malgorzata.a.zak@pwr.wroc.pl

The complex kinematic structure and themethod of support of the spinal motion segments
significantly influencemechanicalproperties of the intervertebraldisc (IVD).Becauseof this,
the aim of this study was to analyse the effect of support of the spinal motion segment on
selected mechanical properties of the intervertebral disc. The research involved two groups
of study: with intact segments (IS) andwith acutely injured segments (AIS). In a long-term
cyclic compression test, the spinal segments were loaded with a force of 150-650N. The
study has shown that in the case of damage to articular processes, intervertebral disc height
decreases by 0.09mm, and this decrease is 50% greater than in the case of intact segments.
Themost significant increase in the stiffness coefficient, greater by 63% in the case of injured
segments, occurs after 50000 cycles, which leads to pathological changes taking place in the
structure of annulus fibrosus. In assessing themechanical properties presented in this study,
we should bear in mind that this is not a description of the properties of the intervertebral
disc alone but also of the elements working with it.

Keywords: spine, intervertebraldisc, cyclic loading,viscoelasticproperties, energydissipation

1. Introduction

Thecomplex structureof the spineenablesperformanceofdifferentmovementswhile transferring
loads during daily activities. The basic unit of the spine that enables execution of these tasks is
themotion segment, which consists of two rigid bony blocks connected by an intervertebral disc.
Themultiplanar range of motion of the spine is possible thanks to, among others, a three-point
support (intervertebral disc and two symmetrical facet joints), which transfers loads acting on
the spine. Specifically, axial loads are transferred to a greater extent by the intervertebral disc
than by articular processes (Nachemson, 1960; Ranu,1990). In the case of a healthy spine, the
posterior column (articular processes) transfers 5-10% of the load. This value increases with the
development of degenerative changes in the intervertebral disc. In such a case, the processes can
take over up to 40% of the load (Pollintine et al., 2004). At the same time, the combination of
flexion-extensionmovements, twistingandshearingof the segmentsdirectlyaffects themechanics
of the intervertebral disc showingviscoelastic properties (Stokes et al., 2002;GaddandShepherd,
2011; Żak and Pezowicz, 2012; Izambert et al., 2003; Campana et al., 2011).
Many authors emphasize that themethodof supportof themotion segments has a significant

impact on kinematics of the spine and mechanical properties of the intervertebral disc (Rohl-
mann et al., 2006; Robertson et al., 2013). However, these results are obtained by static tests,
which, although important for understanding the disc mechanics, do not reflect the conditions
characteristic for long-term repeating loads acting on the spine.
Consequently, these studies donot explain howbiomechanical behaviour of the intervertebral

disc changes in a long-term compression test that corresponds to a load contributing to, among
others, the formation of pathological changes in the spine.
Only a few authors have analysed the impact of cyclic loading (above 20000 cycles) on the

biomechanics of the intervertebral disc, including its viscoelastic properties, change in stiffness



678 M. Żak

and energy dissipation (Johannessen et al., 2004; Koeller et al., 1984; Hasegawa et al., 1995;
Schmidt et al., 2010). However, these works focused mainly on the analysis of the impact of
the applied test protocol (cyclic loading, creep, recovery) in the axial compression test on the
mechanical properties of thedisc.Moreover, theanalyses involved only themotion segmentswith
articular processes removed. Suchaprocedure enables descriptionof thephenomena takingplace
in the intervertebral disc but the adopted test systemdiffers significantly fromthe actual system,
in which the posterior pillar plays equally important role in the transfer of loads as the anterior
column.
Based on the above, the aim of this work was to determine the impact of the three-point

support in spinal motion segments on the mechanical properties of the intervertebral disc in
compression testing. The analysis of the mechanical properties of the intervertebral disc was
performed on the obtained hysteresis loops, determining, as one of the parameters, changes in
energy described by dissipation energy (Wilke et al., 1998; Żak and Pezowicz, 2013; Gardener-
Morse and Stokes, 2003).

