VOL. 91-B, No. 4, APRIL 2009557
The influence of the mechanical environment
on remodelling of the patellar tendon
A. P. Rumian,
E. R. C. Draper,
A. L. Wallace,
A. E. Goodship
From the Institute of
? A. P . Rumian, MA, FRCS(Tr
and Orth), Specialist Registrar
St Mary’s Hospital, Praed
Street, Paddington, London W2
? E. R. C. Draper, PhD, Principal
? A. E. Goodship, BVSc, PhD,
MRCVS, Professor of
Institute of Orthopaedics and
University College, London,
Royal National Orthopaedic
Hospital, Brockley Hill,
Stanmore, Middlesex HA7 4LP ,
? A. L. Wallace, PhD, FRACS,
Surgeon and Honorary Clinical
Hospital of St John and St
Elizabeth, 60 Grove End Road,
London NW8 9NH, UK.
Correspondence should be sent
to Mr A. P . Rumian; e-mail:
©2009 British Editorial Society
of Bone and Joint Surgery
J Bone Joint Surg [Br]
Received 24 July 2008;
Accepted after revision 17
An understanding of the remodelling of tendon is crucial for the development of scientific
methods of treatment and rehabilitation. This study tested the hypothesis that tendon
adapts structurally in response to changes in functional loading. A novel model allowed
manipulation of the mechanical environment of the patellar tendon in the presence of
normal joint movement via the application of an adjustable external fixator mechanism
between the patella and the tibia in sheep, while avoiding exposure of the patellar tendon
itself. Stress shielding caused a significant reduction in the structural and material
properties of stiffness (79%), ultimate load (69%), energy absorbed (61%), elastic modulus
(76%) and ultimate stress (72%) of the tendon compared with controls. Compared with the
material properties the structural properties exhibited better recovery after re-stressing with
stiffness 97%, ultimate load 92%, energy absorbed 96%, elastic modulus 79% and ultimate
stress 80%. The cross-sectional area of the re-stressed tendons was significantly greater
than that of stress-shielded tendons.
The remodelling phenomena exhibited in this study are consistent with a putative
feedback mechanism under strain control. This study provides a basis from which to explore
the interactions of tendon remodelling and mechanical environment.
Disuse of joints may result follow trauma,
degenerative change, inflammatory arthropa-
thies, neurological conditions and infection.
The treatment of injuries involving bones and
joints often involves their immobilisation in
the early stages to protect the healing tissue or
surgical fixation. However, the actual physio-
logical effects of immobilisation and disuse
have only relatively recently been investigated.
Joint disuse has a profound effect on the intra-
and peri-articular tissue, with a sequence of
changes including proliferation of intra-
articular connective tissue, the formation of
adhesions and ulceration of the cartilage, with
joints becoming stiff as a result of muscular
and capsular contracture combined with intra-
Biomechanical properties of tendons and
ligaments can be divided into structural, such
as the cross-sectional area, the length, the ulti-
mate load and stiffness, which relate to the
function of the structure as a whole, and mate-
rial including stress, strain and elastic modulus
which relate to the attributes of the constituent
tissue. Noyes et al3 and Noyes4 investigated the
effect of immobilisation and reconditioning on
the femur-anterior cruciate ligament (ACL)-
tibia complex in primates. After eight weeks of
immobilisation of the limb in a plaster cast, the
bone-ACL complex had an ultimate load of
61% and energy absorbed of 68% compared
with controls, with a significant reduction in
stiffness to 69%. This finding of reduced stiff-
ness in the ligament was in contrast to previous
assumptions that immobility causes contrac-
ture and stiffness in all the peri-articular
tissues.5-7 In animals that were allowed normal
movement for five months after eight weeks of
immobilisation, the ultimate load and energy
absorbed were still only 76% and 78%,
respectively, compared with the control values,
whereas after 12 months of reconditioning
they were 91% and 92%, respectively, demon-
strating that a short period of disuse can result
in long-term consequences.
