Compressive Fatigue Behaviour of a Polymer-Based Osteochondral Scaffold
Y-H. Hsua, C Luptona, J. Tonga, A. Cosseyb, A. Auc
a
Mechanical Behaviour of Materials Laboratory, School of Engineering, University of
Portsmouth, UK
b
c
Queen Alexandra Hospital, Portsmouth, UK
Smith & Nephew, Advanced Surgical Devices, Andover, MA, USA
Abstract
Cyclic loading from daily activities or from intensive exercise can lead to increased risk of
fracture. Implants designed for load bearing purposes, such as repair of articular cartilage and
underlying subchondral bone in knees must have the necessary resistance to fatigue loadings.
To date, virtually no studies have been reported on the fatigue behaviour of osteochondral
scaffolds, despite damage due to repeated loading is of considerable interest for tissue repair
purposes.
In this study, a polymer-based osteochondral scaffold has been studied under cyclic loading
conditions. Multi-step cyclic tests have been carried out with increasing compressive loads in a
phosphate buffered saline solution at 37oC. Changes in secant modulus and residual strain
accumulation are monitored. Morphological parameters of the scaffold are determined using
micro-computed tomography. The secant modulus and the number of cycles to failure of the
scaffold are obtained and compared with those of human trabecular bone (Topolinski et al,
2011).
1. Introduction
A variety of biological and synthetic scaffolds have been developed for articular cartilage and
subchondral bone repair purposes.1-11 However, scaffolds often lack the physical structure and
mechanical properties necessary to sustain long-term applications.12 Although biocompatibility
and bio-related issues have been studied widely, evaluation of mechanical properties has been
an area of underdevelopment, with testing parameters and conditions varied greatly; and
testing under controlled physiological loading conditions similar to those in vivo particularly
lacking. Evaluation of the mechanical properties of scaffolds is not always done in aqueous
solution at 37°C, although the mechanical properties of hydrated scaffold samples are known to
be much lower than those of dry samples.4-6 13 A number of scaffolds and bones were tested in
tension,8,
14, 15
which bears little resemblance to the in vivo loading environment primarily in
compression. Human bone is subjected to a variety of loading patterns during daily routine
activities. A typical loading condition is repeated or cyclic loading as experienced in walking or
running.
Bone response under such loading conditions may be referred to as fatigue
behaviour.16,
17
Fatigue damage is a process of gradual mechanical degradation caused by
repeated loading at stress or strain much lower than those required to fracture in a single
application of force. As a result, damage due to cyclic loading is of significant interest for design
and application of synthetic scaffolds.
In a conventional fatigue test, specimens are subjected to a constant amplitude load till
failure to determine the number of cycle to failure at a given load range. A number of studies
based on this method have been carried out on the fatigue behaviour of bones.15, 18-30 Some
studies have also been carried out for synthetic biopolymers.31,
32
Using this method a great
number of samples may be needed to obtain the fatigue behaviour under variable stress
amplitudes. Stepwise-testing has since been developed which would allow the generation of
fatigue data with only a small numbers of samples.33, 34 In stepwise-tests, samples are subject
to loads of a range of amplitudes in each a number of cycles are allowed to elapse, thus
providing an accelerated testing regime with increased data generation.
parameter obtained from such tests is the evolution of secant modulus
One important
21, 33, 35
which is an
indication of damage accumulation.30, 36
Polymer-based osteochondral scaffolds are synthetic resorbable implants designed to
replace worn-out cartilage surfaces, restoring mobility and relieving joint pain. Although used in
some clinical cases,37-39 there is a lack of published data on the biomechanical properties of the
implant. Knowledge of its mechanical behaviour is essential in order to obtain accurate
prediction of stresses and deformation in clinical applications, where the structural integrity of
the implant is particularly important when cyclic loading is considered. The motivation of the
study is to evaluate the fatigue behaviour of an osteochondral scaffold using the step-wise
testing method and to compare the results with those from human bone in terms of stress-strain
response and secant modulus. Morphological parameters of the scaffold were also obtained
and compared with those of human bone.