2. Material and method

The testswere performedon themotion segments collected postmortem fromsix thoracic spines
of domestic pigs aged 8-9 months and weighing 90-110kg. Currently, the research onmodels of
human preparations (cadaver) is replaced by preparations of animal origin. For studies of the
spine (particularly the intervertebral disc) to the most commonly used animal species include:
pigs, sheep, dogs, rabbits, mice and rats. There are many reasons indicating that the animal
model of the spine is not equivalent to the human spine. However, despite many differences,
the authors of in this study prove that the animal preparations of the spine can replace the
models of the human spine (Szotek et al., 2004; Alini et al., 2008; Lotz, 2004). The selected
segments Th8-Th11 were divided so that they formed the basic functional unit of the spine:
vertebra-intervertebral disc-vertebra. Since themain objective was to analyse the impact of the
spinal support column, the segments were divided into two groups: IS-intact segments (n=5)
prepared in such away as to preserve all supporting elements of the spine (anterior andposterior
columns), andAIS-acutely injured segments (n=5) after removal of the load-bearing elements
of the spine in the posterior column (Fig. 1). Next, the motion segments were stored in plastic
containers at −20◦C until testing. Because hydration has a significant impact on mechanical
properties of the intervertebral disc (Żak and Pezowicz, 2013), the spinal motion segments were
defrosted at room temperature and then hydrated in NaCl saline environment for one hour.

Fig. 1. Schematic diagram of functional spine segments: IS-intact segments (with anterior and posterior
columns), AIS – acutely injured segments (anterior column only). The motion segment consists of the
intervertebral disc located between two vertebrae. The anterior column consists of two vertebral bodies
and an intervertebral disc, whereas the posterior column is formed by articular processes of the

vertebrae and ligaments

The vertebral bodies of the segments were fixedwith screws to the upper and lower brackets
of a purpose-built test system (Fig. 2). The bone parts of the segments were mounted in a



Effect of support on mechanical properties of the intervertebral disc... 679

bracket at one third of the height of the vertebral body. The test system was also equipped
with an element enabling forced physiological bending of the segments during the test at a 6◦

angle (Dunlop et al., 1984; Dolan andAdams, 2001; Callaghan andMcGill, 2001). This loading
method, i.e. compression with bending, leads to faster induced failure in intervertebral disc
structures (Adams and Dolan, 1996).

Fig. 2. Diagram of the motion segmentmounting in the test rig with simulated progress of the process
of loading segments during the test

Daily loads acting on the spinewere simulated on anMTS 858Mini Bionix testingmachine.
The test was performed for 100000 loading cycles at a frequency of 2Hz. The segments were
loaded with an axial force between 150N to 650N, which simulated daily range of loads put
on the spine. It was also assumed that the first 50 cycles corresponded to conditioning cycles
(Żak and Pezowicz, 2013; Żak, 2010). At the same time, during the whole compression test,
the segments were hydrated with saline solution through the superior vertebral body (Huber et
al., 2007). This forced physiological flow of the fluid through the intervertebral disc structure,
eliminating the effect of dehydration on the obtained mechanical parameters (McMillan and
Adams, 1996; Stokes et al., 2002). In addition, in order to prevent drying of the external soft
tissues, the specimens were wrapped in moist gauze.
The effect of cyclic axial loads on the structure of the tested motion segments (IS, AIS)

was determined from the force-displacement curves of the specimens compressed with a force of
150-650N – see Fig. 3.