Amiel et al8 tested the femur-lateral collat-
eral ligament (LCL)-tibia complex from rab-
bit knees immobilised for nine weeks. The
load-elongation curve was similar to that
reported by Noyes et al.3 By demonstrating
that the cross-sectional area had not
decreased significantly, whereas the stress-
strain curve showed significantly inferior
mechanical properties, Amiel et al8 deduced
that the changes must be due to alterations in
the substance of the ligament itself, rather
558 A. P. RUMIAN, E. R. C. DRAPER, A. L. WALLACE, A. E. GOODSHIP
THE JOURNAL OF BONE AND JOINT SURGERY
than simple atrophy of the tissue. Analysis of the patellar
tendon and medial collateral ligament (MCL) from the
immobilised knees showed an increased rate of both col-
lagen synthesis and degradation, with no change in the
total collagen mass. He suggested that newly synthesised
collagen was laid down in a haphazard manner owing to
the lack of the normal mechanical stimulus, resulting in
inferior mechanical properties.
The development of more sophisticated methods of
measuring cross-sectional area and the use of video tech-
nology allowed for more accurate measurement of bio-
mechanical properties, enabling the study of the stress-
strain characteristics of tendon and ligament tissue itself.
Woo et al9 found a significant reduction in the cross-
sectional area of MCLs from rabbit knees immobilised for
nine and 12 weeks. The cross-sectional area of MCLs
from knees remobilised for nine weeks after nine weeks of
immobilisation was not significantly different from that of
the controls. Immobilisation was again shown to signifi-
cantly reduce both the structural and the material proper-
ties, with a reduction in ultimate load and tensile strength
to 31% and approximately 54% respectively, compared
with the controls. After remobilisation, the stress-strain
behaviour of the experimented MCLs was not different
from controls, but the ultimate loads were still lower, i.e.,
the material properties of the MCL appeared to recover
faster than the structural properties. Larsen, Forwood and
Parker10 compared the effects of immobilisation on the
ACL and the posterior cruciate ligament (PCL) from rat
knees immobilised in a plaster cast for four weeks. The
ultimate load of the ACL was significantly reduced,
whereas that of the PCL was not, indicating that different
connective tissue structures from the same joint react
specifically to alterations in loading.
The dynamics of an immobilisation model may result in
very different forces being experienced by the peri-
articular structures, resulting in variations in their
response. The tendons will tend to experience a continu-
ous load owing to the resting tone of their muscles. The
actual amount of stress deprivation induced in individual
tissues by immobilisation has not been quantified, and the
changes observed in the peri-articular tissues could be due
to the position of immobilisation, a change in weight-
bearing or other causative factors produced by joint dis-
use. The evidence from previous studies is contradictory.
For example, nine weeks of immobilisation have been
reported to cause a 50% reduction in elastic modulus,
with no change in cross-sectional area,8 no change in elas-
tic modulus with a reduction in cross-sectional area to
74%,11 or a reduction in both elastic modulus and cross-
sectional area.9 Thus, although the studies discussed
above show that changes do occur in ligaments and ten-
dons after immobilisation, the precise nature of the caus-
ative factor, whether it be decreased strain, decreased
stress, an inflammatory response, or some other unknown
mediator, cannot be specified.
Yamamoto et al12 studied the direct effect of stress shield-
ing the patellar tendon in the rabbit while preserving joint
movement. The patellar tendon was exposed surgically and
a cerclage wire passed between the tendon and the tibia.