2. Materials and methods
2.1 Specimen
A commercial scaffold TRUFIT (Smith and Nephew) was used in the study. It is composed of
polylactide-co-glycolide (PLG) copolymer with calcium-sulfate and polyglycolide (PGA) fibres.
The dual-layer design of the implant contains both a cartilage and a bone phase. Cylinders of
the two layers scaffolds were sectioned to obtain a single layer of TRUFIT Bone, with a
diameter of 10.5mm, a length of 9 mm and an aspect ratio of 0.86. The aspect ratio was
selected based on the information obtained previously,40-42 where reported aspect ratios are
generally less than 1. 33, 43-45 The aspect ratio and dimensions of the TRUFIT Bones are in a
similar range of those of human trabecular bones in Topolinski’s study. 33 The samples were
soaked in phosphate buffered saline (PBS) solution overnight prior to testing.
2.2 Morphological Parameters
The microstructure of the specimens was examined prior to fatigue testing using micro-focus
computed tomography (CT X-Ray Inspection System, Metris X-Tek Systems Ltd). The MicroCT scanner was operated at a voltage of 51 kV, current of 160 μA and a voxel size of 17-20
μm. Bone volume density (BV/TV), mean thickness of the trabeculae in the specimen (Tb.Th)
and the mean distance between trabeculae (Tb.Sp) were obtained by processing the micro-CT
images using Microview software.
2.3 Compression fatigue testing
Fatigue testing was carried out on a Bose ElectroForce 3200 Testing system equipped with an
environmental chamber to which PBS solution was filled and controlled at a temperature of
37˚C. Each specimen was placed carefully at the centre of the platens inside the environmental
chamber. During the testing, the specimens were unconstrained33 between the platens of the
testing machine as fixation of the specimens to the test platens may increase stiffness 46 Five
TRUFIT Bones were tested under load control26, 27 with a stepwise increase of maximum stress
whilst keeping the minimum stress constant, following a testing protocol of Topolinski et al. 33
A preload of 5 N was applied first to ensure good end contact and this preload was
subsequently kept constant as the minimum load throughout the test. The maximum load
started from 10 N with a gain of 10 N at successive steps, as shown in Figure 1. The maximum
load was kept constant during a period of 500 cycles and increased to the next level thereafter.
The loading scheme was adopted from Topolinski et al33 to allow easy comparison with the
results from human trabecular bone.33 The loading waveform was sinusoidal at a frequency of 1
Hz.
Engineering stress and strain were calculated by using the applied load, displacement
and the original dimension of the specimens, where lateral deformation under compression was
not considered. The changes in the secant modulus and the maximum and minimum strains
with fatigue loading were recorded. The change in the secant modulus is considered indicative
of damage accumulation in the specimen30, 36 in fatigue studies of bones from the literature.15, 18,
21, 23-29, 33-35, 47
The secant modulus at a given cycle was defined as Δσ/Δ = (σmax-σmin)/(max-
min), determined from the stress-strain curve. Figure 2 illustrates this as the slope of the line
connecting the lowest and the highest point of a stress-strain loop. The secant modulus and
strains were measured throughout the test. The cyclic stress-strain curves were also compared
with those obtained under monotonic loading conditions.
3. Results and discussion
Table 1 shows the morphometric values of the TRUFIT Bone and human trabecular
bone.33 The average BV/TV of the scaffold (0.343) is well within the range of human trabecular
bone (0.076-0.460). The trabecular thickness of the scaffold is slightly lower (0.086mm) than
that of human trabecular bone (0.105-0.268mm); whilst the trabecular spacing (0.166mm) is
smaller than that of human (0.424-1.829mm). These indicate that the microstructure of the
scaffold consists of thinner but more densely packed struts than that of human trabecular bone.
Table 1 also includes the maximum stress corresponding to the maximum secant modulus.