Fig. 3. Exemplary F(p) function for an intact motion segment obtained in compression testing: typical
data of selected hysteresis loops. Stiffness coefficient (k) was determined at the maximum force

intervals during unloading

Changes in the IVD height for successive hysteresis loops were determined according to Eq.
(2.1) on the basis of changes in the segment displacement at theminimum andmaximum loads

∆h= pFmax−pFmin (2.1)



680 M. Żak

where ∆h [mm] are the changes of the IVDheight, pFmax [mm] –displacement at themaximum
load, PFmin [mm] – displacement at the minimum load.
The stiffness coefficient was determined according to Eq. (2.2) on the basis of the displace-

ment at a range of load 630-650N. It was to correspond with stiffness values obtained at the
maximum load (Fig. 3)

k=
∆F

∆p
(2.2)

where k [N/mm] is the stiffness coefficient, ∆F [N] – the range of load 630-650N, ∆p [mm] –
displacement at loads 630-650N.
The obtained hysteresis loops of the area enclosed by the load-displacement curvewere used

to assess the degree of damping of the tested spinal motion segments, defined as dissipation
energy ∆E determined based on the difference between the surface area during loading EL and
unloading EU, according to Eqs. (2.3)

∆E =EL−EU EL,U =
Fmax∫

Fmin

F(p) dp (2.3)

where ∆E [J] denotes the dissipation energy, EL,U [J] – area of half hysteresis in function F(p):
L – loading, U – unloading.
According to the study by Koeller et al. (1984), the balance of energy changes in successive

hysteresis loops can be used to determine viscoelastic properties of the intervertebral disc. The
authors presented amethod for determiningmaterial properties, inwhich the ratio of dissipation
energy to energy obtained in a loading half cycle defines the so-called viscoelastic factor VEF

VEF =
∆E

EL
(2.4)

where VEF [–] is the viscoelastic factor, ∆E [J] – energy dissipation, EL [J] – area in loading.
The viscoelastic factor can be used to determine whether a material has mostly elastic or

viscousproperties.When VEF is close to 0, thematerial showsmoreelastic properties.However,
when VEF approaches 1, the material showsmore viscous properties.

3. Results and discussion

The values of mechanical parameters, determined in cyclic load testing of specimens, showed
differences between successive cycles and between the examined groups of motion segments of
the spine. Figure 4a shows a decrease in changes of the IVD height in successive cycles. In the
case of both IS and AIS segments in the course of ∆h, we can distinguish two characteristic
stages: first – an initial, dynamic drop in height; and second – stabilization, maintenance of
a constant height. The research by Liu et al. (1983) also showed the presence of characteristic
intervals of displacement changes in function of the number of applied cycles, but the researchers
performed only 10000 cycles.
The first stage consists of the first 10000 loading cycles, and is characterized by similar

dynamics in both test groups. At the same time, we can see that the decrease in changes of
the IVD height (∆h) is significantly greater in the injured segments (AIS) than in the intact
segments (IS).After 10000 cycles, therewas a 47%difference in the height decrease ∆hbetween
IS and AIS.
In the second stage, the segment height stabilises in both groups and stays at the same level

until the end of the test. The average value of ∆h amounts to (4.49±0.14)·10−2mmin the case



Effect of support on mechanical properties of the intervertebral disc... 681

of the IS segment and (9.02±0.22)·10−2mmin the case ofAIS.Also, in the case of loadingwith
a force of 650N, the global difference between the initial and the final displacement amounts to
2.48mm for IS and 2.87mm for AIS. The relative change in the IVD height determined as the
difference between the initial and final value changes of the IVDdisplacement atmaximum load
amounts to 2.48±0.47mm in the case of the IS segment and 2.87±0.38mm in the case of AIS.
The stiffness coefficient k of the tested segments increases with successive loading cyc-

les. Initially, after 10000 cycles the value k amounts to 0.76 ± 0.21kN/mm for IS and
0.81± 0.18kN/mm for AIS. Despite the lack of a significant increase in the displacement at
a force of 650N, in subsequent loading cycles, there is a visible further increase in the stiffness
coefficient of the tested segments (Fig. 4b). In the middle of the test (after 50000 cycles) the
value is 10.29±3.78KN/mm for IS, and is higher by 63% than the value obtained for the AIS
segments.
In the final loading stage (in 100000 cycles), the highest values of the stiffness coefficient are

observed in the AIS segments (121.41±44.81kN/mm), which were 66% higher than the values
obtained in the IS segments (40.93±23.12kN/mm).