The wire was tightened to slacken the tendon and the
wound closed. They found a reduction in the elastic modu-
lus and ultimate stress of the tendon, together with a reduc-
tion in tendon length and an increase in cross-sectional
area. The biomechanical effects depended on the degree of
stress reduction.13 Few data exist on the effect of re-
stressing a tendon that has been stress shielded in the pres-
ence of joint movement: Yamamoto et al14 showed that re-
stressing the patellar tendon of the rabbit with normal
activity after two weeks of stress-shielding produced a
recovery of the properties of the tendon, but they were still
significantly worse than controls even after 12 weeks of re-
stressing. These studies have an advantage over those using
an immobilisation model, in that an individual ligament or
tendon was isolated while attempting to recreate a normal
mechanical environment for the rest of the joint and the
The remodelling of tendons and ligaments is of great
interest owing to the increased use of surgical techniques
such as ACL reconstruction using both auto- and allograft
tissue,15 or rotator cuff repair. In rotator cuff tears it has
recently been demonstrated that part of the observed tissue
retraction is due to remodelling at the myotendinous junc-
tion, and not just due to muscle shortening.16 In reconstruc-
tion of the ACL with autograft tendon, a process of
‘ligamentisation’ has been described, with gradual meta-
plasia occurring over several years.17 It has been suggested
that the properties of the fibroblasts that populate tendon
grafts differ from those found in normal tendons, resulting
in a lower potential for remodelling.18,19 Both excessive and
insufficient stress can be detrimental. Tohyama and
Yasuda20 noted a reduction in the mechanical properties of
a tendon autograft model as a result of increasing the
There has been considerable interest in the potential to
manipulate the remodelling process using agents such as
growth factors and cytokines. A recent experimental study
has investigated the use of osteogenic protein-1 to stimulate
ligament remodelling in a rabbit model of ACL injury.21
However, although mechanical stimuli have been shown to
have a significant long-lasting effect on tendons and liga-
ments, as discussed above, the main controlling stimulus for
remodelling has yet to be clarified. Thus, most rehabilitation
programmes following injury or surgery have an empirical
rather than a quantified scientific basis. An understanding of
tissue remodelling in response to functional demand would
provide a scientific basis for training and rehabilitation regi-
mens that could maximise benefit and minimise the risk of
The patellar tendon is of particular interest as it serves as
a suitable model for ‘general’ tendon behaviour22 and is fre-
quently encountered in clinical practice, either as a graft for
THE INFLUENCE OF THE MECHANICAL ENVIRONMENT ON REMODELLING OF THE PATELLAR TENDON559
VOL. 91-B, No. 4, APRIL 2009
use in ACL reconstruction, or involved in disease or injury itself.
The aim of this study using a novel animal model was to test the
hypothesis that tendon exhibits structural adaptation in
response to functional loading. The model was used to investi-
gate the effects of stress shielding on the patellar tendon in
sheep, and how these effects might be reversed by recondition-
ing after stress shielding. The model uses a technique that avoids
direct exposure or contact with the patellar tendon itself.
Materials and Methods
The patellar tendon in the sheep has been shown to be a
suitable structure for studying tendon biology.22 It was
chosen for use in this study because the distribution of force
and tissue quality have been shown to be fairly uniform
throughout the tendon.23 Surgically, it is easily accessible
and the bony attachments to the patella and tibia allow the
secure insertion of metalwork, and its functional environ-
ment can be manipulated while allowing full joint function.
A change in ultimate stress of 30% was deemed to be clini-
cally important, and a power analysis suggested that a mini-
mum of four subjects and controls would be required for an
unpaired t-test to reach statistical significance, assuming an SD
of 10% (power 0.8, α 0.05). Two groups of animals were
used. In group 1, six sheep had the right patellar tendon stress
shielded for six weeks before being killed. In group 2, six sheep
had the right patellar tendon stress shielded for six weeks,
after which the stress shielding device was removed, allowing
physiological re-stressing for a further six weeks. Biomechan-
ical analysis was performed on the treated tendons and the
untreated contralateral tendons were similarly analysed to
obtain control data for comparison.
Animals. There were 12 skeletally mature Welsh Mule ewes
who were housed extensively in large indoor pens. All the
animal procedures were carried out under licences granted
by the United Kingdom Home Office in accordance with the
Animals (Scientific Procedures) Act of 1986, and had local
ethical committee approval. The animals were killed by
lethal intravenous injection of barbiturate.
Stress shielding the patellar tendon. A custom-built external
fixator was used to stress shield the patellar tendon in the pres-
ence of normal joint movement, as shown in Figure 1.
The surgical procedures were performed under general
anaesthesia using a sterile technique. Pre-medication with
0.05 ml/kg 2% xylazine was administered intramuscularly.
Induction was achieved with 0.2 ml/kg ketamine and
2.5 mg midazolam intravenously. Buprenorphine was used
for analgesia. The sheep were then intubated. A oesopha-
geal tube was used to void rumenal gases, and anaesthesia
was maintained with 2% halothane gas.