Samples with higher values of the maximum stress indicate higher fatigue resistance. It is clear
that the fatigue resistance of the scaffold at an average of 0.462MPa is much lower than the
range (0.859-12.28MPa) from human trabecular bone. A large variation in the results from
human bones may be due to the varied sources (e.g., multiple donors with individual
characteristics and pathologies).33 In contrast, synthetic TRUFIT bones have more consistent
morphometric values. Although a relationship between bone structure and fatigue strength for
human bone was reported,33 it is not possible to obtain such a relation for the scaffold due to
the lack of variety of the microstructure features.
Typical stress-strain curves of a sample tested under the multi-step loading scheme
(LS1 to LS8) are shown in Figure 3. Each block, shown in a different colour, represents the
response to a single loading step with 500 loading cycles. A distinctive characteristic at all load
levels is the accumulation of residual strain, or cyclic creep, with the increase of loading cycles.
Greater strain ratchetting appears to be associated with higher load levels, when non-linear
deformation becomes more evident in the larger hysteresis loops under LS7 and LS8. This is
consistent with the behaviour observed in trabecular bones.26, 29, 35, 47
The evolution of the secant modulus (as defined in Figure 2) with cycles is shown in
Figure 4(a) for the five samples tested. In all cases, it appears that an increase in secant
modulus with cycle persisted for most of the loading steps, particularly the early ones. Only
towards later at higher load levels reductions in secant modulus become evident. The initial
hardening seems to be somewhat unexpected, certainly in contrast to the continuing increase
in the residual strain with cycle, as shown in Figure 4(b), where the maximum and the minimum
compressive strains of the five samples are recorded. Interestingly samples with lower residual
strains (A, B, C) tend to have higher secant modulus (Figure 4(a)). Both maximum and
minimum strains increased with the number of cycles during the entire test and the gap
between the maximum and the minimum strains is roughly constant for each sample, indicating
that the strain range stays constant. In addition, the strain rate increases with the increase of
the number of cycles. It is known that residual strain or cyclic creep plays an important role in
material failure due to the accumulated plastic deformation.30,
35
Increase in strains with the
number of cycles have been generally observed when testing bones under cyclic loading, 27, 34
although increasing strain rate during the entire test was found in bovine trabecular bone. 34
Three stages of deformation during compression fatigue tests have been reported for human
trabecular bone,27 including a transient behaviour characterised by rapid strain increase within
the initial load cycles, saturation of strain and an acceleration towards final catastrophic failure.
When secant modulus of the scaffold is compared with those of human trabecular
bones,33 as shown in Figure 4(c), much lower secant modulus and total number of cycles to
failure were obtained for the scaffold, although the patterns of evolution with cycle appear to be
similar between the two. The initial hardening of the bone is also consistent with the results
under conventional constant-amplitude fatigue testing. Linde and Hvid51 reported that in human
trabecular bones the stiffness increases until a stress level about 50% of ultimate stress is
reached followed by decreasing stiffness, although others reported decreasing in modulus from
the beginning to the end.18, 22, 24-27, 52, 53 Michel et al35 studied the fatigue behaviour of bovine
trabecular bones under load control using a sinusoidal compressive load profile at a frequency
of 2 Hz. The results showed that the pattern of modulus change with the number of cycles was
associated with the load level. At low cyclic load levels the modulus increased initially followed
by a rapid drop in the final stage. At high cyclic loads a continuous decrease in modulus from
the beginning was found. The authors35 suggested that both creep and damage accumulation
may be responsible for fatigue failure of trabecular bone, i.e. bone fails by creep under high
cyclic loads whilst by microcrack damage accumulation at low cyclic loads. A more recent study
suggested, however, that creep effects are negligible in fatigue loading cases for trabecular
bone.54 An initial increase in modulus has been observed for TRUFIT at most of the load levels
except the highest levels, which appears to be consistent with the observation in some of the
reports.35 and 51
Stress-strain loops of first cycles at the beginning of each fatigue loading step are
presented in Figure 5(a). Each centre of the loops was moved to the origin (0,0) then the points
at the top of each loop were linked to form the initial cyclic stress-strain curve. Figure 5(b)
shows the final cyclic stress-strain curve which was obtained similarly using the loops of the
final cycles at the end of each loading step. These cyclic stress-strain loops at the first and the
final cycles do not appear to differ significantly (Figure 6, CSS_1 and CSS_f), suggesting stress
softening may not be significant. Figure 6 shows a comparison of cyclic and monotonic stressstrain curves for a typical specimen of TRUFIT. Here LS1_0 to LS5_0 are monotonic stressstrain curves whilst CSS_1 and CSS_f are the first and the final cyclic stress-strain curves. The
monotonic curves are the loading parts of a stress-strain curve at the beginning of the each
loading step. The slopes of these curves are the modulus of elasticity. A comparison of the
mean elastic modulus of the stress-strain curves is shown in Figure 7. The elastic modulus of
monotonic stress-strain curves increase with the number of loading steps (a) and the moduli of
cyclic curves are generally higher than those of monotonic ones, suggesting stress hardening,
consistent with the trend shown in Figure 4(a). However, the elastic modulus of first cyclic
stress-strain curve is higher than that of final cyclic stress-strain curve, suggesting damage
accumulation due to fatigue.