Fig. 4. The characteristics of changes in the mechanical parameters of the tested segments (IS – intact
segment and AIS – acutely injured segment) in successive loading cycles: (a) changes of the IVD height
(∆h) with marked characteristic stages of decrease in the intervertebral disc height: I – initial dynamic
decrease in height, II – maintenance a constant height; (b) the stiffness coefficient (k) at the maximum

force, taking into account changes in the displacement at 630-650N loading

The results confirm that during physiological loading of the intervertebral disc, there is a
decrease in height and an increase in stiffness (Johannessen et al., 2004; van der Veen et al.,
2007).
Johnnessen et al. (2004)examined segments derived from sheep spine and showed that after

10000 load cycles, the value of the stiffness coefficient falls within the range of 603 to 800N/mm.
It is also the range after which the intervertebral disc can still recover to its previous state by
restoring normal hydration.
At the same time, cyclic loading causes changes in the hydrostatic properties of the interver-

tebral disc, during which there is a change in the direction of the fluid flow in IVD. A loss of



682 M. Żak

water and a drop in IVD height cause simultaneous bulging of the annulus fibrosus (Papadakis
et al., 2011). Subsequent loading cycles lead to a further increase in stiffness (despite lack of
changes in the intervertebral disc displacement), promoting formation of defects in its structure.
On the other hand, Hasegwa et al. (1995) indicated that the increase in stiffness, in the range
of up to 40000 cycles of the load, is primarily associated with changes in viscoelastic properties
of IVD.
As a result of high compressive loads (about 100000 cycles), irreversible changes occur in

the structure of the annulus fibrosus, as shown inmicroscopic observation (Fig. 5). Specifically,
analysis of sagittal cross-sections of themotion segment showed no degenerative changes within
the vertebral body and the end-plate, which often accompany degenerative changes arising
with age. Structural studies indicate that one of the signs of degeneration is delamination of
the annulus fibrosus (Gregory and Bae, 2012). Because of composite structure of the annulus
fibrosus, most of the damage relates primarily to changes within the inner annuli of the disc
(Adams et al., 1996; Cassidy et al.,1990; Pezowicz et al., 2006a,b) (Fig. 5b). Damage in form of
delamination of annulus fibroses lamellae occurred primarily at the posterior intervertebral disc
(Fig. 5d), resulting in loss of coherence between the adjacent lamellae. For some of the analysed
cross-sections, delamination also occurred in the anterior annulus fibrosus, demonstrated by
disorganized distribution of lamellae and clear separation of inner lamellae fromthe superior end
plate (Fig. 5c). Disturbances in the lamellae structure are promoted bymigration of the nucleus
pulposus, which causes nucleus pulposus herniation. In this study, the dehydration effect and
a decrease in the intervertebral disc height cause significant structural changes of the posterior
annulus fibrosus. The resulting structural changes destabilize the functions of the intervertebral
disc and, consequently, cause transfer of the load-bearing capacity to articular processes (Adams
et al., 2010).

Fig. 5. A sagittal cross-section of the spinal motion segment preserved in glutaraldehyde: (a) unloaded,
with clearly visible central nucleus pulposus and an outline of the distribution of annulus fibrous
lamellae; (b) after cyclic loading (acutely injured segment), with clearly disturbed annulus fibrosus
structure; (c) delamination of inner anterior lamellae of the annulus fibrosus; (d) visible delamination

and a clear bulge of posterior lamellae of the annulus fibrosus

The dissipation energy determined for successive loops is ameasure of damping effect of the
elements included in the motion segment. The initial dissipation energy (∆E) after 50 condi-
tioning cycles was 23% greater in the case of the IS segments (24.22± 12.82J) compared to
the energy obtained for AIS (18.68±4.73J). At the same time, the energy in the first loading