Analysis of structural and material properties. The patellar
tendon from each limb was harvested as a bone-patellar
tendon-bone unit and immediately subjected to testing. The
samples were moistened throughout with physiological
Stress shielding the patellar tendon. Diagram showing a) the custom-built external fixator, consisting of a tibial component, a patellar
component and a cable linkage. b) and c) show the fixator as applied to the animal in the coronal and sagittal plane, respectively. The
tibial component was fixed to the tibia using two 5 mm diameter bone half-pins (Orthofix Inc., McKinney, Texas) inserted percutane-
ously. A 3 mm pin was drilled transversely through the body of the patella. An end cap on each side accepted a wire linkage to the tibial
block. After the external fixator was applied, the distance of the inferior pole of the patella from the tibial tuberosity was measured with
a pair of Vernier calipers with the knee in 90° of flexion. The patella was then drawn 15 mm towards the tibia by using the turnbuckle
screw mechanism. This was confirmed by a repeated measurement. The range of movement of the knee was examined and found not
to be limited by this procedure. c) The patellar tendon was palpated to be slack in full flexion, 90° of flexion and full extension. This was
assumed to reflect complete stress shielding of the tendon. During the period of stress shielding, the tendon was palpated in 90° of
knee flexion twice a week to confirm that it was still slack.
560 A. P. RUMIAN, E. R. C. DRAPER, A. L. WALLACE, A. E. GOODSHIP
THE JOURNAL OF BONE AND JOINT SURGERY
Measurement of the cross-sectional area. This was measured
using the method described by Goodship and Birch.25 An alg-
inate dental impression material (Blueprint cremix, Dentsply
De Trey, Germany; supplied by Claudius Ash, Potters Bar,
United Kingdom) was used to make an impression of the
bone-patellar tendon-bone complex. After removal of the
specimen, transverse sections were taken through the mid-
point of the tendon mould, and at points 10 mm either side.
The sections were photographed on a calibration scale using a
mounted 5 megapixel digital camera. Digital images were used
to measure the area of the cavity left by the specimen in the
mould sections using a semi-automated image analysis soft-
ware package (Image-Pro Plus, Media Cybernetics Inc.,
Bethesda, Maryland). The mean of three measurements was
calculated to obtain the value for the cross-sectional area of
Tendon length. The tendon length was defined as the distance
from the most distal part of its insertion into the patella to the
most proximal part of its insertion into the tibia. This was
measured with a Vernier caliper.
Mechanical testing. The bone-tendon unit was mounted in the
specifically designed clamps of a computer-controlled servo-
hydraulic materials testing machine (Dartec/Zwick, GmbH &
Co., Ulm, Germany), which combined pin fixation with a
cryo-clamp technique.26 Thus, the gauge length of the speci-
men being tested was the distance between the two clamps.
The tendon was pre-conditioned to obtain a steady-state
load-deformation curve27,28 using a standard protocol of
20 cycles of loading from 5 N to 50 N at 0.5 Hz.29 It was then
tested to failure under displacement control at a distraction
rate of 40 mm/s, which is comparable to a rate of loading
reported in the patellar tendon of the goat under physiological
conditions.30 Stiffness was defined as the gradient of the linear
part of the load-deformation curve. Likewise, elastic modulus
was the gradient of the stress-strain curve. The ultimate load,
ultimate stress, and ultimate strain were derived from peak
values before failure. Strain energy was defined as the area
under the stress-strain curve. Toe limit strain was defined as
the maximum strain of the initial portion of the stress-strain
curve before the onset of linear elastic behaviour. The mode of
failure of each tendon was also recorded.
Statistical method. All the results are reported as the mean ±
the standard error of the mean (SEM). The Shapiro-Wilks test
was used to confirm the normality of distribution of the data.
Data from the untreated tendons of both groups were tested
for statistical significance using the unpaired t-test. A one-way
analysis of variance was used to examine data between the
two experimental groups and controls. Where statistical dif-
ferences were found, these were further explored using the
Tukey-Kramer method for multiple comparisons. The level of
statistical significance was set at p < 0.05.