4. Conclusions
Multi-step cyclic tests have been carried out on TRUFIT Bones to study the fatigue behaviour of
the scaffold under increasing compressive cyclic loading conditions. Morphological parameters
of TRUFIT scaffold have also been obtained using computed tomography and compared with
those of human trabecular bone. The results show an increase in secant modulus and stress
hardening during the initial steps of fatigue loading, consistent with that observed in human
trabecular bone. The modulus and the number of cycle to failure of the scaffold are, however,
significantly lower than those of human trabecular bone. The elastic modulus of monotonic
stress-strain curves increases with the number of loading steps and the moduli of cyclic curves
are generally higher than those of monotonic curves. Progressive increase in residual strains
has been observed in the scaffold for the entire test duration, indicating that residual strain
accumulation, or cyclic creep, may be the predominant driving force leading to failure of the
scaffold.
Multi-step tests seem to be useful in assessing the essential fatigue behaviour of
scaffolds. These tests allow the reduced number of samples for a reliable analysis of fatigue
properties of biomaterials.
Acknowledgements
The authors would like to thank Smith & Nephew for the provision of samples and University of
Portsmouth for financial support.
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Figure1. The loading scheme of a stepwise fatigue test (Fmax=10N; Fmin=Fpreload=5N), following
the protocol of Topolinski et al, 2011.33
Figure 2. Secant modulus (Ei) is defined as the stress range divided by the strain range at a
given cycle i, which is determined by the slope of the line connecting the minimum and the
maximum stress values of the cycle.
Figure 3. Stress-strain curves from a multi-step fatigue test.
Figure 4. (a) The
evolution of secant modulus as a function of cycles for TRUFIT Bone (b) the development of
the maximum and minimum strains with cycle and (c) comparison of secant modulus of
TRUFIT Bone and human trabecular bone.33
Figure
5. Cyclic stress-strain responses: (a) Loops of first cycles at the beginning of each loading step;
(b) loops of the final cycles at the end of each loading step.
Figure 6. Comparison of the cyclic and the monotonic stress-strain curves of a typical sample.
Figure 7. The elastic modulus of (a) monotonic curves; and (b) cyclic stress-strain curves.
Table 1. Morphometric values and maximum stresses of TRUFIT bone and human
trabecular bone. 33
Bone volume density Trabecular thickness Trabecular spacing
TRUFIT Bone
BV/TV
Tb.Th (mm)
Tb.Sp (mm)
Max Stress (MPa)
(corresponding to
Emax)
A
0.359
0.089
0.161
0.547
B
0.340
0.082
0.158
0.328
C
0.353
0.087
0.159
0.547
D
0.328
0.089
0.184
0.337
E
0.333
0.084
0.169
0.552
Human trabecular
bone [33]
0.076 - 0.460
0.105 - 0.268
0.424 - 1.829
0.859 - 12.280