Effect of support on mechanical properties of the intervertebral disc... 683

stage (to 10000 cycles) decreases linearly to 21.15±9.02J in the case of the IS segments and
to 14.56± 4.83J in the case of the AIS segments. In the second stage, the energy changes of
the tested segments are characterised by an unchanging course. In the range of 15000-100000
cycles, the difference between IS andAIS amounted to 33%. After the completion of the loading
cycles, the smallest dissipation energy loss was recorded for theAIS segments, where the energy
did not exceed 13.50±6.35J andwas lower by 36% than in the case of the IS segments –Fig. 6a.
After 50 conditioning cycles, the viscoelastic factor (VEF) was higher by 19% in the case of

the IS segments (VEF =0.15±0.06) than in the case of theAIS segments (VEF =0.12±0.01).
The initial VEF value at the first loading stage (to 1000 cycles) decreased linearly. The overall
decline in VEF during the tests was 11% for the IS segments and 13% for the AIS segments –
Fig. 6b.

Fig. 6. The characteristics of changes in the viscoelastic parameters of the segments (IS – intact
segment and AIS – acutely injured segment) in successive loading cycles with marked distinctive stages

of changes in: (a) dissipation energy (∆E), (b) viscoelastic factor (VEF)

The nonlinear mechanical properties of IVD result from the complex structure of the tissue
(Panjabi et al., 1994; Kaigle et al., 1997; Gregory and Bae, 2012; Gohari et al., 2013; Kobielarz
and Jankowski, 2013) and are largely related to the loss of water and tissue dehydration (Ko-
eller et al., 1984; Adams and Dolan, 2012). The characteristics of viscoelastic properties of the
intervertebral disc change with loading applied to the motion segment, as shown by the results
obtained for ∆E and VEF. However, the similar course of the ∆E and VEF curves over time
does not give a clear answer to the question on material characteristics of the disc. Therefore,
the usefulness of the viscoelastic factor (VEF) proposed by Koeller et al. (1984) in assessing
the viscoelastic characteristics seems to be negligible.

4. Conclusions

The results of the conducted research show a significant effect of the segment support on me-
chanical properties of the intervertebral disc in long-term compression testing. As a consequ-
ence of damage to the posterior columns (articular processes), there are greater changes in the



684 M. Żak

mechanical properties of the injured segments compared to the intact segments, including a 50%
greater drop in IVD height, an increase in the stiffness coefficient at a constant displacement
rate, and a clear delamination and deformation of the annulus fibrosus. In the segments with
no additional point of support in form of articular processes, the load-bearing function is taken
over in its entirety by the intervertebral disc. This also involves an increased range of motion
within the segment as the primary role of the articular processes is to stabilize the spine and
eliminate its axial rotation during flexion and extension (Adams, 2004).
In assessing themechanical parameters presented in this work, we should bear in mind that

this is not a description of the properties of the intervertebral disc alone, but also of the elements
working with it, such as hyaline cartilage or ligaments, and in the case of a full motion segment,
we should also take into account the articular processes.
In addition, because of thedominant role of the intervertebral disc in the load-bearing system

of the spine, it is important to search for data that would describe themechanical action of the
structure. This is particularly important due to, among other reasons, the increasing percentage
of degenerative intervertebral disc diseases among young people, to whom the use of standard
stabilization of the spine by fusion does not allow for full return to active life. Alternatively, disc
prostheses can be used, which copy the mobility characteristics of a natural disc but in most
cases do not provide adequate flexibility to reflect the amortisation and load-bearing functions
in a manner similar to physiological processes.

Acknowledgements

This work is supported by Polish Ministry of Science and Education within the grant No.
NN518501139.

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Manuscript received November 26, 2013; accepted for print February 7, 2014