In group 1, one animal was excluded because of an infec-
tion of the pin site in the patella. In group 2, one sheep
died immediately after anaesthesia. This left five animals
in each group. The Shapiro-Wilks test revealed no evi-
dence of non-normality of distribution of the data. There
were no significant differences between groups 1 and 2 in
any of the parameters of the untreated tendons. Therefore,
these results were pooled and used as the control data.
Mode of failure. All the tendons failed in the substance of
the ligament. Of the ten control tendons, seven failed in
the middle, two in the proximal and one in the distal third.
All the stress-shielded tendons in group 1 failed in the
middle third. Out of the five re-stressed tendons, four
failed in the middle and one in the proximal third. None
failed due to bone avulsion. No slippage was observed to
have occurred in the testing clamps.
Structural properties. The tendon lengths did not differ
significantly between the three groups. However, the
cross-sectional area of the re-stressed tendons was found
to be significantly greater than the stress-shielded tendons,
with a mean difference of 6.6 mm2 (p = 0.046; 95% con-
fidence interval (CI) 0.1 to 13.2). Neither the stress-
shielded nor the re-stressed tendons were significantly
different from the controls.
The stress-shielded tendons exhibited statistically signif-
icant reduction compared with the controls, with a mean
stiffness of 79% (mean difference 0.074 kN/mm; p = 0.041;
95% CI 0.003 to 0.14), an ultimate load of 69% (mean dif-
ference 0.90 kN; p = 0.0042; 95% CI 0.29 to 1.5) and
energy absorbed of 61% (mean difference 6.5 MPa;
p = 0.039; 95% CI 0.32 to 13). However, the structural
properties of the re-stressed tendons were much closer in
value to, and not significantly different from, the control
tendons, with a mean stiffness of 97%, an ultimate load of
92% and energy absorbed of 96%. The values for
Table I. Table I. Structural properties of control, stress shielded and re-stressed tendons
reported as mean values, with standard error in parentheses
Ultimate force (kN)
Energy absorbed (MPa)
* CSA, cross-sectional area
THE INFLUENCE OF THE MECHANICAL ENVIRONMENT ON REMODELLING OF THE PATELLAR TENDON561
VOL. 91-B, No. 4, APRIL 2009
structural properties are shown in Table I. The load–
deformation curves are shown in Figure 2a.
Material properties. The stress-shielded tendons also exhib-
ited significant deterioration in material properties com-
pared the controls, with a mean elastic modulus that was
76% of the control value (mean difference 88 MPa;
p = 0.026; 95% CI 10 to 167) and a mean ultimate stress of
72% (mean difference 22; p = 0.012; 95% CI 4.6 to 39).
After re-stressing these values only recovered to 79% and
80%, respectively, although this was not found to be signif-
icantly different from either the control or the stress-
shielded tendons. The ultimate strain was similar for all
tendons, as was the toe limit strain. The values for material
properties are shown in Table II. Figure 2b shows the stress-
strain curves for all experimental groups.
In this study the patellar tendon exhibited significant
changes in its biomechanical characteristics, both structural
and material, in response to changes in functional loading.
All the stress-shielded tendons failed in the mid-substance,
indicating that change occurred in the tendon itself rather
than at the sites of bony insertion. If the sites of insertion
were more affected or there was significant resorption of
bone, then one would expect more failures at these sites or
by bone avulsion, as described by Woo et al9 and Noyes4 in
immobilised joints. Fujie et al31 also observed that stress
shielding of the patellar tendon for more than one week in
both mature and immature rabbits resulted in failures in the
midsubstance of the tendon.
Stress shielding for six weeks did not significantly change
the tendon length or the cross-sectional area. This differs
from the findings of Yamamoto et al,12 who observed an
increased cross-sectional area of 140% compared with con-
trols and a shorter tendon length after six weeks of stress
shielding. However, they noted that the cross-sectional area
decreased between three and six weeks of stress shielding,
which they could not explain. Also, in the canine ACL, the
cross-sectional area has been observed to increase after six
weeks of stress shielding, but this effect had disappeared by
12 weeks.32 Changes in the cross-sectional area could be
related to changes in water and glycosaminoglycan content,
or the collagen mass.33,34 The lack of difference in toe limit
strain supports the observation of no change in tendon
length. This limit is dependent on the crimp profile of the
tendon, which would not be expected to change in the
absence of change in length.
Re-stressing tendons after two or three weeks of stress-
shielding has been reported to reduce the cross-sectional
area and increase the tendon length.14 However, we found
Table II. Table II. Material properties of control, stress shielded and re-stressed tendons
reported as mean values, with standard error in parentheses
Ultimate stress (MPa)
Ultimate strain (%)
Elastic modulus (MPa)
Toe limit strain (%)
Graphs showing a) structural properties: load-deformation curve for control, stress shielded and re-stressed tendons, the gradient of the linear por-
tion of the curve represents stiffness, error bars show standard error of the mean and b) material properties: stress-strain curve, the gradient of the
linear portion represents the elastic modulus.
562A. P. RUMIAN, E. R. C. DRAPER, A. L. WALLACE, A. E. GOODSHIP
THE JOURNAL OF BONE AND JOINT SURGERY
that the cross-sectional area was significantly increased in
re-stressed tendons compared with the stress-shielded ten-
dons, although these findings are not directly comparable,
owing to the different lengths of initial stress shielding.
Both the structural and the material properties of the
patellar tendon were significantly reduced by stress shield-
ing. The stiffness and elastic modulus were 79% and 76%
of the control values, respectively, whereas the ultimate
load and ultimate stress were 69% of the controls. Yama-
moto et al12 found much greater reductions in the stress-
shielded patellar tendon in the rabbit knee, with a mini-
mum modulus of approximately 20% of controls after six
weeks of stress-shielding. This is in contrast to Keira et
al,32 who observed no significant change in modulus after
six weeks of stress-shielding of the canine ACL, but a
modulus of 61% of the control value after 12 weeks. The
patellar tendon of the sheep appears to lie in the middle of
Re-stressing tendons for six weeks after six weeks of
stress shielding demonstrated a recovery of structural prop-
erties, with a return to almost 100% of the control values.
This was associated with an increase in cross-sectional area.
However, the material properties exhibited a trend towards
incomplete recovery, achieving only 80% of the control
values. Thus, the tendons are shown to experience struc-
tural adaptation. The re-stressed tendons compensate for
their continued low elastic modulus by the increase in the
A possible reason for the disagreement between studies
regarding the effect of stress shielding on the biomechanical
properties of tendons and ligaments could be differences in
the patterns of activity of the experimental animals, which
have not been accurately quantified in any of the studies, or
due to differing metabolic responses of the tissues.34
Another explanation may be the different strain rates used
in various studies. Those using video analysis systems have
employed low strain rates to enable the capture of images,
whereas the physiological strain rate used in our study is
much higher. Thus the differences in findings could be due
to the sensitivity of tendon to strain rate. Noyes, DeLucas
and Torvik35 found that, for a 100-fold increase in test
speed, the failure load increased by 21%.
Another possible reason is the disparate nature of the
techniques used to achieve the stress shielding. Immobilisa-
tion models are unable to achieve stress shielding of an indi-
vidual structure without affecting the other tissues around a
joint. Previous techniques to functionally isolate one struc-
ture have involved quite extensive surgical exposure and
dissection of the structure under investigation. This, of
necessity, induces an inflammatory healing response
directly adjacent to the structure, which may then influence
its response to the altered mechanical environment. For
example, in the study by Keira et al32 on the canine ACL,
sham operated controls still varied significantly from non-
operated controls. In Yamamoto’s model, sham operation
did not cause significant differences in the patellar tendon
compared with controls. However, this does not exclude
the possibility that the inflammatory response still modu-
lated the behaviour of the tendon to stress shielding. In
order to control for this it would require comparison of the
results of stress shielding the tendon by two different tech-
niques, one using the surgical exposure and one avoiding it.
The novel model presented here involves the use of bone
pins inserted into a site remote from the patellar tendon
itself, and the stress shielding is achieved without the need
for any surgical insult to the structure under investigation.
Proposed ‘strain homeostasis’ feedback control loops governing remodelling behaviour for a) stress shielded and b) re-stressed tendons (CSA, cross-
THE INFLUENCE OF THE MECHANICAL ENVIRONMENT ON REMODELLING OF THE PATELLAR TENDON563
VOL. 91-B, No. 4, APRIL 2009
There are several weaknesses in this study, a major one of
which is the small number of animals. An initial power
analysis suggested that only four animals would be required
to show a 30% reduction in ultimate stress to be statisti-
cally significant. The initial study design included six ani-
mals in each group, although only five remained for
analysis. Despite this, statistically significant differences
were found between control and stress shielded tendons. The
re-stressed tendons, however, exhibited better biomechanical
properties than suggested by previous reports, and the SD
was larger than the 10% initially assumed. Thus, the study
lacked the power to detect differences between the re-
stressed and the other tendons. Another weakness is the lack
of histological or molecular data to correlate with the results
of mechanical testing. It was felt wrong to perform such
analysis on the same tissue, as the results might be influenced
by the disruption of extracellular matrix and intracellular
architecture involved in destructive mechanical testing.
The biomechanical tests were carried out using a cryo-
clamp technique with supplementary pin fixation. The
specimens were mounted carefully so that the length of the
tendon would be equal to the length of gauge submitted to
testing. Although no slippage was observed to have
occurred in the clamps during testing, this was not directly
measured. Also, changes in the sites of insertion of the
patellar tendon may have contributed to the observed
effects of the stress shielding. However, the fact that all ten-
dons failed in the mid-substance supports the assumption
that most change occurred in the tendon itself, and that
slippage was not occurring in the clamps. Use of a video
analysis system to determine strain of the tendon mid-
substance directly would have avoided this uncertainty.
However, the limitations of such a system would not have
allowed mechanical testing at the high, physiologically
based strain rate used in this study.
Although the biomechanical changes in the tendon have
been described here, it is difficult to ascertain how much
deterioration needs to occur before becoming clinically
relevant, or how much recovery is required before full
normal activity can be tolerated. The initial aim in this
study was to detect a 30% reduction in ultimate stress, as
this would be the level at which a catastrophic failure of
the tendon might occur in vivo. However, it may be that
the elastic modulus itself is of more significance in allow-
ing normal function during the stresses experienced in
routine physiological activity.
The nature of the changes in the tissue of a stress-shielded
tendon is just beginning to be clarified. These include an
increase in the number of fibroblasts,12,36 of the number of
small collagen fibrils,36,37 the expression of manganese
superoxide dismutase,38 and the expression of cytokines
such as IL-1β, TNF-α and TGF-β.39 Abiezzi et al40 described
an increase in integrin adhesion subreceptor units in
conjunction with the remodelling of stress-deprived rabbit
ligaments. Mechanical strain has recently been shown to
stimulate the conformational activation of integrins
The biomechanical changes observed in the present study
could be controlled by a feedback loop under strain control
(Fig. 3), similar to that described in a recent computational
model.42 When deprived of stress, the strains experienced
by a tendon are much lower than normal. Mechanotrans-
duction mechanisms, possibly mediated by integrins, initi-
ate the remodelling process. As the elastic modulus
decreases, the strain increases until ‘strain homeostasis’ is
achieved. When once again subjected to stress, the weak-
ened tendons experience greater strains than normal.
Mechanotransduction mechanisms result in structural
adaptation, with an increase in the cross-sectional area.
This once more brings the strain back towards normal
values. Although the tissue exhibits structural adaptation,
the evidence from this and other studies suggests that
changes in material properties due to stress deprivation are
not quickly reversed.
Much further work using this model is planned. Initially,
the histological and biochemical changes occurring in the
stress shielded and re-stressed tendons need to be eluci-
dated. Subsequently, the effects of increased stress on nor-
mal tendons can be investigated by applying a distracting
force across the components of the external fixator mecha-
nism. Mechanical actuators will be used so that the strain
applied can be accurately controlled in terms of rate, cycli-
cal frequency and the number of cycles. One of the primary
aims for the future will be to determine the threshold levels
of stimulation required to control the remodelling process.
This would be of direct clinical relevance and enable us to
elucidate the least amount of activity necessary to prevent
deterioration, when any extra activity ceases to be of bene-
fit; and how much is too much.
No benefits in any form have been received or will be received from a commer-
cial party related directly or indirectly to the subject of this article.
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